Skip Navigation

Nucleic Acids Research 2006 34(10):2887-2905; doi:10.1093/nar/gkl295
This Article
Right arrow Abstract Freely available
Right arrow Print PDF (3201K) Freely available
Right arrow Screen PDF (1886K) Freely available
Right arrow Supplementary Material
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (60)
Right arrow Commercial Re-use Guidelines
for Open Access NAR Content
Google Scholar
Right arrow Articles by Flaus, A.
Right arrow Articles by Owen-Hughes, T.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Flaus, A.
Right arrow Articles by Owen-Hughes, T.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

Published online 31 May 2006

© The Author 2006. Published by Oxford University Press. All rights reserved
The online version of this article has been published under an open access model. Users are entitled to use, reproduce, disseminate, or display the open access version of this article for non-commercial purposes provided that: the original authorship is properly and fully attributed; the Journal and Oxford University Press are attributed as the original place of publication with the correct citation details given; if an article is subsequently reproduced or disseminated not in its entirety but only in part or as a derivative work this must be clearly indicated. For commercial re-use, please contact journals.permissions@oxfordjournals.org

Article

Identification of multiple distinct Snf2 subfamilies with conserved structural motifs

Andrew Flaus, David M. A. Martin1, Geoffrey J. Barton1 and Tom Owen-Hughes*

Division of Gene Regulation and Expression, University of Dundee Dundee DD1 5EH, Scotland, UK 1 Bioinformatics and Computational Biology Research Group, School of Life Sciences, University of Dundee Dundee DD1 5EH, Scotland, UK

*To whom correspondence should be addressed. Tel: +44 0 1382 385796; Fax: +44 0 1382 388702; Email: t.a.owenhughes{at}dundee.ac.uk

Received February 3, 2006. Revised March 18, 2006. Accepted April 5, 2006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUPPLEMENTARY DATA
 REFERENCES
 
The Snf2 family of helicase-related proteins includes the catalytic subunits of ATP-dependent chromatin remodelling complexes found in all eukaryotes. These act to regulate the structure and dynamic properties of chromatin and so influence a broad range of nuclear processes. We have exploited progress in genome sequencing to assemble a comprehensive catalogue of over 1300 Snf2 family members. Multiple sequence alignment of the helicase-related regions enables 24 distinct subfamilies to be identified, a considerable expansion over earlier surveys. Where information is known, there is a good correlation between biological or biochemical function and these assignments, suggesting Snf2 family motor domains are tuned for specific tasks. Scanning of complete genomes reveals all eukaryotes contain members of multiple subfamilies, whereas they are less common and not ubiquitous in eubacteria or archaea. The large sample of Snf2 proteins enables additional distinguishing conserved sequence blocks within the helicase-like motor to be identified. The establishment of a phylogeny for Snf2 proteins provides an opportunity to make informed assignments of function, and the identification of conserved motifs provides a framework for understanding the mechanisms by which these proteins function.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUPPLEMENTARY DATA
 REFERENCES
 
Some 15 years ago Gorbalenya and Koonin (1,2) identified a large group of proteins sharing a series of short ordered motifs. The majority of members with known function were nucleic acid strand separating helicases so the sequences became known as helicase motifs and were labelled sequentially I, Ia, II, III, IV, V and VI. A number of additional conserved blocks with broad distributions within these helicase-like proteins have subsequently been identified, such as the TxGx (3) and Q motifs (4).

Proteins containing the helicase motifs are subdivided into several superfamilies on the basis of similarity. Structural characterizations have revealed that helicase-like superfamilies 1 and 2 (SF1 and SF2) are related with a common core of two recA-like domains (5). The helicase-like enzymes link ATP hydrolysis to a directed change in the relative orientation of these domains (6). Structural and mutagenesis studies have shown that each of the conserved motifs in the active site cleft between the recA-like domains plays a role in the transformation of chemical energy from ATP hydrolysis to mechanical motion. This enzymatic process has been suggested to represent one application of a more general mechanism used in many proteins containing a recA-like domain (7).

Proteins with a helicase-like region of similar primary sequence to Saccharomyces cerevisiae Snf2p comprise the Snf2 family within SF2 (Figure 1A). Indeed, Snf2p was specifically aligned within SF2 by Gorbalenya and Koonin (1). Many of the first identified Snf2 family members were ATPases within chromatin remodelling complexes and it was recognized that the presence of a core polypeptide related to Snf2p is a defining property of ATP-dependent chromatin remodelling (8). It is now apparent that the Snf2 family comprises a large group of ATP-hydrolysing proteins that are ubiquitous in eukaryotes, but also present in eubacteria and archaea.


Figure 1
View larger version (30K):
[in this window]
[in a new window]
  		Figure 1 Tree view of Snf2 family. (A) Schematic diagram illustrating hierarchical classification of superfamily, family and subfamily levels. (B) Unrooted radial neighbour-joining tree from a multiple alignment of helicase-like region sequences excluding insertions at the minor and major insertion regions from motifs I to Ia and conserved blocks C–K for 1306 Snf2 proteins identified in the Uniref database. The clear division into subfamilies is illustrated by wedge backgrounds, coloured by grouping of subfamilies. Subfamilies DRD1 and JBP2 were not clearly separated, as discussed in text. (C) In order to illustrate the relationship between subfamilies, a rooted tree was calculated using HMM profiles for full-length alignments of the helicase regions. Groupings of subfamilies are indicated by colouring as in (B).

 
At least a subset of Snf2 family proteins act as ATP-dependent DNA translocases (9–12). Some of these proteins have also been found to be capable of generating unconstrained superhelical torsion in DNA (11,13–17), proposed to occur as a result of the translocation of DNA into constrained loops. This is substantiated by recent analysis of the action of RSC on single DNA molecules (18). In addition to distorting DNA, the ATP-dependent action of these proteins can disrupt chromatin as measured using a range of different assays (8), although other DNA–protein interactions can also be affected. For example, Rad54 promotes Rad51-dependent strand pairing (13), and Mot1 displaces the TATA-binding protein (TBP) from DNA (19). Thus although many Snf2 family proteins are likely to act to alter chromatin structure, this is not the case for all members of the family.

Early biochemical studies and sequence alignments suggested that members of the Snf2 family could be further subdivided into a number of subfamilies (20). These subfamilies have traditionally taken the name of the archetypal member, such as S.cerevisiae Snf2p (Snf2 subfamily), Drosophila melanogaster Iswi (Iswi subfamily), Mus musculus Chd1 (Chd subfamily) and S.cerevisiae Rad54p (Rad54 subfamily). Snf2p, therefore, lends its name to both the collective Snf2 family and a specific Snf2 subfamily (Figure 1A).

The only comprehensive analysis of the Snf2 family sequences to date was performed by Eisen et al. in 1995 (20). Although it has subsequently been revisited within the context of various biochemical studies (21–24), no broad survey has been conducted for over a decade.

To gain new insights into the Snf2 family, we have catalogued Snf2 family members by scanning for proteins containing spans with similarity in sequence over the helicase-like region, classifying them into subfamilies, analysing the distribution of these subfamilies in complete genomes, and mapping the common sequence characteristics onto the newly available three-dimensional structures. We have identified 24 distinct subfamilies, 11 with near ubiquitous representation in eukaryotic genomes. Many of these subfamilies correlate with known biological function, but there remain a significant number for which little information is currently available. The abundance of Snf2 family members in eukaryotes in comparison to archaea and eubacteria points to their diversification early in eukaryote radiation. This diversity and the currently known functional linkages suggest the Snf2 family helicase-like region is specifically adapted to perform distinct functions within different subfamilies. Underlying this, analysis of the conserved blocks of residues reveals a common core of structural features likely to be fundamental to the mechanism of the Snf2 family motors.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 SUPPLEMENTARY DATA
 REFERENCES
 
Data and software sources
Swissprot/Uniprot (25) release 42 and Uniref100 (26) release 5 were downloaded from the European Bioinformatics Institute (ftp://ftp.ebi.ac.uk/pub/databases/swissprot/ and ftp://ftp.ebi.ac.uk/pub/databases/uniprot/, respectively). The sources and version details for the predicted protein complements of the 54 eukaryotic, 24 archaeal and 269 prokaryotic organisms surveyed are available at the webserver http://www.snf2.net/. Analyses were performed on a cluster of dual Pentium III microcomputers running a customized Debian Linux operating system.

Sequence data were manipulated with the EMBOSS suite version 2.8 (27). Multiple sequence alignments were created with Muscle version 3.0 (28) and MAFFT version 5.667 with parameters retree = 2 and maxiterate = 1000 (29) and visualized with Jalview version 2 (30). Phylogenetic and pairwise trees were constructed with neighbor, protdist and drawtree from the PHYLIP suite version 3.572 (31) and additionally visualized with ATV version 2.03 (32) and Hypertree version 1.0.0 (33). Hidden Markov model (HMM) construction, calibration and searching was performed with the HMMer suite versions 2.1.1 and 2.2g (34), and pairwise comparison of HMMs carried out with PRC version 1.5.3 in global-global mode (35). Sequence LOGOs were generated with WebLogo version 2.8.2 (36) and profile logos generated with logomat-p using the draw_logo method, version 0.71 (37). Protein structures were visualized with PyMol version 0.99 (38). Data were managed using mySQL (http://www.mysql.com) and PostgreSQL (http://www.postgresql.org) relational databases. Calculations were carried out using default parameters except where indicated. All other analyses used custom Perl or Python scripts written by the authors. All supplementary data for this report and an interactive database of the results are publicly available at the web server http://www.snf2.net/.

Experimental methods
A full technical description of the library construction and validation and details of the web server will be available elsewhere (D.M.A. Martin and A. Flaus, manuscript in preparation). The procedure used is summarized in outline below.

Global Snf2 family HMM construction
Twenty-eight biochemically characterized S.cerevisiae Snf2p-like chromatin remodelling proteins or close homologues were selected as seed sequences. The core helicase-like region spanning from 50 amino acids N-terminal to helicase motif I to 50 amino acids C-terminal of helicase motif VI was excised from each protein sequence and multiple alignments were created with Muscle using default parameters. An initial seed HMM was constructed following manual assessment of the alignment.

Swissprot 42 was searched using this profile, expanding the set of Snf2 family sequences to 620 candidates with matches up to E-values of 2 although some matches near this cut-off were helicase-like sequences which were not members of the Snf2 family. Further iterations of HMM construction and searching of Swissprot 42 and model organism databases, followed by curation of sequences to remove fragmented sequences and other artefacts not belonging to the Snf2 family, yielded a set of 948 manually curated sequences which were then aligned by MAFFT.

The resultant profile was employed in searching Uniref100 and identified 5046 sequences with a match of E-value 10 or better of which 3932 had E-values below 1 and 1879 had positive bit-scores. This cut-off may appear generous but was intentional to enable maximum possible inclusion of Snf2 family members. It is predicated by the considerable variation in sequence between helicase motifs III and IV giving rise to poor alignments to the general model in this region and consequently lower bit scores. The cut-offs selected were determined by manual inspection of the hit lists and alignments to include established Snf2 family-like proteins but exclude more distant relatives. The highest E-value for a sequence classified into a subfamily (see below) was 2.2 x 10–16.

Phylogenetic analysis of helicase-like sequences
A multiple sequence alignment with Muscle, followed by distance matrix calculation and neighbour-joining tree reconstruction allowed the curation of 2305 sequences into subgroupings in the Snf2 family based on the sequence of the helicase-like region. 1306 sequences were classified in 24 individual subfamilies within the Snf2 family (Table 1) after the exclusion of 436 which were fragmentary (did not span completely from helicase motifs I to VI) or contained unique large inserts or deletions. A further 220 were assigned to the prokaryotic rapA group and the remainder to more distantly related clusters or as highly truncated outliers which could not be reasonably aligned. An overview of a neighbour-joining tree constructed from a multiple alignment excluding the variable minor and major insertion regions (see text) and visualized using Hypertree demonstrates the clearly distinguishable division of subfamilies (Figure 1B). Each subfamily was individually examined for redundancy and further internal structure (data not shown).


View this table:
[in this window]
[in a new window]
  		Table 1 Summary of subfamilies

 
Construction and use of subfamily profiles
Each subfamily sequence set was realigned by MAFFT, manually curated with Jalview and an HMM profile constructed. These profiles were aligned with PRC in an all-against-all comparison. Although these profile comparisons do not give a true phylogenetic tree, the scores obtained from the pairwise profile alignments can be used to construct a representational tree (Figure 1C), indicating the relationship between the HMM profiles to be consistent with the sequence-based tree (Figure 1B). It was also observed that the subfamilies could be aggregated into some broad groupings that correlate with functional properties, where known (Figure 1).

All 24 subfamily profiles were combined in one HMM library and the hmmpfam application employed in searching individual genomic datasets to provide phylogenomic information about the taxonomic distribution of Snf2-like proteins. The subfamily hit with maximal bitscore >100 was used to assign membership in a semi-automatic procedure. With very few exceptions, classification was extremely clear with strong discrimination between the top hit and the second best hit (data not shown).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
SUPPLEMENTARY DATA
 REFERENCES
 
Starting from a seed set of helicase-like region sequences from 28 demonstrated Snf2p-related proteins or close homologues, we have carried out a broad survey of Snf2 family proteins. This was achieved by iterative cycles of manual curation of multiple alignments and neighbour-joining trees to identify Snf2 proteins by similarity, construction of an HMM profile from the multiple alignments of identified proteins, and scanning of global and model organism protein databases using the HMM profile to uncover further sequences for curation. Our current global Snf2 family profile scan revealed 3932 sequences with E-value under 1 (1879 with bitscore > 0) in Uniref100 release 5 [2.4 million entries (26)]. Of these, 1306 sequences were identified as belonging to the Snf2 family and to span the full helicase region from motifs I to VI without introducing large unique insertions or deletions. A further 220 sequences fall within the rapA group, while other hits appear to belong to more distantly related groups (see below) or were too highly truncated to be aligned. Neighbour-joining trees from multiple alignments of the set of 1306 sequences revealed a well-defined branching structure (Figure 1B) and enabled their assignment to 24 distinct subfamilies (Table 1).

Subfamily-specific HMM profiles were constructed from these assignments and used to characterize the Snf2 family complement for 54 complete eukaryote genomes. The counts of predicted proteins and unique encoding genes for 21 selected genomes are listed in Table 2, part A and B, respectively (see Supplementary Table S1A for full analysis of eukaryotic genomes, and Supplementary Table S2 for gene IDs by subfamily for seven common model organisms). In addition, 24 complete archaeal and 269 bacterial genomes were scanned (Supplementary Tables S1B and S1C).


View this table:
[in this window]
[in a new window]
  		Table 2 Subfamily occurrences in selected complete eukaryotic genomes

 
Subfamilies within the Snf2 family
The clear distinction and significant number of subfamilies based on the helicase-like region (Figure 1B and Table 1) reflects both a remarkable breadth and specificity in the Snf2 family. An additional level of similarity distinguishes apparent groupings of subfamilies (Figure 1), which echo current understanding of their functional diversity (Table 3). Most of the best studied Snf2 family proteins fall into a grouping of ‘Snf2-like’ subfamilies including proteins such as S.cerevisiae Snf2p, D.melanogaster Iswi, mouse Chd1 and human Mi-2, which are core subunits of the well-known ATP-dependent chromatin remodelling complexes. A separate ‘Swr1-like’ grouping encompasses the Swr1, Ino80, EP400 and Etl1 subfamilies. The ‘Rad54-like’ grouping contains the Rad54 subfamily, relatives such as ATRX and Arip4, and also includes the recently recognized DRD1 and JBP2 proteins. A further, unexpected, ‘Rad5/16-like’ grouping links several poorly studied subfamilies, three of which contain RING finger insertions within the helicase-like region (see below). The ‘SSO1653-like’ grouping of Mot1, ERCC6 and SSO1653 is notable because all three subfamilies are thought to have non-chromatin substrates. Finally, we have labelled SMARCAL1 proteins as ‘distant’ because they lack several otherwise conserved sequence hallmarks of the Snf2 family (see below). Although some groupings are clear, further investigations will be required to verify those where the boundaries are less distinct.


View this table:
[in this window]
[in a new window]
  		Table 3 Functional and sequence characteristics of subfamilies

 
Since the subfamily assignments are based only on the common helicase-like region, this suggests that the ‘motor’ at the core of even large multiprotein remodeller complexes is tuned to the mechanistic requirements of its function. Such properties are not unprecedented for motor protein subfamilies. The ubiquitous kinesin and myosin proteins are divided into at least 14 and 17 subfamilies, respectively (39,40), and those subfamilies are recognized to reflect tuning of the motors for enzymatic properties linked to particular functional roles. As this also appears to be true for Snf2 family proteins we can anticipate that mechanistic features of the motors will be shared within subfamilies and groupings. This may be useful in helping to predict function of poorly characterized proteins. For example, owing to the recent observation that Swr1 functions in histone exchange (41–43), it is tempting to speculate that the Snf2 motors within other subfamilies in the Swr1-like grouping may be adapted for related purposes.

Owing to the remarkable diversity revealed by this classification and the occurrence of many subfamilies which have not been intensively investigated, we briefly summarize current functional and biochemical understanding and characteristic features of each subfamily in Table 3.

Defining the Snf2 family
The survey of Snf2 family proteins enables detailed analysis of sequence conservation in the helicase-like region (Figure 2). This reveals a number of unique features distinguishing them from other helicase superfamily SF2 members. First, the conserved helicase motifs show a highly conserved character across the Snf2 family, and some motifs are extended by juxtaposed residues such as conserved blocks E and G (Figure 2 and Supplementary Figure S4). Second, the helicase-like region in the Snf2 family is significantly longer than for many other helicases, primarily due to an increased spacing between motifs III and IV of >160 residues compared to 38 and 78 for typical SF2 helicases NS3 and RecG, respectively (44). Third, a number of unique conserved blocks are found in Snf2 family proteins (Figure 2 and Supplementary Table S5). Several of these blocks have been noted previously (20,45–48), with conserved block B having been confused in a number of early manuscripts with motif IV. Conserved blocks B, C and K are of particular interest because they are located within the characteristic extended inter-motif III–IV region (Figure 3G).


Figure 2
View larger version (64K):
[in this window]
[in a new window]
  		Figure 2 Conserved residues within Snf2 helicase-like region. Sequence logo of global multiple alignment of 1306 Snf2 helicase-like region for alignment positions with residues in >90% of proteins. Helicase motifs are indicated in solid black boxes with roman numerals I–IV, additional conserved blocks are indicated in dashed black boxes with uppercase letters A–N, and conserved hydrophobic residues packing in the core of the structure by grey solid boxes. Motif and box labels as in Thoma et al. (47) with extensions. A comparison to other nomenclatures is in Supplementary Table S5. See Table 4 for actual distances between conserved blocks.

 

Figure 3
View larger version (41K):
[in this window]
[in a new window]
  		Figure 3 Conserved blocks contribute to distinctive structural features of Snf2 family proteins. Structural components of Snf2 family proteins relevant to the conservation are illustrated on the zebrafish Rad54A structure [pdb 1Z3I (153)]. (A) core recA-like domains 1 and 2 including colouring of helicase motifs (I in green, Ia in blue, II in bright red, III in yellow, IV in cyan, V in teal and VI in dark red). (B) Q motif (pink). (C) antiparallel alpha helical protrusions 1 and 2 (red) projecting from recA-like domains 1 and 2, respectively. (D) Linker spanning from protrusion 1 to protrusion 2 (middle blue). (E) Major insertion region behind protrusion 2 (light green). (F) triangular brace (magenta). (G) Schematic diagram showing location of structural elements and helicase motifs coloured as in A–F, with conserved blocks from Figure 2 shown as white boxes. Spans identified by Pfam profiles SNF2_N and Helicase_C are shown flanking the major insertion site.

 
The SMARCAL1 subfamily contains classical helicase motifs which are highly similar to the other subfamilies. It also has an extended motif III–IV spacing, but it nevertheless lack conserved blocks within the motif III–IV region (Supplementary Figure S4). The rapA group has similar properties but is more diverse in overall sequence and retains less similarity in the classical motifs. It is unclear whether the SMARCAL1 subfamily and particularly the rapA group will maintain the structural features of the Snf2 family and they are therefore at the limit of the definition of the Snf2 family. We have also noticed further protein groupings with extended spacing between motifs III and IV and detectable similarity to the classical helicase-like motifs of the Snf2 family sequences (Supplementary Figure S4). These include poxvirus NPH-I related proteins involved in transcription termination (49) and the FANCM/MPH1/Hef group of helicases encompassing yeast Mph1p, archaeal Hef and human FANCM proteins involved in DNA repair (50–52). However, those proteins show low similarity to the Snf2 family between motifs III and IV and appear to lack the characteristic conserved blocks C, J and K of the Snf2 family. Interestingly, comparison of the recently determined Pyrococcus furiosus archaeal Hef helicase structure reveals that the MPH1/Hef group has a related structural organization to Zebrafish Rad54, but contains only a single compact alpha-helical domain encoded between motifs III and IV (Supplementary Figure S6). It has been noted that this extra alpha-helical domain has some similarities with the thumb domain of Taq DNA polymerase which grips the DNA minor groove (53). It is therefore likely that the SMARCAL1 subfamily, rapA group, NPH-I and MPH1/Hef proteins reflect a continuum of diversity while sharing core features with the other Snf2 subfamilies.

Evolution of Snf2 family diversity
None of the 293 scanned archaeal or bacterial genomes contains a protein classified in any of the eukaryotic subfamilies (Supplementary Tables S1B and S1C). All identified archaeal and bacterial proteins belong to the SSO1653 subfamily and rapA group. Conversely, the SSO1653 subfamily and rapA group are likely to be specific to microbial organisms because the only two members of these families identified in eukaryotes (Supplementary Table S1A) appear to be false positives (data not shown). Over two-thirds of complete microbial genomes contain members of the SSO1653 subfamily and/or rapA group. This broad yet incomplete distribution suggests they perform non-essential functions that are sufficiently advantageous to maintain their prevalence.

Although rapA group proteins are distinguished by the lack of several features characteristic of eukaryotic Snf2 family members (see above), the SSO1653 subfamily carries all the Snf2 family sequence and structural hallmarks (Supplementary Figure S4). SSO1653 subfamily members are present in both bacteria and archaea, but they are not ubiquitous in archaeal genomes despite the presence of transcription, replication and repair mechanisms with significant similarity to those of eukaryotes (54,55). There is also no obvious linkage between the presence of histone-like proteins and SSO1653 subfamily members in archaeal genomes (Supplementary Table S1B). Furthermore, the SSO1653 subfamily falls in a grouping (Figure 1C) with the eukaryotic ERCC6 and Mot1 subfamilies whose biochemical role appears not to involve chromatin directly. In contrast to the limited archaeal and bacterial distribution of Snf2 family proteins, all eukaryote genomes contain multiple Snf2 family proteins. The early branching Giardia lamblia and the minimal Encephalozooan cuniculi genomes both encode six different Snf2 family genes falling into subfamilies represented across eukarya (Supplementary Table S1A), several of which have clear linkage to chromatin transactions. It is therefore possible that the microbial SSO1653 subfamily represents an ancestral Snf2-like form from which the eukaryotic subfamilies radiated. Such expansion of the Snf2 family early in eukaryote evolution (20) could have been coincident with the development of high-density nucleosomal packaging (56).

Distribution of Snf2 family members in complete genomes
The linkage between the primary sequence-based definitions of the subfamilies and distinct biological function is strongly supported by the presence of one or more subfamily members in each eukaryotic genome across large evolutionary ranges (Table 2 and Supplementary Table S1A). For example, a common set of subfamilies are found in almost all fungi, plant and animal genomes comprising Snf2, Iswi, Chd1, Swr1, Etl1, Mot1, Ino80, Rad5/16, ERCC6, Rad54 and SHPRH. Increased genomic complexity is also paralleled by increasing numbers of subfamilies and members: E.cuniculi with a genome encoding some 2000 gene products has 6 Snf2 family members from 6 subfamilies, whereas the S.cerevisiae genome encoding some 6000 genes has 17 Snf2 family members from 13 subfamilies, and the human genome encoding some 25 000 genes has 32 Snf2 family genes from 20 subfamilies (Table 2, part B).

The functional linkage across large evolutionary ranges suggests that each subfamily may have distinctive properties of their ATPase motors tuned to their function. This is supported by recent biochemical results demonstrating that helicase-like regions can be swapped within but not between subfamilies (57). However, a counterpoint is that functional redundancy can occur between subfamilies. For example, synthetic deletion of all three of the S.cerevisiae ISW1, ISW2 and CHD1 genes together is required to generate a strong phenotype (58,59). Redundancy also provides an explanation why some genomes lack certain members: the small genome of Schizosaccharomyces pombe lacks an Iswi subfamily member but maintains two Chd1 subfamily members. In addition to the 11 subfamilies represented broadly across eukaryotes are a number of others restricted to specific taxonomic ranges. For example, CHD7 members are found almost exclusively in animals, and ATRX members are found only in animals and plants.

Subfamily-specific properties
A number of specific features contribute to the distinction between subfamilies. First, the spacing between motifs III and IV is extended significantly beyond the minimal ~160 residues for a number of subfamilies (Table 4). For the Rad5/16, Ris1 and SHPRH subfamilies, the additional sequences all include RING fingers, whereas for the Swr1 and EP400 subfamilies they comprise highly proline and serine/threonine-rich spans. Ino80 and ATRX subfamilies also contain large, novel and distinct spans. Remarkably, all these large extra insertions occur at the same location in the primary sequence, between conserved blocks C and K which we term the ‘major insertion site’ (Figure 3G and Supplementary Figure S7A). Even for the subfamilies without large insertions there is variation in the length of sequence in the major insertion site (Table 4). For example, the Zebrafish Rad54 structure contains some 25 more residues forming two additional small alpha helices compared to the Sulfolobus solfataricus SSO1653 structure. When Snf2 family members from different subfamilies are aligned, the variability of the major insertion region strongly disturbs the alignment such that a contiguous pattern becomes difficult to define. This has led to some of the Snf2 family proteins being described as having ‘split’ helicase-like ATPase regions. The discontinuity is also the cause of protein motif databases such as SMART and Pfam defining Snf2 family members as matching a bipartite combination of SNF2_N and Helicase_C profiles (Figure 3G). The C-terminal end of the SNF2_N profile corresponds to conserved block C.


View this table:
[in this window]
[in a new window]
  		Table 4 Spacings between helicase motifs and major conserved blocks by subfamily

 
Second, subfamilies have characteristic small insertions at other sites (Table 4). Two such sites, also in the motif III–IV region, are located between conserved blocks H and B and between J and C (Figure 2). These are likely to influence the length of the long alpha helical protrusions 1 and 2, respectively (see below, Figure 3C), and there is a difference of some 40 residues between the shortest and longest subfamily lengths for each (Table 4). A ‘minor insertion site’ located between motifs I and Ia on the back of recA-like domain 1 is also occupied by recognizable domains in a few subfamilies from the Rad5/16-like grouping such as SHPRH (Supplementary Figure S3B). A number of other small insertions map to loops between various secondary structural elements (data not shown).

Third, although adhering to a general Snf2 family-specific pattern, individual subfamilies show characteristic patterns in the helicase motifs and in other conserved blocks (Supplementary Figure S4). For example, the well-known helicase motif II with typical DEAH pattern favours DEGH in the Snf2, Mot1 and Rad54 subfamilies, DEAQ in the Swr1, EP400, Ino80 and SSO1653 subfamilies or DESH in the SMARCAL1 subfamily. Likewise, for the typical conserved block E—motif I combined pattern ILADEMGLGKT all ATRX subfamily members have histidine instead of aspartate (i.e. ILAHEMGLGKT) and most Mot1 subfamily members have cysteine replacing alanine (i.e. ILCDEMGLGKT). It is also possible to identify other residues correlating with groups of subfamilies. For example, members of the Snf2, Iswi, Chd1, Mi-2, CHD7, ALC1, Rad54, ATRX and Arip4 subfamilies have an arginine immediately following the motif II DEAH. In the zebrafish Rad54 structure this residue R294 interacts with the sulphate which is suggested to mimic the ATP gamma phosphate.

Conserved blocks encode the unique structural features of the Snf2 family
Two structural determinations of the helicase-like regions of Snf2 family members have been presented recently: zebrafish Rad54 (pdb code 1Z3I) (47) and S.solfataricus SSO1653 (pdb codes 1Z6A, 1Z63, 1Z5Z) (46). As expected for members of the Snf2 family, the fold of each core recA-like domain in the Rad54 and SSO1653 structures is substantially similar and related to those of other known SF1 and SF2 helicases. In the zebrafish Rad54 structure the two recA-like domains are oriented equivalently to those of other known helicase structures (Figure 3A and B), whereas in the S.solfataricus SSO1653 structures recA-like domain 2 is flipped by 180° to an arrangement never previously observed for a helicase (Supplementary Figure S7B). This unusual orientation in SSO1653 is observed for both the DNA free and DNA-bound forms (46).

The most striking feature of the Snf2 family structures is the presence of several additional structural elements grafted onto the core helicase structure. These comprise antiparallel alpha helical protrusions from both recA-like domains 1 and 2 (Figure 3C), a structured linker between the recA-like domains (Figure 3D), the major insertion region at the back side of the domain 2 alpha helical protrusion (Figure 3E) and a triangular brace packed against the domain 2 alpha helical protrusion (Figure 3F). The two alpha-helical protrusions and linker are all encoded within the enlarged span between motifs III and IV. The triangular brace is encoded immediately downstream of motif VI.

Remarkably, the primary sequence features of the Snf2 family correspond directly to the additional structural elements (Figure 3G). First, the bases of the protrusions from recA-like domains 1 and 2 are both fixed by conserved blocks. For protrusion 1, this involves conserved block H composed of a repeating pattern of aromatic residues, with additional involvement of aromatics from conserved block A. For protrusion 2 this involves the arrangement of conserved blocks C, J and K. Second, the protrusions themselves are relatively conserved in sequence and length within subfamilies but not across the whole Snf2 family. Although there is no obvious correlation between the lengths of the protrusions 1 and 2, the distribution of protrusion lengths adheres to multiples of the alpha helical repeat (Supplementary Figure S8), suggesting that protrusions retain structure while varying in extension. Third, the Q motif structure found in many SF2 proteins utilizes a different arrangement of residues to DEAD box helicases such as eIF4A, where an aromatic residue orients the adenine base ring for contacts with a downstream glutamine (4) (Figures 3B). In the Snf2 family, the aromatic residue is contributed by conserved block F downstream of the glutamine. The Q motif affects ATP hydrolysis in DEAD box helicases and mutation of the core glutamine in yeast Snf2 subfamily member Sth1p causes slow growth (4). Fourth, the linker connecting protrusions 1 and 2 contains highly conserved dual arginines in conserved block B. Their central location between the ATP-associating and DNA-associating structural elements suggests that they may play an important role in the mechanism of Snf2 family enzymes. Consistent with this, mutation of the second arginine of the pair in Snf2p leads to effectively complete loss of function of the protein in vivo (48). Finally, the brace is composed of a principal alpha helix anchored by conserved block M into the junction at the base of protrusion 2 composed of conserved blocks C, J and K.

The major insertion region is immediately behind protrusion 2, almost diametrically opposite the ATP-binding site in the zebrafish Rad54 structure (Figure 3E). The nearest residues of the major insertion region in Rad54 are some 15 Å from DNA phosphates for docked DNA (Supplementary Figure S7A). However, an appropriately oriented alpha helix of some 20 residues would be sufficient to reach into the major groove, so large insertions at the major insertion site could potentially interact with DNA or other DNA-binding proteins bound in the groove. In the flipped conformation of domain 2 observed in the SSO1653 structure, the major insertion region is juxtaposed immediately adjacent to the DNA such that two non-conserved arginines from the major insertion region make direct DNA phosphate contacts.

As the distinctive structural features are defined by unique and highly conserved blocks, they are likely to confer properties to the ATPase motor that adapts the action of the core recA-like domains for a unique mechanism. We anticipate that while some features of the Snf2 family mechanism will be common to SF2 translocases, other aspects will be distinctive. Knowledge of the conserved residues and their structural location provides important information for understanding these distinctions.

Other levels of Snf2 family identity
We have demonstrated that the common helicase-like region is sufficient to enable classification of Snf2 family members. However, almost all Snf2 family polypeptides contain significant additional sequences likely to harbour accessory domains. For some subfamilies there is good correlation with the presence of particular accessory domain combinations (Supplementary Table S9). For example, almost all Snf2 subfamily members contain a bromodomain, ISWI members contain a SANT domain, and Chd1, Mi-2 and CHD7 members contain a chromodomain. However, many domain profiles in resources used for domain analysis have unidentified function or are unreliable in the context of Snf2 proteins. For example, Pfam lacks a SANT-specific profile and detects <10% of SANT domains with a more generic general ‘Myb_DNA-binding’ profile. We are currently undertaking further analysis to improve the relevant profiles and analyse the linkage of Snf2 family accessory domains in detail.

Finally, many Snf2 family proteins are part of larger multi-protein complexes. Accessory motifs within these complexes are also likely to adapt the function of Snf2 motors for different purposes.


   SUPPLEMENTARY DATA
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUPPLEMENTARY DATA
REFERENCES
 
Supplementary Data are available at NAR Online.


   ACKNOWLEDGEMENTS
 
We gratefully acknowledge Chris Stockdale, Charlie Bond and Helder Ferreira for comments on this manuscript and Diego Miranda-Saavedra and Jim Procter for helpful discussions regarding the analyses. We are also indebted to Andrew Waterhouse for providing essential enhancements to Jalview, and to Jonathan Monk for excellent systems support. We also thank Prof. U. Baumann for coordinates of eIF4A with ADP, Dr Kathleen Sandman and Prof. John Reeve for providing a table of histone-like proteins in archaeal genomes, and Dr Malcolm White for communicating unpublished observations about the SSO1653 protein. AF and TOH are funded by a Wellcome Trust Senior Research Fellowship in Basic Biomedical Science to TOH. Funding to pay the Open Access publication charges for this article was provided by a Wellcome Trust VIP award to the School of Life Sciences in Dundee.

Conflict of interest statement. None declared.


   Footnotes
 
Present address: Andrew Flaus, Department of Biochemistry, National University of Ireland Galway, Ireland


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUPPLEMENTARY DATA
 REFERENCES
 

  1. Gorbalenya, A.E. and Koonin, E.V. (1993) Helicases: amino acid sequence comparisons and structure–function relationship Curr. Opin. Struct. Biol, . 3, 419–429[CrossRef][Web of Science] .

  2. Gorbalenya, A.E., Koonin, E.V., Donchenko, A.P., Blinov, V.M. (1988) A novel superfamily of nucleoside triphosphate-binding motif containing proteins which are probably involved in duplex unwinding in DNA and RNA replication and recombination FEBS Lett, . 235, 16–24[CrossRef][Web of Science][Medline] .

  3. Pause, A. and Sonenberg, N. (1992) Mutational analysis of a DEAD box RNA helicase: the mammalian translation initiation factor eIF-4A EMBO J, . 11, 2643–2654[Web of Science][Medline] .

  4. Tanner, N.K., Cordin, O., Banroques, J., Doere, M., Linder, P. (2003) The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis Mol. Cell, 11, 127–138[CrossRef][Web of Science][Medline] .

  5. Subramanya, H.S., Bird, L.E., Brannigan, J.A., Wigley, D.B. (1996) Crystal structure of a DExx box DNA helicase Nature, 384, 379–383[CrossRef][Medline] .

  6. Singleton, M.R. and Wigley, D.B. (2002) Modularity and specialization in superfamily 1 and 2 helicases J. Bacteriol, . 184, 1819–1826[Free Full Text] .

  7. Ye, J., Osborne, A.R., Groll, M., Rapoport, T.A. (2004) RecA-like motor ATPases—lessons from structures Biochim. Biophys. Acta, 1659, 1–18[Medline] .

  8. Becker, P.B. and Horz, W. (2002) ATP-dependent nucleosome remodeling Annu. Rev. Biochem, . 71, 247–273[CrossRef][Web of Science][Medline] .

  9. Saha, A., Wittmeyer, J., Cairns, B.R. (2002) Chromatin remodeling by RSC involves ATP-dependent DNA translocation Genes Dev, . 16, 2120–2134[Abstract/Free Full Text] .

  10. Whitehouse, I., Stockdale, C., Flaus, A., Szczelkun, M.D., Owen-Hughes, T. (2003) Evidence for DNA translocation by the ISWI chromatin-remodeling enzyme Mol. Cell. Biol, . 23, 1935–1945[Abstract/Free Full Text] .

  11. Jaskelioff, M., Van Komen, S., Krebs, J.E., Sung, P., Peterson, C.L. (2003) Rad54p is a chromatin remodeling enzyme required for heteroduplex DNA joint formation with chromatin J. Biol. Chem, . 278, 9212–9218[Abstract/Free Full Text] .

  12. Xue, Y., Gibbons, R., Yan, Z., Yang, D., McDowell, T.L., Sechi, S., Qin, J., Zhou, S., Higgs, D., Wang, W. (2003) The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies Proc. Natl Acad. Sci. USA, 100, 10635–10640[Abstract/Free Full Text] .

  13. Van Komen, S., Petukhova, G., Sigurdsson, S., Stratton, S., Sung, P. (2000) Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54 Mol. Cell, 6, 563–572[CrossRef][Web of Science][Medline] .

  14. Havas, K., Flaus, A., Phelan, M., Kingston, R., Wade, P.A., Lilley, D.M., Owen-Hughes, T. (2000) Generation of superhelical torsion by ATP-dependent chromatin remodeling activities Cell, 103, 1133–1142[CrossRef][Web of Science][Medline] .

  15. Liu, R., Liu, H., Chen, X., Kirby, M., Brown, P.O., Zhao, K. (2001) Regulation of CSF1 promoter by the SWI/SNF-like BAF complex Cell, 106, 309–318[CrossRef][Web of Science][Medline] .

  16. Rouleau, N., Domans'kyi, A., Reeben, M., Moilanen, A.M., Havas, K., Kang, Z., Owen-Hughes, T., Palvimo, J.J., Janne, O.A. (2002) Novel ATPase of SNF2-like protein family interacts with androgen receptor and modulates androgen-dependent transcription Mol. Biol. Cell, 13, 2106–2119[Abstract/Free Full Text] .

  17. Yu, S., Owen-Hughes, T., Friedberg, E.C., Waters, R., Reed, S.H. (2004) The yeast Rad7/Rad16/Abf1 complex generates superhelical torsion in DNA that is required for nucleotide excision repair DNA Repair (Amst), 3, 277–287[CrossRef][Medline] .

  18. Lia, G., Praly, E., Ferreira, H., Stockdale, C., Tse-Dinh, Y.C., Dunlap, D., Croquette, V., Bensimon, D., Owen-Hughes, T. (2006) Direct observation of DNA distortion by the RSC chromatin remodeling complex Mol. Cell, 21, 417–425[CrossRef][Web of Science][Medline] .

  19. Auble, D.T., Hansen, K.E., Mueller, C.G., Lane, W.S., Thorner, J., Hahn, S. (1994) Mot1, a global repressor of RNA polymerase II transcription, inhibits TBP binding to DNA by an ATP-dependent mechanism Genes Dev, . 8, 1920–1934[Abstract/Free Full Text] .

  20. Eisen, J.A., Sweder, K.S., Hanawalt, P.C. (1995) Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions Nucleic Acids Res, . 23, 2715–2723[Abstract/Free Full Text] .

  21. Lindback, T. and Kolsto, A.B. (1997) A Bacillus cereus member of the SNF2 family Microbiology, 143, 171–174[Abstract/Free Full Text] .

  22. Coleman, M.A., Eisen, J.A., Mohrenweiser, H.W. (2000) Cloning and characterization of HARP/SMARCAL1: a prokaryotic HepA-related SNF2 helicase protein from human and mouse Genomics, 65, 274–282[CrossRef][Web of Science][Medline] .

  23. Linder, B., Cabot, R.A., Schwickert, T., Rupp, R.A. (2004) The SNF2 domain protein family in higher vertebrates displays dynamic expression patterns in Xenopus laevis embryos Gene, 326, 59–66[CrossRef][Web of Science][Medline] .

  24. Bakshi, R., Prakash, T., Dash, D., Brahmachari, V. (2004) In silico characterization of the INO80 subfamily of SWI2/SNF2 chromatin remodeling proteins Biochem. Biophys. Res. Commun, . 320, 197–204[CrossRef][Web of Science][Medline] .

  25. Boeckmann, B., Bairoch, A., Apweiler, R., Blatter, M.C., Estreicher, A., Gasteiger, E., Martin, M.J., Michoud, K., O'Donovan, C., Phan, I., et al. (2003) The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003 Nucleic Acids Res, . 31, 365–370[Abstract/Free Full Text] .

  26. Bairoch, A., Apweiler, R., Wu, C.H., Barker, W.C., Boeckmann, B., Ferro, S., Gasteiger, E., Huang, H., Lopez, R., Magrane, M., et al. (2005) The Universal Protein Resource (UniProt) Nucleic Acids Res, . 33, D154–D159[Abstract/Free Full Text] .

  27. Rice, P., Longden, I., Bleasby, A. (2000) EMBOSS: the European Molecular Biology Open Software Suite Trends Genet, . 16, 276–277[CrossRef][Web of Science][Medline] .

  28. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res, . 32, 1792–1797[Abstract/Free Full Text] .

  29. Katoh, K., Kuma, K., Toh, H., Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment Nucleic Acids Res, . 33, 511–518[Abstract/Free Full Text] .

  30. Clamp, M., Cuff, J., Searle, S.M., Barton, G.J. (2004) The Jalview Java alignment editor Bioinformatics, 20, 426–427[Abstract/Free Full Text] .

  31. Felsenstein, J. (1989) PHYLIP—Phylogeny Inference Package (Version 3.2) Cladistics, 5, 164–166 .

  32. Zmasek, C.M. and Eddy, S.R. (2001) ATV: display and manipulation of annotated phylogenetic trees Bioinformatics, 17, 383–384[Abstract/Free Full Text] .

  33. Bingham, J. and Sudarsanam, S. (2000) Visualizing large hierarchical clusters in hyperbolic space Bioinformatics, 16, 660–661[Abstract/Free Full Text] .

  34. Eddy, S.R. (1998) Profile hidden Markov models Bioinformatics, 14, 755–763[Abstract/Free Full Text] .

  35. Madera, M. (2005) Hidden Markov models for detection of remote homology Cambridge University PhD thesis .

  36. Crooks, G.E., Hon, G., Chandonia, J.M., Brenner, S.E. (2004) WebLogo: a sequence logo generator Genome Res, . 14, 1188–1190[Abstract/Free Full Text] .

  37. Schuster-Bockler, B. and Bateman, A. (2005) Visualizing profile–profile alignment: pairwise HMM logos Bioinformatics, 21, 2912–2913[Abstract/Free Full Text] .

  38. DeLano, W.L. The PyMOL User's Manual, (2002) San Carlos, CA DeLano Scientific .

  39. Miki, H., Okada, Y., Hirokawa, N. (2005) Analysis of the kinesin superfamily: insights into structure and function Trends Cell Biol, . 15, 467–476[CrossRef][Web of Science][Medline] .

  40. Hodge, T. and Cope, M.J. (2000) A myosin family tree J. Cell Sci, . 113, 3353–3354[Free Full Text] .

  41. Mizuguchi, G., Shen, X., Landry, J., Wu, W.H., Sen, S., Wu, C. (2004) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex Science, 303, 343–348[Abstract/Free Full Text] .

  42. Kobor, M.S., Venkatasubrahmanyam, S., Meneghini, M.D., Gin, J.W., Jennings, J.L., Link, A.J., Madhani, H.D., Rine, J. (2004) A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin PLoS Biol, . 2, E131[CrossRef][Medline] .

  43. Krogan, N.J., Keogh, M.C., Datta, N., Sawa, C., Ryan, O.W., Ding, H., Haw, R.A., Pootoolal, J., Tong, A., Canadien, V., et al. (2003) A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1 Mol. Cell, 12, 1565–1576[CrossRef][Web of Science][Medline] .

  44. Flaus, A. and Owen-Hughes, T. (2001) Mechanisms for ATP-dependent chromatin remodelling Curr. Opin. Genet. Dev, . 11, 148–154[CrossRef][Web of Science][Medline] .

  45. Bork, P. and Koonin, E.V. (1993) An expanding family of helicases within the ‘DEAD/H’ superfamily Nucleic Acids Res, . 21, 751–752[Free Full Text] .

  46. Durr, H., Korner, C., Muller, M., Hickmann, V., Hopfner, K.P. (2005) X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA Cell, 121, 363–373[CrossRef][Web of Science][Medline] .

  47. Thoma, N.H., Czyzewski, B.K., Alexeev, A.A., Mazin, A.V., Kowalczykowski, S.C., Pavletich, N.P. (2005) Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54 Nature Struct. Mol. Biol, . 12, 350–356[CrossRef] .

  48. Richmond, E. and Peterson, C.L. (1996) Functional analysis of the DNA-stimulated ATPase domain of yeast SWI2/SNF2 Nucleic Acids Res, . 24, 3685–3692[Abstract/Free Full Text] .

  49. Henikoff, S. (1993) Transcriptional activator components and poxvirus DNA-dependent ATPases comprise a single family Trends Biochem. Sci, . 18, 291–292[CrossRef][Web of Science][Medline] .

  50. Meetei, A.R., Medhurst, A.L., Ling, C., Xue, Y., Singh, T.R., Bier, P., Steltenpool, J., Stone, S., Dokal, I., Mathew, C.G., et al. (2005) A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M Nature Genet, . 37, 958–963[CrossRef][Web of Science][Medline] .

  51. Mosedale, G., Niedzwiedz, W., Alpi, A., Perrina, F., Pereira-Leal, J.B., Johnson, M., Langevin, F., Pace, P., Patel, K.J. (2005) The vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway Nature Struct. Mol. Biol, . 12, 763–771[CrossRef] .

  52. Prakash, R., Krejci, L., Van Komen, S., Anke Schurer, K., Kramer, W., Sung, P. (2005) Saccharomyces cerevisiae MPH1 gene, required for homologous recombination-mediated mutation avoidance, encodes a 3' to 5' DNA helicase J. Biol. Chem, . 280, 7854–7860[Abstract/Free Full Text] .

  53. Nishino, T., Komori, K., Tsuchiya, D., Ishino, Y., Morikawa, K. (2005) Crystal structure and functional implications of Pyrococcus furiosus hef helicase domain involved in branched DNA processing Structure, 13, 143–153[Medline] .

  54. Bartlett, M.S. (2005) Determinants of transcription initiation by archaeal RNA polymerase Curr. Opin. Microbiol, . 8, 677–684[Web of Science][Medline] .

  55. Kelman, Z. and White, M.F. (2005) Archaeal DNA replication and repair Curr. Opin. Microbiol, . 8, 669–676[Web of Science][Medline] .

  56. Minsky, A., Ghirlando, R., Reich, Z. (1997) Nucleosomes: a solution to a crowded intracellular environment? J. Theoret. Biol, . 188, 379–385[CrossRef][Web of Science][Medline] .

  57. Fan, H.Y., Trotter, K.W., Archer, T.K., Kingston, R.E. (2005) Swapping function of two chromatin remodeling complexes Mol. Cell, 17, 805–815[CrossRef][Web of Science][Medline] .

  58. Alen, C., Kent, N.A., Jones, H.S., O'Sullivan, J., Aranda, A., Proudfoot, N.J. (2002) A role for chromatin remodeling in transcriptional termination by RNA polymerase II Mol. Cell, 10, 1441–1452[CrossRef][Web of Science][Medline] .

  59. Tsukiyama, T., Palmer, J., Landel, C.C., Shiloach, J., Wu, C. (1999) Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae Genes Dev, . 13, 686–697[Abstract/Free Full Text] .

  60. Laurent, B.C., Yang, X., Carlson, M. (1992) An essential Saccharomyces cerevisiae gene homologous to SNF2 encodes a helicase-related protein in a new family Mol. Cell. Biol, . 12, 1893–1902[Abstract/Free Full Text] .

  61. Cairns, B.R., Lorch, Y., Li, Y., Zhang, M., Lacomis, L., Erdjument-Bromage, H., Tempst, P., Du, J., Laurent, B., Kornberg, R.D. (1996) RSC, an essential, abundant chromatin-remodeling complex Cell, 87, 1249–1260[CrossRef][Web of Science][Medline] .

  62. Tamkun, J.W., Deuring, R., Scott, M.P., Kissinger, M., Pattatucci, A.M., Kaufman, T.C., Kennison, J.A. (1992) brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2 Cell, 68, 561–572[CrossRef][Web of Science][Medline] .

  63. Muchardt, C. and Yaniv, M. (1993) A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor EMBO J, . 12, 4279–4290[Web of Science][Medline] .

  64. Khavari, P.A., Peterson, C.L., Tamkun, J.W., Mendel, D.B., Crabtree, G.R. (1993) BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription Nature, 366, 170–174[CrossRef][Medline] .

  65. Whitehouse, I., Flaus, A., Cairns, B.R., White, M.F., Workman, J.L., Owen-Hughes, T. (1999) Nucleosome mobilization catalysed by the yeast SWI/SNF complex Nature, 400, 784–787[CrossRef][Medline] .

  66. Kassabov, S.R., Zhang, B., Persinger, J., Bartholomew, B. (2003) SWI/SNF unwraps, slides, and rewraps the nucleosome Mol. Cell, 11, 391–403[CrossRef][Web of Science][Medline] .

  67. Narlikar, G.J., Phelan, M.L., Kingston, R.E. (2001) Generation and interconversion of multiple distinct nucleosomal states as a mechanism for catalyzing chromatin fluidity Mol. Cell, 8, 1219–1230[CrossRef][Web of Science][Medline] .

  68. Lorch, Y., Zhang, M., Kornberg, R.D. (1999) Histone octamer transfer by a chromatin-remodeling complex Cell, 96, 389–392[CrossRef][Web of Science][Medline] .

  69. Bruno, M., Flaus, A., Stockdale, C., Rencurel, C., Ferreira, H., Owen-Hughes, T. (2003) Histone H2A/H2B dimer exchange by ATP-dependent chromatin remodeling activities Mol. Cell, 12, 1599–1606[CrossRef][Web of Science][Medline] .

  70. Xue, Y., Canman, J.C., Lee, C.S., Nie, Z., Yang, D., Moreno, G.T., Young, M.K., Salmon, E.D., Wang, W. (2000) The human SWI/SNF-B chromatin-remodeling complex is related to yeast rsc and localizes at kinetochores of mitotic chromosomes Proc. Natl Acad. Sci. USA, 97, 13015–13020[Abstract/Free Full Text] .

  71. Sif, S., Saurin, A.J., Imbalzano, A.N., Kingston, R.E. (2001) Purification and characterization of mSin3A-containing Brg1 and hBrm chromatin remodeling complexes Genes Dev, . 15, 603–618[Abstract/Free Full Text] .

  72. Harikrishnan, K.N., Chow, M.Z., Baker, E.K., Pal, S., Bassal, S., Brasacchio, D., Wang, L., Craig, J.M., Jones, P.L., Sif, S., et al. (2005) Brahma links the SWI/SNF chromatin-remodeling complex with MeCP2-dependent transcriptional silencing Nature Genet, . 37, 254–264[CrossRef][Web of Science][Medline] .

  73. Xu, W., Cho, H., Kadam, S., Banayo, E.M., Anderson, S., Yates, J.R., III, Emerson, B.M., Evans, R.M. (2004) A methylation-mediator complex in hormone signaling Genes Dev, . 18, 144–156[Abstract/Free Full Text] .

  74. Dunaief, J.L., Strober, B.E., Guha, S., Khavari, P.A., Alin, K., Luban, J., Begemann, M., Crabtree, G.R., Goff, S.P. (1994) The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest Cell, 79, 119–130[CrossRef][Web of Science][Medline] .

  75. Zhang, H.S., Gavin, M., Dahiya, A., Postigo, A.A., Ma, D., Luo, R.X., Harbour, J.W., Dean, D.C. (2000) Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF Cell, 101, 79–89[CrossRef][Web of Science][Medline] .

  76. Moshkin, Y.M., Armstrong, J.A., Maeda, R.K., Tamkun, J.W., Verrijzer, P., Kennison, J.A., Karch, F. (2002) Histone chaperone ASF1 cooperates with the Brahma chromatin-remodelling machinery Genes Dev, . 16, 2621–2626[Abstract/Free Full Text] .

  77. Wilson, C.J., Chao, D.M., Imbalzano, A.N., Schnitzler, G.R., Kingston, R.E., Young, R.A. (1996) RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling Cell, 84, 235–244[CrossRef][Web of Science][Medline] .

  78. Metivier, R., Penot, G., Hubner, M.R., Reid, G., Brand, H., Kos, M., Gannon, F. (2003) Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter Cell, 115, 751–763[CrossRef][Web of Science][Medline] .

  79. Huang, J., Hsu, J.M., Laurent, B.C. (2004) The RSC nucleosome-remodeling complex is required for Cohesin's association with chromosome arms Mol. Cell, 13, 739–750[CrossRef][Web of Science][Medline] .

  80. Peterson, C.L. and Workman, J.L. (2000) Promoter targeting and chromatin remodeling by the SWI/SNF complex Curr. Opin. Genet. Dev, . 10, 187–192[CrossRef][Web of Science][Medline] .

  81. Hassan, A.H., Neely, K.E., Workman, J.L. (2001) Histone acetyltransferase complexes stabilize swi/snf binding to promoter nucleosomes Cell, 104, 817–827[CrossRef][Web of Science][Medline] .

  82. Agalioti, T., Chen, G., Thanos, D. (2002) Deciphering the transcriptional histone acetylation code for a human gene Cell, 111, 381–392[CrossRef][Web of Science][Medline] .

  83. Elfring, L.K., Deuring, R., McCallum, C.M., Peterson, C.L., Tamkun, J.W. (1994) Identification and characterization of Drosophila relatives of the yeast transcriptional activator SNF2/SWI2 Mol. Cell. Biol, . 14, 2225–2234[Abstract/Free Full Text] .

  84. Tsukiyama, T., Daniel, C., Tamkun, J., Wu, C. (1995) ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor Cell, 83, 1021–1026[CrossRef][Web of Science][Medline] .

  85. Ito, T., Bulger, M., Pazin, M.J., Kobayashi, R., Kadonaga, J.T. (1997) ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor Cell, 90, 145–155[CrossRef][Web of Science][Medline] .

  86. Varga-Weisz, P.D., Wilm, M., Bonte, E., Dumas, K., Mann, M., Becker, P.B. (1997) Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II Nature, 388, 598–602[CrossRef][Medline] .

  87. Hamiche, A., Kang, J.G., Dennis, C., Xiao, H., Wu, C. (2001) Histone tails modulate nucleosome mobility and regulate ATP-dependent nucleosome sliding by NURF Proc. Natl Acad. Sci. USA, 98, 14316–14321[Abstract/Free Full Text] .

  88. Clapier, C.R., Nightingale, K.P., Becker, P.B. (2002) A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI Nucleic Acids Res, . 30, 649–655[Abstract/Free Full Text] .

  89. Fazzio, T.G., Gelbart, M.E., Tsukiyama, T. (2005) Two distinct mechanisms of chromatin interaction by the Isw2 chromatin remodeling complex in vivo Mol. Cell. Biol, . 25, 9165–9174[Abstract/Free Full Text] .

  90. Dirscherl, S.S. and Krebs, J.E. (2004) Functional diversity of ISWI complexes Biochem. Cell Biol, . 82, 482–489[CrossRef][Web of Science][Medline] .

  91. Eberharter, A. and Becker, P.B. (2004) ATP-dependent nucleosome remodelling: factors and functions J. Cell Sci, . 117, 3707–3711[Free Full Text] .

  92. Tsukiyama, T. (2002) The in vivo functions of ATP-dependent chromatin-remodelling factors Nature Rev. Mol. Cell Biol, . 3, 422–429[CrossRef][Web of Science][Medline] .

  93. Poot, R.A., Bozhenok, L., van den Berg, D.L., Hawkes, N., Varga-Weisz, P.D. (2005) Chromatin remodeling by WSTF-ISWI at the replication site: opening a window of opportunity for epigenetic inheritance? Cell Cycle, 4, 543–546[Web of Science][Medline] .

  94. Jarvis, C.D., Geiman, T., Vila-Storm, M.P., Osipovich, O., Akella, U., Candeias, S., Nathan, I., Durum, S.K., Muegge, K. (1996) A novel putative helicase produced in early murine lymphocytes Gene, 169, 203–207[CrossRef][Web of Science][Medline] .

  95. Sun, L.Q. and Arceci, R.J. (2005) Altered epigenetic patterning leading to replicative senescence and reduced longevity. A role of a novel SNF2 factor, PASG Cell Cycle, 4, 3–5[Web of Science][Medline] .

  96. Vongs, A., Kakutani, T., Martienssen, R.A., Richards, E.J. (1993) Arabidopsis thaliana DNA methylation mutants Science, 260, 1926–1928[Abstract/Free Full Text] .

  97. Dennis, K., Fan, T., Geiman, T., Yan, Q., Muegge, K. (2001) Lsh, a member of the SNF2 family, is required for genome-wide methylation Genes Dev, . 15, 2940–2944[Abstract/Free Full Text] .

  98. Muegge, K. (2005) Lsh, a guardian of heterochromatin at repeat elements Biochem. Cell Biol, . 83, 548–554[CrossRef][Web of Science][Medline] .

  99. Brzeski, J. and Jerzmanowski, A. (2003) Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors J. Biol. Chem, . 278, 823–828[Abstract/Free Full Text] .

  100. Guan, X.Y., Fang, Y., Sham, J.S., Kwong, D.L., Zhang, Y., Liang, Q., Li, H., Zhou, H., Trent, J.M. (2000) Recurrent chromosome alterations in hepatocellular carcinoma detected by comparative genomic hybridization Genes Chromosomes Cancer, 29, 110–116[CrossRef][Web of Science][Medline] .

  101. Mao, M., Fu, G., Wu, J.S., Zhang, Q.H., Zhou, J., Kan, L.X., Huang, Q.H., He, K.L., Gu, B.W., Han, Z.G., et al. (1998) Identification of genes expressed in human CD34(+) hematopoietic stem/progenitor cells by expressed sequence tags and efficient full-length cDNA cloning Proc. Natl Acad. Sci. USA, 95, 8175–8180[Abstract/Free Full Text] .

  102. Yan, L., Echenique, V., Busso, C., SanMiguel, P., Ramakrishna, W., Bennetzen, J.L., Harrington, S., Dubcovsky, J. (2002) Cereal genes similar to Snf2 define a new subfamily that includes human and mouse genes Mol. Genet. Genomics, 268, 488–499[CrossRef][Web of Science][Medline] .

  103. Karras, G.I., Kustatscher, G., Buhecha, H.R., Allen, M.D., Pugieux, C., Sait, F., Bycroft, M., Ladurner, A.G. (2005) The macro domain is an ADP-ribose binding module EMBO J, . 24, 1911–1920[CrossRef][Web of Science][Medline] .

  104. Delmas, V., Stokes, D.G., Perry, R.P. (1993) A mammalian DNA-binding protein that contains a chromodomain and an SNF2/SWI2-like helicase domain Proc. Natl Acad. Sci. USA, 90, 2414–2418[Abstract/Free Full Text] .

  105. Brehm, A., Tufteland, K.R., Aasland, R., Becker, P.B. (2004) The many colours of chromodomains Bioessays, 26, 133–140[CrossRef][Web of Science][Medline] .

  106. Tajul-Arifin, K., Teasdale, R., Ravasi, T., Hume, D.A., Mattick, J.S. (2003) Identification and analysis of chromodomain-containing proteins encoded in the mouse transcriptome Genome Res, . 13, 1416–1429[Abstract/Free Full Text] .

  107. Woodage, T., Basrai, M.A., Baxevanis, A.D., Hieter, P., Collins, F.S. (1997) Characterization of the CHD family of proteins Proc. Natl Acad. Sci. USA, 94, 11472–11477[Abstract/Free Full Text] .

  108. Tran, H.G., Steger, D.J., Iyer, V.R., Johnson, A.D. (2000) The chromo domain protein chd1p from budding yeast is an ATP-dependent chromatin-modifying factor EMBO J, . 19, 2323–2331[CrossRef][Web of Science][Medline] .

  109. Lusser, A., Urwin, D.L., Kadonaga, J.T. (2005) Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly Nature Struct. Mol. Biol, . 12, 160–166[CrossRef] .

  110. Krogan, N.J., Kim, M., Ahn, S.H., Zhong, G., Kobor, M.S., Cagney, G., Emili, A., Shilatifard, A., Buratowski, S., Greenblatt, J.F. (2002) RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach Mol. Cell. Biol, . 22, 6979–6992[Abstract/Free Full Text] .

  111. Pray-Grant, M.G., Daniel, J.A., Schieltz, D., Yates, J.R., III, Grant, P.A. (2005) Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation Nature, 433, 434–438[CrossRef][Medline] .

  112. Krogan, N.J., Kim, M., Tong, A., Golshani, A., Cagney, G., Canadien, V., Richards, D.P., Beattie, B.K., Emili, A., Boone, C., et al. (2003) Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II Mol. Cell. Biol, . 23, 4207–4218[Abstract/Free Full Text] .

  113. Kelley, D.E., Stokes, D.G., Perry, R.P. (1999) CHD1 interacts with SSRP1 and depends on both its chromodomain and its ATPase/helicase-like domain for proper association with chromatin Chromosoma, 108, 10–25[CrossRef][Web of Science][Medline] .

  114. Walfridsson, J., Bjerling, P., Thalen, M., Yoo, E.J., Park, S.D., Ekwall, K. (2005) The CHD remodeling factor Hrp1 stimulates CENP-A loading to centromeres Nucleic Acids Res, . 33, 2868–2879[Abstract/Free Full Text] .

  115. Jae Yoo, E., Kyu Jang, Y., Ae Lee, M., Bjerling, P., Bum Kim, J., Ekwall, K., Hyun Seong, R., Dai Park, S. (2002) Hrp3, a chromodomain helicase/ATPase DNA binding protein, is required for heterochromatin silencing in fission yeast Biochem. Biophys. Res. Commun, . 295, 970–974[CrossRef][Web of Science][Medline] .

  116. Seelig, H.P., Moosbrugger, I., Ehrfeld, H., Fink, T., Renz, M., Genth, E. (1995) The major dermatomyositis-specific Mi-2 autoantigen is a presumed helicase involved in transcriptional activation Arthritis Rheum, . 38, 1389–1399[Web of Science][Medline] .

  117. Bowen, N.J., Fujita, N., Kajita, M., Wade, P.A. (2004) Mi-2/NuRD: multiple complexes for many purposes Biochim. Biophys. Acta, 1677, 52–57[Medline] .

  118. Bouazoune, K., Mitterweger, A., Langst, G., Imhof, A., Akhtar, A., Becker, P.B., Brehm, A. (2002) The dMi-2 chromodomains are DNA binding modules important for ATP-dependent nucleosome mobilization EMBO J, . 21, 2430–2440[CrossRef][Web of Science][Medline] .

  119. Schultz, D.C., Friedman, J.R., Rauscher, F.J., III. (2001) Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2alpha subunit of NuRD Genes Dev, . 15, 428–443[Abstract/Free Full Text] .

  120. Korenjak, M., Taylor-Harding, B., Binne, U.K., Satterlee, J.S., Stevaux, O., Aasland, R., White-Cooper, H., Dyson, N., Brehm, A. (2004) Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes Cell, 119, 181–193[CrossRef][Web of Science][Medline] .

  121. White, P.S., Thompson, P.M., Gotoh, T., Okawa, E.R., Igarashi, J., Kok, M., Winter, C., Gregory, S.G., Hogarty, M.D., Maris, J.M., et al. (2005) Definition and characterization of a region of 1p36.3 consistently deleted in neuroblastoma Oncogene, 24, 2684–2694[CrossRef][Web of Science][Medline] .

  122. Thompson, P.M., Gotoh, T., Kok, M., White, P.S., Brodeur, G.M. (2003) CHD5, a new member of the chromodomain gene family, is preferentially expressed in the nervous system Oncogene, 22, 1002–1011[CrossRef][Web of Science][Medline] .

  123. Ogas, J., Kaufmann, S., Henderson, J., Somerville, C. (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis Proc. Natl Acad. Sci. USA, 96, 13839–13844[Abstract/Free Full Text] .

  124. Vissers, L.E., van Ravenswaaij, C.M., Admiraal, R., Hurst, J.A., de Vries, B.B., Janssen, I.M., van der Vliet, W.A., Huys, E.H., de Jong, P.J., Hamel, B.C., et al. (2004) Mutations in a new member of the chromodomain gene family cause CHARGE syndrome Nature Genet, . 36, 955–957[CrossRef][Web of Science][Medline] .

  125. Jongmans, M., Admiraal, R., van der Donk, K., Vissers, L., Baas, A., Kapusta, L., van Hagen, A., Donnai, D., de Ravel, T., Veltman, J., et al. (2006) CHARGE syndrome: the phenotypic spectrum of mutations in the CHD7 gene J. Med. Genet, . 43, 306–314[Abstract/Free Full Text] .

  126. Schuster, E.F. and Stoger, R. (2002) CHD5 defines a new subfamily of chromodomain-SWI2/SNF2-like helicases Mamm. Genome, 13, 117–119[CrossRef][Web of Science][Medline] .

  127. Shur, I. and Benayahu, D. (2005) Characterization and functional analysis of CReMM, a novel chromodomain helicase DNA-binding protein J. Mol. Biol, . 352, 646–655[CrossRef][Web of Science][Medline] .

  128. Daubresse, G., Deuring, R., Moore, L., Papoulas, O., Zakrajsek, I., Waldrip, W.R., Scott, M.P., Kennison, J.A., Tamkun, J.W. (1999) The Drosophila kismet gene is related to chromatin-remodeling factors and is required for both segmentation and segment identity Development, 126, 1175–1187[Abstract] .

  129. Srinivasan, S., Armstrong, J.A., Deuring, R., Dahlsveen, I.K., McNeill, H., Tamkun, J.W. (2005) The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA Polymerase II Development, 132, 1623–1635[Abstract/Free Full Text] .

  130. Wu, W.H., Alami, S., Luk, E., Wu, C.H., Sen, S., Mizuguchi, G., Wei, D., Wu, C. (2005) Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange Nature Struct. Mol. Biol, . 12, 1064–1071[CrossRef] .

  131. Noh, Y.S. and Amasino, R.M. (2003) PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis Plant Cell, 15, 1671–1682[Abstract/Free Full Text] .

  132. He, Y. and Amasino, R.M. (2005) Role of chromatin modification in flowering-time control Trends Plant Sci, . 10, 30–35[CrossRef][Web of Science][Medline] .

  133. Ruhf, M.L., Braun, A., Papoulas, O., Tamkun, J.W., Randsholt, N., Meister, M. (2001) The domino gene of Drosophila encodes novel members of the SWI2/SNF2 family of DNA-dependent ATPases, which contribute to the silencing of homeotic genes Development, 128, 1429–1441[Abstract] .

  134. Doyon, Y. and Cote, J. (2004) The highly conserved and multifunctional NuA4 HAT complex Curr. Opin. Genet. Dev, . 14, 147–154[CrossRef][Web of Science][Medline] .

  135. Kusch, T., Florens, L., Macdonald, W.H., Swanson, S.K., Glaser, R.L., Yates, J.R., III, Abmayr, S.M., Washburn, M.P., Workman, J.L. (2004) Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions Science, 306, 2084–2087[Abstract/Free Full Text] .

  136. Johnston, H., Kneer, J., Chackalaparampil, I., Yaciuk, P., Chrivia, J. (1999) Identification of a novel SNF2/SWI2 protein family member, SRCAP, which interacts with CREB-binding protein J. Biol. Chem, . 274, 16370–16376[Abstract/Free Full Text] .

  137. Cai, Y., Jin, J., Florens, L., Swanson, S.K., Kusch, T., Li, B., Workman, J.L., Washburn, M.P., Conaway, R.C., Conaway, J.W. (2005) The mammalian YL1 protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes J. Biol. Chem, . 280, 13665–13670[Abstract/Free Full Text] .

  138. Monroy, M.A., Schott, N.M., Cox, L., Chen, J.D., Ruh, M., Chrivia, J.C. (2003) SNF2-related CBP activator protein (SRCAP) functions as a coactivator of steroid receptor-mediated transcription through synergistic interactions with CARM-1 and GRIP-1 Mol. Endocrinol, . 17, 2519–2528[Abstract/Free Full Text] .

  139. Eissenberg, J.C., Wong, M., Chrivia, J.C. (2005) Human SRCAP and Drosophila melanogaster DOM are homologs that function in the notch signaling pathway Mol. Cell. Biol, . 25, 6559–6569[Abstract/Free Full Text] .

  140. Samuelson, A.V., Narita, M., Chan, H.M., Jin, J., de Stanchina, E., McCurrach, M.E., Fuchs, M., Livingston, D.M., Lowe, S.W. (2005) p400 is required for E1A to promote apoptosis J. Biol. Chem, . 280, 21915–21923[Abstract/Free Full Text] .

  141. Chan, H.M., Narita, M., Lowe, S.W., Livingston, D.M. (2005) The p400 E1A-associated protein is a novel component of the p53 -> p21 senescence pathway Genes Dev, . 19, 196–201[Abstract/Free Full Text] .

  142. Fuchs, M., Gerber, J., Drapkin, R., Sif, S., Ikura, T., Ogryzko, V., Lane, W.S., Nakatani, Y., Livingston, D.M. (2001) The p400 complex is an essential E1A transformation target Cell, 106, 297–307[CrossRef][Web of Science][Medline] .

  143. Underhill, C., Qutob, M.S., Yee, S.P., Torchia, J. (2000) A novel nuclear receptor corepressor complex, N-CoR, contains components of the mammalian SWI/SNF complex and the corepressor KAP-1 J. Biol. Chem, . 275, 40463–40470[Abstract/Free Full Text] .

  144. Cai, Y., Jin, J., Tomomori-Sato, C., Sato, S., Sorokina, I., Parmely, T.J., Conaway, R.C., Conaway, J.W. (2003) Identification of new subunits of the multiprotein mammalian TRRAP/TIP60-containing histone acetyltransferase complex J. Biol. Chem, . 278, 42733–42736[Abstract/Free Full Text] .

  145. Doyon, Y., Selleck, W., Lane, W.S., Tan, S., Cote, J. (2004) Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans Mol. Cell. Biol, . 24, 1884–1896[Abstract/Free Full Text] .

  146. Bachhawat, N., Ouyang, Q., Henry, S.A. (1995) Functional characterization of an inositol-sensitive upstream activation sequence in yeast. A cis-regulatory element responsible for inositol-choline mediated regulation of phospholipid biosynthesis J. Biol. Chem, . 270, 25087–25095[Abstract/Free Full Text] .

  147. Ebbert, R., Birkmann, A., Schuller, H.J. (1999) The product of the SNF2/SWI2 paralogue INO80 of Saccharomyces cerevisiae required for efficient expression of various yeast structural genes is part of a high-molecular-weight protein complex Mol. Microbiol, . 32, 741–751[CrossRef][Web of Science][Medline] .

  148. Shen, X., Mizuguchi, G., Hamiche, A., Wu, C. (2000) A chromatin remodelling complex involved in transcription and DNA processing Nature, 406, 541–544[CrossRef][Medline] .

  149. Jin, J., Cai, Y., Yao, T., Gottschalk, A.J., Florens, L., Swanson, S.K., Gutierrez, J.L., Coleman, M.K., Workman, J.L., Mushegian, A., et al. (2005) A mammalian chromatin remodeling complex with similarities to the yeast INO80 complex J. Biol. Chem, . 280, 41207–41212[Abstract/Free Full Text] .

  150. Morrison, A.J., Highland, J., Krogan, N.J., Arbel-Eden, A., Greenblatt, J.F., Haber, J.E., Shen, X. (2004) INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair Cell, 119, 767–775[CrossRef][Web of Science][Medline] .

  151. van Attikum, H., Fritsch, O., Hohn, B., Gasser, S.M. (2004) Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair Cell, 119, 777–788[CrossRef][Web of Science][Medline] .

  152. Tsukuda, T., Fleming, A.B., Nickoloff, J.A., Osley, M.A. (2005) Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae Nature, 438, 379–383[CrossRef][Medline] .

  153. Downs, J.A. and Cote, J. (2005) Dynamics of chromatin during the repair of DNA double-strand breaks Cell Cycle, 4, 1373–1376[Web of Science][Medline] .

  154. Soininen, R., Schoor, M., Henseling, U., Tepe, C., Kisters-Woike, B., Rossant, J., Gossler, A. (1992) The mouse Enhancer trap locus 1 (Etl-1): a novel mammalian gene related to Drosophila and yeast transcriptional regulator genes Mech. Dev, . 39, 111–123[CrossRef][Web of Science][Medline] .

  155. Adra, C.N., Donato, J.L., Badovinac, R., Syed, F., Kheraj, R., Cai, H., Moran, C., Kolker, M.T., Turner, H., Weremowicz, S., et al. (2000) SMARCAD1, a novel human helicase family-defining member associated with genetic instability: cloning, expression, and mapping to 4q22–q23, a band rich in breakpoints and deletion mutants involved in several human diseases Genomics, 69, 162–173[CrossRef][Web of Science][Medline] .

  156. Clark, M.W., Zhong, W.W., Keng, T., Storms, R.K., Barton, A., Kaback, D.B., Bussey, H. (1992) Identification of a Saccharomyces cerevisiae homolog of the SNF2 transcriptional regulator in the DNA sequence of an 8.6 kb region in the LTE1-CYS1 interval on the left arm of chromosome I Yeast, 8, 133–145[CrossRef][Web of Science][Medline] .

  157. Schoor, M., Schuster-Gossler, K., Roopenian, D., Gossler, A. (1999) Skeletal dysplasias, growth retardation, reduced postnatal survival, and impaired fertility in mice lacking the SNF2/SWI2 family member ETL1 Mech. Dev, . 85, 73–83[CrossRef][Web of Science][Medline] .

  158. Ouspenski, I.I., Elledge, S.J., Brinkley, B.R. (1999) New yeast genes important for chromosome integrity and segregation identified by dosage effects on genome stability Nucleic Acids Res, . 27, 3001–3008[Abstract/Free Full Text] .

  159. Barton, A.B. and Kaback, D.B. (1994) Molecular cloning of chromosome I DNA from Saccharomyces cerevisiae: analysis of the genes in the FUN38-MAK16-SPO7 region J. Bacteriol, . 176, 1872–1880[Abstract/Free Full Text] .

  160. Tan, T.L., Kanaar, R., Wyman, C. (2003) Rad54, a Jack of all trades in homologous recombination DNA Repair (Amst), 2, 787–794[CrossRef][Medline] .

  161. Krogh, B.O. and Symington, L.S. (2004) Recombination proteins in yeast Annu. Rev. Genet, . 38, 233–271[CrossRef][Web of Science][Medline] .

  162. Klein, H.L. (1997) RDH54, a RAD54 homologue in Saccharomyces cerevisiae, is required for mitotic diploid-specific recombination and repair and for meiosis Genetics, 147, 1533–1543[Abstract] .

  163. Tanaka, K., Kagawa, W., Kinebuchi, T., Kurumizaka, H., Miyagawa, K. (2002) Human Rad54B is a double-stranded DNA-dependent ATPase and has biochemical properties different from its structural homolog in yeast, Tid1/Rdh54 Nucleic Acids Res, . 30, 1346–1353[Abstract/Free Full Text] .

  164. Tan, T.L., Essers, J., Citterio, E., Swagemakers, S.M., de Wit, J., Benson, F.E., Hoeijmakers, J.H., Kanaar, R. (1999) Mouse Rad54 affects DNA conformation and DNA-damage-induced Rad51 foci formation Curr. Biol, . 9, 325–328[CrossRef][Web of Science][Medline] .

  165. Petukhova, G., Van Komen, S., Vergano, S., Klein, H., Sung, P. (1999) Yeast Rad54 promotes Rad51-dependent homologous DNA pairing via ATP hydrolysis-driven change in DNA double helix conformation J. Biol. Chem, . 274, 29453–29462[Abstract/Free Full Text] .

  166. Alexeev, A., Mazin, A., Kowalczykowski, S.C. (2003) Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament Nature Struct. Biol, . 10, 182–186[CrossRef][Web of Science][Medline] .

  167. Alexiadis, V. and Kadonaga, J.T. (2002) Strand pairing by Rad54 and Rad51 is enhanced by chromatin Genes Dev, . 16, 2767–2771[Abstract/Free Full Text] .

  168. Gibbons, R.J., Picketts, D.J., Villard, L., Higgs, D.R. (1995) Mutations in a putative global transcriptional regulator cause X-linked mental retardation with alpha-thalassemia (ATR-X syndrome) Cell, 80, 837–845[CrossRef][Web of Science][Medline] .

  169. McDowell, T.L., Gibbons, R.J., Sutherland, H., O'Rourke, D.M., Bickmore, W.A., Pombo, A., Turley, H., Gatter, K., Picketts, D.J., Buckle, V.J., et al. (1999) Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes Proc. Natl Acad. Sci. USA, 96, 13983–13988[Abstract/Free Full Text] .

  170. Gibbons, R.J., McDowell, T.L., Raman, S., O'Rourke, D.M., Garrick, D., Ayyub, H., Higgs, D.R. (2000) Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation Nature Genet, . 24, 368–371[CrossRef][Web of Science][Medline] .

  171. Janne, O.A., Moilanen, A.M., Poukka, H., Rouleau, N., Karvonen, U., Kotaja, N., Hakli, M., Palvimo, J.J. (2000) Androgen-receptor-interacting nuclear proteins Biochem. Soc. Trans, . 28, 401–405[Web of Science][Medline] .

  172. Domanskyi, A., Virtanen, K.T., Palvimo, J.J., Janne, O.A. (2006) Biochemical characterization of androgen receptor-interacting protein 4 Biochem. J, . 393, 789–795[CrossRef][Web of Science][Medline] .

  173. Kanno, T., Mette, M.F., Kreil, D.P., Aufsatz, W., Matzke, M., Matzke, A.J. (2004) Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation Curr. Biol, . 14, 801–805[CrossRef][Web of Science][Medline] .

  174. Kanno, T., Huettel, B., Mette, M.F., Aufsatz, W., Jaligot, E., Daxinger, L., Kreil, D.P., Matzke, M., Matzke, A.J. (2005) Atypical RNA polymerase subunits required for RNA-directed DNA methylation Nature Genet, . 37, 761–765[CrossRef][Web of Science][Medline] .

  175. Kanno, T., Aufsatz, W., Jaligot, E., Mette, M.F., Matzke, M., Matzke, A.J. (2005) A SNF2-like protein facilitates dynamic control of DNA methylation EMBO Rep, . 6, 649–655[CrossRef][Web of Science][Medline] .

  176. DiPaolo, C., Kieft, R., Cross, M., Sabatini, R. (2005) Regulation of trypanosome DNA glycosylation by a SWI2/SNF2-like protein Mol. Cell, 17, 441–451[CrossRef][Web of Science][Medline] .

  177. Hoege, C., Pfander, B., Moldovan, G.L., Pyrowolakis, G., Jentsch, S. (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO Nature, 419, 135–141[CrossRef][Medline] .

  178. Chen, S., Davies, A.A., Sagan, D., Ulrich, H.D. (2005) The RING finger ATPase Rad5p of Saccharomyces cerevisiae contributes to DNA double-strand break repair in a ubiquitin-independent manner Nucleic Acids Res, . 33, 5878–5886[Abstract/Free Full Text] .

  179. Guzder, S.N., Sung, P., Prakash, L., Prakash, S. (1998) The DNA-dependent ATPase activity of yeast nucleotide excision repair factor 4 and its role in DNA damage recognition J. Biol. Chem, . 273, 6292–6296[Abstract/Free Full Text] .

  180. Ramsey, K.L., Smith, J.J., Dasgupta, A., Maqani, N., Grant, P., Auble, D.T. (2004) The NEF4 complex regulates Rad4 levels and utilizes Snf2/Swi2-related ATPase activity for nucleotide excision repair Mol. Cell. Biol, . 24, 6362–6378[Abstract/Free Full Text] .

  181. Hewetson, A., Hendrix, E.C., Mansharamani, M., Lee, V.H., Chilton, B.S. (2002) Identification of the RUSH consensus-binding site by cyclic amplification and selection of targets: demonstration that RUSH mediates the ability of prolactin to augment progesterone-dependent gene expression Mol. Endocrinol, . 16, 2101–2112[Abstract/Free Full Text] .

  182. Moinova, H.R., Chen, W.D., Shen, L., Smiraglia, D., Olechnowicz, J., Ravi, L., Kasturi, L., Myeroff, L., Plass, C., Parsons, R., et al. (2002) HLTF gene silencing in human colon cancer Proc. Natl Acad. Sci. USA, 99, 4562–4567[Abstract/Free Full Text] .

  183. Zhang, Z. and Buchman, A.R. (1997) Identification of a member of a DNA-dependent ATPase family that causes interference with silencing Mol. Cell. Biol, . 17, 5461–5472[Abstract] .

  184. Girdham, C.H. and Glover, D.M. (1991) Chromosome tangling and breakage at anaphase result from mutations in lodestar, a Drosophila gene encoding a putative nucleoside triphosphate-binding protein Genes Dev, . 5, 1786–1799[Abstract/Free Full Text] .

  185. Jiang, Y., Liu, M., Spencer, C.A., Price, D.H. (2004) Involvement of transcription termination factor 2 in mitotic repression of transcription elongation Mol. Cell, 14, 375–385[CrossRef][Web of Science][Medline] .

  186. Hara, R., Selby, C.P., Liu, M., Price, D.H., Sancar, A. (1999) Human transcription release factor 2 dissociates RNA polymerases I and II stalled at a cyclobutane thymine dimer J. Biol. Chem, . 274, 24779–24786[Abstract/Free Full Text] .

  187. Sood, R., Makalowska, I., Galdzicki, M., Hu, P., Eddings, E., Robbins, C.M., Moses, T., Namkoong, J., Chen, S., Trent, J.M. (2003) Cloning and characterization of a novel gene, SHPRH, encoding a conserved putative protein with SNF2/helicase and PHD-finger domains from the 6q24 region Genomics, 82, 153–161[CrossRef][Web of Science][Medline] .

  188. Ramakrishnan, V., Finch, J.T., Graziano, V., Lee, P.L., Sweet, R.M. (1993) Crystal structure of globular domain of histone H5 and its implications for nucleosome binding Nature, 362, 219–223[CrossRef][Medline] .

  189. Clark, K.L., Halay, E.D., Lai, E., Burley, S.K. (1993) Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5 Nature, 364, 412–420[CrossRef][Medline] .

  190. Burley, S.K., Xie, X., Clark, K.L., Shu, F. (1997) Histone-like transcription factors in eukaryotes Curr. Opin. Struct. Biol, . 7, 94–102[CrossRef][Web of Science][Medline] .

  191. Aasland, R., Gibson, T.J., Stewart, A.F. (1995) The PHD finger: implications for chromatin-mediated transcriptional regulation Trends Biochem. Sci, . 20, 56–59[CrossRef][Web of Science][Medline] .

  192. Ragvin, A., Valvatne, H., Erdal, S., Arskog, V., Tufteland, K.R., Breen, K., AM, O.Y., Eberharter, A., Gibson, T.J., Becker, P.B., et al. (2004) Nucleosome binding by the bromodomain and PHD finger of the transcriptional cofactor p300 J. Mol. Biol, . 337, 773–788[CrossRef][Web of Science][Medline] .

  193. Davis, J.L., Kunisawa, R., Thorner, J. (1992) A presumptive helicase (MOT1 gene product) affects gene expression and is required for viability in the yeast Saccharomyces cerevisiae Mol. Cell. Biol, . 12, 1879–1892[Abstract/Free Full Text] .

  194. Chicca, J.J., II, Auble, D.T., Pugh, B.F. (1998) Cloning and biochemical characterization of TAF-172, a human homolog of yeast Mot1 Mol. Cell. Biol, . 18, 1701–1710[Abstract/Free Full Text] .

  195. Auble, D.T., Wang, D., Post, K.W., Hahn, S. (1997) Molecular analysis of the SNF2/SWI2 protein family member MOT1, an ATP-driven enzyme that dissociates TATA-binding protein from DNA Mol. Cell. Biol, . 17, 4842–4851[Abstract] .

  196. Dasgupta, A., Juedes, S.A., Sprouse, R.O., Auble, D.T. (2005) Mot1-mediated control of transcription complex assembly and activity EMBO J, . 24, 1717–1729[CrossRef][Web of Science][Medline] .

  197. Topalidou, I., Papamichos-Chronakis, M., Thireos, G., Tzamarias, D. (2004) Spt3 and Mot1 cooperate in nucleosome remodeling independently of TBP recruitment EMBO J, . 23, 1943–1948[CrossRef][Web of Science][Medline] .

  198. Troelstra, C., van Gool, A., de Wit, J., Vermeulen, W., Bootsma, D., Hoeijmakers, J.H. (1992) ERCC6, a member of a subfamily of putative helicases, is involved in Cockayne's syndrome and preferential repair of active genes Cell, 71, 939–953[CrossRef][Web of Science][Medline] .

  199. van Gool, A.J., Verhage, R., Swagemakers, S.M., van de Putte, P., Brouwer, J., Troelstra, C., Bootsma, D., Hoeijmakers, J.H. (1994) RAD26, the functional S. cerevisiae homolog of the Cockayne syndrome B gene ERCC6 EMBO J, . 13, 5361–5369[Web of Science][Medline] .

  200. Svejstrup, J.Q. (2003) Rescue of arrested RNA polymerase II complexes J. Cell Sci, . 116, 447–451[Abstract/Free Full Text] .

  201. Park, J.S., Marr, M.T., Roberts, J.W. (2002) E. coli transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation Cell, 109, 757–767[CrossRef][Web of Science][Medline] .

  202. Citterio, E., Van Den Boom, V., Schnitzler, G., Kanaar, R., Bonte, E., Kingston, R.E., Hoeijmakers, J.H., Vermeulen, W. (2000) ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor Mol. Cell. Biol, . 20, 7643–7653[Abstract/Free Full Text] .

  203. Beerens, N., Hoeijmakers, J.H., Kanaar, R., Vermeulen, W., Wyman, C. (2005) The CSB protein actively wraps DNA J. Biol. Chem, . 280, 4722–4729[Abstract/Free Full Text] .

  204. Makarova, K.S., Aravind, L., Koonin, E.V. (2002) SWIM, a novel Zn-chelating domain present in bacteria, archaea and eukaryotes Trends Biochem. Sci, . 27, 384–386[CrossRef][Web of Science][Medline] .

  205. Liu, J., Gagnon, Y., Gauthier, J., Furenlid, L., L'Heureux, P.J., Auger, M., Nureki, O., Yokoyama, S., Lapointe, J. (1995) The zinc-binding site of Escherichia coli glutamyl-tRNA synthetase is located in the acceptor-binding domain. Studies by extended x-ray absorption fine structure, molecular modeling, and site-directed mutagenesis J. Biol. Chem, . 270, 15162–15169[Abstract/Free Full Text] .

  206. Boerkoel, C.F., Takashima, H., John, J., Yan, J., Stankiewicz, P., Rosenbarker, L., Andre, J.L., Bogdanovic, R., Burguet, A., Cockfield, S., et al. (2002) Mutant chromatin remodeling protein SMARCAL1 causes Schimke immuno-osseous dysplasia Nature Genet, . 30, 215–220[CrossRef][Web of Science][Medline] .

  207. Muthuswami, R., Truman, P.A., Mesner, L.D., Hockensmith, J.W. (2000) A eukaryotic SWI2/SNF2 domain, an exquisite detector of double-stranded to single-stranded DNA transition elements J. Biol. Chem, . 275, 7648–7655[Abstract/Free Full Text] .

  208. Plambeck, C.A., Kwan, A.H., Adams, D.J., Westman, B.J., van der Weyden, L., Medcalf, R.L., Morris, B.J., Mackay, J.P. (2003) The structure of the zinc finger domain from human splicing factor ZNF265 fold J. Biol. Chem, . 278, 22805–22811[Abstract/Free Full Text] .

  209. Hsia, K.C., Chak, K.F., Liang, P.H., Cheng, Y.S., Ku, W.Y., Yuan, H.S. (2004) DNA binding and degradation by the HNH protein ColE7 Structure (Camb), 12, 205–214[Medline] .

  210. Muzzin, O., Campbell, E.A., Xia, L., Severinova, E., Darst, S.A., Severinov, K. (1998) Disruption of Escherichia coli hepA, an RNA polymerase-associated protein, causes UV sensitivity J. Biol. Chem, . 273, 15157–15161[Abstract/Free Full Text] .

  211. Sukhodolets, M.V., Cabrera, J.E., Zhi, H., Jin, D.J. (2001) RapA, a bacterial homolog of SWI2/SNF2, stimulates RNA polymerase recycling in transcription Genes Dev, . 15, 3330–3341[Abstract/Free Full Text] .


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 Nucleic Acids ResHome page
K. Bouazoune, T. B. Miranda, P. A. Jones, and R. E. Kingston
Analysis of individual remodeled nucleosomes reveals decreased histone-DNA contacts created by hSWI/SNF
Nucleic Acids Res., June 30, 2009; (2009) gkp524v1.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
M. Nongkhlaw, P. Dutta, J. W. Hockensmith, S. S. Komath, and R. Muthuswami
Elucidating the mechanism of DNA-dependent ATP hydrolysis mediated by DNA-dependent ATPase A, a member of the SWI2/SNF2 protein family
Nucleic Acids Res., June 1, 2009; 37(10): 3332 - 3341.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
J. Atkinson and P. McGlynn
Replication fork reversal and the maintenance of genome stability
Nucleic Acids Res., June 1, 2009; 37(11): 3475 - 3492.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
M. Rodriguez-Paredes, M. Ceballos-Chavez, M. Esteller, M. Garcia-Dominguez, and J. C. Reyes
The chromatin remodeling factor CHD8 interacts with elongating RNA polymerase II and controls expression of the cyclin E2 gene
Nucleic Acids Res., May 1, 2009; 37(8): 2449 - 2460.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
J. Somers and T. Owen-Hughes
Mutations to the histone H3 {alpha}N region selectively alter the outcome of ATP-dependent nucleosome-remodelling reactions
Nucleic Acids Res., May 1, 2009; 37(8): 2504 - 2513.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
C. A. Haseltine and S. C. Kowalczykowski
An archaeal Rad54 protein remodels DNA and stimulates DNA strand exchange by RadA
Nucleic Acids Res., May 1, 2009; 37(8): 2757 - 2770.
[Abstract] [Full Text] [PDF]

Home page
 Mol PlantHome page
R. March-Diaz and J. C. Reyes
The Beauty of Being a Variant: H2A.Z and the SWR1 Complex in Plants
Mol Plant, March 31, 2009; (2009) ssp019v1.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
T. Szalontai, I. Gaspar, I. Belecz, I. Kerekes, M. Erdelyi, I. Boros, and J. Szabad
HorkaD, a Chromosome Instability-Causing Mutation in Drosophila, Is a Dominant-Negative Allele of lodestar
Genetics, February 1, 2009; 181(2): 367 - 377.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
S. Yu, J. B. Smirnova, E. C. Friedberg, B. Stillman, M. Akiyama, T. Owen-Hughes, R. Waters, and S. H. Reed
ABF1-binding Sites Promote Efficient Global Genome Nucleotide Excision Repair
J. Biol. Chem., January 9, 2009; 284(2): 966 - 973.
[Abstract] [Full Text] [PDF]

Home page
 J. Gen. Virol.Home page
S. Katsuma, T. Fujii, S. Kawaoka, and T. Shimada
Bombyx mori nucleopolyhedrovirus SNF2 global transactivator homologue (Bm33) enhances viral pathogenicity in B. mori larvae
J. Gen. Virol., December 1, 2008; 89(12): 3039 - 3046.
[Abstract] [Full Text] [PDF]

Home page
 ScienceHome page
T. Yusufzai and J. T. Kadonaga
HARP Is an ATP-Driven Annealing Helicase
Science, October 31, 2008; 322(5902): 748 - 750.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
A. Motegi, H.-J. Liaw, K.-Y. Lee, H. P. Roest, A. Maas, X. Wu, H. Moinova, S. D. Markowitz, H. Ding, J. H. J. Hoeijmakers, et al.
Polyubiquitination of proliferating cell nuclear antigen by HLTF and SHPRH prevents genomic instability from stalled replication forks
PNAS, August 26, 2008; 105(34): 12411 - 12416.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
B. A. Thompson, V. Tremblay, G. Lin, and D. A. Bochar
CHD8 Is an ATP-Dependent Chromatin Remodeling Factor That Regulates {beta}-Catenin Target Genes
Mol. Cell. Biol., June 15, 2008; 28(12): 3894 - 3904.
[Abstract] [Full Text] [PDF]

Home page
 GENES CELLSHome page
T. Ohba, H. Nishijima, H. Nishitani, and T. Nishimoto
Schizosaccharomyces pombe Snf2SR, a novel SNF2 family protein, interacts with Ran GTPase and modulates both RanGEF and RanGAP activities.
Genes Cells, June 1, 2008; 13(6): 571 - 582.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
Y. Kwon, C. Seong, P. Chi, E. C. Greene, H. Klein, and P. Sung
ATP-dependent Chromatin Remodeling by the Saccharomyces cerevisiae Homologous Recombination Factor Rdh54
J. Biol. Chem., April 18, 2008; 283(16): 10445 - 10452.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
M. Murawska, N. Kunert, J. van Vugt, G. Langst, E. Kremmer, C. Logie, and A. Brehm
dCHD3, a Novel ATP-Dependent Chromatin Remodeler Associated with Sites of Active Transcription
Mol. Cell. Biol., April 15, 2008; 28(8): 2745 - 2757.
[Abstract] [Full Text] [PDF]

Home page
 Plant Physiol.Home page
I-P. Chen, A. Mannuss, N. Orel, F. Heitzeberg, and H. Puchta
A Homolog of ScRAD5 Is Involved in DNA Repair and Homologous Recombination in Arabidopsis
Plant Physiology, April 1, 2008; 146(4): 1786 - 1796.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
K. Gendler, T. Paulsen, and C. Napoli
ChromDB: The Chromatin Database
Nucleic Acids Res., January 11, 2008; 36(suppl_1): D298 - D302.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
K. Myant and I. Stancheva
LSH Cooperates with DNA Methyltransferases To Repress Transcription
Mol. Cell. Biol., January 1, 2008; 28(1): 215 - 226.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
B. A. McKinley and M. V. Sukhodolets
Escherichia coli RNA polymerase-associated SWI/SNF protein RapA: evidence for RNA-directed binding and remodeling activity
Nucleic Acids Res., December 18, 2007; 35(21): 7044 - 7060.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
K. Rippe, A. Schrader, P. Riede, R. Strohner, E. Lehmann, and G. Langst
DNA sequence- and conformation-directed positioning of nucleosomes by chromatin-remodeling complexes
PNAS, October 2, 2007; 104(40): 15635 - 15640.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
S. Barbaric, T. Luckenbach, A. Schmid, D. Blaschke, W. Horz, and P. Korber
Redundancy of Chromatin Remodeling Pathways for the Induction of the Yeast PHO5 Promoter in Vivo
J. Biol. Chem., September 21, 2007; 282(38): 27610 - 27621.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Biol. CellHome page
J. E. Sillibourne, B. Delaval, S. Redick, M. Sinha, and S. J. Doxsey
Chromatin Remodeling Proteins Interact with Pericentrin to Regulate Centrosome Integrity
Mol. Biol. Cell, September 1, 2007; 18(9): 3667 - 3680.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
S. Nakanishi, R. Prasad, S. H. Wilson, and M. Smerdon
Different structural states in oligonucleosomes are required for early versus late steps of base excision repair
Nucleic Acids Res., July 26, 2007; 35(13): 4313 - 4321.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
F.-P. Zhang, A. Domanskyi, J. J. Palvimo, H. Sariola, J. Partanen, and O. A. Janne
An Adenosine Triphosphatase of the Sucrose Nonfermenting 2 Family, Androgen Receptor-Interacting Protein 4, Is Essential for Mouse Embryonic Development and Cell Proliferation
Mol. Endocrinol., June 1, 2007; 21(6): 1430 - 1442.
[Abstract] [Full Text] [PDF]

Home page
 BioinformaticsHome page
B. E. Suzek, H. Huang, P. McGarvey, R. Mazumder, and C. H. Wu
UniRef: comprehensive and non-redundant UniProt reference clusters
Bioinformatics, May 15, 2007; 23(10): 1282 - 1288.
[Abstract] [Full Text] [PDF]

Home page
 Genes Dev.Home page
S. Kundu, P. J. Horn, and C. L. Peterson
SWI/SNF is required for transcriptional memory at the yeast GAL gene cluster
Genes & Dev., April 15, 2007; 21(8): 997 - 1004.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
X. Nan, J. Hou, A. Maclean, J. Nasir, M. J. Lafuente, X. Shu, S. Kriaucionis, and A. Bird
Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation
PNAS, February 20, 2007; 104(8): 2709 - 2714.
[Abstract] [Full Text] [PDF]

Home page
 Plant CellHome page
S. Bezhani, C. Winter, S. Hershman, J. D. Wagner, J. F. Kennedy, C. S. Kwon, J. Pfluger, Y. Su, and D. Wagner
Unique, Shared, and Redundant Roles for the Arabidopsis SWI/SNF Chromatin Remodeling ATPases BRAHMA and SPLAYED
PLANT CELL, February 1, 2007; 19(2): 403 - 416.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
H. Durr, A. Flaus, T. Owen-Hughes, and K.-P. Hopfner
Snf2 family ATPases and DExx box helicases: differences and unifying concepts from high-resolution crystal structures
Nucleic Acids Res., September 10, 2006; 34(15): 4160 - 4167.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Print PDF (3201K) Freely available
Right arrow Screen PDF (1886K) Freely available
Right arrow Supplementary Material
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (60)
Right arrow Commercial Re-use Guidelines
for Open Access NAR Content
Google Scholar
Right arrow Articles by Flaus, A.
Right arrow Articles by Owen-Hughes, T.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Flaus, A.
Right arrow Articles by Owen-Hughes, T.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?