Jef Rozenski1, Pamela F. Crain1,* and James A. McCloskey1,2
1Department of Medicinal Chemistry and 2Department of Biochemistry, University of Utah, 30 S. 2000 East,Salt Lake City, UT 84112-5820, USA
Received October 1, 1998;Accepted October 7, 1998
ABSTRACT
The RNA Modification Database (http://medlib.med.utah.edu/RNAmods/ ) provides a comprehensive listing of naturally modified nucleosides in RNA. Each file includes: chemical structure; common name and symbol; type(s) of RNA in which found and corresponding phylogenetic distribution; Chemical Abstracts registry number and index name; and initial literature citations for structure characterization and chemical synthesis. New features include capability to search database files by name or substructural features, modifications in tmRNA, and links to related data and sites.
More than 95 different post-transcriptionally modified nucleosides are presently known in all types of RNA across all three primary phylogenetic domains. The discovery and structural characterization of new nucleosides, as well as additional reports of the phylogenetic distribution of known nucleosides, mandates a need for a comprehensive database of RNA nucleosides. The RNA Modification Database is continuously maintained as an update and extension of the initial printed report (1), and contains discussion and literature citations for a number of related topics. These data serve expanding interests (2) in the occurrence and functions of RNA modifications (3-5).
The authors invite comments concerning existing entries, errors or omissions, and suggestions for improvement. The Email address for this purpose is: RNAmods{at}lib.med.utah.edu
In general, each nucleoside file consists of the following information.
(i) Chemical structure of the nucleoside.
(ii) Common chemical name, symbol, elemental composition and mass.
(iii) Type(s) of RNA in which the nucleoside occurs: tRNA, rRNA, mRNA, tmRNA, snRNA, chromosomal RNA and other RNAs.
(iv) Phylogenetic occurrence of the nucleoside: archaea (archaebacteria), (eu)bacteria, eukarya, and the corresponding literature citations for each. Ribosomal RNA entries are further distinguished by RNA subunit, e.g., 16S, 28S.
(v) Chemical Abstracts registry numbers for the ribonucleoside, and corresponding base (if assigned), to permit computer-searching of the literature.
(vi) Chemical Abstracts index name, which in some cases includes stereochemical information not shown in the database chemical structure.
(vii) Literature citation to structure assignment of the nucleoside.
(viii) Literature citation to the first reported chemical synthesis of the nucleoside, or in limited cases of the base. Subsequent reports of synthesis, which often include refinements, can be accessed effectively in the literature through the Chemical Abstracts registry numbers.
(ix) Comments on any of the above entries, including additional literature citations or alternate nomenclature.
An example of a single file is given in Figure 1, for 5-methyluridine. The database currently (as of October, 1998) contains 95 ribonucleoside entries, distributed by RNA type and phylogenetic source as shown in Table 1. Users of the database are requested to cite the present paper as the source of information.
Figure1. Database record for the modified nucleoside 5-methyluridine.
Changes in the database implemented during recent months include the following.
(i) Revision in the structure of the database, including provision for file searching by name, by substructural features (e.g., `methylguanosine', `thio' or `deaza'), or by the column and row headings shown in Table 1.
(ii) Inclusion of tmRNA (formerly named 10Sa RNA) as a category of RNA in which modifications are found (6).
(iii) Expanded list of modifications reported in archaeal rRNA (7).
We are grateful to N. Lombardo, S. Dennis and S. Roberts in the Eccles Health Sciences Library for their assistance in implementing recent changes in the electronic version of the database. Maintenance of the database is supported through NIH grant GM29812.
F. A.P. Vendeix, A. M. Munoz, and P. F. Agris Free energy calculation of modified base-pair formation in explicit solvent: A predictive model
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Y. Suzuki, A. Noma, T. Suzuki, R. Ishitani, and O. Nureki Structural basis of tRNA modification with CO2 fixation and methylation by wybutosine synthesizing enzyme TYW4
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C. Takemoto, L. L. Spremulli, L. A. Benkowski, T. Ueda, T. Yokogawa, and K. Watanabe Unconventional decoding of the AUA codon as methionine by mitochondrial tRNAMet with the anticodon f5CAU as revealed with a mitochondrial in vitro translation system
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S. Muller, A. Urban, A. Hecker, F. Leclerc, C. Branlant, and Y. Motorin Deficiency of the tRNATyr:{Psi}35-synthase aPus7 in Archaea of the Sulfolobales order might be rescued by the H/ACA sRNA-guided machinery
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A. Noma, Y. Sakaguchi, and T. Suzuki Mechanistic characterization of the sulfur-relay system for eukaryotic 2-thiouridine biogenesis at tRNA wobble positions
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M. Schaefer, T. Pollex, K. Hanna, and F. Lyko RNA cytosine methylation analysis by bisulfite sequencing
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F. Juhling, M. Morl, R. K. Hartmann, M. Sprinzl, P. F. Stadler, and J. Putz tRNAdb 2009: compilation of tRNA sequences and tRNA genes
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P. Gurha and R. Gupta Archaeal Pus10 proteins can produce both pseudouridine 54 and 55 in tRNA
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R. Ero, L. Peil, A. Liiv, and J. Remme Identification of pseudouridine methyltransferase in Escherichia coli
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E. Purta, K. H. Kaminska, J. M. Kasprzak, J. M. Bujnicki, and S. Douthwaite YbeA is the m3{Psi} methyltransferase RlmH that targets nucleotide 1915 in 23S rRNA
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P. S. Pallan, C. Kreutz, S. Bosio, R. Micura, and M. Egli Effects of N2,N2 -dimethylguanosine on RNA structure and stability: Crystal structure of an RNA duplex with tandem m2 2G:A pairs
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T. Ohtsuki, T. Fujimoto, M. Kamimukai, C. Kumano, M. Kitamatsu, and M. Sisido Isolation of Small RNAs using Biotinylated PNAs
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M. P. Westbye, E. Feyzi, P. A. Aas, C. B. Vagbo, V. A. Talstad, B. Kavli, L. Hagen, O. Sundheim, M. Akbari, N.-B. Liabakk, et al. Human AlkB Homolog 1 Is a Mitochondrial Protein That Demethylates 3-Methylcytosine in DNA and RNA
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H. Walbott, N. Leulliot, H. Grosjean, and B. Golinelli-Pimpaneau The crystal structure of Pyrococcus abyssi tRNA (uracil-54, C5)-methyltransferase provides insights into its tRNA specificity
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T. Toyooka, T. Awai, T. Kanai, T. Imanaka, and H. Hori Stabilization of tRNA (m1G37) methyltransferase [TrmD] from Aquifex aeolicus by an intersubunit disulfide bond formation
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S. R. Nallagatla and P. C. Bevilacqua Nucleoside modifications modulate activation of the protein kinase PKR in an RNA structure-specific manner
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M. J. O. Johansson, A. Esberg, B. Huang, G. R. Bjork, and A. S. Bystrom Eukaryotic Wobble Uridine Modifications Promote a Functionally Redundant Decoding System
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W. A. Decatur and M. N. Schnare Different Mechanisms for Pseudouridine Formation in Yeast 5S and 5.8S rRNAs
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28(10):
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S. Muller, F. Leclerc, I. Behm-Ansmant, J.-B. Fourmann, B. Charpentier, and C. Branlant Combined in silico and experimental identification of the Pyrococcus abyssi H/ACA sRNAs and their target sites in ribosomal RNAs
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D. Piekna-Przybylska, W. A. Decatur, and M. J. Fournier The 3D rRNA modification maps database: with interactive tools for ribosome analysis
Nucleic Acids Res.,
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D178 - D183.
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P. P. Vaidyanathan, M. P. Deutscher, and A. Malhotra RluD, a highly conserved pseudouridine synthase, modifies 50S subunits more specifically and efficiently than free 23S rRNA
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Q. Dai, R. Fong, M. Saikia, D. Stephenson, Y.-t. Yu, T. Pan, and J. A. Piccirilli Identification of recognition residues for ligation-based detection and quantitation of pseudouridine and N6-methyladenosine
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R. Oliva, A. Tramontano, and L. Cavallo Mg2+ binding and archaeosine modification stabilize the G15 C48 Levitt base pair in tRNAs
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September 1, 2007;
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S. Muller, J.-B. Fourmann, C. Loegler, B. Charpentier, and C. Branlant Identification of determinants in the protein partners aCBF5 and aNOP10 necessary for the tRNA:{Psi}55-synthase and RNA-guided RNA:{Psi}-synthase activities
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gkm606v1.
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S. Sunita, E. Purta, M. Durawa, K. L. Tkaczuk, J. Swaathi, J. M. Bujnicki, and J. Sivaraman Functional specialization of domains tandemly duplicated within 16S rRNA methyltransferase RsmC
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H. Walbott, C. Husson, S. Auxilien, and B. Golinelli-Pimpaneau Cysteine of sequence motif VI is essential for nucleophilic catalysis by yeast tRNA m5C methyltransferase
RNA,
July 1, 2007;
13(7):
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J. Urbonavicius, G. Jager, and G. R. Bjork Amino acid residues of the Escherichia coli tRNA(m5U54)methyltransferase (TrmA) critical for stability, covalent binding of tRNA and enzymatic activity
Nucleic Acids Res.,
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3297 - 3305.
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G. Emmerechts, S. Barbe, P. Herdewijn, J. Anne, and J. Rozenski Post-transcriptional modification mapping in the Clostridium acetobutylicum 16S rRNA by mass spectrometry and reverse transcriptase assays
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35(10):
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D. Piekna-Przybylska, W. A. Decatur, and M. J. Fournier New bioinformatic tools for analysis of nucleotide modifications in eukaryotic rRNA
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March 1, 2007;
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305 - 312.
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K. Miyauchi, T. Ohara, and T. Suzuki Automated parallel isolation of multiple species of non-coding RNAs by the reciprocal circulating chromatography method
Nucleic Acids Res.,
February 28, 2007;
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E. Picardi, T. M. R. Regina, A. Brennicke, and C. Quagliariello REDIdb: the RNA editing database
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H. Takeda, T. Toyooka, Y. Ikeuchi, S.-i. Yokobori, K. Okadome, F. Takano, T. Oshima, T. Suzuki, Y. Endo, and H. Hori The substrate specificity of tRNA (m1G37) methyltransferase (TrmD) from Aquifex aeolicus
Genes Cells,
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K. Watanabe, O. Nureki, S. Fukai, Y. Endo, and H. Hori Functional Categorization of the Conserved Basic Amino Acid Residues in TrmH (tRNA (Gm18) Methyltansferase) Enzymes
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M. Saikia, Q. Dai, W. A. Decatur, M. J. Fournier, J. A. Piccirilli, and T. Pan A systematic, ligation-based approach to study RNA modifications
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J. W. Hardin and R. T. Batey The bipartite architecture of the sRNA in an archaeal box C/D complex is a primary determinant of specificity
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M. Roovers, C. Hale, C. Tricot, M. P. Terns, R. M. Terns, H. Grosjean, and L. Droogmans Formation of the conserved pseudouridine at position 55 in archaeal tRNA
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J. Mengel-Jorgensen, S. S. Jensen, A. Rasmussen, J. Poehlsgaard, J. J. L. Iversen, and F. Kirpekar Modifications in Thermus thermophilus 23 S Ribosomal RNA Are Centered in Regions of RNA-RNA Contact
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281(31):
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Y. DING Statistical and Bayesian approaches to RNA secondary structure prediction.
RNA,
March 1, 2006;
12(3):
323 - 331.
[Abstract][Full Text][PDF]
Z. Meng and P. A. Limbach Mass spectrometry of RNA: linking the genome to the proteome
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March 1, 2006;
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87 - 95.
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M. Helm Post-transcriptional nucleotide modification and alternative folding of RNA
Nucleic Acids Res.,
February 1, 2006;
34(2):
721 - 733.
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G. Gabant, S. Auxilien, I. Tuszynska, M. Locard, M. J. Gajda, G. Chaussinand, B. Fernandez, A. Dedieu, H. Grosjean, B. Golinelli-Pimpaneau, et al. THUMP from archaeal tRNA:m22G10 methyltransferase, a genuine autonomously folding domain.
Nucleic Acids Res.,
January 1, 2006;
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S. Dunin-Horkawicz, A. Czerwoniec, M. J. Gajda, M. Feder, H. Grosjean, and J. M. Bujnicki MODOMICS: a database of RNA modification pathways
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January 1, 2006;
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B. Diop-Frimpong, T. P. Prakash, K. G. Rajeev, M. Manoharan, and M. Egli Stabilizing contributions of sulfur-modified nucleotides: crystal structure of a DNA duplex with 2'-O-[2-(methoxy)ethyl]-2-thiothymidines
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M.-H. RENALIER, N. JOSEPH, C. GASPIN, P. THEBAULT, and A. MOUGIN The Cm56 tRNA modification in archaea is catalyzed either by a specific 2'-O-methylase, or a C/D sRNP
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July 1, 2005;
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T. Kato, Y. Daigo, S. Hayama, N. Ishikawa, T. Yamabuki, T. Ito, M. Miyamoto, S. Kondo, and Y. Nakamura A Novel Human tRNA-Dihydrouridine Synthase Involved in Pulmonary Carcinogenesis
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B. HUANG, M. J.O. JOHANSSON, and A. S. BYSTROM An early step in wobble uridine tRNA modification requires the Elongator complex
RNA,
April 1, 2005;
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K. Watanabe, O. Nureki, S. Fukai, R. Ishii, H. Okamoto, S. Yokoyama, Y. Endo, and H. Hori Roles of Conserved Amino Acid Sequence Motifs in the SpoU (TrmH) RNA Methyltransferase Family
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March 18, 2005;
280(11):
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M. DEL CAMPO, C. RECINOS, G. YANEZ, S. C. POMERANTZ, R. GUYMON, P. F. CRAIN, J. A. MCCLOSKEY, and J. OFENGAND Number, position, and significance of the pseudouridines in the large subunit ribosomal RNA of Haloarcula marismortui and Deinococcus radiodurans
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February 1, 2005;
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H. Okamoto, K. Watanabe, Y. Ikeuchi, T. Suzuki, Y. Endo, and H. Hori Substrate tRNA Recognition Mechanism of tRNA (m7G46) Methyltransferase from Aquifex aeolicus
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November 19, 2004;
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M. LIU, G. W. NOVOTNY, and S. DOUTHWAITE Methylation of 23S rRNA nucleotide G745 is a secondary function of the RlmAI methyltransferase
RNA,
November 18, 2004;
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J. Hager, B. L. Staker, and U. Jakob Substrate Binding Analysis of the 23S rRNA Methyltransferase RrmJ
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J. Armengaud, J. Urbonavicius, B. Fernandez, G. Chaussinand, J. M. Bujnicki, and H. Grosjean N2-Methylation of Guanosine at Position 10 in tRNA Is Catalyzed by a THUMP Domain-containing, S-Adenosylmethionine-dependent Methyltransferase, Conserved in Archaea and Eukaryota
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August 27, 2004;
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F. Xing, S. L. Hiley, T. R. Hughes, and E. M. Phizicky The Specificities of Four Yeast Dihydrouridine Synthases for Cytoplasmic tRNAs
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April 23, 2004;
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K. Das, T. Acton, Y. Chiang, L. Shih, E. Arnold, and G. T. Montelione Crystal structure of RlmAI: Implications for understanding the 23S rRNA G745/G748-methylation at the macrolide antibiotic-binding site
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U. Varshney, V. Ramesh, A. Madabushi, R. Gaur, H. S. Subramanya, and U. L. RajBhandary Mycobacterium tuberculosis Rv2118c codes for a single-component homotetrameric m1A58 tRNA methyltransferase
Nucleic Acids Res.,
February 11, 2004;
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R. Leipuviene, Q. Qian, and G. R. Bjork Formation of Thiolated Nucleosides Present in tRNA from Salmonella enterica serovar Typhimurium Occurs in Two Principally Distinct Pathways
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February 1, 2004;
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758 - 766.
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P. F. Agris Decoding the genome: a modified view
Nucleic Acids Res.,
January 9, 2004;
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223 - 238.
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H. R. Kalhor and S. Clarke Novel Methyltransferase for Modified Uridine Residues at the Wobble Position of tRNA
Mol. Cell. Biol.,
December 15, 2003;
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K. Takai and S. Yokoyama Roles of 5-substituents of tRNA wobble uridines in the recognition of purine-ending codons
Nucleic Acids Res.,
November 15, 2003;
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K. R. Noon, R. Guymon, P. F. Crain, J. A. McCloskey, M. Thomm, J. Lim, and R. Cavicchioli Influence of Temperature on tRNA Modification in Archaea: Methanococcoides burtonii (Optimum Growth Temperature [Topt], 23{degrees}C) and Stetteria hydrogenophila (Topt, 95{degrees}C)
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September 15, 2003;
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C. T. Madsen, J. Mengel-Jorgensen, F. Kirpekar, and S. Douthwaite Identifying the methyltransferases for m5U747 and m5U1939 in 23S rRNA using MALDI mass spectrometry
Nucleic Acids Res.,
August 15, 2003;
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H. Hori, S. Kubota, K. Watanabe, J.-M. Kim, T. Ogasawara, T. Sawasaki, and Y. Endo Aquifex aeolicus tRNA (Gm18) Methyltransferase Has Unique Substrate Specificity: tRNA RECOGNITION MECHANISM OF THE ENZYME
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June 27, 2003;
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25081 - 25090.
[Abstract][Full Text][PDF]
Y. KAYA and J. OFENGAND A novel unanticipated type of pseudouridine synthase with homologs in bacteria, archaea, and eukarya
RNA,
June 1, 2003;
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711 - 721.
[Abstract][Full Text][PDF]
J. URBONAVICIUS, G. STAHL, J. M.B. DURAND, S. N. BEN SALEM, Q. QIAN, P. J. FARABAUGH, and G. R. BJORK Transfer RNA modifications that alter +1 frameshifting in general fail to affect -1 frameshifting
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June 1, 2003;
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760 - 768.
[Abstract][Full Text][PDF]
L. SIMPSON, S. SBICEGO, and R. APHASIZHEV Uridine insertion/deletion RNA editing in trypanosome mitochondria: A complex business
RNA,
March 1, 2003;
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265 - 276.
[Abstract][Full Text][PDF]
W. A. Decatur and M. J. Fournier RNA-guided Nucleotide Modification of Ribosomal and Other RNAs
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January 3, 2003;
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K. Nilsson, H. K. Lundgren, T. G. Hagervall, and G. R. Bjork The Cysteine Desulfurase IscS Is Required for Synthesis of All Five Thiolated Nucleosides Present in tRNA from Salmonella enterica Serovar Typhimurium
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6830 - 6835.
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J. Mengel-Jorgensen and F. Kirpekar Detection of pseudouridine and other modifications in tRNA by cyanoethylation and MALDI mass spectrometry
Nucleic Acids Res.,
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T. K. Dineshkumar, S. Thanedar, C. Subbulakshmi, and U. Varshney An unexpected absence of queuosine modification in the tRNAs of an Escherichia coli B strain
Microbiology,
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J. Urbonavicius, J. M. B. Durand, and G. R. Bjork Three Modifications in the D and T Arms of tRNA Influence Translation in Escherichia coli and Expression of Virulence Genes in Shigella flexneri
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F. Lecointe, O. Namy, I. Hatin, G. Simos, J.-P. Rousset, and H. Grosjean Lack of Pseudouridine 38/39 in the Anticodon Arm of Yeast Cytoplasmic tRNA Decreases in Vivo Recoding Efficiency
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[Abstract][Full Text][PDF]
J. Kufel, C. Allmang, L. Verdone, J. D. Beggs, and D. Tollervey Lsm Proteins Are Required for Normal Processing of Pre-tRNAs and Their Efficient Association with La-Homologous Protein Lhp1p
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M. Liu and S. Douthwaite Activity of the Ketolide Telithromycin Is Refractory to Erm Monomethylation of Bacterial rRNA
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[Abstract][Full Text][PDF]
S. Agarwalla, J. T. Kealey, D. V. Santi, and R. M. Stroud Characterization of the 23 S Ribosomal RNA m5U1939 Methyltransferase from Escherichia coli
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[Abstract][Full Text][PDF]
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