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Analysis of the chicken TBP-like protein (tlp) gene: evidence for a striking conservation of vertebrate TLPs and for a close relationship between vertebrate tbp and tlp genes
Introduction
Materials And Methods
Cloning of chicken tlp cDNA and genomic DNA
Protein extraction, antibody and western blotting
Computer programs
FISH detection for chicken tbp and tlp genes
Results And Discussion
Cloning of chicken tlp cDNA
Similarity to other TBP-related proteins
Identification of chicken tlp gene
Exon-intron configuration of the tlp-related genes
How did the tlp gene evolve?
Functional aspects of TLP
Acknowledgements
References
Analysis of the chicken TBP-like protein (tlp) gene: evidence for a striking conservation of vertebrate TLPs and for a close relationship between vertebrate tbp and tlp genes
Received March 23, 1999; Revised and Accepted June 22, 1999
DDBJ/EMBL/GenBank accession no. AB024489
ABSTRACT TLP (TBP-like protein), which is a new protein discovered by us, has a structure similar to that of the C-terminal conserved domain (CCD) of TBP, although its function has not yet been elucidated. We isolated cDNA and genomic DNA that encode chicken TLP (cTLP) and determined their structures. The predicted amino acid sequence of cTLP was 98 and 91% identical to that of its mammalian and Xenopus counterparts, respectively, and its translation product was ubiquitously observed in chicken tissues. FISH detection showed that chicken tlp and tbp genes were mapped at 3q2.6-2.8 and 3q2.4-2.6 of the same chromosome, respectively. Genome analysis revealed that the chicken tlp gene was spliced with five introns. Interestingly, the vertebrate tbp genes were also found to be split by five introns when we focused on the CCDs, and their splicing points were similar to those of tlp. On the contrary, another TBP-resembling gene of Drosophila, trf1, is split by only one intron, as is the Drosophila's tbp gene. These results support our earlier assumption that vertebrate TLPs did not directly descend from Drosophila TRF1. On the basis of these results together with phylogenetical examination, we speculate that tlp diverged from an ancestral tbp gene through a process of gene duplication and point mutations.
INTRODUCTION
TATA-binding protein (TBP) is one of the general transcription factors (GTFs). TBP is required for eukaryotic transcription as it triggers the assembly of multiple GTFs as well as RNA polymerase on a promoter which leads to the formation of preinitiation complexes (1,2). TBP is involved in all three eukaryotic RNA polymerases, and it is therefore regarded as a universal transcription factor (1,3). In the case of RNA polymerase-II genes, many genes have a TATA-box in their promoter regions around 30 bp upstream from the transcription initiation site (4-6).
Tbp cDNAs have been isolated from various eukaryotes in a wide range of organisms from yeast to human, and even in archaea (7-12). However, the N-terminal portion of TBP varies among organisms and the C-terminal 180 amino acid of TBP is highly conserved (9,13). This conserved C-terminal domain (CCD) is essential, and maybe sufficient, for TBP functions such as activation of transcription and TATA-box binding (14). The CCD has a saddle-shaped configuration consisting of multiple anti-parallel [beta]-sheets, and this unique structure enables interaction of TBP with various proteins (15).
Since TBP is recognized as being a critical factor for transcriptional regulation, a number of investigations have been performed to identify tbp or its related genes. A genome project of Saccharomyces cerevisiae revealed a single tbp gene but no other tbp-related genes (16). Except for in higher plants, all of the eukaryotes examined so far have a unique TBP protein. However, in 1993, Crowley et al. (17) demonstrated a TBP-related factor from Drosophila that has an intrinsic TATA-binding activity. This protein was recently re-named as TRF1. Afterward, TRF1 was shown to govern transcription initiation like the conventional TBP (18). TRF1 was discovered from a mutant fly `shaker' having a defect in the nervous system, and it was thought to play a role in neurogenesis as well as neural gene expression in Drosophila (17,18). Since then, however, no TRF1 homologs have been reported in other organisms.
Recently, we reported a new TBP-resembling protein in mouse and human cells (19,20). This novel protein was named TBP-like protein (TLP). Unlike TBP and TRF1, TLP was not capable of TATA-box binding or of TATA-directed transcriptional activation in the reconstituted in vitro system. Actually, multiple amino acids that are critical for the TBP function were substituted in TLP. Although we do not know the physiological role of TLP yet, it is thought to be involved, as is TBP, in essential biological processes including transcriptional regulation, because of its structural similarity to TBP.
Mammalian TLP is 186 amino acids-long and covers the whole 180 amino acids of TBP's CCD. This protein was 38% identical and 76% similar to TBP of a corresponding organism. Although Drosophila TRF1 and TBP were 56% identical, the identity of Drosophila TRF1 versus mammalian TLP was only 35%. These findings suggest that TLP is not a direct descendent of TRF1. It would be interesting to clarify whether other vertebrates have TLP or not. Moreover, analysis of genomic DNA for TLP could lead to the elucidation of the evolutional relationship between tlp and tbp genes. In the present study, we investigated cDNA and genomic DNA for chicken TLP (cTLP) to address the above questions.
MATERIALS AND METHODS
Cloning of chicken tlp cDNA and genomic DNA
Chicken RNA was extracted from a chicken B lymphocyte-derived cell line DT40 (21,22). Two primers (5[prime]-GCACTGGAGCAACAAGTGAAGAAGAAGC, 5[prime]-GGGCCCTGTCA-TGTGATGCTTCCTGTTG) were constructed based on sequences from 475 to 504 of the mouse TLP (mTLP) cDNA (GenBank accession no. AB017697) and from 425 to 454 of the human TLP (hTLP) cDNA (GenBank accession no. AB020881), respectively. These oligonucleotides were used for RT-PCR with 2 µg of total cellular RNAs as previously reported (19). The obtained cTLP cDNAs were subcloned into the pGEM-T Easy Vector (Promega). The sequences at both termini of cTLP were determined by 5[prime]- and 3[prime]-RACE with the adaptor primer (Takara Shuzo) and internal primers (primer 1; 5[prime]-TGAGGACCAAATTGTGGCTGTAATCCTAGG and primer 2; 5[prime]-CCAGAACTTCATCCTGCTGTGTGCTACAG) within the cloned cTLP (Fig. 1). Finally, the cDNA fragment for cTLP that contained an entire open reading frame (ORF) was isolated using a set of primers (primer 3; 5[prime]-GATCTTCATGG- TGAACTGGTGTGAGAACTG and primer 4; 5-GTCTGTATTCCTCTGCTATAGTTGGTCCAG). The cTLP genomic DNA was isolated by PCR with high molecular weight chicken genomic DNA prepared from DT40 cells. PCR was performed using 10 ng of the chicken genomic DNA and primers 3 and 4. The resultant PCR fragment was subcloned into the pGEM-T Easy Vector.
Figure 1. Identification of cTLP cDNA. (A) Nucleotide and predicted amino acid sequences of cTLP. Amino acid positions were numbered from the putative translation initiation codon at nucleotide position 48. Oligonucleotide primers (primers 1-4) used in the PCR cloning are indicated by arrows. Vertical arrowheads indicate positions of the introns. (B) Comparison of amino acid sequences of hTLP, mTLP and cTLP. The alignment was performed using the CLUSTAL W program. Identical and similar amino acid residues between the three proteins are denoted by asterisks and dots, respectively. Single and double dots denote low and high similarities, respectively.
Protein extraction, antibody and western blotting
The whole-cell extracts of chicken tissues were prepared by the method described by Laemmli (23). MTLP was expressed in Escherichia coli and purified as described previously (19,24). The rabbit polyclonal antibody for mTLP was described previously (19). For western blotting, proteins were separated by 12% SDS-PAGE, electrophoretically transferred to a PVDF membrane (Millipore), and detected by the polyclonal rabbit anti-mTLP antibody using the ECL system (Amersham).
Computer programs
Comparison of amino acid sequences among TBP-resembling proteins and determination of the aligned score were performed by using the CLUSTAL W program (25). For analyzing the phylogenetic divergencies of the various TBP-related proteins, we focused on the direct repeat in the C-terminal domain of TBP or its corresponding sequence, e.g., nucleotide positions 410-647 of hTLP, 460-697 of mTLP, 235-472 of cTLP, and 266-502 of Xenopus TLF (TBP-like factor; GenBank accession no. A1238441). Nucleotide sequences in the direct repeats of the various proteins were aligned using the CLUSTAL W program. A phylogenetical rooted tree was drawn by using the Tree View program (26).
FISH detection for chicken tbp and tlp genes
Chromosome preparation and FISH detection were performed as described previously (27,28) with slight modifications. Mitogen-stimulated splenocyte culture was synchronized by a thymidine block, and the 5-bromodeoxyuridine was incorporated into the culture. The chromosomes were stained with Hoechst 33258. The chromosome slides were denatured at 70°C in 70% formamide/2× SSC, and dehydrated in ethanol. The probes of chicken tbp cDNA (1.5 kb) and genomic DNA of tlp gene (3.5 kb) were labeled with biotin 16-dUTP (Boehringer) following the manufacturer's protocol. The labeled DNA fragments were denatured at 75°C for 10 min in 100% formamide. When the genomic DNA fragment was used as a probe, 20 times excess amounts of Cot-1 DNA (Gibco BRL) were added. Hybridization was performed at 37°C overnight in 50% formamide, 2× SSC, 10% dextran sulfate, 2 mg/ml BSA and 250 ng labeled DNA. After rinsing in 4× SSC, the slides were incubated under a coverslip with Cy2-labeled streptavidin (Amersham) in 1% BSA/4× SSC at 37°C for 1 h. After washing with 0.1% NP-40/4× SSC, the slides were rinsed with 2× SSC and stained with 0.5 µg/ml propidium iodide.
RESULTS AND DISCUSSION
Cloning of chicken tlp cDNA
We amplified one DNA fragment by RT-PCR with a pair of primers and chicken DT40 cell-derived mRNAs. The primers were designed according to a sequence of already submitted mTLP. Using amplified DNA, we detected sequences at both termini by 3[prime]- and 5[prime]-RACE (Fig. 1A). One long ORF with 183 amino acids was observed in the isolated DNA, and amino acid similarity of the predicted protein to that of mTLP was 97%. Thus, we concluded that we had obtained a chicken tlp cDNA. Six amino acids of mammalian TLP were substituted in the chicken protein. Curiously, cTLP was 3 amino acids shorter at its C-terminus than the mammalian counterpart, even though its following two codons were the same as those of the mammalian TLP (i.e., glutamic acid at 184 of the mammalian TLP was changed to the stop codon in cTLP) (Fig. 1B). We extensively analyzed DNA sequences for this portion using DT40 genomic DNA and native chicken tissue (brain and heart)-derived tlp cDNA, and we found the same stop codon at the same position observed in the DT40 cell-derived cDNA. Thus, it was determined that cTLP is 3 amino acids shorter than mammalian TLP at the C-terminus. It is interesting that chicken TBP is also shorter than mammalian TBPs (29). Mammalian TLPs covered an entire region of the corresponding CCD of TBP (19,20). To be exact, however, C-termini of mammalian and cTLP are 1 amino acid longer and 1 amino acid shorter, respectively, than TBP.
We investigated the tissue distribution pattern for cTLP protein using the anti-mTLP antibody (Fig. 2). Since recombinant cTLP reacted with the antibody (Fig. 2, lane 1), mTLP and cTLP were thought to be immunologically related. We found that cTLP was present in the brain, heart, liver and gizzard, suggesting that cTLP was a not a tissue-specific protein, as has been demonstrated for mammalian TLPs. This localization pattern was slightly inconsistent with that of the mTLP, which we reported previously (19). On the other hand, the TLP expression pattern in the chicken was similar to that of chicken TBP reported by Yamauchi et al. (29). These findings suggest that the tissue-localizing pattern of TLP and TBP are comparable in a given organism.
Figure 2. Expression of TLP protein in chicken tissues. Immunoblotting of whole cell-extracts (10 µg) from various tissues was carried out using the anti-mTLP antibody. Arrowheads indicate positions of recombinant mTLP and cTLP proteins. Lane 1, histidine tag-carrying mTLP (1 ng).
Similarity to other TBP-related proteins
Figure 3A shows the structures of TBP and TBP-resembling proteins in several eukaryotes and also shows calculated amino acid identities of the CCD-corresponding regions relative to cTLP. Figure 3B shows the identities between representative TBP-resembling proteins. We included a newly discovered Drosophila TBP-resembling protein, TRF2 (30) in Figure 3. The amino acid sequences in mTLP and hTLP are identical (Fig. 3A), although the nucleotide sequences of those two genes were only 94% identical (data not shown). Similarities of TBP and TLP for mouse versus chicken were 90 (data not shown) and 98% (Fig. 3), respectively. Moreover, similarities of mouse and chicken for TBP versus TLP were also similar: 39 (data not shown) and 38% (Fig. 3B), respectively. On the other hand, Drosophila TRF1 exhibited significant (56%) similarity to Drosophila TBP (Fig. 3B). However, Drosophila TRF1 was only distantly related to mammalian (35%) and chicken (36%) TLPs (Fig. 3). Nucleotide sequence identities between Drosophila tbp versus chicken tlp and between Drosophila trf1 versus chicken tlp were 23 and 16%, respectively (data not shown). These findings suggest that ctlp gene is phylogenetically much closer to Drosophila tbp gene than to Drosophila trf1 gene although amino acid sequence similarity between those proteins is almost the same.
Figure 3. The amino acid identity within the CCD of the TBP-resembling proteins. (A) Schematic representation of the structures of representative TBP and TBP-resembling proteins and the identities relative to cTLP. Positions of characteristic regions; Q-run (hatched boxes), CCD (shaded boxes), and direct-repeats 1 and 2 are indicated. (B) Percent identity in the CCD between representative TBP-resembling proteins. Similarity was calculated by the CLUSTAL W program. Numbers in parentheses are the calculated scores based on the entire coding region.
Based on the nucleotide sequence data of direct-repeat regions in the CCD for multiple TBP-resembling proteins, we drew a phylogenetical tree using a computer-assisted program. The conclusion deduced from the obtained phylogenetical tree was nearly consistent with that proposed by Hancock (13), who also constructed a phylogenetical tree of TBP and TRF1 based on the conservation of the third bases of the codons in the CCD. The phylogenetical tree in Figure 4 suggests that an ancestor tbp gene was originally transmitted to yeasts/plants and animal kingdoms. Tbp genes might have then evolved to yeast, plant, invertebrate and vertebrate lineages. It is possible that tbp genes duplicated in multicellular organisms. In higher plants, the two tbp genes mutated little (12,31). However, trf1 did diverge from tbp in Drosophila, and, finally, it diverged into native tbp and tlp in vertebrates. Hence, there is thought to be no evolutionary link between TLP and TRF1. We did not include TRF2 in Figure 4 because the phylogenetical position of TRF2 altered drastically depending on the region of TRF2 used for the calculation, and thus we could not obtain a solid conclusion (discussed below in detail).
Figure 4. Phylogenetical tree for TBP-resembling proteins. The phylogram was drawn according to sequences of the direct repeat regions in the C-terminal conserved domain of TBP-resembling proteins. Lengths of the branches do not precisely correspond to the nucleotide substitution frequencies.
Identification of chicken tlp gene
We isolated chicken genomic DNA including the TLP-coding sequence using PCR with a set of primers based on the chicken tlp cDNA sequence. The obtained clone was 5.3 kb in length, covering the entire TLP-coding region. From a comparison of nucleotide sequences between cDNA and genomic DNA for cTLP, we found that the coding region of the chicken tlp gene was split by five introns. Insertion points of the first to fifth introns were mapped at G45/K46, S73/S73, Q94/V95, S129/S129 and G161/G161, respectively.
We determined chromosomal positions of chicken tlp and tbp genes by FISH using genomic DNA and cDNA probe, respectively (Fig. 5). Nucleotide identity between chicken tbp and tlp was only 33%, suggesting that probe DNAs did not cross-react with each other under our hybridization conditions. This assumption is most likely true since each probe specified different chromosomal regions (see below). The chicken cell has five major autosomes, two (Z and W) sex chromosomes, and multiple mini-chromosomes. FISH detection revealed that tlp and tbp signals were mapped on chromosome 3 at 3q2.6-2.8 and 3q2.4-2.6, respectively. We examined 75 metaphase spreads for the chromosomal mapping of tbp gene. Nine percent of the observed metaphase spreads exhibited complete twin spots on both homologs, and 26% had twin spots on either homolog. In tlp gene mapping, 18% of 100 metaphase spreads exhibited complete twin spots and 34% had twin spots on either homolog. Interestingly, human tlp 6q22.1-22.3 and tbp 6q27 genes were also mapped on an identical chromosome (20,32). A similar mechanism might have been involved in the gene duplication of chicken tbp and tlp.
Figure 5. Chromosome mapping for chicken tbp and tlp. (A) Chromosomal localization of chicken tbp (a, b) and tlp (c, d) genes by fluorescence in situ hybridization. The hybridization signals are indicated by arrows. The metaphase spreads were photographed using Nikon B-2A (a, c) and UV-2A (b, d) filters. G-banded patterns are demonstrated in (b, d). (B) Schematic representation of chicken chromosome 3. Positions of the tbp and tlp genes are indicated.
Exon-intron configuration of the tlp-related genes
In this study, we initially determined the gene organization of a novel TBP-resembling protein, TLP, using chickens. We compared its intron-insertion pattern with other tbp-related genes (Fig. 6). Mammalian tbp genes commonly contain seven introns (33,34). The first and second ones are located in the 5[prime]-non-coding region and the N-terminal variable domain, respectively. CCD of vertebrate tbp is split by five (third to seventh) introns (29,33-35). The third intron is located around the junction point between the N-terminal variable domain and CCD. The fourth and sixth introns are located at two loop regions, each being situated at a position parallel to the saddle-shaped TBP molecule. The seventh intron is located at the end of a [beta]-sheet. In short, introns in the CCD of mammalian TBPs generally exist at termini of loops and [beta]-sheets, and at parallel positions on the three-dimensional TBP structure (33). Moreover, two direct repeats in the CCD are separated by introns.
Figure 6. Exon-intron organization of the tbp-resembling genes The boxes correspond to amino acid stretches encoded by each exon. Amino acid positions interrupted by the introns are indicated, and corresponding amino acid positions of the different genes are linked by dashed lines. Bold roman and arabic numbers presented just below human TBP and cTLP, respectively, indicate orders of the introns. Numbers for introns of the chicken tlp represent the order of the intron within the coding region. The hatched and shaded boxes correspond to the variable N-terminal domain and the CCD, respectively. Coding regions for cTLP and Drosophila TRF1 are shown by closed and open boxes, respectively.
As observed in Figure 6, five introns (III-VII) in the CCDs of various vertebrate tbp genes were nearly the same. Interestingly, positions for introns III and IV were also conserved in the plant (Arabidopsis) (31). Moreover, the position of vertebrate intron VI was the same as those in plants and Schizosaccharomyces pombe (36). Additionally, S.pombe tbp has three introns, and two of them were mapped at similar positions to vertebrate ones. On the contrary, Drosophila tbp gene was split by only one intron, which did not correspond to any vertebrate one (37). These results suggested that, except for Drosophila and S.cerevisiae, intron insertion patterns for tbp were highly conserved in eukaryotes.
From chicken genome analysis, we found that chicken tlp had five introns (1-5), the same as vertebrate tbps (III-VII). Moreover, the exon-intron configuration for chicken tlp was similar to those for vertebrate tbps. We found two differences in the gene-split pattern between tlp and tbp. The second intron of tbp was absent in the tlp gene. Additionally, the tlp gene possesses one new intron at the middle of the proteins, the position of which was mapped at an intermediary position of tbp between the fifth and sixth introns. More interestingly, this split position corresponded to the unique intron of Drosophila tbps. On the contrary, Drosophila trf1 gene contained a unique intron at Q52/Q52, where no corresponding splice site was observed in any of the other tbp-related genes examined so far.
How did the tlp gene evolve?
In this study, we identified cTLP and its genomic DNA. TLP is structurally closer to vertebrate TBPs than to Drosophila TBP and Drosophila TRF1 (Fig. 3). The computer-assisted program implies that yeast, plant, fly and vertebrate TBPs each have their own distinct lineage (Fig. 4). Drosophila TRF1 was closer to Drosophila TBP than vertebrate TLPs. Therefore, it is evident that TRF1 is not a direct ancestor of the vertebrate TLPs. The gene expression pattern of TLP (Fig. 2) further supports this notion, because, unlike TRF1, cTLP is not a neural-specific gene. Recently, Xenopus TLF (TBP-like factor) was submitted to the database (GenBank accession no. A1238441). Since a tentative sequence of Xenopus TLP, which had been obtained by our preliminary examination, was matched to that of Xenopus TLF (data not shown), we concluded that the TLF is a true Xenopus counterpart of TLP. Moreover, Xenopus TLP was highly (91%) homologous to cTLP (Fig. 3), and we included Xenopus TLF in the TLP lineage (Fig. 4). Vertebrate tbps are much more conserved than are vertebrate tbps. In the case of TBP, the CCD regions of Drosophila (88%) and even yeast (80%) TBPs exhibit high identity to those of the vertebrate TBPs (data not shown). No gene has so far been determined in invertebrates that exhibits such high similarity to the vertebrate tlps. Hence, there is a possibility that TLP may be a vertebrate-specific protein.
Rabenstein et al. (30) recently identified the third TBP-resembling protein of Drosophila, TRF2 (Fig. 3). The whole coding region of TRF2 was much longer than that of vertebrate TLPs, and it exhibited extremely low identity (17%) to cTLP (Fig. 3B). However, when the central domain of TRF2 was extracted, its identity to the CCD of cTLP was higher (56%) than that of TRF1 (36%) (Fig. 3). Therefore, it is possible that TRF2 is a Drosophila TLP. If this is the case, the tlp gene must have diverged from an ancestral tbp. Consistent with this hypothesis, Rabenstein et al. (30) also identified a trf2 gene in Caenorhabditis elegans. However, nematode TRF2 was found to be only 38% identical to cTLP even when we focused on its direct-repeat sequence in the CCD-corresponding region (Fig. 3B). Furthermore, since the CCD-corresponding region of nematode TRF2 is split by a long insertion, the net similarity between nematode TRF2 and cTLP is only 22% (Fig. 3B). Hence, if the second hypothesis is correct, ancestral trf2 must have evolved in a distinct direction in animals. However, the evidence that the splicing patterns of vertebrate tlp and tbp were similar seems to be inconsistent with the above model. Perhaps, a third explanation, that TLPs evolved from an ancestral tbp of each animal phylum independently, and that the resultant proteins eventually had a common motif consisting of the CCD-corresponding region is possible. Further investigation is needed to clarify these issues.
Functional aspects of TLP
Consistent with a recent report (30), we found that mTLP binds to TFIIA (our unpublished observation). Mammalian TRF2 (i.e. TLP) was also demonstrated to bind to TFIIB (30). Although, TLP has not been demonstrated to participate in transcriptional activation or TATA-box binding (19,30), we think that TLP does participate in gene regulation in some situations. The tissue distribution pattern of cTLP differs slightly from that of mTLP (19 and Fig. 2). We suggest that, unlike TRF1, TLP does not regulate particular tissue-specific genes. Drosophila TRF2 (30) and mammalian TLPs (38) were supposed to regulate genes that conventional TFIID does not engage. TLP and TBP may be involved in the regulation of distinct sets of genes within a cell.
ACKNOWLEDGEMENTS
The authors thank Drs S. Kato (University of Tokyo), K. Ohashi (Chiba University), M. Abe (National Institute of Radiological Science of Japan) and S. Takeda (Kyoto University) for valuable discussions and for providing plasmids and cells. We also thank Ms K. Osano and M. Kasahara for their technical assistance. This work was supported in part by a Grant-In-Aid For Scientific Research From The Japanese Ministry Of Education, Science, Culture, and Sports. T.N. is a research fellow of The Japan Society for The Promotion Of Science.
REFERENCES
*To whom correspondence should be addressed. Tel: +81 43 290 2823; Fax: +81 43 290 2824; Email: btamura{at}nature.s.chiba-u.ac.jp
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