Similarities in transcription factor IIIC subunits that bind to the posterior regions of internal promoters for RNA polymerase III
© Matsutani; licensee BioMed Central Ltd. 2004
Received: 30 March 2004
Accepted: 09 August 2004
Published: 09 August 2004
In eukaryotes, RNA polymerase III (RNAP III) transcribes the genes for small RNAs like tRNAs, 5S rRNA, and several viral RNAs, and short interspersed repetitive elements (SINEs). The genes for these RNAs and SINEs have internal promoters that consist of two regions. These two regions are called the A and B blocks. The multisubunit transcription factor TFIIIC is required for transcription initiation of RNAP III; in transcription of tRNAs, the B-block binding subunit of TFIIIC recognizes a promoter. Although internal promoter sequences are conserved in eukaryotes, no evidence of homology between the B-block binding subunits of vertebrates and yeasts has been reported previously.
Here, I reported the results of PSI-BLAST searches using the B-block binding subunits of human and Shizosacchromyces pombe as queries, showing that the same Arabidopsis proteins were hit with low E-values in both searches. Comparison of the convergent iterative alignments obtained by these PSI-BLAST searches revealed that the vertebrate, yeast, and Arabidopsis proteins have similarities in their N-terminal one-third regions. In these regions, there were three domains with conserved sequence similarities, one located in the N-terminal end region. The N-terminal end region of the B-block binding subunit of Saccharomyces cerevisiae is tentatively identified as a HMG box, which is the DNA binding motif. Although I compared the alignment of the N-terminal end regions of the B-block binding subunits, and their homologs, with that of the HMG boxes, it is not clear whether they are related.
Molecular phylogenetic analyses using the small subunit rRNA and ubiquitous proteins like actin and α-tubulin, show that fungi are more closely related to animals than either is to plants. Interestingly, the results obtained in this study show that, with respect to the B-block binding subunits of TFIIICs, animals appear to be evolutionarily closer to plants than to fungi.
Phylogenetic relationships among animals, fungi, and plants have been a controversial issue. Although fungi traditionally had been considered more closely related to plants than to animals, Whittaker and Margulis  classified the fungi as a separate kingdom in their five-kingdom classification: the three major multicellular groups of animals, fungi, and green plants were each given the status of kingdoms derived from different protistan lineages of uncertain affinities. With the determination of the primary structures of homologous macromolecules in various organisms, spanning several kingdoms, molecular phylogenetic techniques resulted in new hypotheses about the relationships among eukaryotes. Small subunit rRNA, and the proteins like actin and α-tubulin, exist ubiquitously and their primary structures are highly conserved. Thus, these sequences have been used to make molecular trees [for examples, [2, 3]]. Most of these studies place fungi as more closely related to animals than either is to plants [3–6].
Eukaryotic RNA polymerase III (RNAP III) transcribes a variety of small RNAs like tRNAs, 5S rRNA, and several viral RNAs . Short interspersed repetitive elements (SINEs) are also transcribed by RNAP III . Genes for these small RNAs have internal promoters that consist of two regions called the A and B blocks . These promoter sequences are well-conserved in diverse eukaryotes . Transcription by RNAP III requires the multisubunit transcription factor TFIIIC, which plays an important role in transcription initiation . TFIIIC contains a B-block binding subunit, which recognizes the RNAP III promoter in the transcription of tRNAs and several viral RNAs, orienting its associated subunits along the DNA . TFIIIC that is oriented toward the start site, promotes TFIIIB binding and assists in directing accurate initiation by RNAP III [12, 13].
In TFIIIC of Saccharomyces cerevisiae, a subunit of 138 kDa binds to a B-block, and its gene which is called TFC3, has been cloned . The open reading frame for the B-block binding subunit is interrupted by one intron . TFC3 is a single-copy gene and essential for cell viability . In human and rat, the B-block binding subunits of TFIIICs are 243 kDa and 220 kDa respectively [14, 15], and there is great similarity between them at the amino acid sequence level . However, B-block binding subunit from mammals has been thought to show no homology to the S. cerevisiae 138 kDa subunit, although all of them bind to similar DNA regions, suggesting a significant degree of evolutionary divergence for RNAP III factors [15, 16]. Huang et al.  identified several subunits of S. pombe TFIIIC from the S. pombe sequence database by homology searches using the S. cerevisiae TFIIIC subunits as queries; one of these subunits named Sfc3p, is similar to the S. cerevisiae B-block binding subunit. It has been thought that, like the B-block binding subunit from S. cerevisiae, Sfc3p does not share homology with the human B-block binding subunit. On the other hand, Sfc1p, Sfc4p, and Sfc6p, which are other subunits of S. pombe TFIIIC, show homologies not only to S. cerevisiae TFIIIC subunits but also to human TFIIIC subunits . It has been shown that Sfc1p, Sfc3p, Sfc4p, and Sfc6p are associated in vivo, and the isolated Sfc3p complex is active in the in vitro RNAP III-mediated transcription of S. pombe tRNA genes .
PSI-BLAST search using the human B-block binding subunit as a query
PSI-BLAST using the yeast B-block binding subunits as queries
The S. cerevisiae B-block binding subunit exhibits 21 % identity and 39 % similarity to the S. pombe Sfc3p protein, and these similarities extend to the overall sequences (Background; ). When I performed a PSI-BLAST search using the S. cerevisiae B-block binding subunit as a query, five sequences were hit with E-values better than threshold after three iterations: the Neurospora crassa hypothetical protein (GI 32412546) with 0.0, S. pombe Sfc3p with e-159, the Magnaporthe grisea hypothetical protein (GI 38108450) with e-121, the Saccharomyces bayanus hypothetical protein fragment (GI 10863079) with e-100, and the Arabidopsis hypothetical protein (GI 15218016) with 0.002 (data not shown). It is noteworthy that the Arabidopsis protein of GI 15218016 was hit although the E-value was not so good. This protein was hit also in the PSI-BLAST search using the human B-block binding subunit as a query (Fig. 2A).
Next, I performed a PSI-BLAST search using the S. pombe Sfc3p protein as a query. Fig. 2B is a summary of the result. The Magnaporthe grisea and Neurospora crassa hypothetical proteins (GI 38108450 and GI 32412546), were hit with very good E-values (0 and e-168 respectively) (Fig. 2B). The Aspergillus nidulans protein GI 49107000 also was hit with a robust E-value (data not shown). Four hypothetical proteins of Arabidopsis thaliana were hit with E-values worse than those of the two fungi proteins but well above the threshold: GI 15218016 with e-113, GI 25402830 with e-88, GI 9665127 with 2e-88, and GI 25404859 with 7e-70 (Fig. 2B). The Arabidopsis protein GI 15218016 was found also in the result of the PSI-BLAST search using the S. cerevisiae subunit as a query, but in the search with S. pombe Sfc3p it had a much better E-value. Surprisingly, these four Arabidopsis proteins were identical to the proteins that were hit with low E-values in the PSI-BLAST search using the human B-block binding subunit as a query (Fig. 2A). While both the N-terminal half regions and C- terminal end regions were similar between the Arabidopsis proteins and the human subunit, their similarities to S. pombe Sfc3p were only in the N-terminal halves (Figs. 2A and 2B). The B-block binding subunits of rat and human also were hit in this search, but with E-values of 5e-5 and 0.20, respectively (data not shown); the N-terminal 350 amino acid sequences of the rat and human subunits showed similarities to the N-terminal region of S. pombe Sfc3p protein.
PSI-BLAST using the B-block binding subunit homolog found in Arabidopsis as a query
The four Arabidopsis proteins (GIs 25402830, 9665127, 15218016, and 25404859), were hit with low E-values in both of the PSI-BLAST searches using the human and S. pombe subunits as queries. Thus, I performed a PSI-BLAST search using one of these Arabidopsis proteins (GI 25402830) as a query. Fig. 2C shows a summary of the result. Six hypothetical Arabidopsis proteins were hit with E-values of 0, and three of them were identical to the proteins which were hit in the PSI-BLAST searches using the human and S. pombe subunits as queries. In addition to these, the human and rat subunits were hit with low E-values (e-132 and e-108 respectively). The N-terminal 700 amino acids of the human and rat subunits were most similar to the Arabidopsis proteins, but the short regions of the C-terminal ends also were similar (Fig. 2C). The hypothetical mouse protein (GI 38087408) which was hit in the PSI-BLAST search using the human subunit as a query, also was hit in the PSI-BLAST search with Arabidopsis GI 25402830 (Fig. 2C). The B-block binding subunits of S. pombe and S. cerevisiae were hit with E-values worse than threshold (0.024 and 1.1 respectively) (data not shown). However, it should be noted that these Arabidopsis proteins were hit with E-values better than threshold when a PSI-BLAST search was performed using the S. pombe B-block binding protein as a query.
It is interesting that the four Arabidopsis proteins were similar to the B-block binding subunits of vertebrates and yeasts, despite the fact that vertebrate and yeast subunits share no recognizable homology [15–17]. These results seemed to imply that the Arabidopsis proteins of GIs 25402830, 9665127, 15218016, and 25404859 represent a 'missing link' between the vertebrate and yeast B-block binding subunits.
Alignment of the B-block binding subunits and their homologs
When a PSI-BLAST search was performed using the human B-block binding subunit as a query, it was shown that the C-terminal region also is conserved (Fig. 2A); for examples, Chironomus, Anopheres, Drosophila, and Arabidopsis (GIs, 25402830, 9665127, and 15218016) proteins are hit with E-values of e-29, 3e-7, 6e-54, 2e-20, 2e-39, and 2e-21 respectively (data not shown). These regions contain the domains shown to have sequence similarities  (see above). When a PSI-BLAST search was performed using the S. pombe B-block binding subunit as a query, alignments consisting of its C-terminal region and each of the Magnaporthe, Neurospora, and S. cerevisiae sequences were generated, but no homology to the C-terminal regions of the Arabidopsis proteins was suggested (Fig. 2B). However, in agreement with the result of Rozenfeld and Thuriaux , when the S. cerevisiae B-block binding subunit was used as a query, the C-terminal region of the Arabidopsis protein (GI 9665127) was hit after four iterations; aa positions 1032–1146 of the S. cerevisiae subunit aligned to positions 1673–1774 of the Arabidopsis protein (GI 9665127) with an E-value of 5e-21 (data not shown). Consequently, the C-terminal sequences of the human, rat, mosquitoes, Drosophila, Arabidopsis and fungi proteins, can be aligned by Clustal W (Fig. 3D).
Are the HMG boxes in the B-block binding proteins?
Evolutionary relationships of the B-block binding proteins
I also searched for a B-block binding protein homolog in the genome of green alga Chlamydomonas reinhardtii. I performed a tblastn search using the Arabidopsis protein GI 25402830 as a query and the C. reinhardtii genome sequence ver2 in the Joint Genome Institute website (see Methods). The Arabidopsis sequences at aa positions of 83–144, 234–262, 698–713, and 1812–1847 showed similarities to sequences corresponding to bp positions of 539027-538842, 527862-537776, 534044-533997, and 526942-526835 in the C. reinhardtii scaffold 16, with E-values of 9.7e-5, 80.2, 80.2, and 9.7e-5 respectively (Fig. 5C). The amino acid sequences deduced from bp positions 539027-538842 and 526942-526835 corresponded to the domains conserved among the B-block binding proteins that were aligned by Clustal W, as shown in Figs. 3B and 3D. These results suggest that the Chlamydomonas B-block binding protein is encoded in these DNA regions. Subsequently, I performed PSI-BLAST searches using the two amino acid sequences of C. reinhardtii with the highest similarities to the Arabidopsis protein (Fig. 5D). The query sequence from bp positions 539231-538197 in C. reinhardtii, showed similarities to the rat B-block binding subunit and its homolog in mouse (E-values of 7.1 and 5.8 respectively) (Fig. 5D). Although these E-values are not robust, no fungal B-block binding proteins was hit with E-values better than 10. The other query sequence encoded in bp positions 527524-526466 of C. reinhardtii also had greater similarities to the B-block binding proteins in animals than to those in fungi: for examples, the human and rat subunits were hit with E-values of 4e-68 and 2e-56 respectively, while no fungal proteins were hit with E-values better than 10 (Fig. 5D). The results of these PSI-BLAST searches with Oryza and Chlamydomonas query sequences indicate that the greater similarity in TFIIIC B-block binding proteins between animals and plants, with yeast as more distant, across the broad diversity of the animal and plant kingdoms.
Because yeasts may not be representative of all fungi, it is important to demonstrate that the greater similarity between the animal and plant B-block binding proteins extends beyond the yeast taxa. To this end, I searched for homologs of the B-block binding protein in the basidiomycete genomes. I performed a PSI-BLAST search using the S. pombe subunit as a query, limiting the search to the fungi database. The sequence hit with the best E-value among the basidiomycete sequences, was the Ustilago maydis protein GI 461005911 (Fig. 2B). The Cryptococcus and Coccidiodes sequences were not hit with E-values better than 10. In the Ustilago sequence GI 461005911, three regions show similarities to the S. pombe subunit, particularly the N-terminal one-third and the C-terminal regions as is true of other homologs in fungi (Fig. 2B). Subsequently, a PSI-BLAST search was performed using the human B-block binding subunit as a query of the fungi database. Although the S. cerevisiae B-block binding subunit was hit with an E-value of 5e-7, the Ustilago sequence of GI 46100591 was not hit with an E-value better than 10 (data not shown). Moreover, a PSI-BLAST search performed using the Arabidopsis homolog (GI 25402830) as a query of the fungi database also did not hit the Ustilago sequence of GI 46100591 with an E-value better than 10, although the S. cerevisiae and S. pombe B-block binding subunits were hit with E-values of 0.93 and 9.7 respectively (data not shown). These results indicate that animal and plant B-block binding subunits are more similar to the yeast subunits than to the Ustilago protein GI 46100591. The overall results in this section demonstrate that the greater similarity between the plant and animal B-block binding proteins extends to the green alga protein, and the greater differences in fungi go beyond the yeast taxa.
In this study, I have demonstrated that the B-block binding subunits of TFIIICs in vertebrates are apparently homologous to those of yeasts, by identifying the homologs of each in Arabidopsis. The Arabidopsis proteins (GIs 25402830, 9665127, 15218016, and 25404859), which show strong similarity to B-block binding subunits, are the hypothetical proteins translated conceptually from the nucleotide sequences of the chromosome I [; see also http://0-www.ncbi.nlm.nih.gov.brum.beds.ac.uk/entrez]. The lengths of the inferred amino acid sequences of three of these Arabidopsis proteins (GIs 25402830, 9665127, and 15218016), are close to those of the amino acid sequences of the vertebrate subunits (Fig. 2). These Arabidopsis proteins probably function as the B-block binding subunits in vivo. B-block binding subunits act on the RNAP III promoters, the sequences of which are conserved in diverse eukaryotes (Background; Fig. 1). Thus, the domains of the subunits that bind to these promoters also should be conserved in vertebrates and yeasts. The N-terminal one-third regions of the human, yeast, and the Arabidopsis homologs found in this study probably associate with the B-block sequences. It is interesting that the HMG boxes predicted in the S. cerevisiae B-block binding subunit  overlap with the regions conserved in many of these putative B-block binding subunits.
There is a striking degree of similarity in most of the RNAP III transcription machinery in human, S. pombe, and S. cerevisiae; RNAP III, TFIIIA, TFIIIB, and the TFIIIC subunits that interact with the transcription initiation site, are highly conserved in these three organisms . On the other hand, the TFIIIC subunits, which interact with downstream promoter regions including the B-block binding subunits, are more divergent . There is the possibility that substitution rates of the amino acid residues in the B-block binding subunits vary among animals, fungi, and plants, resulting in the high divergence between the human and fungi proteins, and the similarity between the human and plant proteins. Alternatively, evolutionary inferences based on the RNAP III transcription machinery may be different from those of the genes that generally have been used to examine phylogenetic relationships in animals, fungi, and plants. RNAP III transcribes genes encoding tRNA, 5S rRNA, and several viral RNAs, and SINEs (Background). It was reported that molecular phylogenies based on tRNA sequences place plants as the sister group to the animals, although the tRNA data set available at the time was small . Generally, it is thought that 5S rRNA is convenient for intrakingdom phylogenies, but cannot resolve the question of the animal-plant-fungal divergence because of its short length and high divergence [32, 33]. It should be noted that more recent investigations of the proteins involved in RNA metabolism, the mRNA capping apparatus, and several key components that regulate the cell cycle, also suggest a close relationship between animals and plants, with fungi as more distant [34–36].
Previously, no evidence of homology between the B-block binding subunits of TFIIICs of vertebrates and yeasts has been reported. PSI-BLAST searches presented here provided the evidence that these subunits are homologous, and that the Arabidopsis proteins can be used to link them. These results imply that, with respect to the B-block binding subunits, animals are evolutionarily closer to Arabidopsis than to yeasts. Comparisons of the B-block binding proteins from additional plant taxa showed that the greater similarity between plants and animals extends to the green algae Chlamydomonas. It was also demonstrated that the differences in fungi go beyond the yeast texa, and occur in basidiomycetes. These are interesting because molecular phylogenetic analyses using the small subunit rRNA and ubiquitous proteins, show that fungi are more closely related to animals than either is to plants.
To search for similarities between the B-block binding subunits of vertebrates and yeasts, I used the PSI-BLAST program in the NCBI website http://0-www.ncbi.nlm.nih.gov.brum.beds.ac.uk/BLAST/. PSI-BLAST searches were performed by default: matrix was BLOSUM62; gap costs were Existence 11 and Extension 1; and the E-value of threshold was 0.005. Peptide sequence databases used for the PSI-BLAST searches were all non-redundant GenBank CDS translations, RefSeq proteins, PDB, SwissProt, PIR, and PRF (total 1605642 sequences). The PSI-BLAST was limited searches of the eukaryota databases, when the amino acid sequences from the Oryza and Chlamydomonas coding regions were used as queries. The fungi database was used in a search for homologs of the S. pombe B-block binding subunit in basidiomycetes. PSI-BLAST was run three times for each of the queries. To search for homologs of the Arabidopsis protein GI25402830 in the plant sequences, the tblastn program was used http://0-www.ncbi.nlm.nih.gov.brum.beds.ac.uk/BLAST/. To search for homologs of the Arabidopsis protein GI25402830 in the Chlamydomonas reinhardtii sequences, the tblastn program at the Joint Genome Institute website http://genome.jgi-psf.org/cgi-bin/runBlast.pl?db=chlre2, was used. Clustal W in the EMBL-EBI website http://www.ebi.ac.uk/clustalw/ was used to align the multiple amino acid sequences . Clustal W was performed by default: matrix was Gonnet 250; the penalty for opening a gap was 10; the penalty for extending a gap was 0.05; and gap separation penalty was 8. Secondary structures of the proteins were predicted by using the PSIPRED protein structure prediction server (PSIPRED v2.4 in http://bioinf.cs.ucl.ac.uk/psipred/) .
- Whittaker RH, Margulis L: Protist classification and kingdoms of organisms. Biosystems. 1978, 10: 3-18. 10.1016/0303-2647(78)90023-0.View ArticlePubMedGoogle Scholar
- Woese CR, Kandler O, Wheelis ML: Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA. 1990, 87: 4576-4579.PubMed CentralView ArticlePubMedGoogle Scholar
- Baldauf SL, Palmer JD: Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. Proc Natl Acad Sci USA. 1993, 90: 11558-11562.PubMed CentralView ArticlePubMedGoogle Scholar
- Hasegawa M, Hashimoto T, Adachi J, Iwabe N, Miyata T: Early branchings in the evolution of eukaryotes: ancient divergence of entamoeba that lacks mitochondria revealed by protein sequence data. J Mol Evol. 1993, 36: 380-388.View ArticlePubMedGoogle Scholar
- Wainright PO, Hinkle G, Sogin ML, Stickel SK: Monophyletic origins of the metazoa: an evolutionary link with fungi. Science. 1993, 260: 340-342.View ArticlePubMedGoogle Scholar
- Borchiellini C, Boury-Esnault N, Vacelet J, Le Parco Y: Phylogenetic analysis of the Hsp70 sequences reveals the monophyly of Metazoa and specific phylogenetic relationships between animals and fungi. Mol Biol Evol. 1998, 15: 647-655.View ArticlePubMedGoogle Scholar
- Geiduschek EP, Tocchini-Valentini GP: Transcription by RNA polymerase III. Annu Rev Biochem. 1998, 57: 873-914. 10.1146/annurev.bi.57.070188.004301.View ArticleGoogle Scholar
- Weiner AM, Deininger PL, Efstratiadis A: Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of the genetic information. Annu Rev Biochem. 1986, 55: 631-661. 10.1146/annurev.bi.55.070186.003215.View ArticlePubMedGoogle Scholar
- Galli G, Hofstetter H, Birnstiel ML: Two conserved sequence blocks within eukaryotic tRNA genes are major promoter elements. Nature. 1981, 294: 626-631.View ArticlePubMedGoogle Scholar
- Lassar AB, Martin PL, Roeder RG: Transcription of class III genes: formation of preinitiation complexes. Science. 1983, 222: 740-748.View ArticlePubMedGoogle Scholar
- Willis IM: RNA polymerase III. Genes, factors and transcription specificity. Eur J Biochem. 1993, 212: 1-11.View ArticlePubMedGoogle Scholar
- Kassavetis GA, Braun BR, Nguyen LH, Geiduschek EP: S. cerevisiae TFIIIB is the transcription initiation factor proper of RNA polymerase III, while TFIIIA and TFIIIC are assembly factors. Cell. 1990, 60: 235-245.View ArticlePubMedGoogle Scholar
- Flores A, Briand JF, Gadal O, Andrau JC, Rubbi L, Van Mullem V, Boschiero C, Goussot M, Marck C, Carles C, Thuriaux P, Sentenac A, Werner M: A protein-protein interaction map of yeast RNA polymerase III. Proc Natl Acad Sci USA. 1999, 96: 7815-7820. 10.1073/pnas.96.14.7815.PubMed CentralView ArticlePubMedGoogle Scholar
- Lefebvre O, Carles C, Conesa C, Swanson RN, Bouet F, Riva M, Sentenac A: TFC3 : gene encoding the B-block binding subunit of the yeast transcription factor IIIC. Proc Natl Acad Sci USA. 1992, 89: 10512-10516.PubMed CentralView ArticlePubMedGoogle Scholar
- Lagna G, Kovelman R, Sukegawa J, Roeder RG: Cloning and characterization of an evolutionary divergent DNA-binding subunit of mammalian TFIIIC. Mol Cell Biol. 1994, 14: 3053-3064.PubMed CentralView ArticlePubMedGoogle Scholar
- L'Etoile ND, Fahnestock ML, Shen Y, Aebersold R, Berk AJ: Human transcription factor IIIC box B binding subunit. Proc Natl Acad Sci USA. 1994, 91: 1652-1656.PubMed CentralView ArticlePubMedGoogle Scholar
- Huang Y, Hamada M, Maraia RJ: Isolation and cloning of four subunits of a fission yeast TFIIIC complex that includes an ortholog of the human regulatory protein TFIIICβ. J Biol Chem. 2000, 275: 31480-31487. 10.1074/jbc.M004635200.View ArticlePubMedGoogle Scholar
- Folk WR, Hofstetter H, Birnstiel ML: Some bacterial tRNA genes are transcribed by eukaryotic RNA polymerase III. Nucl Acids Res. 1982, 10: 7153-7162.PubMed CentralView ArticlePubMedGoogle Scholar
- Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DL: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res. 1997, 25: 3389-3402. 10.1093/nar/25.17.3389.PubMed CentralView ArticlePubMedGoogle Scholar
- Sabri N, Farrants AK, Hellman U, Visa N: Evidence for a posttranscriptional role of a TFIIICα-like protein Chironomus tentans. Molec Biol Cell. 2002, 13: 1765-1777. 10.1091/mbc.01-09-0436.PubMed CentralView ArticlePubMedGoogle Scholar
- Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res. 1994, 22: 4673-4680.PubMed CentralView ArticlePubMedGoogle Scholar
- Rozenfeld S, Thuriaux P: Genetic interactions within TFIIIC, the promoter-binding factor of yeast RNA polymerase III. Mol Genet Genomics. 2001, 265: 705-710. 10.1007/s004380100467.View ArticlePubMedGoogle Scholar
- Bianchi ME: The HMG-box domain. In DNA-Protein: Structural Interactions. Edited by: Lilley DMJ. 1995, Oxford: IRL Press at Oxford University Press, 177-200.Google Scholar
- Laudet V, Stehelin D, Clevers H: Ancestry and diversity of the HMG box superfamily. Nucl Acids Res. 1993, 21: 2493-2501.PubMed CentralView ArticlePubMedGoogle Scholar
- Weir HM, Kraulis PJ, Hill CH, Raine ARC, Laue ED, Thomas JO: Structure of the HMG box motif in the B-domain of HMG1. EMBO J. 1993, 12: 1311-1319.PubMed CentralPubMedGoogle Scholar
- Baxevanis AD, Bryant SH, Landsman D: Homology model building of the HMG-1 box structural domain. Nucl Acids Res. 1995, 23: 1019-1029.PubMed CentralView ArticlePubMedGoogle Scholar
- Jones DN, Searles MA, Shaw GL, Churchill ME, Ner SS, Keeler J, Travers AA, Neuhaus D: The solution structure and dynamics of the DNA-binding domain of HMG-D from Drosophila melanogaster. Structure. 1994, 2: 609-627.View ArticlePubMedGoogle Scholar
- Werner MH, Huth JR, Gronenborn AM, Clore GM: Molecular basis of human 46X, Y sex reversal revealed from the three-dimensional solution structure of the human SRY-DNA complex. Cell. 1995, 81: 705-714. 10.1016/0092-8674(95)90532-4.View ArticlePubMedGoogle Scholar
- McGuffin LJ, Bryson K, Jones DT: The PSIPRED protein structure prediction server. Bioinformatics. 2000, 16: 404-405. 10.1093/bioinformatics/16.4.404.View ArticlePubMedGoogle Scholar
- Theologis A, Ecker JR, Palm CJ, Federspiel NA, Kaul S, White O, Alonso J, Altafi H, Araujo R, Bowman CL, Brooks SY, Buehler E, Chan A, Chao Q, Chen H, Cheuk RF, Chin CW, Chung MK, Conn L, Conway AB, Conway AR, Creasy TH, Dewar K, Dunn P, Etgu P, Feldblyum TV, Feng J, Fong B, Fujii CY, Gill JE, Goldsmith AD, Haas B, Hansen NF, Hughes B, Huizar L, Hunter JL, Jenkins J, Johnson-Hopson C, Khan S, Khaykin E, Kim CJ, Koo HL, Kremenetskaia I, Kurtz DB, Kwan A, Lam B, Langin-Hooper S, Lee A, Lee JM, Lenz CA, Li JH, Li Y, Lin X, Liu SX, Liu ZA, Luros JS, Maiti R, Marziali A, Militscher J, Miranda M, Nguyen M, Nierman WC, Osborne BI, Pai G, Peterson J, Pham PK, Rizzo M, Rooney T, Rowley D, Sakano H, Salzberg SL, Schwartz JR, Shinn P, Southwick AM, Sun H, Tallon LJ, Tambunga G, Toriumi MJ, Town CD, Utterback T, Van Aken S, Vaysberg M, Vysotskaia VS, Walker M, Wu D, Yu G, Fraser CM, Venter JC, Davis RW: Sequence and analysis of chromosome 1 of the plant Arabidopsis thaliana. Nature. 2000, 408: 816-820. 10.1038/35048500.View ArticlePubMedGoogle Scholar
- Huang Y, Maraia RJ: Comparison of the RNA polymerase III transcription machinery in Schizosaccharomyces pombe, Saccharomyces cerevisiae and human. Nucl Acid Res. 2001, 29: 2675-2690. 10.1093/nar/29.13.2675.View ArticleGoogle Scholar
- Gouy M, Li WH: Molecular phylogeny of the kingdoms Animalia, Plantae, and Fungi. Mol Biol Evol. 1989, 6: 109-122.PubMedGoogle Scholar
- Hori H, Ohsawa S: Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol. 1987, 4: 445-472.PubMedGoogle Scholar
- Anantharaman V, Koonin EV, Aravind L: Comparative genomics and evolution of proteins involved in RNA metabolism. Nucl Acids Res. 2002, 30: 1427-1464. 10.1093/nar/30.7.1427.PubMed CentralView ArticlePubMedGoogle Scholar
- Shuman S: What messenger RNA capping tells us about eukaryotic evolution. Nature Reviews Mol Cell Biol. 2002, 3: 619-625. 10.1038/nrm880.View ArticleGoogle Scholar
- Oakenfull EA, Riou-Khamlichi C, Murray JAH: Plant D-type cyclins and the control of G1 progression. Phil Trans R Soc Lond B Biol Sci. 2002, 357: 749-760. 10.1098/rstb.2002.1085.View ArticleGoogle Scholar
- Hofstetter H, Kressman A, Birnstiel ML: A split promoter for a eucaryotic tRNA gene. Cell. 1981, 24: 573-585. 10.1016/0092-8674(81)90348-2.View ArticlePubMedGoogle Scholar
- Sakonju S, Brown DD, Engelke D, Ng SY, Shastry BS, Roeder RG: The binding of a transcription factor to deletion mutants of a 5S ribosomal RNA gene. Cell. 1981, 23: 665-669. 10.1016/0092-8674(81)90429-3.View ArticlePubMedGoogle Scholar
- Rohan RM, Ketner G: A comprehensive collection of point mutations in the internal promoter of the adenoviral VAI gene. J Biol Chem. 1987, 262: 8500-8507.PubMedGoogle Scholar
- Perez-Stable C, Ayres TM, Shen CKJ: Distinctive sequence organization and functional programming of an Alu repeat promoter. Proc Natl Acad Sci USA. 1984, 81: 5291-5295.PubMed CentralView ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an open-access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.