Journal of Molecular Evolution

, Volume 76, Issue 1–2, pp 28–47 | Cite as

Evolution of General Transcription Factors

Article

Abstract

Three genes GTF2IRD1, GTF2I, and GTF2IRD2, which encode members of the GTF2I (or TFII-I) family of so-called general transcription factors, were discovered and studied during the last two decades. Chromosome location and similarity of exon–intron structures suggest that the family evolved by duplications. The initial duplication of ancestral proto-GTF2IRD1 gene likely occurred in early vertebrates prior to origin of cartilaginous fish and led to formation of GTF2I (>450 MYA), which was later lost in bony fish but successfully evolved in the land vertebrates. The second duplication event, which created GTF2IRD2, occurred prior to major radiation events of eutherian mammalian evolution (>100 MYA). During recent steps of primate evolution there was another duplication which led to formation of GTF2IRD2B (<4 MYA). Two latest duplications were coupled with inversions. Genes belonging to the family have several highly conservative repeats which are implicated in DNA binding. Phylogenetic analysis of the repeats revealed a pattern of intragenic duplications, deletions and substitutions which led to diversification of the genes and proteins. Distribution of statistically rare atypical substitutions (p ≤ 0.01) sheds some light on structural differentiation of repeats and hence evolution of the genes. The atypical substitutions are often located on secondary structures joining α-helices and affect 3D arrangement of the protein globule. Such substitutions are commonly traced at the early stages of evolution in Tetrapoda, Amniota, and Mammalia.

Keywords

Evolution Gene family Exon–intron structure Intragenic repeats Amino acid substitution and protein structure 

Notes

Acknowledgments

The supercomputer calculations were supported by the following grants: SB RAS projects No. 130, 39; Russian State Contracts No. P857, 07.514.11.4011 and 07.514.11.4003.

Supplementary material

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References

  1. Afonnikov DA, Medvedev KE, Gunbin KV, Kolchanov NA (2011) Important role of hydrophobic interactions in high-pressure adaptation of proteins. Dokl Biochem Biophys 438:113–116PubMedCrossRefGoogle Scholar
  2. Anisimova M, Gil M, Dufayard JF, Dessimoz C, Gascuel O (2011) Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst Biol 60:685–699PubMedCrossRefGoogle Scholar
  3. Arvestad L (2006) Efficient methods for estimating amino acid replacement rates. J Mol Evol 62:663–673PubMedCrossRefGoogle Scholar
  4. Bayarsaihan D, Ruddle FH (2000) Isolation and characterization of BEN, a member of the TFII-I family of DNA-binding proteins containing distinct helix-loop-helix domains. Proc Natl Acad Sci USA 97:7342–7347PubMedCrossRefGoogle Scholar
  5. Bayarsaihan D, Dunai J, Greally JM, Kawasaki K, Sumiyama K, Enkhmandakh B, Shimizu N, Ruddle FH (2002) Genomic organization of the genes Gtf2ird1, Gtf2i, and Ncf1 at the mouse chromosome 5 region syntenic to the human chromosome 7q11.23 Williams syndrome critical region. Genomics 79:137–143PubMedCrossRefGoogle Scholar
  6. Bayarsaihan D, Makeyev AV, Enkhmandakh B (2012) Epigenetic modulation by TFII-I during embryonic stem cell differentiation. J Cell Biochem. doi: 10.1002/jcb.24202
  7. Beiko RG, Keith JM, Harlow TJ, Ragan MA (2006) Searching for convergence in phylogenetic Markov chain Monte Carlo. Syst Biol 55:553–565PubMedCrossRefGoogle Scholar
  8. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2011) GenBank. Nucleic Acids Res 39:D32–D37PubMedCrossRefGoogle Scholar
  9. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235–242PubMedCrossRefGoogle Scholar
  10. Buckley TR (2002) Model misspecification and probabilistic tests of topology: evidence from empirical data sets. Syst Biol 51:509–523PubMedCrossRefGoogle Scholar
  11. Caraveo G, van Rossum DB, Patterson RL, Snyder SH, Desiderio S (2006) Action of TFII-I outside the nucleus as an inhibitor of agonist-induced calcium entry. Science 314:122–125PubMedCrossRefGoogle Scholar
  12. Cheriyath V, Roy AL (2001) Structure-function analysis of TFII-I. Roles of the N-terminal end, basic region, and I-repeats. J Biol Chem 276:8377–8383PubMedCrossRefGoogle Scholar
  13. Chimge NO, Mungunsukh O, Ruddle F, Bayarsaihan D (2007a) Expression profiling of BEN regulated genes in mouse embryonic fibroblasts. J Exp Zool B Mol Dev Evol 308:209–224PubMedCrossRefGoogle Scholar
  14. Chimge NO, Mungunsukh O, Ruddle F, Bayarsaihan D (2007b) Gene expression analysis of TFII-I modulated genes in mouse embryonic fibroblasts. J Exp Zool B Mol Dev Evol 308:225–235PubMedCrossRefGoogle Scholar
  15. Chimge NO, Makeyev AV, Ruddle FH, Bayarsaihan D (2008) Identification of the TFII-I family target genes in the vertebrate genome. Proc Natl Acad Sci USA 105:9006–9010PubMedCrossRefGoogle Scholar
  16. Chimge NO, Makeyev AV, Waigel SJ, Enkhmandakh B, Bayarsaihan D (2012) PI3 K/Akt-dependent functions of TFII-I transcription factors in mouse embryonic stem cells. J Cell Biochem 113:1122–1131PubMedCrossRefGoogle Scholar
  17. Crusselle-Davis VJ, Zhou Z, Anantharaman A, Moghimi B, Dodev T, Huang S, Bungert J (2007) Recruitment of coregulator complexes to the beta-globin gene locus by TFII-I and upstream stimulatory factor. FEBS J 274:6065–6073PubMedCrossRefGoogle Scholar
  18. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165PubMedCrossRefGoogle Scholar
  19. Doi-Katayama Y, Hayashi F, Inoue M, Yabuki T, Aoki M, Seki E, Matsuda T, Kigawa T, Yoshida M, Shirouzu M, Terada T, Hayashizaki Y, Yokoyama S, Hirota H (2007) Solution structure of the general transcription factor 2I domain in mouse TFII-I protein. Protein Sci 16:1788–1792PubMedCrossRefGoogle Scholar
  20. Enkhmandakh B, Makeyev AV, Erdenechimeg L, Ruddle FH, Chimge NO, Tussie-Luna MI, Roy AL, Bayarsaihan D (2009) Essential functions of the Williams-Beuren syndrome-associated TFII-I genes in embryonic development. Proc Natl Acad Sci USA 106:181–186PubMedCrossRefGoogle Scholar
  21. Fletcher W, Yang Z (2009) INDELible: a flexible simulator of biological sequence evolution. Mol Biol Evol 26:1879–1888PubMedCrossRefGoogle Scholar
  22. Flicek P, Amode MR, Barrell D, Beal K, Brent S, Chen Y, Clapham P, Coates G, Fairley S, Fitzgerald S, Gordon L, Hendrix M, Hourlier T, Johnson N, Kähäri A, Keefe D, Keenan S, Kinsella R, Kokocinski F, Kulesha E, Larsson P, Longden I, McLaren W, Overduin B, Pritchard B, Riat HS, Rios D, Ritchie GR, Ruffier M, Schuster M, Sobral D, Spudich G, Tang YA, Trevanion S, Vandrovcova J, Vilella AJ, White S, Wilder SP, Zadissa A, Zamora J, Aken BL, Birney E, Cunningham F, Dunham I, Durbin R, Fernández-Suarez XM, Herrero J, Hubbard TJ, Parker A, Proctor G, Vogel J, Searle SM (2011) Ensembl 2011. Nucleic Acids Res 39:D800–D806PubMedCrossRefGoogle Scholar
  23. Forslund K, Huson DH, Moulton V (2004) VisRD–visual recombination detection. Bioinformatics 20:3654–3655PubMedCrossRefGoogle Scholar
  24. Franke Y, Peoples RJ, Francke U (1999) Identification of GTF2IRD1, a putative transcription factor within the Williams–Beuren syndrome deletion at 7q11.23. Cytogenet Cell Genet 86:296–304PubMedCrossRefGoogle Scholar
  25. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321PubMedCrossRefGoogle Scholar
  26. Gunbin KV, Suslov VV, Turnaev II, Afonnikov DA, Kolchanov NA (2011) Molecular evolution of cyclin proteins in animals and fungi. BMC Evol Biol 11:224PubMedCrossRefGoogle Scholar
  27. Gunbin KV, Suslov VV, Genaev MA, Afonnikov DA (2012) Computer System for Analysis of Molecular Evolution Modes (SAMEM): analysis of molecular evolution modes at deep inner branches of the phylogenetic tree. In Silico Biol 11(3–4):109–23. doi: 10.3233/ISB-2012-0446
  28. Han MV, Zmasek CM (2009) phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinformatics 10:356PubMedCrossRefGoogle Scholar
  29. Hedges BS (2009) Vertebrates (Vertebrata). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, New York, pp 309–314Google Scholar
  30. Hobolth A, Christensen OF, Mailund T, Schierup MH (2007) Genomic relationships and speciation times of human, chimpanzee, and gorilla inferred from a coalescent hidden Markov model. PLoS Genet 3:e7PubMedCrossRefGoogle Scholar
  31. Howard ML, Palmer SJ, Taylor KM, Arthurson GJ, Spitzer MW, Du X, Pang TY, Renoir T, Hardeman EC, Hannan AJ (2012) Mutation of Gtf2ird1 from the Williams–Beuren syndrome critical region results in facial dysplasia, motor dysfunction, and altered vocalisations. Neurobiol Dis 45:913–922PubMedCrossRefGoogle Scholar
  32. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  33. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267PubMedCrossRefGoogle Scholar
  34. Huson DH, Rupp R (2008) Summarizing multiple gene trees using cluster networks, algorithms in bioinformatics. Lect Notes Comput Sci 5251(2008):296–305CrossRefGoogle Scholar
  35. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R (2007) Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8:460PubMedCrossRefGoogle Scholar
  36. Huson DH, Rupp R, Berry V, Gambette P, Paul C (2009) Computing galled networks from real data. Bioinformatics 25:i85–i93PubMedCrossRefGoogle Scholar
  37. Imamura H, Karro JE, Chuang JH (2009) Weak preservation of local neutral substitution rates across mammalian genomes. BMC Evol Biol 9:89PubMedCrossRefGoogle Scholar
  38. Inberg A, Linial M (2010) Protection of pancreatic beta-cells from various stress conditions is mediated by DJ-1. J Biol Chem 285:25686–25698PubMedCrossRefGoogle Scholar
  39. Jackson TA, Taylor HE, Sharma D, Desiderio S, Danoff SK (2005) Vascular endothelial growth factor receptor-2: counter-regulation by the transcription factors, TFII-I and TFII-IRD1. J Biol Chem 280:29856–29863PubMedCrossRefGoogle Scholar
  40. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282PubMedGoogle Scholar
  41. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577–2637PubMedCrossRefGoogle Scholar
  42. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277–D280PubMedCrossRefGoogle Scholar
  43. Kawashima S, Pokarowski P, Pokarowska M, Kolinski A, Katayama T, Kanehisa M (2008) AAindex: amino acid index database, progress report 2008. Nucleic Acids Res 36:D202–D205PubMedCrossRefGoogle Scholar
  44. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, Mclnerney JO (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6:29PubMedCrossRefGoogle Scholar
  45. Kelley LA, Sternberg MJ (2009) Protein structure prediction on the web: a case study using the Phyre server. Nat Protoc 4:363–371PubMedCrossRefGoogle Scholar
  46. Lartillot N, Philippe H (2004) A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol 21:1095–1109PubMedCrossRefGoogle Scholar
  47. Lartillot N, Lepage T, Blanquart S (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25:2286–2288PubMedCrossRefGoogle Scholar
  48. Lazebnik MB, Tussie-Luna MI, Roy AL (2008) Determination and functional analysis of the consensus binding site for TFII-I family member BEN, implicated in Williams–Beuren syndrome. J Biol Chem 283:11078–11082PubMedCrossRefGoogle Scholar
  49. Lazebnik MB, Tussie-Luna MI, Hinds PW, Roy AL (2009) Williams-Beuren syndrome-associated transcription factor TFII-I regulates osteogenic marker genes. J Biol Chem 284:36234–36239PubMedCrossRefGoogle Scholar
  50. Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320PubMedCrossRefGoogle Scholar
  51. Letunic I, Bork P (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:W475–W478PubMedCrossRefGoogle Scholar
  52. Lucena J, Pezzi S, Aso E, Valero MC, Carreiro C, Dubus P, Sampaio A, Segura M, Barthelemy I, Zindel MY, Sousa N, Barbero JL, Maldonado R, Perez-Jurado LA, Campuzano V (2010) Essential role of the N-terminal region of TFII-I in viability and behavior. BMC Med Genet 11:61PubMedCrossRefGoogle Scholar
  53. Makeyev AV, Bayarsaihan D (2009) Alternative splicing and promoter use in TFII-I genes. Gene 433:16–25PubMedCrossRefGoogle Scholar
  54. Makeyev AV, Bayarsaihan D (2011) Molecular basis of Williams–Beuren syndrome: TFII-I regulated targets involved in craniofacial development. Cleft Palate Craniofac J 48:109–116PubMedCrossRefGoogle Scholar
  55. Makeyev AV, Erdenechimeg L, Mungunsukh O, Roth JJ, Enkhmandakh B, Ruddle FH, Bayarsaihan D (2004) GTF2IRD2 is located in the Williams–Beuren syndrome critical region 7q11.23 and encodes a protein with two TFII-I-like helix-loop-helix repeats. Proc Natl Acad Sci USA 101:11052–11057PubMedCrossRefGoogle Scholar
  56. Malcolm T, Chen J, Chang C, Sadowski I (2007) Induction of chromosomally integrated HIV-1 LTR requires RBF-2 (USF/TFII-I) and Ras/MAPK signaling. Virus Genes 35:215–223PubMedCrossRefGoogle Scholar
  57. Malcolm T, Kam J, Pour PS, Sadowski I (2008) Specific interaction of TFII-I with an upstream element on the HIV-1 LTR regulates induction of latent provirus. FEBS Lett 582:3903–3908PubMedCrossRefGoogle Scholar
  58. Malenfant P, Liu X, Hudson ML, Qiao Y, Hrynchak M, Riendeau N, Hildebrand MJ, Cohen IL, Chudley AE, Forster-Gibson C, Mickelson EC, Rajcan-Separovic E, Lewis ME, Holden JJ (2012) Association of GTF2i in the Williams–Beuren syndrome critical region with autism spectrum disorders. J Autism Dev Disord 42:1459–1469PubMedCrossRefGoogle Scholar
  59. Mammoto A, Connor KM, Mammoto T, Yung CW, Huh D, Aderman CM, Mostoslavsky G, Smith LE, Ingber DE (2009) A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457:1103–1108PubMedCrossRefGoogle Scholar
  60. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463PubMedCrossRefGoogle Scholar
  61. Meredith RW, Janecka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ (2011) Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334:521–524PubMedCrossRefGoogle Scholar
  62. Mervis CB, Dida J, Lam E, Crawford-Zelli NA, Young EJ, Henderson DR, Onay T, Morris CA, Woodruff-Borden J, Yeomans J, Osborne LR (2012) Duplication of GTF2I results in separation anxiety in mice and humans. Am J Hum Genet 90:1064–1070PubMedCrossRefGoogle Scholar
  63. Mobley CM, Sealy L (2000) The Rous sarcoma virus long terminal repeat promoter is regulated by TFII-I. J Virol 74:6511–6519PubMedCrossRefGoogle Scholar
  64. Morikawa N, Clarke TR, Novina CD, Watanabe K, Haqq C, Weiss M, Roy AL, Donahoe PK (2000) Human Mullerian-inhibiting substance promoter contains a functional TFII-I-binding initiator. Biol Reprod 63:1075–1083PubMedCrossRefGoogle Scholar
  65. Murphy WJ, Eizrik E (2009) Placental mammals (Eutheria). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, New York, pp 471–474Google Scholar
  66. Ohazama A, Sharpe PT (2007) TFII-I gene family during tooth development: candidate genes for tooth anomalies in Williams syndrome. Dev Dyn 236:2884–2888PubMedCrossRefGoogle Scholar
  67. O’Leary J, Osborne LR (2011) Global analysis of gene expression in the developing brain of Gtf2ird1 knockout mice. PLoS ONE 6:e23868PubMedCrossRefGoogle Scholar
  68. Palmer SJ, Santucci N, Widagdo J, Bontempo SJ, Taylor KM, Tay ES, Hook J, Lemckert F, Gunning PW, Hardeman EC (2010) Negative autoregulation of GTF2IRD1 in Williams–Beuren syndrome via a novel DNA binding mechanism. J Biol Chem 285:4715–4724PubMedCrossRefGoogle Scholar
  69. Pei J, Tang M, Grishin NV (2008) PROMALS3D web server for accurate multiple protein sequence and structure alignments. Nucleic Acids Res 36:W30–W34PubMedCrossRefGoogle Scholar
  70. Poitras L, Yu M, Lesage-Pelletier C, Macdonald RB, Gagne JP, Hatch G, Kelly I, Hamilton SP, Rubenstein JL, Poirier GG, Ekker M (2010) An SNP in an ultra conserved regulatory element affects Dlx5/Dlx6 regulation in the forebrain. Development 137:3089–3097PubMedCrossRefGoogle Scholar
  71. Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutiérrez EL, Dubchak I, Garcia-Fernàndez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin-I T, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071PubMedCrossRefGoogle Scholar
  72. Rambaut A, Drummond AJ (2009) Tracer v1.5. http://beast.bio.ed.ac.uk/Tracer
  73. Ren X, Siegel R, Kim U, Roeder RG (2011) Direct interactions of OCA-B and TFII-I regulate immunoglobulin heavy-chain gene transcription by facilitating enhancer-promoter communication. Mol Cell 42:342–355PubMedCrossRefGoogle Scholar
  74. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  75. Roy AL (2006) Transcription factor TFII-I conducts a cytoplasmic orchestra. ACS Chem Biol 1:619–622PubMedCrossRefGoogle Scholar
  76. Roy AL (2012) Biochemistry and biology of the inducible multifunctional transcription factor TFII-I: 10 years later. Gene 492:32–41PubMedCrossRefGoogle Scholar
  77. Roy AL, Du H, Gregor PD, Novina CD, Martinez E, Roeder RG (1997) Cloning of an inr- and E-box-binding protein, TFII-I, that interacts physically and functionally with USF1. EMBO J 16:7091–7104PubMedCrossRefGoogle Scholar
  78. Sacristan C, Schattgen SA, Berg LJ, Bunnell SC, Roy AL, Rosenstein Y (2009) Characterization of a novel interaction between transcription factor TFII-I and the inducible tyrosine kinase in T cells. Eur J Immunol 39:2584–2595PubMedCrossRefGoogle Scholar
  79. Sakurai T, Dorr NP, Takahashi N, McInnes LA, Elder GA, Buxbaum JD (2011) Haploinsufficiency of Gtf2i, a gene deleted in Williams syndrome, leads to increases in social interactions. Autism Res 4:28–39PubMedCrossRefGoogle Scholar
  80. Schneider T, Skitt Z, Liu Y, Deacon RM, Flint J, Karmiloff-Smith A, Rawlins NJ, Tassabehji M (2012) Anxious, hypoactive phenotype combined with motor deficits in Gtf2ird1 null mouse model relevant to Williams syndrome. Behav Brain Res 233:458–473PubMedCrossRefGoogle Scholar
  81. Tapia-Paez I, Tammimies K, Massinen S, Roy AL, Kere J (2008) The complex of TFII-I, PARP1, and SFPQ proteins regulates the DYX1C1 gene implicated in neuronal migration and dyslexia. FASEB J 22:3001–3009PubMedCrossRefGoogle Scholar
  82. Tay ES, Guven KL, Subramaniam N, Polly P, Issa LL, Gunning PW, Hardeman EC (2003) Regulation of alternative splicing of Gtf2ird1 and its impact on slow muscle promoter activity. Biochem J 374:359–367PubMedCrossRefGoogle Scholar
  83. Tipney HJ, Hinsley TA, Brass A, Metcalfe K, Donnai D, Tassabehji M (2004) Isolation and characterisation of GTF2IRD2, a novel fusion gene and member of the TFII-I family of transcription factors, deleted in Williams–Beuren syndrome. Eur J Hum Genet 12:551–560PubMedCrossRefGoogle Scholar
  84. Tomii K, Kanehisa M (1996) Analysis of amino acid indices and mutation matrices for sequence comparison and structure prediction of proteins. Protein Eng 9:27–36PubMedCrossRefGoogle Scholar
  85. Tussie-Luna MI, Bayarsaihan D, Seto E, Ruddle FH, Roy AL (2002) Physical and functional interactions of histone deacetylase 3 with TFII-I family proteins and PIASxbeta. Proc Natl Acad Sci USA 99:12807–12812PubMedCrossRefGoogle Scholar
  86. Venkatesh B, Kirkness EF, Loh YH, Halpern AL, Lee AP, Johnson J, Dandona N, Viswanathan LD, Tay A, Venter JC, Strausberg RL, Brenner S (2007) Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLoS Biol 5:e101PubMedCrossRefGoogle Scholar
  87. Vullhorst D, Buonanno A (2005) Multiple GTF2I-like repeats of general transcription factor 3 exhibit DNA binding properties. Evidence for a common origin as a sequence-specific DNA interaction module. J Biol Chem 280:31722–31731PubMedCrossRefGoogle Scholar
  88. Wen YD, Cress WD, Roy AL, Seto E (2003) Histone deacetylase 3 binds to and regulates the multifunctional transcription factor TFII-I. J Biol Chem 278:1841–1847PubMedCrossRefGoogle Scholar
  89. Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699PubMedCrossRefGoogle Scholar
  90. Yan X, Zhao X, Qian M, Guo N, Zhu X (2000) Characterization and gene structure of a novel retinoblastoma-protein-associated protein similar to the transcription regulator TFII-I. Biochem J 345:749–757PubMedCrossRefGoogle Scholar
  91. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591PubMedCrossRefGoogle Scholar
  92. Yang W, Desiderio S (1997) BAP-135, a target for Bruton’s tyrosine kinase in response to B cell receptor engagement. Proc Natl Acad Sci USA 94:604–609PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  1. 1.Institute of Cytology and Genetics of Russian Academy of SciencesNovosibirskRussia
  2. 2.University of New EnglandArmidaleAustralia

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