Evolution of the vertebrate gene regulatory network controlled by the transcriptional repressor REST

Molecular Biology and Evolution

Volumn 26, Issue 7, 2009, Pages 1491-1507

  Johnson, Rory ^a   Samuel, John ^b   Ng, Calista Keow Leng ^a   Jauch, Ralf ^a   Stanton, Lawrence W ^a   Wood, Ian C ^b  

^a GENOME INSTITUTE OF SINGAPORE   (Singapore)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Evolution; Gene regulation; Human specific; Lineage specific; Motif; Network; Neural gene; NRSF; Primate; Primate specific; RE1; REST; Transcription factor binding

Indexed keywords

REPRESSOR ELEMENT 1 SILENCING TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ACCURACY; ARTICLE; BINDING AFFINITY; BINDING SITE; COMPARATIVE STUDY; CONTROLLED STUDY; EVOLUTION; GENE CONTROL; GENE REGULATORY NETWORK; GENE TARGETING; GENOMICS; HUMAN; METHODOLOGY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN MOTIF; REPRESSOR GENE; VERTEBRATE;

ANIMALS; BASE SEQUENCE; DNA-BINDING PROTEINS; GENE REGULATORY NETWORKS; GENOME; GENOME, HUMAN; HUMANS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PROTEIN BINDING; REPRESSOR PROTEINS; SEQUENCE ALIGNMENT; VERTEBRATES;

PRIMATES; VERTEBRATA;

EID: 67649313831     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp058     Document Type: Article

References (66)

1. Ballas N, Grunseich C, Lu DD, Speh JC, Mandel G. 2005. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell. 121:645-657.
2. Belyaev ND, Wood IC, Bruce AW, Street M, Trinh J-B, Buckley NJ. 2004. Distinct RE-1 silencing transcription factor-containing complexes interact with different target genes. 10.1074/jbc.M310353200. J Biol Chem. 279:556-561.
3. Berg OG, von Hippel PH. 1987. Selection of DNA binding sites by regulatory proteins. Statistical-mechanical theory and application to operators and promoters. J Mol Biol. 193:723-750.
4. Blanchette M, Kent WJ, Riemer C, et al. (11 co-authors). 2004. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res. 14:708-715.
5. Britten RJ, Davidson EH. 1969. Gene regulation for higher cells: a theory. Science. 165:349-357.
6. Bruce AW, Donaldson IJ, Wood IC, Yerbury SA, Sadowski MI, Chapman M, Gottgens B, Buckley NJ. 2004. Genome-wide analysis of repressor element 1 silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) target genes. 10.1073/pnas.0401827101. Proc Natl Acad Sci USA. 101:10458-10463.
7. Bustamante CD, Fledel-Alon A, Williamson S, et al. (13 coauthors). 2005. Natural selection on protein-coding genes in the human genome. Nature. 437:1153-1157.
8. Chen K, Rajewsky N. 2006. Natural selection on human microRNA binding sites inferred from SNP data. Nat Genet. 38:1452-1456.
9. Chen X, Xu H, Yuan P. (22 co-authors). 2008. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell. 133:1106-1117.
10. Chen Z-F, Paquette AJ, Anderson DJ. 1998. NRSF/REST is required in vivo for repression of multiple neuronal target genes during embryogenesis. Nat Genet. 20:136-142.
11. Cheong A, Bingham A, Li J, et al. (10 co-authors). 2005. Downregulated REST transcription factor is a switch enabling critical potassium channel expression and cell proliferation. Mol Cell. 20:45-52.
12. Chong J, Tapia-Ramirez J, Kim S, Toledo-Aral J, Zheng Y, Boutros M, Altshuller Y, Frohman M, Kraner S, Mandel G. 1995. REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell. 80:949-957.
13. Chou HH, Takematsu H, Diaz S, Iber J, Nickerson E, Wright KL, Muchmore EA, Nelson DL, Warren ST, Varki A. 1998. A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc Natl Acad Sci USA. 95:11751-11756.
14. Cuddapah S, Jothi R, Schones DE, Roh TY, Cui K, Zhao K. 2009. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res. 19:24-32.
15. Dorus S, Vallender EJ, Evans PD, Anderson JR, Gilbert SL, Mahowald M, Wyckoff GJ, Malcom CM, Lahn BT. 2004. Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell. 119:1027-1040.
16. Enard W, Khaitovich P, Klose J, et al. (13 co-authors). 2002. Intra- and interspecific variation in primate gene expression patterns. Science. 296:340-343.
17. Enard W, Przeworski M, Fisher SE, Lai CS, Wiebe V, Kitano T, Monaco AP, Paabo S. 2002. Molecular evolution of FOXP2, a gene involved in speech and language. Nature. 418:869-872.
18. Evans PD, Anderson JR, Vallender EJ, Gilbert SL, Malcom CM, Dorus S, Lahn BT. 2004. Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans. Hum Mol Genet. 13:489-494.
19. Evans PD, Gilbert SL, Mekel-Bobrov N, Vallender EJ, Anderson JR, Vaez-Azizi LM, Tishkoff SA, Hudson RR, Lahn BT. 2005. Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science. 309:1717-1720.
20. Feschotte C. 2008. Transposable elements and the evolution of regulatory networks. Nat Rev Genet. 9:397-405.
21. Field Y, Kaplan N, Fondufe-Mittendorf Y, Moore IK, Sharon E, Lubling Y, Widom J, Segal E. 2008. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput Biol. 4:e1000216.
22. Giardine B, Riemer C, Hardison RC, et al. (12 co-authors). 2005. Galaxy: a platform for interactive large-scale genome analysis. Genome Res. 15:1451-1455.
23. Gompel N, Prud'homme B, Wittkopp PJ, Kassner VA, Carroll SB. 2005. Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature. 433:481-487.
24. Greenway DJ, Street M, Jeffries A, Buckley NJ. 2007. RE1 silencing transcription factor maintains a repressive chromatin environment in embryonic hippocampal neural stem cells 10.1634/stemcells.2006-0207. Stem Cells. 25:354-363.
25. Hoekstra HE, Coyne JA. 2007. The locus of evolution: evo devo and the genetics of adaptation. Evolution. 61:995-1016.
26. Jauch R, Ng CK, Saikatendu KS, Stevens RC, Kolatkar PR. 2008. Crystal structure and DNA binding of the homeodomain of the stem cell transcription factor Nanog. J Mol Biol. 376:758-770.
27. Johnson D, Mortazavi A, Myers R, Wold B. 2007. Genome-wide mapping of in vivo protein-DNA interactions. Science. 316:1497-1502.
28. Johnson R, Gamblin RJ, Ooi L, Bruce AW, Donaldson IJ, Westhead DR, Wood IC, Jackson RM, Buckley NJ. 2006. Identification of the REST regulon reveals extensive transposable element-mediated binding site duplication. 10.1093/nar/gkl525. Nucl Acids Res. 34:3862-3877.
29. Johnson R, Teh CHI, Kunarso G, et al. (13 co-authors). 2008. REST regulates distinct transcriptional networks in embryonic and neural stem cells. PLoS Biol. 6:e256.
30. Jordan IK, Rogozin IB, Glazko GV, Koonin EV. 2003. Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet. 19:68-72.
31. Karolchik D, Kuhn RM, Baertsch R, et al. (24 co-authors). 2008. The UCSC Genome Browser Database: 2008 update. Nucleic Acids Res. 36:D773-D779.
32. Kim SY, Pritchard JK. 2007. Adaptive evolution of conserved noncoding elements in mammals. PLoS Genet. 3:1572-1586.
33. King MC, Wilson AC. 1975. Evolution at two levels in humans and chimpanzees. Science. 188:107-116.
34. Kumar S, Filipski A. 2007.Multiple sequence alignment: in pursuit of homologous DNA positions. Genome Res. 17:127-135.
35. Kuwabara T, Hsieh J, Nakashima K, Warashina M, Taira K, Gage FH. 2005. The NRSE smRNA specifies the fate of adult hippocampal neural stem cells. Nucleic Acids Symp Ser (Oxf). 87-88.
36. Kuwahara K, Saito Y, Takano M, et al. (22 co-authors). 2003. NRSF regulates the fetal cardiac gene program and maintains normal cardiac structure and function. EMBO J. 22:6310-6321.
37. Li XY, MacArthur S, Bourgon R, et al. (22 co-authors). 2008. Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol. 6:e27.
38. Loh Y-H, Wu Q, Chew J-L, et al. (22 co-authors). 2006. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Gen. 38:431-440.
39. Mortazavi A, Thompson ECL, Garcia ST, Myers RM, Wold B. 2006. Comparative genomics modeling of the NRSF/REST repressor network: from single conserved sites to genome-wide repertoire. 10.1101/gr.4997306. Genome Res. 16:1208-1221.
40. Moses AM, Chiang DY, Pollard DA, Iyer VN, Eisen MB. 2004. MONKEY: identifying conserved transcription-factor binding sites in multiple alignments using a binding site-specific evolutionary model. Genome Biol. 5:R98.
41. Moses AM, Pollard DA, Nix DA, Iyer VN, Li XY, Biggin MD, Eisen MB. 2006. Large-scale turnover of functional transcription factor binding sites in Drosophila. PLoS Comput Biol. 2:e130.
42. Mullen RD, Colvin SC, Hunter CS, Savage JJ, Walvoord EC, Bhangoo AP, Ten S, Weigel J, Pfaffle RW, Rhodes SJ. 2007. Roles of the LHX3 and LHX4 LIM-homeodomain factors in pituitary development.Mol Cell Endocrinol. 265-266:190-195.
43. Nallamsetty S, Austin BP, Penrose KJ, Waugh DS. 2005. Gateway vectors for the production of combinatorially-tagged His6-MBP fusion proteins in the cytoplasm and periplasm of Escherichia coli. Protein Sci. 14:2964-2971.
44. Nei M, Kumar S. 2000. Molecular evolution and phylogenetics. New York: Oxford University Press.
45. Odom DT, Dowell RD, Jacobsen ES, Gordon W, Danford TW, MacIsaac KD, Rolfe PA, Conboy CM, Gifford DK, Fraenkel E. 2007. Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat Genet. 39:730-732.
46. Ooi L, Belyaev ND, Miyake K, Wood IC, Buckley NJ. 2006. BRG1 chromatin remodeling activity Is required for efficient chromatin binding by repressor element 1-silencing transcription factor (REST) and facilitates REST-mediated repression. J Biol Chem. 281:38974-38980.
47. Ooi L, Wood IC. 2007. Chromatin crosstalk in development and disease: lessons from REST. Nat Rev Genet. 8:544-554.
48. Pheasant M, Mattick JS. 2007. Raising the estimate of functional human sequences. Genome Res. 17:1245-1253.
49. Prabhakar S, Noonan JP, Paabo S, Rubin EM. 2006. Accelerated evolution of conserved noncoding sequences in humans. Science. 314:786.
50. Schoenherr C, Anderson D. 1995. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuronspecific genes. Science. 5202:1360-1363.
51. Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, Moore IK, Wang JP, Widom J. 2006. A genomic code for nucleosome positioning. Nature. 442:772-778.
52. Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS, Jonsson B, Schluter D, Kingsley DM. 2004. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature. 428:717-723.
53. Singh SK, Kagalwala MN, Parker-Thornburg J, Adams H, Majumder S. 2008. REST maintains self-renewal and pluripotency of embryonic stem cells. Nature. 453:223-227.
54. Stone JR, Wray GA. 2001. Rapid evolution of cis-regulatory sequences via local point mutations. Mol Biol Evol. 18:1764-1770.
55. Sun Y-M, Greenway DJ, Johnson R, Street M, Belyaev ND, Deuchars J, Bee T, Wilde S, Buckley NJ. 2005. Distinct profiles of REST interactions with its target genes at different stages of neuronal development. Mol Biol Cell. 16: 5630-5638.
56. Tanay A. 2006. Extensive low-affinity transcriptional interactions in the yeast genome. Genome Res. 16:962-972.
57. Tautz D. 2000. Evolution of transcriptional regulation. Curr Opin Genet Dev. 10:575-579.
58. Tsong AE, Miller MG, Raisner RM, Johnson AD. 2003. Evolution of a combinatorial transcriptional circuit: a case study in yeasts. Cell. 115:389-399.
59. Wang T, Zeng J, Lowe CB, Sellers RG, Salama SR, Yang M, Burgess SM, Brachmann RK, Haussler D. 2007. Speciesspecific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. 10.1073/pnas.0703637104. Proc Natl Acad Sci. 104:18613-18618.
60. Wei CL, Wu Q, Vega VB, et al. (21 co-authors). 2006. A global map of p53 transcription-factor binding sites in the human genome. Cell. 124:207-219.
61. Winter H, Langbein L, Krawczak M, Cooper DN, Jave-Suarez LF, Rogers MA, Praetzel S, Heidt PJ, Schweizer J. 2001. Human type I hair keratin pseudogene phihHaA has functional orthologs in the chimpanzee and gorilla: evidence for recent inactivation of the human gene after the Pan-Homo divergence. Hum Genet. 108:37-42.
62. Wittkopp PJ, Haerum BK, Clark AG. 2004. Evolutionary changes in cis and trans gene regulation. Nature. 430:85-88.
63. Wood IC, Belyaev ND, Bruce AW, Jones C, Mistry M, Roopra A, Buckley NJ. 2003. Interaction of the repressor element 1-silencing transcription factor (REST) with target genes. J Mol Biol. 334:863-874.
64. Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV, Romano LA. 2003. The Evolution of Transcriptional Regulation in Eukaryotes. 10.1093/molbev/msg140. Mol Biol Evol. 20:1377-1419.
65. Wu J, Xie X. 2006. Comparative sequence analysis reveals an intricate network among REST, CREB and miRNA in mediating neuronal gene expression. Genome Biol. 7:R85.
66. Yang Z. 1997. PAML: a programpackage for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556.