Favorable genomic environments for cis-regulatory evolution: A novel theoretical framework

Seminars in Cell and Developmental Biology

Volumn 57, Issue , 2016, Pages 2-10

  Maeso, Ignacio ^a   Tena, Juan J ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

Chromatin environment; Cis regulation; Enhancer evolution; Enhancer overprinting; Transcription factor binding site (TFBS); Transposable element

Indexed keywords

CHROMATIN; CONCEPTUAL FRAMEWORK; DNA SEQUENCE; DNA STRUCTURE; ENHANCER REGION; GENE CONTROL; GENE EXPRESSION; MODEL; TRANSPOSON; ANIMAL; BIOLOGICAL MODEL; GENETICS; GENOME; HUMAN; MOLECULAR EVOLUTION; REGULATORY SEQUENCE;

ANIMALS; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENOME; HUMANS; MODELS, GENETIC; REGULATORY SEQUENCES, NUCLEIC ACID;

EID: 84950150832     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2015.12.003     Document Type: Review

References (110)

1. [1] Carroll, S.B., Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:1 (2008), 25–36.
2. [2] Slattery, M., et al. Absence of a simple code: how transcription factors read the genome. Trends Biochem. Sci. 39:9 (2014), 381–399.
3. [3] Todeschini, A.L., Georges, A., Veitia, R.A., Transcription factors: specific DNA binding and specific gene regulation. Trends Genet. 30:6 (2014), 211–219.
4. [4] Villar, D., Flicek, P., Odom, D.T., Evolution of transcription factor binding in metazoans—mechanisms and functional implications. Nat. Rev. Genet. 15:4 (2014), 221–233.
5. [5] Stergachis, A.B., et al. Conservation of trans-acting circuitry during mammalian regulatory evolution. Nature 515:7527 (2014), 365–370.
6. [6] Vierstra, J., et al. Mouse regulatory DNA landscapes reveal global principles of cis-regulatory evolution. Science 346:6212 (2014), 1007–1012.
7. [7] Cotney, J., et al. The evolution of lineage-specific regulatory activities in the human embryonic limb. Cell 154:1 (2013), 185–196.
8. [8] Reilly, S.K., et al. Evolutionary genomics. Evolutionary changes in promoter and enhancer activity during human corticogenesis. Science 347:6226 (2015), 1155–1159.
9. [9] Tena, J.J., et al. Comparative epigenomics in distantly related teleost species identifies conserved cis-regulatory nodes active during the vertebrate phylotypic period. Genome Res. 24:7 (2014), 1075–1085.
10. [10] Villar, D., et al. Enhancer evolution across 20 mammalian species. Cell 160:3 (2015), 554–566.
11. [11] Engstrom, P.G., et al. Genomic regulatory blocks underlie extensive microsynteny conservation in insects. Genome Res. 17:12 (2007), 1898–1908.
12. [12] Irimia, M., et al. Contrasting 5′ and 3′ evolutionary histories and frequent evolutionary convergence in Meis/hth gene structures. Genome Biol. Evol. 3 (2011), 551–564.
13. [13] Irimia, M., et al. Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints. Genome Res. 22:12 (2012), 2356–2367.
14. [14] Kikuta, H., et al. Genomic regulatory blocks encompass multiple neighboring genes and maintain conserved synteny in vertebrates. Genome Res. 17:5 (2007), 545–555.
15. [15] Maeso, I., et al. Deep conservation of cis-regulatory elements in metazoans. Philos. Trans. R. Soc. London, Ser. B: Biol. Sci., 368(1632), 2013, 20130020.
16. [16] Maeso, I., et al. An ancient genomic regulatory block conserved across bilaterians and its dismantling in tetrapods by retrogene replacement. Genome Res. 22:4 (2012), 642–655.
17. [17] Nelson, C.E., Hersh, B.M., Carroll, S.B., The regulatory content of intergenic DNA shapes genome architecture. Genome Biol., 5(4), 2004, R25.
18. [18] Stone, J.R., Wray, G.A., Rapid evolution of cis-regulatory sequences via local point mutations. Mol. Biol. Evol. 18:9 (2001), 1764–1770.
19. [19] Georges, A.B., et al. Generic binding sites, generic DNA-binding domains: where does specific promoter recognition come from?. FASEB J. 24:2 (2010), 346–356.
20. [20] Ballester, B., et al. Multi-species, multi-transcription factor binding highlights conserved control of tissue-specific biological pathways. Elife, 3, 2014, e02626.
21. [21] Robertson, G., et al. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat. Methods 4:8 (2007), 651–657.
22. [22] Fisher, W.W., et al. DNA regions bound at low occupancy by transcription factors do not drive patterned reporter gene expression in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 109:52 (2012), 21330–21335.
23. [23] Sakabe, N.J., Nobrega, M.A., Beyond the ENCODE project: using genomics and epigenomics strategies to study enhancer evolution. Philos. Trans. R. Soc. London, Ser. B Biol. Sci., 368(1632), 2013, 20130022.
24. [24] Pasquali, L., et al. Pancreatic islet enhancer clusters enriched in type 2 diabetes risk-associated variants. Nat. Genet. 46:2 (2014), 136–143.
25. [25] Duque, T., et al. Simulations of enhancer evolution provide mechanistic insights into gene regulation. Mol. Biol. Evol. 31:1 (2014), 184–200.
26. [26] Duque, T., Sinha, S., What does it take to evolve an enhancer?. A simulation-based study of factors influencing the emergence of combinatorial regulation. Genome Biol. Evol. 7:6 (2015), 1415–1431.
27. [27] Levo, M., et al. Unraveling determinants of transcription factor binding outside the core binding site. Genome Res. 25:7 (2015), 1018–1029.
28. [28] Zhou, T., et al. Quantitative modeling of transcription factor binding specificities using DNA shape. Proc. Natl. Acad. Sci. U.S.A. 112:15 (2015), 4654–4659.
29. [29] Becker, P.B., Workman, J.L., Nucleosome remodeling and epigenetics. Cold Spring Harb. Perspect. Biol., 5(9), 2013 a017905.
30. [30] Chen, T., Dent, S.Y., Chromatin modifiers and remodellers: regulators of cellular differentiation. Nat. Rev. Genet. 15:2 (2014), 93–100.
31. [31] Panne, D., The enhanceosome. Curr. Opin. Struct. Biol. 18:2 (2008), 236–242.
32. [32] Wasson, T., Hartemink, A.J., An ensemble model of competitive multi-factor binding of the genome. Genome Res. 19:11 (2009), 2101–2112.
33. [33] Lee, N., Steitz, J.A., Noncoding RNA-guided recruitment of transcription factors: A prevalent but undocumented mechanism?. Bioessays 37:9 (2015), 936–941.
34. [34] Hancock, R., The crowded nucleus. Int. Rev. Cell Mol. Biol. 307 (2014), 15–26.
35. [35] Nolin, F., et al. Changes to cellular water and element content induced by nucleolar stress: investigation by a cryo-correlative nano-imaging approach. Cell. Mol. Life Sci. 70:13 (2013), 2383–2394.
36. [36] Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y., Greenleaf, W.J., Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 10:12 (2013), 1213–1218.
37. [37] Thurman, R.E., et al. The accessible chromatin landscape of the human genome. Nature 489:7414 (2012), 75–82.
38. [38] Bogdanovic, O., et al. Dynamics of enhancer chromatin signatures mark the transition from pluripotency to cell specification during embryogenesis. Genome Res. 22:10 (2012), 2043–2053.
39. [39] Bonn, S., et al. Tissue-specific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development. Nat. Genet. 44:2 (2012), 148–156.
40. [40] Hawkins, R.D., et al. Dynamic chromatin states in human ES cells reveal potential regulatory sequences and genes involved in pluripotency. Cell Res. 21:10 (2011), 1393–1409.
41. [41] Rada-Iglesias, A., et al. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470:7333 (2011), 279–283.
42. [42] Creyghton, M.P., et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. U.S.A. 107:50 (2010), 21931–21936.
43. [43] Kim, T.K., et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 465:7295 (2010), 182–187.
44. [44] Visel, A., Rubin, E.M., Pennacchio, L.A., Genomic views of distant-acting enhancers. Nature 461:7261 (2009), 199–205.
45. [45] Heintzman, N.D., et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:7243 (2009), 108–112.
46. [46] Heintzman, N.D., et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39:3 (2007), 311–318.
47. [47] Schwaiger, M., et al. Evolutionary conservation of the eumetazoan gene regulatory landscape. Genome Res. 24:4 (2014), 639–650.
48. [48] Kim, T.K., Shiekhattar, R., Architectural and functional commonalities between enhancers and promoters. Cell 162:5 (2015), 948–959.
49. [49] Andersson, R., Promoter or enhancer, what's the difference? Deconstruction of established distinctions and presentation of a unifying model. Bioessays 37:3 (2015), 314–323.
50. [50] Koshikawa, S., et al. Gain of cis-regulatory activities underlies novel domains of wingless gene expression in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 112:24 (2015), 7524–7529.
51. [51] Boyd, J.L., et al. Human-chimpanzee differences in a FZD8 enhancer alter cell-cycle dynamics in the developing neocortex. Curr. Biol. 25:6 (2015), 772–779.
52. [52] Rogers, W.A., et al. Recurrent modification of a conserved cis-regulatory element underlies fruit fly pigmentation diversity. PLoS Genet., 9(8), 2013, e1003740.
53. [53] Pearson, J.C., Watson, J.D., Crews, S.T., Drosophila melanogaster Zelda and Single-minded collaborate to regulate an evolutionarily dynamic CNS midline cell enhancer. Dev. Biol. 366:2 (2012), 420–432.
54. [54] Rebeiz, M., et al. Evolutionary origin of a novel gene expression pattern through cooption of the latent activities of existing regulatory sequences. Proc. Natl. Acad. Sci. U.S.A. 108:25 (2011), 10036–10043.
55. [55] Prabhakar, S., et al. Human-specific gain of function in a developmental enhancer. Science 321:5894 (2008), 1346–1350.
56. [56] Eichenlaub, M.P., Ettwiller, L., De novo genesis of enhancers in vertebrates. PLoS Biol., 9(11), 2011, e1001188.
57. [57] Dong, X., et al. Exonic remnants of whole-genome duplication reveal cis-regulatory function of coding exons. Nucleic Acids Res. 38:4 (2010), 1071–1085.
58. [58] Birnbaum, R.Y., et al. Coding exons function as tissue-specific enhancers of nearby genes. Genome Res. 22:6 (2012), 1059–1068.
59. [59] de la Calle-Mustienes, E., et al. A functional survey of the enhancer activity of conserved non-coding sequences from vertebrate Iroquois cluster gene deserts. Genome Res. 15:8 (2005), 1061–1072.
60. [60] McEwen, G.K., et al. Early evolution of conserved regulatory sequences associated with development in vertebrates. PLoS Genet., 5(12), 2009, e1000762.
61. [61] Berman, B.P., et al. Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc. Natl. Acad. Sci. U.S.A. 99:2 (2002), 757–762.
62. [62] Gotea, V., et al. Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res. 20:5 (2010), 565–577.
63. [63] He, X., Duque, T.S., Sinha, S., Evolutionary origins of transcription factor binding site clusters. Mol. Biol. Evol. 29:3 (2012), 1059–1070.
64. [64] Allo, M., et al. Argonaute-1 binds transcriptional enhancers and controls constitutive and alternative splicing in human cells. Proc. Natl. Acad. Sci. U.S.A. 111:44 (2014), 15622–15629.
65. [65] Becker, T.S., Lenhard, B., The random versus fragile breakage models of chromosome evolution: a matter of resolution. Mol. Genet. Genomics 278:5 (2007), 487–491.
66. [66] Peterson, B.K., et al. Big genomes facilitate the comparative identification of regulatory elements. PLoS ONE, 4(3), 2009, e4688.
67. [67] de Wit, E., de Laat, W., A decade of 3C technologies: insights into nuclear organization. Genes Dev. 26:1 (2012), 11–24.
68. [68] Dekker, J., Two ways to fold the genome during the cell cycle: insights obtained with chromosome conformation capture. Epigenet. Chromatin, 7(1), 2014, 25.
69. [69] Gorkin, D.U., Leung, D., Ren, B., The 3D genome in transcriptional regulation and pluripotency. Cell Stem Cell 14:6 (2014), 762–775.
70. [70] Ong, C.T., Corces, V.G., CTCF: an architectural protein bridging genome topology and function. Nat. Rev. Genet. 15:4 (2014), 234–246.
71. [71] Phillips-Cremins, J.E., Corces, V.G., Chromatin insulators: linking genome organization to cellular function. Mol. Cell 50:4 (2013), 461–474.
72. [72] Gomez-Marin, C., et al. Evolutionary comparison reveals that diverging CTCF sites are signatures of ancestral topological associating domains borders. Proc. Natl. Acad. Sci. U.S.A. 112:24 (2015), 7542–7547.
73. [73] Rao, S.S., et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159:7 (2014), 1665–1680.
74. [74] Montavon, T., et al. A regulatory archipelago controls Hox genes transcription in digits. Cell 147:5 (2011), 1132–1145.
75. [75] Gonzalez, F., Duboule, D., Spitz, F., Transgenic analysis of Hoxd gene regulation during digit development. Dev. Biol. 306:2 (2007), 847–859.
76. [76] van Arensbergen, J., van Steensel, B., Bussemaker, H.J., In search of the determinants of enhancer-promoter interaction specificity. Trends Cell Biol. 24:11 (2014), 695–702.
77. [77] Spitz, F., Gonzalez, F., Duboule, D., A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell 113:3 (2003), 405–417.
78. [78] Irimia, M., et al. Ancient cis-regulatory constraints and the evolution of genome architecture. Trends Genet. 29:9 (2013), 521–528.
79. [79] Hong, J.W., Hendrix, D.A., Levine, M.S., Shadow enhancers as a source of evolutionary novelty. Science, 321(5894), 2008, 1314.
80. [80] Tena, J.J., et al. An evolutionarily conserved three-dimensional structure in the vertebrate Irx clusters facilitates enhancer sharing and coregulation. Nat. Commun., 2, 2011, 310.
81. [81] Edelman, L.B., Fraser, P., Transcription factories: genetic programming in three dimensions. Curr. Opin. Genet. Dev. 22:2 (2012), 110–114.
82. [82] Razin, S.V., et al. Transcription factories in the context of the nuclear and genome organization. Nucleic Acids Res. 39:21 (2011), 9085–9092.
83. [83] Cande, J., Goltsev, Y., Levine, M.S., Conservation of enhancer location in divergent insects. Proc. Natl. Acad. Sci. U.S.A. 106:34 (2009), 14414–14419.
84. [84] Hare, E.E., et al. Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation. PLoS Genet., 4(6), 2008, e1000106.
85. [85] Martinez-Morales, J.R., Toward understanding the evolution of vertebrate gene regulatory networks: comparative genomics and epigenomic approaches. Brief. Funct. Genom., 2015, 10.1093/bfgp/elv032.
86. [86] Zaret, K.S., Carroll, J.S., Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25:21 (2011), 2227–2241.
87. [87] Putnam, N.H., et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 453:7198 (2008), 1064–1071.
88. [88] McEwen, G.K., et al. Ancient duplicated conserved noncoding elements in vertebrates: a genomic and functional analysis. Genome Res. 16:4 (2006), 451–465.
89. [89] Irimia, M., Maeso, I., Garcia-Fernandez, J., Convergent evolution of clustering of Iroquois homeobox genes across metazoans. Mol. Biol. Evol. 25:8 (2008), 1521–1525.
90. [90] Jimenez-Delgado, S., et al. Evolutionary genomics of the recently duplicated amphioxus Hairy genes. Int. J. Biol. Sci. 2:2 (2006), 66–72.
91. [91] Fort, A., et al. Deep transcriptome profiling of mammalian stem cells supports a regulatory role for retrotransposons in pluripotency maintenance. Nat. Genet. 46:6 (2014), 558–566.
92. [92] Gifford, W.D., Pfaff, S.L., Macfarlan, T.S., Transposable elements as genetic regulatory substrates in early development. Trends Cell Biol. 23:5 (2013), 218–226.
93. [93] Macfarlan, T.S., et al. Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487:7405 (2012), 57–63.
94. [94] Schmidt, D., et al. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148:1–2 (2012), 335–348.
95. [95] Kunarso, G., et al. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 42:7 (2010), 631–634.
96. [96] Bourque, G., Transposable elements in gene regulation and in the evolution of vertebrate genomes. Curr. Opin. Genet. Dev. 19:6 (2009), 607–612.
97. [97] Bourque, G., et al. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res. 18:11 (2008), 1752–1762.
98. [98] Sundaram, V., et al. Widespread contribution of transposable elements to the innovation of gene regulatory networks. Genome Res. 24:12 (2014), 1963–1976.
99. [99] Richardson, S.R., et al. The Influence of LINE-1 and SINE Retrotransposons on Mammalian Genomes. Microbiol. Spectr., 3(2), 2015 MDNA3-0061-2014.
100. [100] Lynch, V.J., et al. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet. 43:11 (2011), 1154–1159.
101. [101] Notwell, J.H., et al. A family of transposable elements co-opted into developmental enhancers in the mouse neocortex. Nat. Commun., 6, 2015, 6644.
102. [102] Lynch, V.J., et al. Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep. 10:4 (2015), 551–561.
103. [103] Domene, S., et al. Enhancer turnover and conserved regulatory function in vertebrate evolution. Philos. Trans. R. Soc. London, Ser. B Biol. Sci., 368(1632), 2013, 20130027.
104. [104] Emera, D., et al. Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol. Biol. Evol. 29:1 (2012), 239–247.
105. [105] Sasaki, T., et al. Possible involvement of SINEs in mammalian-specific brain formation. Proc. Natl. Acad. Sci. U.S.A. 105:11 (2008), 4220–4225.
106. [106] Bejerano, G., et al. A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature 441:7089 (2006), 87–90.
107. [107] Vietri Rudan, M., et al. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep. 10:8 (2015), 1297–1309.
108. [108] Farre, M., Robinson, T.J., Ruiz-Herrera, A., An Integrative Breakage Model of genome architecture, reshuffling and evolution: the Integrative Breakage Model of genome evolution, a novel multidisciplinary hypothesis for the study of genome plasticity. Bioessays 37:5 (2015), 479–488.
109. [109] Irimia, M., et al. Comparative genomics of the Hedgehog loci in chordates and the origins of Shh regulatory novelties. Sci. Rep.(2), 2012, 433.
110. [110] Lettice, L.A., et al. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum. Mol. Genet. 12:14 (2003), 1725–1735.