Ever-Changing Landscapes: Transcriptional Enhancers in Development and Evolution

Cell

Volumn 167, Issue 5, 2016, Pages 1170-1187

  Long, Hannah K ^a   Prescott, Sara L ^a   Wysocka, Joanna ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCEOSOME;

BINDING SITE; DNA METHYLATION; ENHANCER REGION; GENE CONTROL; GENE CONVERSION; GENE DUPLICATION; GENE EXPRESSION; GENETIC CODE; GENOME ANALYSIS; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION REGULATION; TRANSPOSON; BLOOD; BLOOD CELL; EPIGENETICS; GENETIC TRANSCRIPTION; GENOME-WIDE ASSOCIATION STUDY; HEMATOPOIESIS; HUMAN; METABOLISM; QUANTITATIVE TRAIT LOCUS;

BLOOD; BLOOD CELLS; ENHANCER ELEMENTS, GENETIC; EPIGENOMICS; EVOLUTION, MOLECULAR; GENOME-WIDE ASSOCIATION STUDY; HEMATOPOIESIS; HUMANS; QUANTITATIVE TRAIT LOCI; TRANSCRIPTION, GENETIC;

EID: 84995753074     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.09.018     Document Type: Review

References (153)

1. Abe, N., Dror, I., Yang, L., Slattery, M., Zhou, T., Bussemaker, H.J., Rohs, R., Mann, R.S., Deconvolving the recognition of DNA shape from sequence. Cell 161 (2015), 307–318.
2. Agoglia, R.M., Fraser, H.B., Disentangling sources of selection on exonic transcriptional enhancers. Mol. Biol. Evol. 33 (2016), 585–590.
3. Allan, C.M., Walker, D., Taylor, J.M., Evolutionary duplication of a hepatic control region in the human apolipoprotein E gene locus. Identification of a second region that confers high level and liver-specific expression of the human apolipoprotein E gene in transgenic mice. J. Biol. Chem. 270 (1995), 26278–26281.
4. Arnold, C.D., Gerlach, D., Spies, D., Matts, J.A., Sytnikova, Y.A., Pagani, M., Lau, N.C., Stark, A., Quantitative genome-wide enhancer activity maps for five Drosophila species show functional enhancer conservation and turnover during cis-regulatory evolution. Nat. Genet. 46 (2014), 685–692.
5. Arnosti, D.N., Kulkarni, M.M., Transcriptional enhancers: Intelligent enhanceosomes or flexible billboards?. J. Cell. Biochem. 94 (2005), 890–898.
6. Arnosti, D.N., Barolo, S., Levine, M., Small, S., The eve stripe 2 enhancer employs multiple modes of transcriptional synergy. Development 122 (1996), 205–214.
7. Barolo, S., Shadow enhancers: frequently asked questions about distributed cis-regulatory information and enhancer redundancy. BioEssays 34 (2012), 135–141.
8. Bartman, C.R., Hsu, S.C., Hsiung, C.C.S., Raj, A., Blobel, G.A., Enhancer Regulation of Transcriptional Bursting Parameters Revealed by Forced Chromatin Looping. Mol. Cell 62 (2016), 237–247.
9. Birnbaum, R.Y., Clowney, E.J., Agamy, O., Kim, M.J., Zhao, J., Yamanaka, T., Pappalardo, Z., Clarke, S.L., Wenger, A.M., Nguyen, L., et al. Coding exons function as tissue-specific enhancers of nearby genes. Genome Res. 22 (2012), 1059–1068.
10. Blow, M.J., McCulley, D.J., Li, Z., Zhang, T., Akiyama, J.A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F., et al. ChIP-Seq identification of weakly conserved heart enhancers. Nat. Genet. 42 (2010), 806–810.
11. Boffelli, D., Nobrega, M.A., Rubin, E.M., Comparative genomics at the vertebrate extremes. Nat. Rev. Genet. 5 (2004), 456–465.
12. Bothma, J.P., Garcia, H.G., Ng, S., Perry, M.W., Gregor, T., Levine, M., Enhancer additivity and non-additivity are determined by enhancer strength in the Drosophila embryo. eLife 4 (2015), 1–14.
13. Bourque, G., Leong, B., Vega, V.B., Chen, X., Lee, Y.L., Srinivasan, K.G., Chew, J., Ruan, Y., Wei, C., Ng, H.H., et al. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res. 18 (2008), 1752–1762.
14. Bridges, C.B., Salivary chromosome maps with a key to the banding of the chromosomes of Drosophila melanogaster. J. Hered. 26 (1935), 60–64.
15. Buecker, C., Wysocka, J., Enhancers as information integration hubs in development: lessons from genomics. Trends Genet. 28 (2012), 276–284.
16. Burz, D.S., Rivera-Pomar, R., Jäckle, H., Hanes, S.D., Cooperative DNA-binding by Bicoid provides a mechanism for threshold-dependent gene activation in the Drosophila embryo. EMBO J. 17 (1998), 5998–6009.
17. Calo, E., Wysocka, J., Modification of enhancer chromatin: what, how, and why?. Mol. Cell 49 (2013), 825–837.
18. Cande, J.D., Chopra, V.S., Levine, M., Evolving enhancer-promoter interactions within the tinman complex of the flour beetle, Tribolium castaneum. Development 136 (2009), 3153–3160.
19. Carroll, S.B., Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134 (2008), 25–36.
20. Chuong, E.B., Elde, N.C., Feschotte, C., Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 351 (2016), 1083–1087.
21. Crane, E., Bian, Q., McCord, R.P., Lajoie, B.R., Wheeler, B.S., Ralston, E.J., Uzawa, S., Dekker, J., Meyer, B.J., Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature 523 (2015), 240–244.
22. Cretekos, C.J., Wang, Y., Green, E.D., Martin, J.F., Rasweiler, J.J. 4th, Behringer, R.R., Regulatory divergence modifies limb length between mammals. Genes Dev. 22 (2008), 141–151.
23. Crocker, J., Abe, N., Rinaldi, L., McGregor, A.P., Frankel, N., Wang, S., Alsawadi, A., Valenti, P., Plaza, S., Payre, F., et al. Low affinity binding site clusters confer hox specificity and regulatory robustness. Cell 160 (2015), 191–203.
24. de Wit, E., de Laat, W., A decade of 3C technologies: insights into nuclear organization. Genes Dev. 26 (2012), 11–24.
25. Dib, S., Denarier, E., Dionne, N., Beaudoin, M., Friedman, H.H., Peterson, A.C., Regulatory modules function in a non-autonomous manner to control transcription of the mbp gene. Nucleic Acids Res. 39 (2011), 2548–2558.
26. Dixon, J.R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J.S., Ren, B., Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485 (2012), 376–380.
27. Dowen, J.M., Fan, Z.P., Hnisz, D., Ren, G., Abraham, B.J., Zhang, L.N., Weintraub, A.S., Schuijers, J., Lee, T.I., Zhao, K., Young, R.A., Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 159 (2014), 374–387.
28. Duncan, B.K., Miller, J.H., Mutagenic deamination of cytosine residues in DNA. Nature 287 (1980), 560–561.
29. Dunipace, L., Ozdemir, A., Stathopoulos, A., Complex interactions between cis-regulatory modules in native conformation are critical for Drosophila snail expression. Development 138 (2011), 4075–4084.
30. 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 (2015), 1415–1431.
31. Eagen, K.P., Hartl, T.A., Kornberg, R.D., Stable Chromosome Condensation Revealed by Chromosome Conformation Capture. Cell 163 (2015), 934–946.
32. El-Sherif, E., Levine, M., Shadow enhancers mediate dynamic shifts of gap gene expression in the Drosophila embryo. Curr. Biol. 26 (2016), 1164–1169.
33. Erceg, J., Saunders, T.E., Girardot, C., Devos, D.P., Hufnagel, L., Furlong, E.E., Subtle changes in motif positioning cause tissue-specific effects on robustness of an enhancer's activity. PLoS Genet., 10, 2014, e1004060.
34. Fabre, P.J., Benke, A., Joye, E., Nguyen Huynh, T.H., Manley, S., Duboule, D., Nanoscale spatial organization of the HoxD gene cluster in distinct transcriptional states. Proc. Natl. Acad. Sci. USA 112 (2015), 13964–13969.
35. Farley, E.K., Olson, K.M., Zhang, W., Brandt, A.J., Rokhsar, D.S., Levine, M.S., Suboptimization of developmental enhancers. Science 350 (2015), 325–328.
36. Farré, 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 (2015), 479–488.
37. Feng, S., Cokus, S.J., Schubert, V., Zhai, J., Pellegrini, M., Jacobsen, S.E., Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol. Cell 55 (2014), 694–707.
38. Feschotte, C., Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9 (2008), 397–405.
39. Flavahan, W.A., Drier, Y., Liau, B.B., Gillespie, S.M., Venteicher, A.S., Stemmer-Rachamimov, A.O., Suvà, M.L., Bernstein, B.E., Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature 529 (2016), 110–114.
40. Frankel, N., Davis, G.K., Vargas, D., Wang, S., Payre, F., Stern, D.L., Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 466 (2010), 490–493.
41. Frankel, N., Erezyilmaz, D.F., McGregor, A.P., Wang, S., Payre, F., Stern, D.L., Morphological evolution caused by many subtle-effect substitutions in regulatory DNA. Nature 474 (2011), 598–603.
42. Fudenberg, G., Imakaev, M., Lu, C., Goloborodko, A., Abdennur, N., Mirny, L.A., Formation of Chromosomal Domains by Loop Extrusion. Cell Rep. 15 (2015), 2038–2049.
43. Fukaya, T., Lim, B., Levine, M., Enhancer Control of Transcriptional Bursting. Cell 166 (2016), 358–368.
44. Gallego Romero, I., Pavlovic, B.J., Hernando-Herraez, I., Zhou, X., Ward, M.C., Banovich, N.E., Kagan, C.L., Burnett, J.E., Huang, C.H., Mitrano, A., et al. A panel of induced pluripotent stem cells from chimpanzees: a resource for comparative functional genomics. Elife, 4, 2015, e07103.
45. Galtier, N., Duret, L., Adaptation or biased gene conversion? Extending the null hypothesis of molecular evolution. Trends Genet. 23 (2007), 273–277.
46. Giorgetti, L., Galupa, R., Nora, E.P., Piolot, T., Lam, F., Dekker, J., Tiana, G., Heard, E., Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription. Cell 157 (2014), 950–963.
47. Giorgetti, L., Lajoie, B.R., Carter, A.C., Attia, M., Zhan, Y., Xu, J., Chen, C.J., Kaplan, N., Chang, H.Y., Heard, E., Dekker, J., Structural organization of the inactive X chromosome in the mouse. Nature 535 (2016), 575–579.
48. Gómez-Marín, C., Tena, J.J., Acemel, R.D., López-Mayorga, M., Naranjo, S., de la Calle-Mustienes, E., Maeso, I., Beccari, L., Aneas, I., Vielmas, E., et al. Evolutionary comparison reveals that diverging CTCF sites are signatures of ancestral topological associating domains borders. Proc. Natl. Acad. Sci. USA 112 (2015), 7542–7547.
49. Goode, D.K., Callaway, H.A., Cerda, G.A., Lewis, K.E., Elgar, G., Minor change, major difference: divergent functions of highly conserved cis-regulatory elements subsequent to whole genome duplication events. Development 138 (2011), 879–884.
50. Gordân, R., Shen, N., Dror, I., Zhou, T., Horton, J., Rohs, R., Bulyk, M.L., Genomic regions flanking E-box binding sites influence DNA binding specificity of bHLH transcription factors through DNA shape. Cell Rep. 3 (2013), 1093–1104.
51. Grob, S., Schmid, M.W., Grossniklaus, U., Hi-C analysis in Arabidopsis identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. Mol. Cell 55 (2014), 678–693.
52. Grubert, F., Zaugg, J.B., Kasowski, M., Ursu, O., Spacek, D.V., Martin, A.R., Greenside, P., Srivas, R., Phanstiel, D.H., Pekowska, A., et al. Genetic Control of Chromatin States in Humans Involves Local and Distal Chromosomal Interactions. Cell 162 (2015), 1051–1065.
53. Guo, Y., Xu, Q., Canzio, D., Shou, J., Li, J., Gorkin, D.U., Jung, I., Wu, H., Zhai, Y., Tang, Y., et al. CRISPR Inversion of CTCF Sites Alters Genome Topology and Enhancer/Promoter Function. Cell 162 (2015), 900–910.
54. Guturu, H., Doxey, A.C., Wenger, A.M., Bejerano, G., Structure-aided prediction of mammalian transcription factor complexes in conserved non-coding elements. Philos. Trans. R. Soc. Lond. B Biol. Sci., 368, 2013, 20130029.
55. Harmston, N., Ing-simmons, E., Tan, G., Perry, M., Merkenschlager, M., and Lenhard, B. (2016). Topologically associated domains are ancient features that coincide with Metazoan clusters of extreme noncoding conservation. bioRxiv, http://dx.doi.org/10.1101/042952.
56. Hay, D., Hughes, J.R., Babbs, C., Davies, J.O., Graham, B.J., Hanssen, L.L., Kassouf, M.T., Oudelaar, A.M., Sharpe, J.A., Suciu, M.C., et al. Genetic dissection of the α-globin super-enhancer in vivo. Nat. Genet. 48 (2016), 895–903.
57. Heger, P., Marin, B., Bartkuhn, M., Schierenberg, E., Wiehe, T., The chromatin insulator CTCF and the emergence of metazoan diversity. Proc. Natl. Acad. Sci. USA 109 (2012), 17507–17512.
58. Hilton, I.B., D'Ippolito, A.M., Vockley, C.M., Thakore, P.I., Crawford, G.E., Reddy, T.E., Gersbach, C.A., Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat. Biotechnol. 33 (2015), 510–517.
59. Hnisz, D., Abraham, B.J., Lee, T.I., Lau, A., Saint-André, V., Sigova, A.A., Hoke, H.A., Young, R.A., Super-enhancers in the control of cell identity and disease. Cell 155 (2013), 934–947.
60. Hong, J.-W., Hendrix, D.A., Levine, M.S., Shadow enhancers as a source of evolutionary novelty. Science, 321, 2008, 1314.
61. Hsieh, T.-H.S., Weiner, A., Lajoie, B., Dekker, J., Friedman, N., Rando, O.J., Mapping Nucleosome Resolution Chromosome Folding in Yeast by Micro-C. Cell 162 (2015), 108–119.
62. Hou, C., Li, L., Qin, Z.S., Corces, V.G., Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol. Cell 48 (2012), 471–484.
63. Iampietro, C., Gummalla, M., Mutero, A., Karch, F., Maeda, R.K., Initiator elements function to determine the activity state of BX-C enhancers. PLoS Genet., 6, 2010, e1001260.
64. Jacques, P.-É., Jeyakani, J., Bourque, G., The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet., 9, 2013, e1003504.
65. Jolma, A., Yin, Y., Nitta, K.R., Dave, K., Popov, A., Taipale, M., Enge, M., Kivioja, T., Morgunova, E., Taipale, J., DNA-dependent formation of transcription factor pairs alters their binding specificity. Nature 527 (2015), 384–388.
66. Jones, P.A., Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 13 (2012), 484–492.
67. Junion, G., Spivakov, M., Girardot, C., Braun, M., Gustafson, E.H., Birney, E., Furlong, E.E.M., A transcription factor collective defines cardiac cell fate and reflects lineage history. Cell 148 (2012), 473–486.
68. Kearns, N.A., Pham, H., Tabak, B., Genga, R.M., Silverstein, N.J., Garber, M., Maehr, R., Functional annotation of native enhancers with a Cas9-histone demethylase fusion. Nat. Methods 12 (2015), 401–403.
69. Kim, T.-K., Shiekhattar, R., Architectural and Functional Commonalities between Enhancers and Promoters. Cell 162 (2015), 948–959.
70. Kleinjan, D.A., Bancewicz, R.M., Gautier, P., Dahm, R., Schonthaler, H.B., Damante, G., Seawright, A., Hever, A.M., Yeyati, P.L., van Heyningen, V., Coutinho, P., Subfunctionalization of duplicated zebrafish pax6 genes by cis-regulatory divergence. PLoS Genet., 4, 2008, e29.
71. Kolovos, P., Knoch, T.A., Grosveld, F.G., Cook, P.R., Papantonis, A., Enhancers and silencers: an integrated and simple model for their function. Epigenetics Chromatin, 5, 2012, 1.
72. Kostka, D., Hubisz, M.J., Siepel, A., Pollard, K.S., The role of GC-biased gene conversion in shaping the fastest evolving regions of the human genome. Mol. Biol. Evol. 29 (2012), 1047–1057.
73. Krasnov, A.N., Mazina, M.Y., Nikolenko, J.V., Vorobyeva, N.E., On the way of revealing coactivator complexes cross-talk during transcriptional activation. Cell Biosci., 6, 2016, 15.
74. Kvon, E.Z., Kazmar, T., Stampfel, G., Yáñez-Cuna, J.O., Pagani, M., Schernhuber, K., Dickson, B.J., Stark, A., Genome-scale functional characterization of Drosophila developmental enhancers in vivo. Nature 512 (2014), 91–95.
75. Lan, X., Pritchard, J.K., Coregulation of tandem duplicate genes slows evolution of subfunctionalization in mammals. Science 352 (2015), 1009–1013.
76. Lander, E.S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M.C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., et al. Initial sequencing and analysis of the human genome. Nature 409 (2001), 860–921.
77. Le, T.B., Imakaev, M.V., Mirny, L.A., Laub, M.T., High-resolution mapping of the spatial organization of a bacterial chromosome. Science 342 (2013), 731–734.
78. Leddin, M., Perrod, C., Hoogenkamp, M., Ghani, S., Assi, S., Heinz, S., Wilson, N.K., Follows, G., Schönheit, J., Vockentanz, L., et al. Two distinct auto-regulatory loops operate at the PU.1 locus in B cells and myeloid cells. Blood 117 (2011), 2827–2838.
79. Lettice, L.A., Heaney, S.J.H., Purdie, L.A., Li, L., de Beer, P., Oostra, B.A., Goode, D., Elgar, G., Hill, R.E., de Graaff, E., A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum. Mol. Genet. 12 (2003), 1725–1735.
80. Levine, M., Transcriptional enhancers in animal development and evolution. Curr. Biol. 20 (2010), R754–R763.
81. Levo, M., Zalckvar, E., Sharon, E., Dantas Machado, A.C., Kalma, Y., Lotam-Pompan, M., Weinberger, A., Yakhini, Z., Rohs, R., Segal, E., Unraveling determinants of transcription factor binding outside the core binding site. Genome Res. 25 (2015), 1018–1029.
82. Ludwig, M.Z., Bergman, C., Patel, N.H., Kreitman, M., Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403 (2000), 564–567.
83. Lupiáñez, D.G., Kraft, K., Heinrich, V., Krawitz, P., Brancati, F., Klopocki, E., Horn, D., Kayserili, H., Opitz, J.M., Laxova, R., et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161 (2015), 1012–1025.
84. Lynch, V.J., Leclerc, R.D., May, G., Wagner, G.P., Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet. 43 (2011), 1154–1159.
85. Maeda, R.K., Karch, F., Gene expression in time and space: additive vs hierarchical organization of cis-regulatory regions. Curr. Opin. Genet. Dev. 21 (2011), 187–193.
86. Maekawa, T., Imamoto, F., Merlino, G.T., Pastan, I., Ishii, S., Cooperative function of two separate enhancers of the human epidermal growth factor receptor proto-oncogene. J. Biol. Chem. 264 (1989), 5488–5494.
87. Malik, S., Roeder, R.G., The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat. Rev. Genet. 11 (2010), 761–772.
88. Marinić, M., Aktas, T., Ruf, S., Spitz, F., An integrated holo-enhancer unit defines tissue and gene specificity of the Fgf8 regulatory landscape. Dev. Cell 24 (2013), 530–542.
89. Mavragani-Tsipidou, P., Scouras, Z.G., Kastritsis, C.D., Comparison of the polytene chromosomes of the salivary gland, the fat body and the midgut nuclei of Drosophila auraria. Genetica 81 (1990), 99–108.
90. May, D., Blow, M.J., Kaplan, T., McCulley, D.J., Jensen, B.C., Akiyama, J.A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., et al. Large-scale discovery of enhancers from human heart tissue. Nat. Genet. 44 (2011), 89–93.
91. Mihaly, J., Barges, S., Sipos, L., Maeda, R., Cléard, F., Hogga, I., Bender, W., Gyurkovics, H., Karch, F., Dissecting the regulatory landscape of the Abd-B gene of the bithorax complex. Development 133 (2006), 2983–2993.
92. Miller, J.A., Widom, J., Collaborative Competition Mechanism for Gene Activation In Vivo. Mol. Cell Biol. 23 (2003), 1623–1632.
93. Minezaki, Y., Homma, K., Kinjo, A.R., Nishikawa, K., Human transcription factors contain a high fraction of intrinsically disordered regions essential for transcriptional regulation. J. Mol. Biol. 359 (2006), 1137–1149.
94. Mirny, L.A., Nucleosome-mediated cooperativity between transcription factors. Proc. Natl. Acad. Sci. USA 107 (2010), 22534–22539.
95. Mizuguchi, T., Fudenberg, G., Mehta, S., Belton, J., Taneja, N., Folco, H.D., Cohesin-dependent globules and heterochromatin shape 3D genome architecture in S. pombe. Nature 516 (2014), 432–435.
96. Narendra, V., Rocha, P.P., An, D., Raviram, R., Skok, J.A., Mazzoni, E.O., Reinberg, D., CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science 347 (2015), 1017–1021.
97. Naumova, N., Imakaev, M., Fudenberg, G., Zhan, Y., Lajoie, B.R., Mirny, L.A., Dekker, J., Organization of the mitotic chromosome. Science 342 (2013), 948–953.
98. Ng, F.S., Schütte, J., Ruau, D., Diamanti, E., Hannah, R., Kinston, S.J., Göttgens, B., Constrained transcription factor spacing is prevalent and important for transcriptional control of mouse blood cells. Nucleic Acids Res. 42 (2014), 13513–13524.
99. Nitta, K.R., Jolma, A., Yin, Y., Morgunova, E., Kivioja, T., Akhtar, J., Hens, K., Toivonen, J., Deplancke, B., Furlong, E.E.M., Taipale, J., Conservation of transcription factor binding specificities across 600 million years of bilateria evolution. eLife 4 (2015), 1–20.
100. Nora, E.P., Lajoie, B.R., Schulz, E.G., Giorgetti, L., Okamoto, I., Servant, N., Piolot, T., van Berkum, N.L., Meisig, J., Sedat, J., et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485 (2012), 381–385.
101. Perry, M.W., Boettiger, A.N., Levine, M., Multiple enhancers ensure precision of gap gene-expression patterns in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 108 (2011), 13570–13575.
102. Phillips-Cremins, J.E., Sauria, M.E.G., Sanyal, A., Gerasimova, T.I., Lajoie, B.R., Bell, J.S.K., Ong, C.T., Hookway, T.A., Guo, C., Sun, Y., et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 153 (2013), 1281–1295.
103. Prazak, L., Fujioka, M., Gergen, J.P., Non-additive interactions involving two distinct elements mediate sloppy-paired regulation by pair-rule transcription factors. Dev. Biol. 344 (2010), 1048–1059.
104. Prescott, S.L., Srinivasan, R., Marchetto, M.C., Grishina, I., Narvaiza, I., Selleri, L., Gage, F.H., Swigut, T., Wysocka, J., Enhancer divergence and cis-regulatory evolution in the human and chimp neural crest. Cell 163 (2015), 68–83.
105. Rada-Iglesias, A., Bajpai, R., Swigut, T., Brugmann, S.A., Flynn, R.A., Wysocka, J., A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470 (2011), 279–283.
106. Rao, S.S.P., Huntley, M.H., Durand, N.C., Stamenova, E.K., Bochkov, I.D., Robinson, J.T., Sanborn, A.L., Machol, I., Omer, A.D., Lander, E.S., Aiden, E.L., A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159 (2014), 1665–1680.
107. Rebeiz, M., Jikomes, N., Kassner, V.A., Carroll, S.B., Evolutionary origin of a novel gene expression pattern through co-option of the latent activities of existing regulatory sequences. Proc. Natl. Acad. Sci. USA 108 (2011), 10036–10043.
108. Roeder, R.G., Transcriptional regulation and the role of diverse coactivators in animal cells. FEBS Lett. 579 (2005), 909–915.
109. Sakabe, N.J., Nobrega, M.A., Beyond the ENCODE project: using genomics and epigenomics strategies to study enhancer evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci., 368, 2013, 20130022.
110. Sanborn, A.L., Rao, S.S., Huang, S.-C., Durand, N.C., Huntley, M.H., Jewett, A.I., Bochkov, I.D., Chinnappan, D., Cutkosky, A., Li, J., et al. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc. Natl. Acad. Sci. USA 112 (2015), E6456–E6465.
111. Scacheri, C.A., Scacheri, P.C., Mutations in the noncoding genome. Curr. Opin. Pediatr. 27 (2015), 659–664.
112. Schaffner, W., Enhancers, enhancers - from their discovery to today's universe of transcription enhancers. Biol. Chem. 396 (2015), 311–327.
113. Seitan, V.C., Faure, A.J., Zhan, Y., McCord, R.P., Lajoie, B.R., Ing-Simmons, E., Lenhard, B., Giorgetti, L., Heard, E., Fisher, A.G., et al. Cohesin-based chromatin interactions enable regulated gene expression within preexisting architectural compartments. Genome Res. 23 (2013), 2066–2077.
114. Sexton, T., Yaffe, E., Kenigsberg, E., Bantignies, F., Leblanc, B., Hoichman, M., Parrinello, H., Tanay, A., Cavalli, G., Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148 (2012), 458–472.
115. Slattery, M., Zhou, T., Yang, L., Dantas Machado, A.C., Gordân, R., Rohs, R., Absence of a simple code: how transcription factors read the genome. Trends Biochem. Sci. 39 (2014), 381–399.
116. Smith, R.P., Taher, L., Patwardhan, R.P., Kim, M.J., Inoue, F., Shendure, J., Ovcharenko, I., Ahituv, N., Massively parallel decoding of mammalian regulatory sequences supports a flexible organizational model. Nat. Genet. 45 (2013), 1021–1028.
117. Smith, R.P., Riesenfeld, S.J., Holloway, A.K., Li, Q., Murphy, K.K., Feliciano, N.M., Orecchia, L., Oksenberg, N., Pollard, K.S., Ahituv, N., A compact, in vivo screen of all 6-mers reveals drivers of tissue-specific expression and guides synthetic regulatory element design. Genome Biol., 14, 2013, R72.
118. Sofueva, S., Yaffe, E., Chan, W.-C., Georgopoulou, D., Vietri Rudan, M., Mira-Bontenbal, H., Pollard, S.M., Schroth, G.P., Tanay, A., Hadjur, S., Cohesin-mediated interactions organize chromosomal domain architecture. EMBO J. 32 (2013), 3119–3129.
119. Spitz, F., Furlong, E.E.M., Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet. 13 (2012), 613–626.
120. Stampfel, G., Kazmar, T., Frank, O., Wienerroither, S., Reiter, F., Stark, A., Transcriptional regulators form diverse groups with context-dependent regulatory functions. Nature 528 (2015), 147–151.
121. Stergachis, A.B., Haugen, E., Shafer, A., Fu, W., Vernot, B., Reynolds, A., Raubitschek, A., Ziegler, S., LeProust, E.M., Akey, J.M., Stamatoyannopoulos, J.A., Exonic transcription factor binding directs codon choice and affects protein evolution. Science 342 (2013), 1367–1372.
122. Stine, Z.E., McGaughey, D.M., Bessling, S.L., Li, S., McCallion, A.S., Steroid hormone modulation of RET through two estrogen responsive enhancers in breast cancer. Hum. Mol. Genet. 20 (2011), 3746–3756.
123. Su, M., Han, D., Boyd-Kirkup, J., Yu, X., Han, J.D.J., Evolution of Alu elements toward enhancers. Cell Rep. 7 (2014), 376–385.
124. Sved, J., Bird, A., The expected equilibrium of the CpG dinucleotide in vertebrate genomes under a mutation model. Proc. Natl. Acad. Sci. USA 87 (1990), 4692–4696.
125. Symmons, O., Uslu, V.V., Tsujimura, T., Ruf, S., Nassari, S., Schwarzer, W., Ettwiller, L., Spitz, F., Functional and topological characteristics of mammalian regulatory domains. Genome Res. 24 (2014), 390–400.
126. Taatjes, D.J., Marr, M.T., Tjian, R., Regulatory diversity among metazoan co-activator complexes. Nat. Rev. Mol. Cell Biol. 5 (2004), 403–410.
127. Taher, L., McGaughey, D.M., Maragh, S., Aneas, I., Bessling, S.L., Miller, W., Nobrega, M.A., McCallion, A.S., Ovcharenko, I., Genome-wide identification of conserved regulatory function in diverged sequences. Genome Res. 21 (2011), 1139–1149.
128. Tak, Y.G., Farnham, P.J., Making sense of GWAS: using epigenomics and genome engineering to understand the functional relevance of SNPs in non-coding regions of the human genome. Epigenetics Chromatin, 8, 2015, 57.
129. Taylor, J.S., Raes, J., Duplication and divergence: the evolution of new genes and old ideas. Annu. Rev. Genet. 38 (2004), 615–643.
130. Thanos, D., Maniatis, T., Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome. Cell 83 (1995), 1091–1100.
131. Tillo, D., Kaplan, N., Moore, I.K., Fondufe-Mittendorf, Y., Gossett, A.J., Field, Y., Lieb, J.D., Widom, J., Segal, E., Hughes, T.R., High nucleosome occupancy is encoded at human regulatory sequences. PLoS One, 5, 2010, e9129.
132. Ting, C.N., Rosenberg, M.P., Snow, C.M., Samuelson, L.C., Meisler, M.H., Endogenous retroviral sequences are required for tissue-specific expression of a human salivary amylase gene. Genes Dev. 6 (1992), 1457–1465.
133. Ulianov, S.V., Khrameeva, E.E., Gavrilov, A.A., Flyamer, I.M., Kos, P., Mikhaleva, E.A., Penin, A.A., Logacheva, M.D., Imakaev, M.V., Chertovich, A., et al. Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains. Genome Res. 26 (2016), 70–84.
134. Van Bortle, K., Nichols, M.H., Li, L., Ong, C.-T., Takenaka, N., Qin, Z.S., Corces, V.G., Insulator function and topological domain border strength scale with architectural protein occupancy. Genome Biol., 15, 2014, R82.
135. Vierstra, J., Rynes, E., Sandstrom, R., Zhang, M., Canfield, T., Hansen, R.S., Stehling-sun, S., Sabo, P.J., Byron, R., Humbert, R., et al. Mouse regulatory DNA landscapes reveal global principles of cis-regulatory evolution. Science 346 (2014), 1007–1013.
136. Vietri Rudan, M., Barrington, C., Henderson, S., Ernst, C., Odom, D.T., Tanay, A., Hadjur, S., Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep. 10 (2015), 1297–1309.
137. Villar, D., Berthelot, C., Aldridge, S., Rayner, T.F., Lukk, M., Pignatelli, M., Park, T.J., Deaville, R., Erichsen, J.T., Jasinska, A.J., et al. Enhancer evolution across 20 mammalian species. Cell 160 (2015), 554–566.
138. Visel, A., Bristow, J., Pennacchio, L.A., Enhancer identification through comparative genomics. Semin. Cell Dev. Biol. 18 (2007), 140–152.
139. Visel, A., Akiyama, J.A., Shoukry, M., Afzal, V., Rubin, E.M., Pennacchio, L.A., Functional autonomy of distant-acting human enhancers. Genomics 93 (2009), 509–513.
140. Waszak, S.M., Delaneau, O., Gschwind, A.R., Kilpinen, H., Raghav, S.K., Witwicki, R.M., Orioli, A., Wiederkehr, M., Panousis, N.I., Yurovsky, A., et al. Population Variation and Genetic Control of Modular Chromatin Architecture in Humans. Cell 162 (2015), 1039–1050.
141. Weake, V.M., Workman, J.L., Inducible gene expression: diverse regulatory mechanisms. Nat. Rev. Genet. 11 (2010), 426–437.
142. Whitaker, J.W., Nguyen, T.T., Zhu, Y., Wildberg, A., Wang, W., Computational schemes for the prediction and annotation of enhancers from epigenomic assays. Methods 72 (2015), 86–94.
143. Whyte, W.A., Orlando, D.A., Hnisz, D., Abraham, B.J., Lin, C.Y., Kagey, M.H., Rahl, P.B., Lee, T.I., Young, R.A., Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153 (2013), 307–319.
144. Williamson, W.I., Lettice, L.A., Hill, R., Bickmore, W.A., Shh and ZRS enhancer co-localisation is specific to the zone of polarizing activity. Development 143 (2016), 2994–3001.
145. Wittkopp, P.J., Kalay, G., Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat. Rev. Genet. 13 (2012), 59–69.
146. Xing, K., He, X., Reassessing the “duon” hypothesis of protein evolution. Mol. Biol. Evol. 32 (2015), 1056–1062.
147. Yuh, C.H., Davidson, E.H., Modular cis-regulatory organization of Endo16, a gut-specific gene of the sea urchin embryo. Development 122 (1996), 1069–1082.
148. Yuh, C.H., Bolouri, H., Davidson, E.H., Genomic cis-regulatory logic: experimental and computational analysis of a sea urchin gene. Science 279 (1998), 1896–1902.
149. Zaret, K.S., Carroll, J.S., Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25 (2011), 2227–2241.
150. Zemojtel, T., Kielbasa, S.M., Arndt, P.F., Chung, H.-R., Vingron, M., Methylation and deamination of CpGs generate p53-binding sites on a genomic scale. Trends Genet. 25 (2009), 63–66.
151. Zhu, X., Ling, J., Zhang, L., Pi, W., Wu, M., Tuan, D., A facilitated tracking and transcription mechanism of long-range enhancer function. Nucleic Acids Res. 35 (2007), 5532–5544.
152. Zhu, B., Zhang, W., Zhang, T., Liu, B., Jiang, J., Genome-Wide Prediction and Validation of Intergenic Enhancers in Arabidopsis Using Open Chromatin Signatures. Plant Cell 27 (2015), 2415–2426.
153. Zuin, J., Dixon, J.R., van der Reijden, M.I.J., Ye, Z., Kolovos, P., Brouwer, R.W., van de Corput, M.P., van de Werken, H.J., Knoch, T.A., van IJcken, W.F., et al. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. Proc. Natl. Acad. Sci. USA 111 (2014), 996–1001.