Enhancer Divergence and cis-Regulatory Evolution in the Human and Chimp Neural Crest

Cell

Volumn 163, Issue 1, 2015, Pages 68-83

  Prescott, Sara L ^a   Srinivasan, Rajini ^a   Marchetto, Maria Carolina ^b   Grishina, Irina ^c   Narvaiza, Iñigo ^b   Selleri, Licia ^c   Gage, Fred H ^b,d   Swigut, Tomek ^a   Wysocka, Joanna ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d San Diego   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CHIMPANZEE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENHANCER REGION; EPIGENETICS; EVOLUTION; GENE; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR GENETICS; MORPHOLOGY; NEURAL CREST CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTIVE VALUE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RETROPOSON; TISSUE SPECIFICITY; ANIMAL; ANIMAL EMBRYO; CYTOLOGY; GENETIC ENHANCEMENT; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOUSE; NEURAL CREST; PAN TROGLODYTES; PLURIPOTENT STEM CELL; PROCEDURES; SPECIES DIFFERENCE; TRANSGENIC MOUSE;

ANIMALS; EMBRYO, MAMMALIAN; EPIGENOMICS; EVOLUTION, MOLECULAR; GENETIC ENHANCEMENT; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; MICE, TRANSGENIC; NEURAL CREST; PAN TROGLODYTES; SPECIES SPECIFICITY;

EID: 84948457844     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.08.036     Document Type: Article

References (54)

1. A. Abzhanov, M. Protas, B.R. Grant, P.R. Grant, and C.J. Tabin Bmp4 and morphological variation of beaks in Darwin's finches Science 305 2004 1462 1465
2. R.C. Albertson, J.T. Streelman, T.D. Kocher, and P.C. Yelick Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies Proc. Natl. Acad. Sci. USA 102 2005 16287 16292
3. C. Attanasio, A.S. Nord, Y. Zhu, M.J. Blow, Z. Li, D.K. Liberton, H. Morrison, I. Plajzer-Frick, A. Holt, R. Hosseini, and et al. Fine tuning of craniofacial morphology by distant-acting enhancers Science 342 2013 1241006
4. R. Bajpai, D.A. Chen, A. Rada-Iglesias, J. Zhang, Y. Xiong, J. Helms, C.-P. Chang, Y. Zhao, T. Swigut, and J. Wysocka CHD7 cooperates with PBAF to control multipotent neural crest formation Nature 463 2010 958 962
5. A. Bilsborough, and B.A. Wood Cranial morphometry of early hominids: facial region Am. J. Phys. Anthropol. 76 1988 61 86
6. M. Bonilla-Claudio, J. Wang, Y. Bai, E. Klysik, J. Selever, and J.F. Martin Bmp signaling regulates a dose-dependent transcriptional program to control facial skeletal development Development 139 2012 709 719
7. R.K. Bradley, X.-Y. Li, C. Trapnell, S. Davidson, L. Pachter, H.C. Chu, L.A. Tonkin, M.D. Biggin, and M.B. Eisen Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species PLoS Biol. 8 2010 e1000343
8. M.E. Bronner, and N.M. LeDouarin Development and evolution of the neural crest: an overview Dev. Biol. 366 2012 2 9
9. C. Buecker, R. Srinivasan, Z. Wu, E. Calo, D. Acampora, T. Faial, A. Simeone, M. Tan, T. Swigut, and J. Wysocka Reorganization of enhancer patterns in transition from naive to primed pluripotency Cell Stem Cell 14 2014 838 853
10. J.D. Buenrostro, P.G. Giresi, L.C. Zaba, H.Y. Chang, and W.J. Greenleaf Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position Nat. Methods 10 2013 1213 1218
11. C.E. Cain, R. Blekhman, J.C. Marioni, and Y. Gilad Gene expression differences among primates are associated with changes in a histone epigenetic modification Genetics 187 2011 1225 1234
12. S.B. Carroll Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution Cell 134 2008 25 36
13. R. Cordaux, and M.A. Batzer The impact of retrotransposons on human genome evolution Nat. Rev. Genet. 10 2009 691 703
14. D.R. Cordero, S. Brugmann, Y. Chu, R. Bajpai, M. Jame, and J.A. Helms Cranial neural crest cells on the move: their roles in craniofacial development Am. J. Med. Genet. A. 155A 2011 270 279
15. J. Cotney, J. Leng, J. Yin, S.K. Reilly, L.E. DeMare, D. Emera, A.E. Ayoub, P. Rakic, and J.P. Noonan The evolution of lineage-specific regulatory activities in the human embryonic limb Cell 154 2013 185 196
16. M.P. Creyghton, A.W. Cheng, G.G. Welstead, T. Kooistra, B.W. Carey, E.J. Steine, J. Hanna, M.A. Lodato, G.M. Frampton, P.A. Sharp, and et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state Proc. Natl. Acad. Sci. USA 107 2010 21931 21936
17. J.L. Fish, R.S. Sklar, K.C. Woronowicz, and R.A. Schneider Multiple developmental mechanisms regulate species-specific jaw size Development 141 2014 674 684
18. N. Gompel, B. Prud'homme, P.J. Wittkopp, V.A. Kassner, and S.B. Carroll Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila Nature 433 2005 481 487
19. I. Gronau, L. Arbiza, J. Mohammed, and A. Siepel Inference of natural selection from interspersed genomic elements based on polymorphism and divergence Mol. Biol. Evol. 30 2013 1159 1171
20. Q. He, A.F. Bardet, B. Patton, J. Purvis, J. Johnston, A. Paulson, M. Gogol, A. Stark, and J. Zeitlinger High conservation of transcription factor binding and evidence for combinatorial regulation across six Drosophila species Nat. Genet. 43 2011 414 420
21. N.D. Heintzman, R.K. Stuart, G. Hon, Y. Fu, C.W. Ching, R.D. Hawkins, L.O. Barrera, S. Van Calcar, C. Qu, K.A. Ching, and et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome Nat. Genet. 39 2007 311 318
22. J.-W. Hong, D.A. Hendrix, and M.S. Levine Shadow enhancers as a source of evolutionary novelty Science 321 2008 1314
23. M.J. Hubisz, and K.S. Pollard Exploring the genesis and functions of Human Accelerated Regions sheds light on their role in human evolution Curr. Opin. Genet. Dev. 29 2014 15 21
24. A.H. Jheon, and R.A. Schneider The cells that fill the bill: neural crest and the evolution of craniofacial development J. Dent. Res. 88 2009 12 21
25. H. Kaessmann, V. Wiebe, and S. Pääbo Extensive nuclear DNA sequence diversity among chimpanzees Science 286 1999 1159 1162
26. M.C. King, and A.C. Wilson Evolution at two levels in humans and chimpanzees Science 188 1975 107 116
27. H.-L. Liang, C.-Y. Nien, H.-Y. Liu, M.M. Metzstein, N. Kirov, and C. Rushlow The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila Nature 456 2008 400 403
28. D.E. Lieberman Sphenoid shortening and the evolution of modern human cranial shape Nature 393 1998 158 162
29. F. Liu, F. van der Lijn, C. Schurmann, G. Zhu, M.M. Chakravarty, P.G. Hysi, A. Wollstein, O. Lao, M. de Bruijne, M.A. Ikram, and et al. A genome-wide association study identifies five loci influencing facial morphology in Europeans PLoS Genet. 8 2012 e1002932
30. A. Mansouri, A. Stoykova, M. Torres, and P. Gruss Dysgenesis of cephalic neural crest derivatives in Pax7-/- mutant mice Development 122 1996 831 838
31. M.C.N. Marchetto, I. Narvaiza, A.M. Denli, C. Benner, T.A. Lazzarini, J.L. Nathanson, A.C.M. Paquola, K.N. Desai, R.H. Herai, M.D. Weitzman, and et al. Differential L1 regulation in pluripotent stem cells of humans and apes Nature 503 2013 525 529
32. C.Y. McLean, P.L. Reno, A.A. Pollen, A.I. Bassan, T.D. Capellini, C. Guenther, V.B. Indjeian, X. Lim, D.B. Menke, B.T. Schaar, and et al. Human-specific loss of regulatory DNA and the evolution of human-specific traits Nature 471 2011 216 219
33. D.T. Odom, R.D. Dowell, E.S. Jacobsen, W. Gordon, T.W. Danford, K.D. MacIsaac, P.A. Rolfe, C.M. Conboy, D.K. Gifford, and E. Fraenkel Tissue-specific transcriptional regulation has diverged significantly between human and mouse Nat. Genet. 39 2007 730 732
34. L. Paternoster, A.I. Zhurov, A.M. Toma, J.P. Kemp, B. St Pourcain, N.J. Timpson, G. McMahon, W. McArdle, S.M. Ring, G.D. Smith, and et al. Genome-wide association study of three-dimensional facial morphology identifies a variant in PAX3 associated with nasion position Am. J. Hum. Genet. 90 2012 478 485
35. K.S. Pollard, S.R. Salama, N. Lambert, M.-A. Lambot, S. Coppens, J.S. Pedersen, S. Katzman, B. King, C. Onodera, A. Siepel, and et al. An RNA gene expressed during cortical development evolved rapidly in humans Nature 443 2006 167 172
36. S. Prabhakar, F. Poulin, M. Shoukry, V. Afzal, E.M. Rubin, O. Couronne, and L.A. Pennacchio Close sequence comparisons are sufficient to identify human cis-regulatory elements Genome Res. 16 2006 855 863
37. S. Prabhakar, A. Visel, J.A. Akiyama, M. Shoukry, K.D. Lewis, A. Holt, I. Plajzer-Frick, H. Morrison, D.R. Fitzpatrick, V. Afzal, and et al. Human-specific gain of function in a developmental enhancer Science 321 2008 1346 1350
38. A. Rada-Iglesias, R. Bajpai, T. Swigut, S.A. Brugmann, R.A. Flynn, and J. Wysocka A unique chromatin signature uncovers early developmental enhancers in humans Nature 470 2011 279 283
39. A. Rada-Iglesias, R. Bajpai, S. Prescott, S.A. Brugmann, T. Swigut, and J. Wysocka Epigenomic annotation of enhancers predicts transcriptional regulators of human neural crest Cell Stem Cell 11 2012 633 648
40. R. Satija, and R.K. Bradley The TAGteam motif facilitates binding of 21 sequence-specific transcription factors in the Drosophila embryo Genome Res. 22 2012 656 665
41. D. Schmidt, M.D. Wilson, B. Ballester, P.C. Schwalie, G.D. Brown, A. Marshall, C. Kutter, S. Watt, C.P. Martinez-Jimenez, S. Mackay, and et al. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding Science 328 2010 1036 1040
42. M.D. Shapiro, M.E. Marks, C.L. Peichel, B.K. Blackman, K.S. Nereng, B. Jónsson, D. Schluter, and D.M. Kingsley Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks Nature 428 2004 717 723
43. Y. Shibata, N.C. Sheffield, O. Fedrigo, C.C. Babbitt, M. Wortham, A.K. Tewari, D. London, L. Song, B.-K. Lee, V.R. Iyer, and et al. Extensive evolutionary changes in regulatory element activity during human origins are associated with altered gene expression and positive selection PLoS Genet. 8 2012 e1002789
44. F. Spoor, B. Wood, and F. Zonneveld Implications of early hominid labyrinthine morphology for evolution of human bipedal locomotion Nature 369 1994 645 648
45. K. Stefflova, D. Thybert, M.D. Wilson, I. Streeter, J. Aleksic, P. Karagianni, A. Brazma, D.J. Adams, I. Talianidis, J.C. Marioni, and et al. Cooperativity and rapid evolution of cobound transcription factors in closely related mammals Cell 154 2013 530 540
46. P. Tremblay, M. Kessel, and P. Gruss A transgenic neuroanatomical marker identifies cranial neural crest deficiencies associated with the Pax3 mutant Splotch Dev. Biol. 171 1995 317 329
47. S.R.F. Twigg, S.L. Versnel, G. Nürnberg, M.M. Lees, M. Bhat, P. Hammond, R.C.M. Hennekam, A.J.M. Hoogeboom, J.A. Hurst, D. Johnson, and et al. Frontorhiny, a distinctive presentation of frontonasal dysplasia caused by recessive mutations in the ALX3 homeobox gene Am. J. Hum. Genet. 84 2009 698 705
48. J. Vierstra, E. Rynes, R. Sandstrom, M. Zhang, T. Canfield, R.S. Hansen, S. Stehling-Sun, P.J. Sabo, R. Byron, R. Humbert, and et al. Mouse regulatory DNA landscapes reveal global principles of cis-regulatory evolution Science 346 2014 1007 1012
49. D. Villar, C. Berthelot, S. Aldridge, T.F. Rayner, M. Lukk, M. Pignatelli, T.J. Park, R. Deaville, J.T. Erichsen, A.J. Jasinska, and et al. Enhancer evolution across 20 mammalian species Cell 160 2015 554 566
50. A. Visel, S. Minovitsky, I. Dubchak, and L.A. Pennacchio VISTA Enhancer Browser - a database of tissue-specific human enhancers Nucleic Acids Res. 35 2007 D88 D92
51. W.A. Whyte, D.A. Orlando, D. Hnisz, B.J. Abraham, C.Y. Lin, M.H. Kagey, P.B. Rahl, T.I. Lee, and R.A. Young Master transcription factors and mediator establish super-enhancers at key cell identity genes Cell 153 2013 307 319
52. E.S. Wong, D. Thybert, B.M. Schmitt, K. Stefflova, D.T. Odom, and P. Flicek Decoupling of evolutionary changes in transcription factor binding and gene expression in mammals Genome Res. 2014
53. G.A. Wray The evolutionary significance of cis-regulatory mutations Nat. Rev. Genet. 8 2007 206 216
54. X. Zhou, C.E. Cain, M. Myrthil, N. Lewellen, K. Michelini, E.R. Davenport, M. Stephens, J.K. Pritchard, and Y. Gilad Epigenetic modifications are associated with inter-species gene expression variation in primates Genome Biol. 15 2014 547