Insights into neural crest development and evolution from genomic analysis

Genome Research

Volumn 23, Issue 7, 2013, Pages 1069-1080

  Simões Costa, Marcos ^a   Bronner, Marianne E ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SOX2;

CHROMATIN; EVOLUTION; GENE CONTROL; GENE REGULATORY NETWORK; GENETIC ANALYSIS; GENETIC CONSERVATION; MOLECULAR GENETICS; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; NEURAL CREST CELL; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; SUMOYLATION; VERTEBRATE;

ANIMALS; CONGENITAL ABNORMALITIES; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GENOMICS; HUMANS; NEURAL CREST; NEUROGENESIS; ORGAN SPECIFICITY;

EID: 84880065533     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.157586.113     Document Type: Review

References (120)

1. Abitua PB, Wagner E, Navarrete IA, Levine M. 2012. Identification of a rudimentary neural crest in a non-vertebrate chordate. Nature 492: 104-107.
2. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA. 2009. Epithelial-mesenchymal transitions: The importance of changing cell state in development and disease. J Clin Invest 119: 1438-1449.
3. Adams MS, Gammill LS, Bronner-Fraser M. 2008. Discovery of transcription factors and other candidate regulators of neural crest development. Dev Dyn 237: 1021-1033.
4. Agarwal P, Verzi MP, Nguyen T, Hu J, Ehlers ML, McCulley DJ, Xu SM, Dodou E, Anderson JP,Wei ML, et al. 2011. The MADS box transcription factor MEF2C regulates melanocyte development and is a direct transcriptional target and partner of SOX10. Development 138: 2555-2565.
5. Akiyama H, Chaboissier MC, Behringer RR, Rowitch DH, Schedl A, Epstein JA, de Crombrugghe B. 2004. Essential role of Sox9 in the pathway that controls formation of cardiac valves and septa. Proc Natl Acad Sci 101: 6502-6507.
6. Bagheri-Fam S, Barrionuevo F, Dohrmann U, Gunther T, Schule R, Kemler R, Mallo M, Kanzler B, Scherer G. 2006. Long-range upstream and downstream enhancers control distinct subsets of the complex spatiotemporal Sox9 expression pattern. Dev Biol 291: 382-397.
7. Barrallo-Gimeno A, Nieto MA. 2005. The Snail genes as inducers of cell movement and survival: Implications in development and cancer. Development 132: 3151-3161.
8. Barraud P, Seferiadis AA, Tyson LD, Zwart MF, Szabo-Rogers HL, Ruhrberg C, Liu KJ, Baker CV. 2010. Neural crest origin of olfactory ensheathing glia. Proc Natl Acad Sci 107: 21040-21045.
9. Beaty TH, Murray JC, Marazita ML, Munger RG, Ruczinski I, Hetmanski JB, Liang KY, Wu T, Murray T, Fallin MD, et al. 2010. A genome-wide association study of cleft lip with and without cleft palate identifies risk variants near MAFB and ABCA4. Nat Genet 42: 525-529.
10. Bernier FP, Caluseriu O, Ng S, Schwartzentruber J, Buckingham KJ, Innes AM, Jabs EW, Innis JW, Schuette JL, Gorski JL, et al. 2012. Haploinsufficiency of SF3B4, a component of the pre-mRNA spliceosomal complex, causes Nager syndrome. Am J Hum Genet 90: 925-933.
11. Betancur P, Bronner-Fraser M, Sauka-Spengler T. 2010a. Assembling neural crest regulatory circuits into a gene regulatory network. Annu Rev Cell Dev Biol 26: 581-603.
12. Betancur P, Bronner-Fraser M, Sauka-Spengler T. 2010b. Genomic code for Sox10 activation reveals a key regulatory enhancer for cranial neural crest. Proc Natl Acad Sci 107: 3570-3575.
13. Brewer S, FengW, Huang J, Sullivan S,Williams T. 2004. Wnt1-Cre-mediated deletion of AP-2a causes multiple neural crest-related defects. Dev Biol 267: 135-152.
14. Bronner-Fraser M, Fraser S. 1988. Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 335: 161-164.
15. Bronner-Fraser M, Fraser S. 1989. Developmental potential of avian trunk neural crest cells in situ. Neuron 3: 755-766.
16. Calloni GW, Le Douarin NM, Dupin E. 2009. High frequency of cephalic neural crest cells shows coexistence of neurogenic, melanogenic, and osteogenic differentiation capacities. Proc Natl Acad Sci 106: 8947-8952.
17. Chan KK, Chen YS, Yau TO, Fu M, Lui VC, Tam PK, Sham MH. 2005. Hoxb3 vagal neural crest-specific enhancer element for controlling enteric nervous system development. Dev Dyn 233: 473-483.
18. Chimge NO, Bayarsaihan D. 2010. Generation of neural crest progenitors from human embryonic stem cells. J Exp Zoolog B Mol Dev Evol 314: 95-103.
19. Cooper GM, Sidow A. 2003. Genomic regulatory regions: Insights from comparative sequence analysis. Curr Opin Genet Dev 13: 604-610.
20. Cox SG, Kim H, Garnett AT, Medeiros DM, An W, Crump JG. 2012. An essential role of variant histone H3.3 for ectomesenchyme potential of the cranial neural crest. PLoS Genet 8: e1002938.
21. Crane JF, Trainor PA. 2006. Neural crest stem and progenitor cells. Annu Rev Cell Dev Biol 22: 267-286.
22. Cremer T, Cremer C. 2001. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2: 292-301.
23. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, et al. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci 107: 21931-21936.
24. Curchoe CL, Maurer J, McKeown SJ, Cattarossi G, Cimadamore F, Nilbratt M, Snyder EY, Bronner-Fraser M, Terskikh AV. 2010. Early acquisition of neural crest competence during hESCs neuralization. PLoS ONE 5: e13890.
25. Davidson E. 2009. The regulatory genome: Gene regulatory networks in development and evolution. Elsevier, Burlington, MA.
26. Degenhardt KR, Milewski RC, Padmanabhan A, Miller M, Singh MK, Lang D, Engleka KA, Wu M, Li J, Zhou D, et al. 2010. Distinct enhancers at the Pax3 locus can function redundantly to regulate neural tube and neural crest expressions. Dev Biol 339: 519-527.
27. Delsuc F, Brinkmann H, Chourrout D, Philippe H. 2006. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439: 965-968.
28. Dixon J, Jones NC, Sandell LL, Jayasinghe SM, Crane J, Rey JP, Dixon MJ, Trainor PA. 2006. Tcof1/Treacle is required for neural crest cell formation and proliferation deficiencies that cause craniofacial abnormalities. Proc Natl Acad Sci 103: 13403-13408.
29. Dixon MJ, Marazita ML, Beaty TH, Murray JC. 2011. Cleft lip and palate: Understanding genetic and environmental influences. Nat Rev Genet 12: 167-178.
30. Dudas M, Sridurongrit S, Nagy A, Okazaki K, Kaartinen V. 2004. Craniofacial defects in mice lacking BMP type I receptor Alk2 in neural crest cells. Mech Dev 121: 173-182.
31. Dupin E, Calloni GW, Le Douarin NM. 2010. The cephalic neural crest of amniote vertebrates is composed of a large majority of precursors endowed with neural, melanocytic, chondrogenic and osteogenic potentialities. Cell Cycle 9: 238-249.
32. Echelard Y, Vassileva G, McMahon AP. 1994. Cis-acting regulatory sequences governing Wnt-1 expression in the developing mouse CNS. Development 120: 2213-2224.
33. The ENCODE Project Consortium. 2004. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 306: 636-640.
34. Fisher S, Grice EA, Vinton RM, Bessling SL, Urasaki A, Kawakami K, McCallion AS. 2006. Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish. Nat Protoc 1: 1297-1305.
35. Gammill LS, Bronner-Fraser M. 2002. Genomic analysis of neural crest induction. Development 129: 5731-5741.
36. Gammill LS, Bronner-Fraser M. 2003. Neural crest specification: Migrating into genomics. Nat Rev Neurosci 4: 795-805.
37. Gans C, Northcutt RG. 1983. Neural crest and the origin of vertebrates: A new head. Science 220: 268-273.
38. Garnett AT, Square TA, Medeiros DM. 2012. BMP, Wnt and FGF signals are integrated through evolutionarily conserved enhancers to achieve robust expression of Pax3 and Zic genes at the zebrafish neural plate border. Development 139: 4220-4231.
39. Grant SF, Wang K, Zhang H, Glaberson W, Annaiah K, Kim CE, Bradfield JP, Glessner JT, Thomas KA, Garris M, et al. 2009. A genome-wide association study identifies a locus for nonsyndromic cleft lip with or without cleft palate on 8q24. J Pediatr 155: 909-913.
40. Green SA, Bronner ME. 2013. Gene duplications and the early evolution of neural crest development. Semin Cell Dev Biol 24: 95-100.
41. Hall BK. 1999. The neural crest in development and evolution. Springer, Berlin.
42. Hall BK, Gillis JA. 2013. Incremental evolution of the neural crest, neural crest cells and neural crest-derived skeletal tissues. J Anat 222: 19-31.
43. Häming D, Simoes-Costa M, Uy B, Valencia J, Sauka-Spengler T, Bronner-Fraser M. 2011. Expression of sympathetic nervous system genes in lamprey suggests their recruitment for specification of a new vertebrate feature. PLoS ONE 6: e26543.
44. Hendrix MJ, Seftor EA, Seftor RE, Kasemeier-Kulesa J, Kulesa PM, Postovit LM. 2007. Reprogramming metastatic tumour cells with embryonic microenvironments. Nat Rev Cancer 7: 246-255.
45. His W. 1868. Untersuchungen über die erste Anlage des Wirbeltierleibes. Die erste Entwickelung des Hühnchens im Ei. FCW Vogel, Leipzig.
46. Hochheiser H, Aronow BJ, Artinger K, Beaty TH, Brinkley JF, Chai Y, Clouthier D, Cunningham ML, Dixon M, Donahue LR, et al. 2011. The FaceBase Consortium: A comprehensive program to facilitate craniofacial research. Dev Biol 355: 175-182.
47. Honoré SM, Aybar MJ, Mayor R. 2003. Sox10 is required for the early development of the prospective neural crest in Xenopus embryos. Dev Biol 260: 79-96.
48. Horstadius S. 1950. The neural crest. Oxford University Press, Oxford, UK
49. Hu N, Strobl-Mazzulla P, Sauka-Spengler T, Bronner ME. 2012. DNA methyltransferase3A as a molecular switch mediating the neural tubeto-neural crest fate transition. Genes Dev 26: 2380-2385.
50. Ito Y, Yeo JY, Chytil A, Han J, Bringas P Jr, Nakajima A, Shuler CF, Moses HL, Chai Y. 2003. Conditional inactivation of Tgfbr2 in cranial neural crest causes cleft palate and calvaria defects. Development 130: 5269-5280.
51. Jayasena CS, Bronner ME. 2012. Rbms3 functions in craniofacial development by posttranscriptionally modulating TGF-b signaling. J Cell Biol 199: 453-466.
52. Jeffery WR. 2006. Ascidian neural crest-like cells: Phylogenetic distribution, relationship to larval complexity, and pigment cell fate. J Exp Zool B Mol Dev Evol 306: 470-480.
53. Jeffery WR, Strickler AG, Yamamoto Y. 2004. Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 431: 696-699.
54. Jeffery WR, Chiba T, Krajka FR, Deyts C, Satoh N, Joly JS. 2008. Trunk lateral cells are neural crest-like cells in the ascidian Ciona intestinalis: Insights into the ancestry and evolution of the neural crest. Dev Biol 324: 152-160.
55. Jiang X, Rowitch DH, Soriano P,McMahon AP, Sucov HM. 2000. Fate of the mammalian cardiac neural crest. Development 127: 1607-1616.
56. Jones NC, Trainor PA. 2004. The therapeutic potential of stem cells in the treatment of craniofacial abnormalities. Expert Opin Biol Ther 4: 645-657.
57. Kulesa PM, Kasemeier-Kulesa JC, Teddy JM,Margaryan NV, Seftor EA, Seftor RE, Hendrix MJ. 2006. Reprogramming metastatic melanoma cells to assume a neural crest cell-like phenotype in an embryonic microenvironment. Proc Natl Acad Sci 103: 3752-3757.
58. Lan X, Farnham PJ, Jin VX. 2012. Uncovering transcription factor modules using one- and three-dimensional analyses. J Biol Chem 287: 30914-30921.
59. Le Douarin NM. 1986. Investigations on the neural crest. Methodological aspects and recent advances. Ann NY Acad Sci 486: 66-86.
60. Le Douarin N, Kalcheim C. 1999. The neural crest. Cambridge University Press, Cambridge, UK.
61. Le Douarin NM, Creuzet S, Couly G, Dupin E. 2004. Neural crest cell plasticity and its limits. Development 131: 4637-4650.
62. Lee JM, Dedhar S, Kalluri R, Thompson EW. 2006. The epithelialmesenchymal transition: New insights in signaling, development, and disease. J Cell Biol 172: 973-981.
63. Lee G, Kim H, Elkabetz Y, Al Shamy G, Panagiotakos G, Barberi T, Tabar V, Studer L. 2007. Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat Biotechnol 25: 1468-1475.
64. Lee G, Papapetrou EP, Kim H, Chambers SM, Tomishima MJ, Fasano CA, Ganat YM, Menon J, Shimizu F, Viale A, et al. 2009. Modelling pathogenesis and treatment of familial dysautonomia using patientspecific iPSCs. Nature 461: 402-406.
65. Lee PC, Taylor-Jaffe KM, Nordin KM, Prasad MS, Lander RM, LaBonne C. 2012. SUMOylated SoxE factors recruit Grg4 and function as transcriptional repressors in the neural crest. J Cell Biol 198: 799-813.
66. Li G, Ruan X, Auerbach RK, Sandhu KS, Zheng M,Wang P, Poh HM, Goh Y, Lim J, Zhang J, et al. 2012. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 148: 84-98.
67. Liu F, van der Lijn F, Schurmann C, Zhu G, Chakravarty MM, Hysi PG, Wollstein A, Lao O, de Bruijne M, Ikram MA, et al. 2012. A genome-wide association study identifies five loci influencing facial morphology in Europeans. PLoS Genet 8: e1002932.
68. Mangold E, Ludwig KU, Birnbaum S, Baluardo C, Ferrian M, Herms S, Reutter H, de Assis NA, Chawa TA, Mattheisen M, et al. 2010. Genome-wide association study identifies two susceptibility loci for nonsyndromic cleft lip with or without cleft palate. Nat Genet 42: 24-26.
69. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al. 2008. The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715.
70. Manzanares M, Wada H, Itasaki N, Trainor PA, Krumlauf R, Holland PW. 2000. Conservation and elaboration of Hox gene regulation during evolution of the vertebrate head. Nature 408: 854-857.
71. Mateos-Langerak J, Goetze S, Leonhardt H, Cremer T, van Driel R, Lanctot C. 2007. Nuclear architecture: Is it important for genome function and can we prove it? J Cell Biochem 102: 1067-1075.
72. McCauley DW, Bronner-Fraser M. 2006. Importance of SoxE in neural crest development and the evolution of the pharynx. Nature 441: 750-752.
73. Medeiros D 2013. The evolution of the neural crest: New perspectives from lamprey and invertebrate neural crest-like cells. WIREs Dev Biol 2: 1-15.
74. Meulemans D, Bronner-Fraser M. 2002. Amphioxus and lamprey AP-2 genes: Implications for neural crest evolution and migration patterns. Development 129: 4953-4962.
75. Meulemans D, Bronner-Fraser M. 2004. Gene-regulatory interactions in neural crest evolution and development. Dev Cell 7: 291-299.
76. Meulemans D, McCauley D, Bronner-Fraser M. 2003. Id expression in amphioxus and lamprey highlights the role of gene cooption during neural crest evolution. Dev Biol 264: 430-442.
77. Milewski RC, Chi NC, Li J, Brown C, Lu MM, Epstein JA. 2004. Identification of minimal enhancer elements sufficient for Pax3 expression in neural crest and implication of Tead2 as a regulator of Pax3. Development 131: 829-837.
78. Murisier F, Guichard S, Beermann F. 2006. A conserved transcriptional enhancer that specifies Tyrp1 expression to melanocytes. Dev Biol 298: 644-655.
79. Nakamura T, Colbert MC, Robbins J. 2006. Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system. Circ Res 98: 1547-1554.
80. Ng SB, Buckingham KJ, Lee C, Bigham AW, Tabor HK, Dent KM, Huff CD, Shannon PT, Jabs EW, Nickerson DA, et al. 2010. Exome sequencing identifies the cause of a Mendelian disorder. Nat Genet 42: 30-35.
81. Nicol JAC. 1952. Autonomic nervous systems in lower chordates. Biol Rev Camb Philos Soc 27: 1-50.
82. Nikitina N, Sauka-Spengler T, Bronner-Fraser M. 2008. Dissecting early regulatory relationships in the lamprey neural crest gene network. Proc Natl Acad Sci 105: 20083-20088.
83. Northcutt RG. 2005. The new head hypothesis revisited. J Exp Zool BMol Dev Evol 304: 274-297.
84. Okawa T, Kamiya H, Himeno T, Kato J, Seino Y, Fujiya A, Kondo M, Tsunekawa S, Naruse K, Hamada Y, et al. 2012. Transplantation of neural crest like cells derived from induced pluripotent stem cells improves diabetic polyneuropathy in mice. Cell Transplant doi: 10.3727/096368912X657710.
85. Peter IS, Faure E, Davidson EH. 2012. Predictive computation of genomic logic processing functions in embryonic development. Proc Natl Acad Sci 109: 16434-16442.
86. Philippe H, Lartillot N, Brinkmann H. 2005. Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. Mol Biol Evol 22: 1246-1253.
87. Rada-Iglesias A, Bajpai R, Prescott S, Brugmann SA, Swigut T, Wysocka J. 2012. Epigenomic annotation of enhancers predicts transcriptional regulators of human neural crest. Cell Stem Cell 11: 633-648.
88. Rios AC, Serralbo O, Salgado D, Marcelle C. 2011. Neural crest regulates myogenesis through the transient activation of NOTCH. Nature 473: 532-535.
89. Sandhu KS, Li G, Poh HM, Quek YL, Sia YY, Peh SQ, Mulawadi FH, Lim J, Sikic M, Menghi F et al. 2012. Large-scale functional organization of long-range chromatin interaction networks. Cell Rep 2: 1207-1219.
90. Sanyal A, Bau D, Marti-Renom MA, Dekker J. 2011. Chromatin globules: A common motif of higher order chromosome structure? Curr Opin Cell Biol 23: 325-331.
91. Sanyal A, Lajoie BR, Jain G, Dekker J. 2012. The long-range interaction landscape of gene promoters. Nature 489: 109-113.
92. Sato T, Sasai N, Sasai Y. 2005. Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development 132: 2355-2363.
93. Sauka-Spengler T, Barembaum M. 2008. Gain- and loss-of-function approaches in the chick embryo. Methods Cell Biol 87: 237-256.
94. Sauka-Spengler T, Bronner-Fraser M. 2008a. Evolution of the neural crest viewed from a gene regulatory perspective. Genesis 46: 673-682.
95. Sauka-Spengler T, Bronner-Fraser M. 2008b. A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol 9: 557-568.
96. Sauka-Spengler T, Bronner-Fraser M. 2008c. Insights from a sea lamprey into the evolution of neural crest gene regulatory network. Biol Bull 214: 303-314.
97. Sauka-Spengler T, Meulemans D, Jones M, Bronner-Fraser M. 2007. Ancient evolutionary origin of the neural crest gene regulatory network. Dev Cell 13: 405-420.
98. Schubert M, Escriva H, Xavier-Neto J, Laudet V. 2006. Amphioxus and tunicates as evolutionary model systems. Trends Ecol Evol 21: 269-277.
99. Shakhova O, Zingg D, Schaefer SM, Hari L, Civenni G, Blunschi J, Claudinot S, Okoniewski M, Beermann F, Mihic-Probst D, et al. 2012. Sox10 promotes the formation and maintenance of giant congenital naevi and melanoma. Nat Cell Biol 14: 882-890.
100. Shirley SH, Greene VR, Duncan LM, Torres Cabala CA, GrimmEA, Kusewitt DF. 2012. Slug expression during melanoma progression. Am J Pathol 180: 2479-2489.
101. Sieber-Blum M, Cohen AM. 1980. Clonal analysis of quail neural crest cells: They are pluripotent and differentiate in vitro in the absence of noncrest cells. Dev Biol 80: 96-106.
102. Simões-Costa MS, McKeown SJ, Tan-Cabugao J, Sauka-Spengler T, Bronner ME. 2012. Dynamic and differential regulation of stem cell factor FoxD3 in the neural crest is encrypted in the genome. PLoS Genet 8: e1003142.
103. Smith A, Robinson V, Patel K, Wilkinson DG. 1997. The EphA4 and EphB1 receptor tyrosine kinases and ephrin-B2 ligand regulate targeted migration of branchial neural crest cells. Curr Biol 7: 561-570.
104. Soriano P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71.
105. Stemple DL, Anderson DJ. 1992. Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71: 973-985.
106. Stemple DL, Anderson DJ. 1993. Lineage diversification of the neural crest: In vitro investigations. Dev Biol 159: 12-23.
107. Strobl-Mazzulla PH, Bronner ME. 2012. A PHD12-Snail2 repressive complex epigeneticallymediates neural crest epithelial-to-mesenchymal transition. J Cell Biol 198: 999-1010.
108. Strobl-Mazzulla PH, Sauka-Spengler T, Bronner-Fraser M. 2010. Histone demethylase JmjD2A regulates neural crest specification. Dev Cell 19: 460-468.
109. Takemoto T, Uchikawa M, Yoshida M, Bell DM, Lovell-Badge R, Papaioannou VE, Kondoh H. 2011. Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 470: 394-398.
110. Trainor PA. 2010. Craniofacial birth defects: The role of neural crest cells in the etiology and pathogenesis of Treacher Collins syndrome and the potential for prevention. Am J Med Genet A 152A: 2984-2994.
111. The Treacher Collins Syndrome Collaborative Group. 1996. Positional cloning of a gene involved in the pathogenesis of Treacher Collins syndrome. Nat Genet 12: 130-136.
112. Trentin A, Glavieux-Pardanaud C, Le Douarin NM, Dupin E. 2004. Selfrenewal capacity is a widespread property of various types of neural crest precursor cells. Proc Natl Acad Sci 101: 4495-4500.
113. Uchikawa M, Ishida Y, Takemoto T, Kamachi Y, Kondoh H. 2003. Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals. Dev Cell 4: 509-519.
114. Uchikawa M, Takemoto T, Kamachi Y, Kondoh H. 2004. Efficient identification of regulatory sequences in the chicken genome by a powerful combination of embryo electroporation and genome comparison. Mech Dev 121: 1145-1158.
115. Valouev A, Johnson DS, Sundquist A, Medina C, Anton E, Batzoglou S, Myers RM, Sidow A. 2008. Genome-wide analysis of transcription factor binding sites based on ChIP-seq data. Nat Methods 5: 829-834.
116. Wang J, Kumar RM, Biggs VJ, Lee H, Chen Y, Kagey MH, Young RA, Abate-Shen C. 2011. TheMsx1 homeoprotein recruits polycomb to the nuclear periphery during development. Dev Cell 21: 575-588.
117. Weiss MB, Abel EV, Mayberry MM, Basile KJ, Berger AC, Aplin AE. 2012. TWIST1 is an ERK1/2 effector that promotes invasion and regulates MMP-1 expression in human melanoma cells. Cancer Res 72: 6382-6392.
118. Yang J, Weinberg RA. 2008. Epithelial-mesenchymal transition: At the crossroads of development and tumor metastasis. Dev Cell 14: 818-829.
119. Yokota Y, Saito D, Tadokoro R, Takahashi Y. 2011. Genomically integrated transgenes are stably and conditionally expressed in neural crest cellspecific lineages. Dev Biol 353: 382-395.
120. Yu JK, Meulemans D, McKeown SJ, Bronner-Fraser M. 2008. Insights from the amphioxus genome on the origin of vertebrate neural crest. Genome Res 18: 1127-1132.