Evolution of the neural crest viewed from a gene regulatory perspective

Genesis

Volumn 46, Issue 11, 2008, Pages 673-682

  Sauka Spengler, Tatjana ^a   Bronner Fraser, Marianne ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Development; Evolution; Gene regulation; Network; Neural crest

Indexed keywords

BONE MORPHOGENETIC PROTEIN; COLLAGEN TYPE 2; EPHRIN; FIBROBLAST GROWTH FACTOR; FORKHEAD TRANSCRIPTION FACTOR; HOMEODOMAIN PROTEIN; INTEGRIN; MATRIX METALLOPROTEINASE; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MYC PROTEIN; NEUROPILIN 2; PROTEIN RET; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR PAX7; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR SOX9; TYROSINASE RELATED PROTEIN 2; WNT PROTEIN;

CELL DIFFERENTIATION; CELL MIGRATION; CELL TYPE; DEVELOPMENTAL BIOLOGY; EMBRYO CELL; EVOLUTION; GENETIC REGULATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; VERTEBRATE;

VERTEBRATA;

ANIMALS; BIOLOGICAL EVOLUTION; GENE REGULATORY NETWORKS; NEURAL CREST; VERTEBRATES;

EID: 67649371214     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.20436     Document Type: Review

References (100)

1. Aoki Y, Saint-Germain N, Gyda M, Magner-Fink E, Lee YH, Credidio C, Saint-Jeannet JP. 2003. Sox10 regulates the development of neural crest-derived melanocytes in Xenopus. Dev Biol 259:19-33.
2. Aruga J, Tohmonda T, Homma S, Mikoshiba K. 2002. Zic1 promotes the expansion of dorsal neural progenitors in spinal cord by inhibiting neuronal differentiation. Dev Biol 244:329-341.
3. Aybar MJ, Nieto MA, Mayor R. 2003. Snail precedes slug in the genetic cascade required for the specification and migration of the Xenopus neural crest. Development 130:483-494.
4. Bang AG, Papalopulu N, Goulding MD, Kintner C. 1999. Expression of Pax-3 in the lateral neural plate is dependent on a Wnt-mediated signal from posterior nonaxial mesoderm. Dev Biol 212:366-380.
5. Barrallo-Gimeno A, Holzschuh J, Driever W, Knapik EW. 2004. Neural crest survival and differentiation in zebrafish depends on mont blanc/tfap2a gene function. Development 131:1463-1477.
6. Basch ML, Bronner-Fraser M, Garcia-Castro MI. 2006. Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 441:218-222.
7. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A. 2000. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2:84-89.
8. Bellmeyer A, Krase J, Lindgren J, LaBonne C. 2003. The protooncogene c-myc is an essential regulator of neural crest formation in xenopus. Dev Cell 4:827-839.
9. Bondurand N, Pingault V, Goerich DE, Lemort N, Sock E, Le Caignec C, Wegner M, Goossens M. 2000. Interaction among SOX10, PAX3 and MITF, three genes altered in Waardenburg syndrome. Hum Mol Genet 9:1907-1917.
10. Burstyn-Cohen T, Kalcheim C. 2002. Association between the cell cycle and neural crest delamination through specific regulation of G1/S transition. Dev Cell 3:383-395.
11. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. 2000. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2:76-83.
12. Cheung M, Chaboissier MC, Mynett A, Hirst E, Schedl A, Briscoe J. 2005. The transcriptional control of trunk neural crest induction, survival, and delamination. Dev Cell 8:179-192.
13. Creuzet SE, Martinez S, Le Douarin NM. 2006. The cephalic neural crest exerts a critical effect on forebrain and midbrain development. Proc Natl Acad Sci U S A 103:14033-14038.
14. De Calisto J, Araya C, Marchant L, Riaz CF, Mayor R. 2005. Essential role of non-canonical Wnt signalling in neural crest migration. Development 132:2587-2597.
15. Deardorff MA, Tan C, Saint-Jeannet JP, Klein PS. 2001. A role for frizzled 3 in neural crest development. Development 128:3655-3663.
16. Dottori M, Gross MK, Labosky P, Goulding M. 2001. The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate. Development 128:4127-4138.
17. Elworthy S, Lister JA, Carney TJ, Raible DW, Kelsh RN. 2003. Transcriptional regulation of mitfa accounts for the sox10 requirement in zebrafish melanophore development. Development 130:2809-2818.
18. Endo Y, Osumi N, Wakamatsu Y. 2002. Bimodal functions of Notch-mediated signaling are involved in neural crest formation during avian ectoderm development. Development 129:863-873.
19. Gans C, Northcutt RG. 1983. Neural crest and the origin of vertebrates: A new head. Science 220:268-273.
20. Garcia-Castro MI, Marcelle C, Bronner-Fraser M. 2002. Ectodermal Wnt function as a neural crest inducer. Science 297:848-851.
21. Glavic A, Maris Honore S, Gloria Feijoo C, Bastidas F, Allende ML, Mayor R. 2004a. Role of BMP signaling and the homeoprotein Iroquois in the specification of the cranial placodal field. Dev Biol 272:89-103.
22. Glavic A, Silva F, Aybar MJ, Bastidas F, Mayor R. 2004b. Interplay between Notch signaling and the homeoprotein Xiro1 is required for neural crest induction in Xenopus embryos. Development 131:347-359.
23. Gostling NJ, Shimeld SM. 2003. Protochordate Zic genes define primitive somite compartments and highlight molecular changes underlying neural crest evolution. Evol Dev 5:136-144.
24. Hall BKH, S. 1988. The Neural Crest. Oxford:: Oxford University Press.
25. Holland LZ, Schubert M, Kozmik Z, Holland ND. 1999. AmphiPax3/7, an amphioxus paired box gene: insights into chordate myogenesis, neurogenesis, and the possible evolutionary precursor of definitive vertebrate neural crest. Evol Dev 1:153-165.
26. Holland ND, Panganiban G, Henyey EL, Holland LZ. 1996. Sequence and developmental expression of AmphiDll, an amphioxus Distalless gene transcribed in the ectoderm, epidermis and nervous system: insights into evolution of craniate forebrain and neural crest. Development 122:2911-2920.
27. Hollyday M, McMahon JA, McMahon AP. 1995. Wnt expression patterns in chick embryo nervous system. Mech Dev 52:9-25.
28. Honore 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.
29. Huber WE, Price ER, Widlund HR, Du J, Davis IJ, Wegner M, Fisher DE. 2003. A tissue-restricted cAMP transcriptional response: SOX10 modulates alpha-melanocyte-stimulating hormone-triggered expression of microphthalmia-associated transcription factor in melanocytes. J Biol Chem 278:45224-45230.
30. Ikenouchi J, Matsuda M, Furuse M, Tsukita S. 2003. Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. J Cell Sci 116:1959-1967.
31. Imai KS, Hino K, Yagi K, Satoh N, Satou Y. 2004. Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: Towards a comprehensive understanding of gene networks. Development 131:4047-4058.
32. Imai KS, Levine M, Satoh N, Satou Y. 2006. Regulatory blueprint for a chordate embryo. Science 312:1183-1187.
33. Imai KS, Satoh N, Satou Y. 2002. An essential role of a FoxD gene in notochord induction in Ciona embryos. Development 129:3441-3453.
34. Jeffery WR, Strickler AG, Yamamoto Y. 2004. Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 431:696-699.
35. Jones NC, Trainor PA. 2005. Role of morphogens in neural crest cell determination. J Neurobiol 64:388-404.
36. Kaji T, Artinger KB. 2004. dlx3b and dlx4b function in the development of Rohon-Beard sensory neurons and trigeminal placode in the zebrafish neurula. Dev Biol 276:523-540.
37. Kee Y, Bronner-Fraser M. 2005. To proliferate or to die: role of Id3 in cell cycle progression and survival of neural crest progenitors. Genes Dev 19:744-755.
38. Kelsh RN. 2006. Sorting out Sox10 functions in neural crest development. Bioessays 28:788-798.
39. Khadka D, Luo T, Sargent TD. 2006. Msx1 and Msx2 have shared essential functions in neural crest but may be dispensable in epidermis and axis formation in Xenopus. Int J Dev Biol 50:499-502.
40. Kim J, Lo L, Dormand E, Anderson DJ. 2003. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 38:17-31.
41. Knecht AK, Bronner-Fraser M. 2002. Induction of the neural crest: a multigene process. Nat Rev Genet 3:453-461.
42. Knight RD, Javidan Y, Zhang T, Nelson S, Schilling TF. 2005. AP2-dependent signals from the ectoderm regulate craniofacial development in the zebrafish embryo. Development 132:3127-3138.
43. Knight RD, Nair S, Nelson SS, Afshar A, Javidan Y, Geisler R, Rauch GJ, Schilling TF. 2003. lockjaw encodes a zebrafish tfap2a required for early neural crest development. Development 130:5755-5768.
44. LaBonne C, Bronner-Fraser M. 1998. Neural crest induction in Xenopus: evidence for a two-signal model. Development 125:2403-2414.
45. LaBonne C, Bronner-Fraser M. 2000. Snail-related transcriptional repressors are required in Xenopus for both the induction of the neural crest and its subsequent migration. Dev Biol 221:195-205.
46. Langeland JA, Tomsa JM, Jackman WR, Jr., Kimmel CB. 1998. An amphioxus snail gene: expression in paraxial mesoderm and neural plate suggests a conserved role in patterning the chordate embryo. Dev Genes Evol 208:569-577.
47. Le Douarin NMaK C. 1999. The neural crest, 2nd ed. New York: Cambridge University Press.
48. Lee YH, Aoki Y, Hong CS, Saint-Germain N, Credidio C, Saint-Jeannet JP. 2004. Early requirement of the transcriptional activator Sox9 for neural crest specification in Xenopus. Dev Biol 275:93-103.
49. Lewis JL, Bonner J, Modrell M, Ragland JW, Moon RT, Dorsky RI, Raible DW. 2004. Reiterated Wnt signaling during zebrafish neural crest development. Development 131:1299-1308.
50. Light W, Vernon AE, Lasorella A, Iavarone A, LaBonne C. 2005. Xenopus Id3 is required downstream of Myc for the formation of multipotent neural crest progenitor cells. Development 132:1831-1841.
51. Linker C, Bronner-Fraser M, Mayor R. 2000. Relationship between gene expression domains of Xsnail, Xslug, and Xtwist and cell movement in the prospective neural crest of Xenopus. Dev Biol 224:215-225.
52. Ludwig A, Rehberg S, Wegner M. 2004. Melanocyte-specific expression of dopachrome tautomerase is dependent on synergistic gene activation by the Sox10 and Mitf transcription factors. FEBS Lett 556:236-244.
53. Luo T, Lee YH, Saint-Jeannet JP, Sargent TD. 2003. Induction of neural crest in Xenopus by transcription factor AP2alpha. Proc Natl Acad Sci U S A 100:532-537.
54. Luo T, Matsuo-Takasaki M, Sargent TD. 2001. Distinct roles for Distalless genes Dlx3 and Dlx5 in regulating ectodermal development in Xenopus. Mol Reprod Dev 60:331-337.
55. Ma L, Swalla BJ, Zhou J, Dobias SL, Bell JR, Chen J, Maxson RE, Jeffery WR. 1996. Expression of an Msx homeobox gene in ascidians: insights into the archetypal chordate expression pattern. Dev Dyn 205:308-318.
56. Maroulakou IG, Papas TS, Green JE. 1994. Differential expression of ets-1 and ets-2 proto-oncogenes during murine embryogenesis. Oncogene 9:1551-1565.
57. Mayor R, Aybar MJ. 2001. Induction and development of neural crest in Xenopus laevis. Cell Tissue Res 305:203-209.
58. Mayor R, Guerrero N, Martinez C. 1997. Role of FGF and noggin in neural crest induction. Dev Biol 189:1-12.
59. Mayor R, Morgan R, Sargent MG. 1995. Induction of the prospective neural crest of Xenopus. Development 121:767-777.
60. Meulemans D, Bronner-Fraser M. 2002. Amphioxus and lamprey AP-2 genes: Implications for neural crest evolution and migration patterns. Development 129:4953-4962.
61. Meulemans D, Bronner-Fraser M. 2004. Gene-regulatory interactions in neural crest evolution and development. Dev Cell 7:291-299.
62. Meulemans D, Bronner-Fraser M. 2005. Central role of gene cooption in neural crest evolution. J Exp Zoolog B Mol Dev Evol 304:298-303.
63. Meulemans D, Bronner-Fraser M. 2007. Insights from amphioxus into the evolution of vertebrate cartilage. PLoS ONE 2:e787.
64. 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.
65. Meyer D, Durliat M, Senan F, Wolff M, Andre M, Hourdry J, Remy P. 1997. Ets-1 and Ets-2 proto-oncogenes exhibit differential and restricted expression patterns during Xenopus laevis oogenesis and embryogenesis. Int J Dev Biol 41:607-620.
66. Monsoro-Burq AH, Fletcher RB, Harland RM. 2003. Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. Development 130:3111-3124.
67. Monsoro-Burq AH, Wang E, Harland R. 2005. Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. Dev Cell 8:167-178.
68. Montero-Balaguer M, Lang MR, Sachdev SW, Knappmeyer C, Stewart RA, De La Guardia A, Hatzopoulos AK, Knapik EW. 2006. The mother superior mutation ablates foxd3 activity in neural crest progenitor cells and depletes neural crest derivatives in zebrafish. Dev Dyn 235:3199-3212.
69. Nguyen VH, Schmid B, Trout J, Connors SA, Ekker M, Mullins MC. 1998. Ventral and lateral regions of the zebrafish gastrula, including the neural crest progenitors, are established by a bmp2b/swirl pathway of genes. Dev Biol 199:93-110.
70. Nieto MA, Sargent MG, Wilkinson DG, Cooke J. 1994. Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science 264:835-839.
71. Northcutt RG, Gans C. 1983. The genesis of neural crest and epidermal placodes: A reinterpretation of vertebrate origins. Q Rev Biol 58:1-28.
72. O'Brien EK, d'Alencon C, Bonde G, Li W, Schoenebeck J, Allende ML, Gelb BD, Yelon D, Eisen JS, Cornell RA. 2004. Transcription factor Ap-2alpha is necessary for development of embryonic melanophores, autonomic neurons and pharyngeal skeleton in zebrafish. Dev Biol 265:246-261.
73. O'Donnell M, Hong CS, Huang X, Delnicki RJ, Saint-Jeannet JP. 2006. Functional analysis of Sox8 during neural crest development in Xenopus. Development 133:3817-3826.
74. Potterf SB, Mollaaghababa R, Hou L, Southard-Smith EM, Hornyak TJ, Arnheiter H, PavanWJ. 2001. Analysis of SOX10 function in neural crestderived melanocyte development: SOX10-dependent transcriptional control of dopachrome tautomerase.Dev Biol 237:245-257.
75. Roelink H, Nusse R. 1991. Expression of two members of the Wnt family during mouse development-restricted temporal and spatial patterns in the developing neural tube. Genes Dev 5:381-388.
76. Saint-Jeannet JP, He X, Varmus HE, Dawid IB. 1997. Regulation of dorsal fate in the neuraxis by Wnt-1 and Wnt-3a. Proc Natl Acad Sci U S A 94:13713-13718.
77. Sasai N, Mizuseki K, Sasai Y. 2001. Requirement of FoxD3-class signaling for neural crest determination in Xenopus. Development 128:2525-2536.
78. Sasai Y, De Robertis EM. 1997. Ectodermal patterning in vertebrate embryos. Dev Biol 182:5-20.
79. 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.
80. Satou Y, Imai KS, Levine M, Kohara Y, Rokhsar D, Satoh N. 2003. A genomewide survey of developmentally relevant genes in Ciona intestinalis. I. Genes for bHLH transcription factors. Dev Genes Evol 213:213-221.
81. Sauka-Spengler T, Bronner-Fraser M. 2006. Development and evolution of the migratory neural crest: a gene regulatory perspective. Curr Opin Genet Dev 16:360-366.
82. Sauka-Spengler T, Bronner-Fraser M. 2008. A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cel Biol 9:557-568.
83. 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.
84. Schmidt C, McGonnell IM, Allen S, Otto A, Patel K. 2007. Wnt6 controls amniote neural crest induction through the non-canonical signaling pathway. Dev Dyn 236:2502-2511.
85. Selleck MA, Garcia-Castro MI, Artinger KB, Bronner-Fraser M. 1998. Effects of Shh and Noggin on neural crest formation demonstrate that BMP is required in the neural tube but not ectoderm. Development 125:4919-4930.
86. Sharman AC, Shimeld SM, Holland PW. 1999. An amphioxus Msx gene expressed predominantly in the dorsal neural tube. Dev Genes Evol 209:260-263.
87. Spokony RF, Aoki Y, Saint-Germain N, Magner-Fink E, Saint-Jeannet JP. 2002. The transcription factor Sox9 is required for cranial neural crest development in Xenopus. Development 129:421-432.
88. Stewart RA, Arduini BL, Berghmans S, George RE, Kanki JP, Henion PD, Look AT. 2006. Zebrafish foxd3 is selectively required for neural crest specification, migration and survival. Dev Biol 292: 174-188.
89. Tahtakran SA, Selleck MA. 2003. Ets-1 expression is associated with cranial neural crest migration and vasculogenesis in the chick embryo. Gene Expr Patterns 3:455-458.
90. Tamai K, Semenov M, Kato Y, Spokony R, Liu C, Katsuyama Y, Hess F, Saint-Jeannet JP, He X. 2000. LDL-receptor-related proteins in Wnt signal transduction. Nature 407:530-535.
91. Taneyhill LA, Coles EG, Bronner-Fraser M. 2007. Snail2 directly represses cadherin6B during epithelial-to-mesenchymal transitions of the neural crest. Development 134:1481-1490.
92. Taylor KM, Labonne C. 2005. SoxE factors function equivalently during neural crest and inner ear development and their activity is regulated by SUMOylation. Dev Cell 9:593-603.
93. Tribulo C, Aybar MJ, Nguyen VH, Mullins MC, Mayor R. 2003. Regulation of Msx genes by a Bmp gradient is essential for neural crest specification. Development 130:6441-6452.
94. Wada H, Holland PW, Sato S, Yamamoto H, Satoh N. 1997. Neural tube is partially dorsalized by overexpression of HrPax-37: the ascidian homologue of Pax-3 and Pax-7. Dev Biol 187:240-252.
95. Wada S, Saiga H. 2002. HrzicN, a new Zic family gene of ascidians, plays essential roles in the neural tube and notochord development. Development 129:5597-5608.
96. Wu J, Yang J, Klein PS. 2005. Neural crest induction by the canonical Wnt pathway can be dissociated from anterior-posterior neural patterning in Xenopus. Dev Biol 279:220-232.
97. Yan YL,Willoughby J, Liu D, Crump JG,Wilson C,Miller CT, Singer A, Kimmel C, Westerfield M, Postlethwait JH. 2005. A pair of Sox: Distinct and overlapping functions of zebrafish sox9 co-orthologs in craniofacial and pectoral fin development. Development 132:1069-1083.
98. Yu JK, Holland ND, Holland LZ. 2002. An amphioxus winged helix/forkhead gene, AmphiFoxD: Insights into vertebrate neural crest evolution. Dev Dyn 225:289-297.
99. 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.
100. Yu JK, Satou Y, Holland ND, Shin IT, Kohara Y, Satoh N, Bronner-Fraser M, Holland LZ. 2007. Axial patterning in cephalochordates and the evolution of the organizer. Nature 445:613-617.