1932

Abstract

Neural crest stem/progenitor cells arise early during vertebrate embryogenesis at the border of the forming central nervous system. They subsequently migrate throughout the body, eventually differentiating into diverse cell types ranging from neurons and glia of the peripheral nervous system to bones of the face, portions of the heart, and pigmentation of the skin. Along the body axis, the neural crest is heterogeneous, with different subpopulations arising in the head, neck, trunk, and tail regions, each characterized by distinct migratory patterns and developmental potential. Modern genomic approaches like single-cell RNA- and ATAC-sequencing (seq) have greatly enhanced our understanding of cell lineage trajectories and gene regulatory circuitry underlying the developmental progression of neural crest cells. Here, we discuss how genomic approaches have provided new insights into old questions in neural crest biology by elucidating transcriptional and posttranscriptional mechanisms that govern neural crest formation and the establishment of axial level identity.

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2021-11-23
2024-05-07
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Literature Cited

  1. 1. 
    Ahrens K, Schlosser G. 2005. Tissues and signals involved in the induction of placodal Six1 expression in Xenopus laevis. Dev. Biol. 288:140–59
    [Google Scholar]
  2. 2. 
    Albazerchi A, Stern CD. 2007. A role for the hypoblast (AVE) in the initiation of neural induction, independent of its ability to position the primitive streak. Dev. Biol. 301:2489–503
    [Google Scholar]
  3. 3. 
    Alföldi J, Di Palma F, Grabherr M, Williams C, Kong L et al. 2011. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477:7366587–91
    [Google Scholar]
  4. 4. 
    Baggiolini A, Varum S, Mateos JM, Bettosini D, John N et al. 2015. Premigratory and migratory neural crest cells are multipotent in vivo. Cell Stem Cell 16:3314–22
    [Google Scholar]
  5. 5. 
    Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y et al. 2010. CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463:7283958–62
    [Google Scholar]
  6. 6. 
    Barembaum M, Bronner-Fraser M. 2005. Early steps in neural crest specification. Semin. Cell Dev. Biol. 16:6642–46
    [Google Scholar]
  7. 7. 
    Barembaum M, Bronner ME. 2013. Identification and dissection of a key enhancer mediating cranial neural crest specific expression of transcription factor, Ets-1. Dev. Biol. 382:2567–75
    [Google Scholar]
  8. 8. 
    Barlow AJ, Wallace AS, Thapar N, Burns AJ. 2008. Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation. Development 135:91681–91
    [Google Scholar]
  9. 9. 
    Basch ML, Bronner-Fraser M, García-Castro MI. 2006. Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 441:7090218–22
    [Google Scholar]
  10. 10. 
    Basch ML, García-Castro MI, Bronner-Fraser M. 2004. Molecular mechanisms of neural crest induction. Birth Defects Res. C Embryo Today 72:2109–23
    [Google Scholar]
  11. 11. 
    Betancur P, Bronner-Fraser M, Sauka-Spengler T. 2010. Assembling neural crest regulatory circuits into a gene regulatory network. Annu. Rev. Cell Dev. Biol. 26:581–603
    [Google Scholar]
  12. 12. 
    Betancur P, Bronner-Fraser M, Sauka-Spengler T 2010. Genomic code for Sox10 activation reveals a key regulatory enhancer for cranial neural crest. PNAS 107:83570–75
    [Google Scholar]
  13. 13. 
    Betancur P, Sauka-Spengler T, Bronner M. 2011. A Sox10 enhancer element common to the otic placode and neural crest is activated by tissue-specific paralogs. Development 138:173689–98
    [Google Scholar]
  14. 14. 
    Bockman DE, Redmond ME, Waldo K, Davis H, Kirby ML. 1987. Effect of neural crest ablation on development of the heart and arch arteries in the chick. Am. J. Anat. 180:4332–41
    [Google Scholar]
  15. 15. 
    Bogni S, Trainor P, Natarajan D, Krumlauf R, Pachnis V. 2008. Non-cell-autonomous effects of Ret deletion in early enteric neurogenesis. Development 135:183007–11
    [Google Scholar]
  16. 16. 
    Brewer S, Feng W, Huang J, Sullivan S, Williams T. 2004. Wnt1-Cre-mediated deletion of AP-2α causes multiple neural crest-related defects. Dev. Biol. 267:1135–52
    [Google Scholar]
  17. 17. 
    Briggs JA, Weinreb C, Wagner DE, Megason S, Peshkin L et al. 2018. The dynamics of gene expression in vertebrate embryogenesis at single-cell resolution. Science 360:6392eaar5780
    [Google Scholar]
  18. 18. 
    Bronner-Fraser M. 1986. Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1. Dev. Biol. 115:144–55
    [Google Scholar]
  19. 19. 
    Bronner-Fraser M, Fraser SE. 1988. Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 335:6186161–64
    [Google Scholar]
  20. 20. 
    Bronner ME, LeDouarin NM. 2012. Development and evolution of the neural crest: An overview. Dev. Biol. 366:12–9
    [Google Scholar]
  21. 21. 
    Brunskill EW, Park JS, Chung E, Chen F, Magella B, Potter SS 2014. Single cell dissection of early kidney development: multilineage priming. Development 141:153093–101
    [Google Scholar]
  22. 22. 
    Buitrago-Delgado E, Nordin K, Rao A, Geary L, LaBonne C. 2015. Shared regulatory programs suggest retention of blastula-stage potential in neural crest cells. Science 348:62411332–35Shows that Xenopus neural crest cells retain expression of a pluripotency program during specification.
    [Google Scholar]
  23. 23. 
    Burns AJ, Champeval D, Le Douarin NM 2000. Sacral neural crest cells colonise aganglionic hindgut in vivo but fail to compensate for lack of enteric ganglia. Dev. Biol. 219:130–43
    [Google Scholar]
  24. 24. 
    Burstyn-Cohen T, Stanleigh J, Sela-Donenfeld D, Kalcheim C 2004. Canonical Wnt activity regulates trunk neural crest delamination linking BMP/noggin signaling with G1/S transition. Development 131:215327–39
    [Google Scholar]
  25. 25. 
    Calloni GW, Le Douarin NM, Dupin E 2009. High frequency of cephalic neural crest cells shows coexistence of neurogenic, melanogenic, and osteogenic differentiation capacities. PNAS 106:228947–52
    [Google Scholar]
  26. 26. 
    Chai Y, Jiang X, Ito Y, Bringas P, Han J et al. 2000. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127:81671–79
    [Google Scholar]
  27. 27. 
    Chibon PP. 1967. Marquage nucléaire par la thymidine tritiée des dérivés de la crête neurale chez l'Amphibien Urodèle Pleurodeles waltlii Michah. J. Embryol. Exp. Morphol. 18:3343–58
    [Google Scholar]
  28. 28. 
    Copeland J, Simões-Costa M 2021. Post-transcriptional tuning of FGF signaling mediates neural crest induction. PNAS 117:5233305–16
    [Google Scholar]
  29. 29. 
    Couly GF, Coltey PM, Le Douarin NM 1992. The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114:11–15
    [Google Scholar]
  30. 30. 
    Couly GF, Coltey PM, Le Douarin NM 1993. The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117:2409–29
    [Google Scholar]
  31. 31. 
    Creazzo TL, Godt RE, Leatherbury L, Conway SJ, Kirby ML. 1998. Role of cardiac neural crest cells in cardiovascular development. Annu. Rev. Physiol. 60:267–86
    [Google Scholar]
  32. 32. 
    D'Amico-Martel A, Noden DM. 1983. Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. Am. J. Anat. 166:4445–68
    [Google Scholar]
  33. 33. 
    Davidson EH. 1991. Spatial mechanisms of gene regulation in metazoan embryos. Development 113:11–26
    [Google Scholar]
  34. 34. 
    De Crozé N, Maczkowiak F, Monsoro-Burq AH 2011. Reiterative AP2a activity controls sequential steps in the neural crest gene regulatory network. PNAS 108:1155–60
    [Google Scholar]
  35. 35. 
    Dupin E, Creuzet S, Le Douarin NM 2006. The contribution of the neural crest to the vertebrate body. Adv. Exp. Med. Biol. 589:96–119
    [Google Scholar]
  36. 36. 
    Epstein ML, Mikawa T, Brown AMC, McFarlin DR. 1994. Mapping the origin of the avian enteric nervous system with a retroviral marker. Dev. Dyn. 201:3236–44
    [Google Scholar]
  37. 37. 
    Escot S, Blavet C, Härtle S, Duband J-L, Fournier-Thibault C. 2013. Misregulation of SDF1-CXCR4 signaling impairs early cardiac neural crest cell migration leading to conotruncal defects. Circ. Res. 113:5505–16
    [Google Scholar]
  38. 38. 
    Espinosa-Medina I, Jevans B, Boismoreau F, Chettouh Z, Enomoto H et al. 2017. Dual origin of enteric neurons in vagal Schwann cell precursors and the sympathetic neural crest. PNAS 114:4511980–85
    [Google Scholar]
  39. 39. 
    Ezin AM, Sechrist JW, Zah A, Bronner M, Fraser SE. 2011. Early regulative ability of the neuroepithelium to form cardiac neural crest. Dev. Biol. 349:2238–49
    [Google Scholar]
  40. 40. 
    Fernández-Garre P, Rodríguez-Gallardo L, Gallego-Díaz V, Alvarez IS, Puelles L. 2002. Fate map of the chicken neural plate at stage 4. Development 129:122807–22
    [Google Scholar]
  41. 41. 
    Gammill LS, Bronner-Fraser M. 2002. Genomic analysis of neural crest induction. Development 129:245731–41
    [Google Scholar]
  42. 42. 
    Gammill LS, Bronner-Fraser M. 2003. Neural crest specification: migrating into genomics. Nat. Rev. Neurosci. 4:10795–805
    [Google Scholar]
  43. 43. 
    Gandhi S, Bronner ME. 2018. Insights into neural crest development from studies of avian embryos. Int. J. Dev. Biol. 62:1–3183–94
    [Google Scholar]
  44. 44. 
    Gandhi S, Ezin M, Bronner ME. 2020. Reprogramming axial level identity to rescue neural-crest-related congenital heart defects. Dev. Cell 53:3300–15.e4Shows that ectopic expression of a cardiac subcircuit alters trunk neural crest fate and identity.
    [Google Scholar]
  45. 45. 
    Gandhi S, Hutchins EJ, Maruszko K, Park JH, Thomson M, Bronner ME 2020. Bimodal function of chromatin remodeler Hmga1 in neural crest induction and Wnt-dependent emigration. eLife 9:e57779
    [Google Scholar]
  46. 46. 
    Gandhi S, Li Y, Tang W, Christensen JB, Urrutia HA, Vieceli FM et al. 2021. A single-plasmid approach for genome editing coupled with long-term lineage analysis in chick embryos. Development 148:7dev193565
    [Google Scholar]
  47. 47. 
    Gandhi S, Piacentino ML, Vieceli FM, Bronner ME. 2017. Optimization of CRISPR/Cas9 genome editing for loss-of-function in the early chick embryo. Dev. Biol. 432:186–97
    [Google Scholar]
  48. 48. 
    Gans C, Northcutt RG. 1983. Neural crest and the origin of vertebrates: a new head. Science 220:4594268–73
    [Google Scholar]
  49. 49. 
    Gao Z, Kim GH, Mackinnon AC, Flagg AE, Bassett B et al. 2010. Ets1 is required for proper migration and differentiation of the cardiac neural crest. Development 137:91543–51
    [Google Scholar]
  50. 50. 
    Garriock RJ, Chalamalasetty RB, Kennedy MW, Canizales LC, Lewandoski M, Yamaguchi TP. 2015. Lineage tracing of neuromesodermal progenitors reveals novel Wnt-dependent roles in trunk progenitor cell maintenance and differentiation. Development 142:91628–38
    [Google Scholar]
  51. 51. 
    George RM, Maldonado-Velez G, Firulli AB. 2020. The heart of the neural crest: cardiac neural crest cells in development and regeneration. Development 147:20dev188706
    [Google Scholar]
  52. 52. 
    Gouti M, Tsakiridis A, Wymeersch FJ, Huang Y, Kleinjung J et al. 2014. In vitro generation of neuromesodermal progenitors reveals distinct roles for Wnt signalling in the specification of spinal cord and paraxial mesoderm identity. PLOS Biol 12:8e1001937
    [Google Scholar]
  53. 53. 
    Green SA, Simões-Costa M, Bronner ME. 2015. Evolution of vertebrates as viewed from the crest. Nature 520:7548474–82
    [Google Scholar]
  54. 54. 
    Grossfeld PD, Mattina T, Lai Z, Favier R, Lyons Jones K et al. 2004. The 11q terminal deletion disorder: a prospective study of 110 cases. Am. J. Med. Genet. 129A:51–61
    [Google Scholar]
  55. 55. 
    Hall BK. 2000. The neural crest as a fourth germ layer and vertebrates as quadroblastic not triploblastic. Evol. Dev. 2:13–5
    [Google Scholar]
  56. 56. 
    Hanchate NK, Kondoh K, Lu Z, Kuang D, Ye X et al. 2015. Single-cell transcriptomics reveals receptor transformations during olfactory neurogenesis. Science 350:62651251–55
    [Google Scholar]
  57. 57. 
    Hillier LW, Miller W, Birney E, Warren W, Hardison RC et al. 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:7018695–716
    [Google Scholar]
  58. 58. 
    Hu N, Strobl-Mazzulla PH, Bronner ME. 2014. Epigenetic regulation in neural crest development. Dev. Biol. 396:2159–68
    [Google Scholar]
  59. 59. 
    Hu N, Strobl-Mazzulla P, Sauka-Spengler T, Bronner ME. 2012. DNA methyltransferase3A as a molecular switch mediating the neural tube-to-neural crest fate transition. Genes Dev 26:212380–85
    [Google Scholar]
  60. 60. 
    Huang S, Guo YP, May G, Enver T 2007. Bifurcation dynamics in lineage-commitment in bipotent progenitor cells. Dev. Biol. 305:2695–713
    [Google Scholar]
  61. 61. 
    Huang ZP, Chen JF, Regan JN, Maguire CT, Tang RH et al. 2010. Loss of MicroRNAs in neural crest leads to cardiovascular syndromes resembling human congenital heart defects. Arterioscler. Thromb. Vasc. Biol. 30:122575–86
    [Google Scholar]
  62. 62. 
    Hutchins EJ, Bronner ME. 2018. Draxin acts as a molecular rheostat of canonical Wnt signaling to control cranial neural crest EMT. J. Cell Biol 217:103683–97
    [Google Scholar]
  63. 63. 
    Hutchins EJ, Bronner ME. 2019. Draxin alters laminin organization during basement membrane remodeling to control cranial neural crest EMT. Dev. Biol. 446:2151–58
    [Google Scholar]
  64. 64. 
    Hutchins EJ, Chacon J, Bronner ME. 2020. RNA-binding protein Elavl1/HuR is required for maintenance of cranial neural crest specification. bioRxiv 2020.10.14.338715. https://doi.org/10.1101/2020.10.14.338715
    [Crossref]
  65. 65. 
    Hutson MR, Kirby ML. 2003. Neural crest and cardiovascular development: a 20-year perspective. Birth Defects Res. C Embryo Today 69:12–13
    [Google Scholar]
  66. 66. 
    Hutson MR, Kirby ML. 2007. Model systems for the study of heart development and disease. Cardiac neural crest and conotruncal malformations. Semin. Cell Dev. Biol. 18:1101–10
    [Google Scholar]
  67. 67. 
    Ito Y, Yeo JY, Chytil A, Han J, Bringas P Jr. et al. 2003. Conditional inactivation of Tgfbr2 in cranial neural crest causes cleft palate and calvaria defects. Development 130:215269–80
    [Google Scholar]
  68. 68. 
    Iwafuchi-Doi M, Zaret KS. 2016. Cell fate control by pioneer transcription factors. Development 143:111833–37
    [Google Scholar]
  69. 69. 
    Iwashita T, Kruger GM, Pardal R, Kiel MJ, Morrison SJ. 2003. Hirschsprung disease is linked to defects in neural crest stem cell function. Science 301:5635972–76
    [Google Scholar]
  70. 70. 
    Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM. 2002. Tissue origins and interactions in the mammalian skull vault. Dev. Biol. 241:1106–16
    [Google Scholar]
  71. 71. 
    Jiang X, Rowitch DH, Soriano P, McMahon AP, Sucov HM. 2000. Fate of the mammalian cardiac neural crest. Development 127:81607–16
    [Google Scholar]
  72. 72. 
    Katayama KI, Melendez J, Baumann JM, Leslie JR, Chauhan BK et al. 2011. Loss of RhoA in neural progenitor cells causes the disruption of adherens junctions and hyperproliferation. PNAS 108:187607–12
    [Google Scholar]
  73. 73. 
    Kaucka M, Ivashkin E, Gyllborg D, Zikmund T, Tesarova M et al. 2016. Analysis of neural crest–derived clones reveals novel aspects of facial development. Sci. Adv. 2:8e1600060
    [Google Scholar]
  74. 74. 
    Kerosuo L, Bronner ME. 2016. cMyc regulates the size of the premigratory neural crest stem cell pool. Cell Rep 17:102648–59
    [Google Scholar]
  75. 75. 
    Kirby ML. 1989. Plasticity and predetermination of mesencephalic and trunk neural crest transplanted into the region of the cardiac neural crest. Dev. Biol. 134:2402–12
    [Google Scholar]
  76. 76. 
    Kirby ML, Gale TF, Stewart DE 1983. Neural crest cells contribute to normal aorticopulmonary septation. Science 220:46011059–61Shows that ablation of the dorsal hindbrain results in cardiovascular defects, including persistent truncus arteriosus.
    [Google Scholar]
  77. 77. 
    Kirby ML, Stewart DE. 1983. Neural crest origin of cardiac ganglion cells in the chick embryo: identification and extirpation. Dev. Biol. 97:2433–43
    [Google Scholar]
  78. 78. 
    Kirby ML, Turnage KL, Hays BM. 1985. Characterization of conotruncal malformations following ablation of “cardiac” neural crest. Anat. Rec. 213:187–93
    [Google Scholar]
  79. 79. 
    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 132:133127–38
    [Google Scholar]
  80. 80. 
    Knight RD, Nair S, Nelson SS, Afshar A, Javidan Y et al. 2003. lockjaw encodes a zebrafish tfap2a required for early neural crest development. Development 130:235755–68
    [Google Scholar]
  81. 81. 
    Kuo BR, Erickson CA. 2010. Regional differences in neural crest morphogenesis. Cell Adhes. Migr. 4:4567–85
    [Google Scholar]
  82. 82. 
    Kuo BR, Erickson CA. 2011. Vagal neural crest cell migratory behavior: a transition between the cranial and trunk crest. Dev. Dyn. 240:92084–100
    [Google Scholar]
  83. 83. 
    Laslo P, Spooner CJ, Warmflash A, Lancki DW, Lee HJ et al. 2006. Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 126:4755–66
    [Google Scholar]
  84. 84. 
    Le Douarin NM 1969. Details of the interphase nucleus in Japanese quail (Coturnix coturnix japonica). Bull. Biol. Fr. Belg. 103:3435–52
    [Google Scholar]
  85. 85. 
    Le Douarin NM 1973. A biological cell labeling technique and its use in experimental embryology. Dev. Biol. 30:1217–22
    [Google Scholar]
  86. 86. 
    Le Douarin NM 1980. The ontogeny of the neural crest in avian embryo chimaeras. Nature 286:5774663–69
    [Google Scholar]
  87. 87. 
    Le Douarin NM, Kalcheim C. 1999. The neural crest: a source of mesenchymal cells. The Neural Crest60–152 Cambridge, UK: Cambridge Univ. Press. , 2nd ed..
    [Google Scholar]
  88. 88. 
    Le Douarin NM, Dupin E 2014. The neural crest, a fourth germ layer of the vertebrate embryo: significance in chordate evolution. Neural Crest Cells: Evolution, Development and Disease PA Trainor 3–26 London: Elsevier
    [Google Scholar]
  89. 89. 
    Le Douarin NM, Kalcheim C. 1999. The Neural Crest Cambridge, UK: Cambridge Univ. Press. , 2nd ed..
  90. 90. 
    Le Douarin NM, Teillet MA. 1971. Localization, by the method of interspecific grafts of the neural area from which adrenal cells arise in the bird embryo. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D 272:3481–84
    [Google Scholar]
  91. 91. 
    Le Douarin NM, Teillet MA. 1973. The migration of neural crest cells to the wall of the digestive tract in avian embryo. J. Embryol. Exp. Morphol. 30:131–48
    [Google Scholar]
  92. 92. 
    Le Douarin NM, Teillet MA. 1974. Experimental analysis of the migration and differentiation of neuro-blasts of the autonomic nervous system and of neurectodermal mesenchymal derivatives, using a biological cell marking technique. Dev. Biol. 41:1162–84
    [Google Scholar]
  93. 93. 
    Lignell A, Kerosuo L, Streichan SJ, Cai L, Bronner ME. 2017. Identification of a neural crest stem cell niche by Spatial Genomic Analysis. Nat. Commun. 8:1830
    [Google Scholar]
  94. 94. 
    Lindblad-Toh K, Garber M, Zuk O, Lin MF, Parker BJ et al. 2011. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478:7370476–82
    [Google Scholar]
  95. 95. 
    Ling ITC, Sauka-Spengler T. 2019. Early chromatin shaping predetermines multipotent vagal neural crest into neural, neuronal and mesenchymal lineages. Nat. Cell Biol. 21:121504–17
    [Google Scholar]
  96. 96. 
    Liu F, Walmsley M, Rodaway A, Patient R. 2008. Fli1 acts at the top of the transcriptional network driving blood and endothelial development. Curr. Biol. 18:161234–40
    [Google Scholar]
  97. 97. 
    Long HK, Osterwalder M, Welsh IC, Hansen K, Davies JOJ et al. 2020. Loss of extreme long-range enhancers in human neural crest drives a craniofacial disorder. Cell Stem Cell 27:5765–783.e14
    [Google Scholar]
  98. 98. 
    Lukoseviciute M, Gavriouchkina D, Williams RM, Hochgreb-Hagele T, Senanayake U et al. 2018. From pioneer to repressor: Bimodal foxd3 activity dynamically remodels neural crest regulatory landscape in vivo. Dev. Cell 47:5608–628.e6Argues that Foxd3 acts as a pioneer factor to govern neural crest specification and differentiation.
    [Google Scholar]
  99. 99. 
    Lukoseviciute M, Mayes S, Sauka-Spengler T. 2021. Neuromesodermal progenitor origin of trunk neural crest in vivo. bioRxiv 2021.02.10.430513. https://doi.org/10.1101/2021.02.10.430513
    [Crossref]
  100. 100. 
    Luo T, Lee Y-H, Saint-Jeannet J-P, Sargent TD 2003. Induction of neural crest in Xenopus by transcription factor AP2α. PNAS 100:2532–37
    [Google Scholar]
  101. 101. 
    Martik ML, Bronner ME. 2017. Regulatory logic underlying diversification of the neural crest. Trends Genet 33:10715–27
    [Google Scholar]
  102. 102. 
    Martik ML, Gandhi S, Uy BR, Gillis JA, Green SA et al. 2019. Evolution of the new head by gradual acquisition of neural crest regulatory circuits. Nature 574:7780675–78Argues that a cranial crest subcircuit was co-opted during evolution to give rise to craniofacial derivatives.
    [Google Scholar]
  103. 103. 
    Merrill AE, Bochukova EG, Brugger SM, Ishii M, Pilz DT et al. 2006. Cell mixing at a neural crest-mesoderm boundary and deficient ephrin-Eph signaling in the pathogenesis of craniosynostosis. Hum. Mol. Genet. 15:81319–28
    [Google Scholar]
  104. 104. 
    Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL et al. 2007. Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 447:7141167–77
    [Google Scholar]
  105. 105. 
    Monsoro-Burq A-H, Fletcher RB, Harland RM. 2003. Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. Development 130:143111–24
    [Google Scholar]
  106. 106. 
    Nakamura H, Ayer-le Lievre CS. 1982. Mesectodermal capabilities of the trunk neural crest of birds. J. Embryol. Exp. Morphol. 70:1–18
    [Google Scholar]
  107. 107. 
    Neeb Z, Lajiness JD, Bolanis E, Conway SJ. 2013. Cardiac outflow tract anomalies. Wiley Interdiscip. Rev. Dev. Biol. 2:4499–530
    [Google Scholar]
  108. 108. 
    Nie X, Wang Q, Jiao K. 2011. Dicer activity in neural crest cells is essential for craniofacial organogenesis and pharyngeal arch artery morphogenesis. Mech. Dev. 128:3–4200–7
    [Google Scholar]
  109. 109. 
    Nieto MA, Sargent MG, Wilkinson DG, Cooke J. 1994. Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science 264:5160835–39
    [Google Scholar]
  110. 110. 
    Noden DM. 1975. An analysis of the migratory behavior of avian cephalic neural crest cells. Dev. Biol. 42:1106–30
    [Google Scholar]
  111. 111. 
    Noden DM. 1978. The control of avian cephalic neural crest cytodifferentiation: I. Skeletal and connective tissues. Dev. Biol. 67:2296–312
    [Google Scholar]
  112. 112. 
    Northcutt RG. 2005. The new head hypothesis revisited. J. Exp. Zool. B Mol. Dev. Evol. 304B:4274–97
    [Google Scholar]
  113. 113. 
    O'Donnell M, Hong C-S, Huang X, Delnicki RJ, Saint-Jeannet J-P. 2006. Functional analysis of Sox8 during neural crest development in Xenopus. Development 133:193817–26
    [Google Scholar]
  114. 114. 
    Osório L, Teillet M-A, Catala M. 2009. Role of noggin as an upstream signal in the lack of neuronal derivatives found in the avian caudal-most neural crest. Development 136:101717–26
    [Google Scholar]
  115. 115. 
    Pattyn A, Morin X, Cremer H, Goridis C, Brunet J-F. 1999. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399:6734366–70
    [Google Scholar]
  116. 116. 
    Pieper M, Ahrens K, Rink E, Peter A, Schlosser G. 2012. Differential distribution of competence for panplacodal and neural crest induction to non-neural and neural ectoderm. Development 139:61175–87
    [Google Scholar]
  117. 117. 
    Platt JB. 1893. Ectodermic origin of the cartilages of the head. Anatomi. Anz. 8:506–9
    [Google Scholar]
  118. 118. 
    Powell DR, Blasky AJ, Britt SG, Artinger KB. 2013. Riding the crest of the wave: parallels between the neural crest and cancer in epithelial-to-mesenchymal transition and migration. Wiley Interdiscip. Rev. Syst. Biol. Med. 5:4511–22
    [Google Scholar]
  119. 119. 
    Rabadán MA, Herrera A, Fanlo L, Usieto S, Carmona-Fontaine C et al. 2016. Delamination of neural crest cells requires transient and reversible Wnt inhibition mediated by Dact1/2. Development 143:122194–205
    [Google Scholar]
  120. 120. 
    Reeves R, Beckerbauer L. 2001. HMGI/Y proteins: flexible regulators of transcription and chromatin structure. Biochim. Biophys. Acta Gene Struct. Expr. 1519:1–213–29
    [Google Scholar]
  121. 121. 
    Resar L, Chia L, Xian L. 2018. Lessons from the crypt: HMGA1—amping up Wnt for stem cells and tumor progression. Cancer Res 78:81890–97
    [Google Scholar]
  122. 122. 
    Rex M, Orme A, Uwanogho D, Tointon K, Wigmore PM et al. 1997. Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev. Dyn. 209:3323–32
    [Google Scholar]
  123. 123. 
    Rickmann M, Fawcett JW, Keynes RJ. 1985. The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. J. Embryol. Exp. Morphol. 90:437–55
    [Google Scholar]
  124. 124. 
    Roellig D, Tan-Cabugao J, Esaian S, Bronner ME 2017. Dynamic transcriptional signature and cell fate analysis reveals plasticity of individual neural plate border cells. eLife 6:331–42Shows that neural plate border precursors coexpress markers associated with neural, neural crest, and ectodermal lineages.
    [Google Scholar]
  125. 125. 
    Rogers CD, Ferzli GS, Casey ES. 2011. The response of early neural genes to FGF signaling or inhibition of BMP indicate the absence of a conserved neural induction module. BMC Dev. Biol. 11:174
    [Google Scholar]
  126. 126. 
    Rothstein M, Bhattacharya D, Simões-Costa M. 2018. The molecular basis of neural crest axial identity. Dev. Biol. 444:S170–80
    [Google Scholar]
  127. 127. 
    Rothstein M, Simões-Costa M. 2020. Heterodimerization of TFAP2 pioneer factors drives epigenomic remodeling during neural crest specification. Genome Res 30:135–48
    [Google Scholar]
  128. 128. 
    Sauka-Spengler T, Bronner-Fraser M. 2008. A gene regulatory network orchestrates neural crest formation. Nat. Rev. Mol. Cell Biol. 9:7557–68
    [Google Scholar]
  129. 129. 
    Schoenwolf GC, Sheard P. 1990. Fate mapping the avian epiblast with focal injections of a fluorescent-histochemical marker: ectodermal derivatives. J. Exp. Zool. 255:3323–39
    [Google Scholar]
  130. 130. 
    Serbedzija GN, Bronner-Fraser M, Fraser SE. 1989. A vital dye analysis of the timing and pathways of avian trunk neural crest cell migration. Development 106:4809–16
    [Google Scholar]
  131. 131. 
    Shah SN, Resar LMS. 2012. High mobility group A1 and cancer: potential biomarker and therapeutic target. Histol. Histopathol. 27:5567–79
    [Google Scholar]
  132. 132. 
    Sieber-Blum M, Reed W, Lidov HGW 1983. Serotoninergic differentiation of quail neural crest cells in vitro. Dev. Biol. 99:2352–58
    [Google Scholar]
  133. 133. 
    Sieber-Blum M, Sieber F, Yamada KM. 1981. Cellular fibronectin promotes adrenergic differentiation of quail neural crest cells in vitro. Exp. Cell Res. 133:2285–95
    [Google Scholar]
  134. 134. 
    Simões-Costa M, Bronner ME. 2015. Establishing neural crest identity: a gene regulatory recipe. Development 142:2242–57
    [Google Scholar]
  135. 135. 
    Simões-Costa M, Bronner ME 2016. Reprogramming of avian neural crest axial identity and cell fate. Science 352:62931570–73Shows that ectopic expression of a cranial subcircuit in the trunk results in a broad developmental potential.
    [Google Scholar]
  136. 136. 
    Simões-Costa M, 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 8:12e1003142
    [Google Scholar]
  137. 137. 
    Simões-Costa M, Stone M, Bronner ME. 2015. Axud1 integrates Wnt signaling and transcriptional inputs to drive neural crest formation. Dev. Cell 34:5544–54
    [Google Scholar]
  138. 138. 
    Simões-Costa M, Tan-Cabugao J, Antoshechkin I, Sauka-Spengler T, Bronner ME. 2014. Transcriptome analysis reveals novel players in the cranial neural crest gene regulatory network. Genome Res 24:2281–90
    [Google Scholar]
  139. 139. 
    Skene PJ, Henikoff S 2017. An efficient targeted nuclease strategy for high-resolution mapping of DNA binding sites. eLife 6:e21856
    [Google Scholar]
  140. 140. 
    Smith J. 1990. The avian neural crest as a model system for the study of cell lineages. Int. J. Dev. Biol. 34:1157–62
    [Google Scholar]
  141. 141. 
    Snider P, Olaopa M, Firulli AB, Conway SJ. 2007. Cardiovascular development and the colonizing cardiac neural crest lineage. ScientificWorldJournal 7:1090–113
    [Google Scholar]
  142. 142. 
    Soldatov R, Kaucka M, Kastriti ME, Petersen J, Chontorotzea T et al. 2019. Spatiotemporal structure of cell fate decisions in murine neural crest. Science 364:6444eaas9536Shows that ectopic expression of Twist1 confers mesenchymal identity onto trunk neural crest cells.
    [Google Scholar]
  143. 143. 
    Stemple DL, Anderson DJ. 1992. Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71:6973–85
    [Google Scholar]
  144. 144. 
    Stern CD, Downs KM. 2012. The hypoblast (visceral endoderm): an evo-devo perspective. Development 139:61059–69
    [Google Scholar]
  145. 145. 
    Stoller JZ, Epstein JA. 2005. Cardiac neural crest. Semin. Cell Dev. Biol 16:6704–15
    [Google Scholar]
  146. 146. 
    Streit A. 2002. Extensive cell movements accompany formation of the otic placode. Dev. Biol. 249:2237–54
    [Google Scholar]
  147. 147. 
    Streit A, Berliner AJ, Papanayotou C, Sirulnik A, Stern CD. 2000. Initiation of neural induction by FGF signalling before gastrulation. Nature 406:679174–78
    [Google Scholar]
  148. 148. 
    Streit A, Stern CD. 1999. Establishment and maintenance of the border of the neural plate in the chick: involvement of FGF and BMP activity. Mech. Dev. 82:1–251–66
    [Google Scholar]
  149. 149. 
    Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T et al. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:5861–72
    [Google Scholar]
  150. 150. 
    Tallquist MD, Soriano P. 2003. Cell autonomous requirement for PDGFRα in populations of cranial and cardiac neural crest cells. Development 130:3507–18
    [Google Scholar]
  151. 151. 
    Tang W, Bronner ME. 2020. Neural crest lineage analysis: from past to future trajectory. Development 147:20dev193193
    [Google Scholar]
  152. 152. 
    Tang W, Li Y, Li A, Bronner ME 2021. Clonal analysis and dynamic imaging identify multipotency of individual Gallus gallus caudal hindbrain neural crest cells toward cardiac and enteric fates. Nat. Commun. 12:1894
    [Google Scholar]
  153. 153. 
    Tang W, Martik ML, Li Y, Bronner ME. 2019. Cardiac neural crest contributes to cardiomyocytes in amniotes and heart regeneration in zebrafish. eLife 8:e47929Shows that a cardiac neural crest gene regulatory network is reactivated in response to cardiac injury.
    [Google Scholar]
  154. 154. 
    Tani-Matsuhana S, Vieceli FM, Gandhi S, Inoue K, Bronner ME. 2018. Transcriptome profiling of the cardiac neural crest reveals a critical role for MafB. Dev. Biol. 444:S209–18
    [Google Scholar]
  155. 155. 
    Thawani A, Groves AK. 2020. Building the border: development of the chordate neural plate border region and its derivatives. Front. Physiol. 11:608880
    [Google Scholar]
  156. 156. 
    Théveneau E, Duband J-L, Altabef M. 2007. Ets-1 confers cranial features on neural crest delamination. PLOS ONE 2:11e1142
    [Google Scholar]
  157. 157. 
    Treutlein B, Brownfield DG, Wu AR, Neff NF, Mantalas GL et al. 2014. Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq. Nature 509:7500371–75
    [Google Scholar]
  158. 158. 
    Tucker RP. 2004. Neural crest cells: a model for invasive behavior. Int. J. Biochem. Cell Biol. 36:2173–77
    [Google Scholar]
  159. 159. 
    Vega-Lopez GA, Cerrizuela S, Aybar MJ. 2017. Trunk neural crest cells: formation, migration and beyond. Int. J. Dev. Biol. 61:1–25–15
    [Google Scholar]
  160. 160. 
    Vincentz JW, Firulli BA, Lin A, Spicer DB, Howard MJ, Firulli AB. 2013. Twist1 controls a cell-specification switch governing cell fate decisions within the cardiac neural crest. PLOS Genet 9:3e1003405
    [Google Scholar]
  161. 161. 
    Waldo KL, Kirby ML. 1993. Cardiac neural crest contribution to the pulmonary artery and sixth aortic arch artery complex in chick embryos aged 6 to 18 days. Anat. Rec. 237:3385–99
    [Google Scholar]
  162. 162. 
    Waldo KL, Miyagawa-Tomita S, Kumiski D, Kirby ML. 1998. Cardiac neural crest cells provide new insight into septation of the cardiac outflow tract: aortic sac to ventricular septal closure. Dev. Biol. 196:2129–44
    [Google Scholar]
  163. 163. 
    Walmsley M, Ciau-Uitz A, Patient R. 2002. Adult and embryonic blood and endothelium derive from distinct precursor populations which are differentially programmed by BMP in Xenopus. Development 129:245683–95
    [Google Scholar]
  164. 164. 
    Williams RM, Candido-Ferreira I, Repapi E, Gavriouchkina D, Senanayake U et al. 2019. Reconstruction of the global neural crest gene regulatory network in vivo. Dev. Cell 51:2255–76.e7Description of the first top-down unbiased gene regulatory network that controls cranial neural crest development.
    [Google Scholar]
  165. 165. 
    Williams RM, Senanayake U, Artibani M, Taylor G, Wells D et al. 2018. Genome and epigenome engineering CRISPR toolkit for in vivo modulation of cis-regulatory interactions and gene expression in the chicken embryo. Development 145:4dev160333
    [Google Scholar]
  166. 166. 
    Xi J, Wu Y, Li G, Ma L, Feng K et al. 2017. Mir-29b mediates the neural tube versus neural crest fate decision during embryonic stem cell neural differentiation. Stem Cell Rep 9:2571–86
    [Google Scholar]
  167. 167. 
    Xian L, Georgess D, Huso T, Cope L, Belton A et al. 2017. HMGA1 amplifies Wnt signalling and expands the intestinal stem cell compartment and Paneth cell niche. Nat. Commun. 8:15008
    [Google Scholar]
  168. 168. 
    Ye M, Coldren C, Liang X, Mattina T, Goldmuntz E et al. 2009. Deletion of ETS-1, a gene in the Jacobsen syndrome critical region, causes ventricular septal defects and abnormal ventricular morphology in mice. Hum. Mol. Genet. 19:4648–56
    [Google Scholar]
  169. 169. 
    Ye M, Yin Y, Fukatsu K, Grossfeld P 2016. Evidence that deletion of ETS-1, a gene in the Jacobsen syndrome (11q-) cardiac critical region, causes congenital heart defects through impaired cardiac neural crest cell function. Etiology and Morphogenesis of Congenital Heart Disease: From Gene Function and Cellular Interaction to Morphology T Nakanishi, R Markwald, H Baldwin, B Keller, D Srivastava, H Yamagishi 361–69 Tokyo: Springer
    [Google Scholar]
  170. 170. 
    Yoshida T, Vivatbutsiri P, Morriss-Kay G, Saga Y, Iseki S. 2008. Cell lineage in mammalian craniofacial mesenchyme. Mech. Dev. 125:9–10797–808
    [Google Scholar]
  171. 171. 
    Zalc A, Sinha R, Gulati GS, Wesche DJ, Daszczuk P et al. 2021. Reactivation of the pluripotency program precedes formation of the cranial neural crest. Science 371:6529eabb4776Shows that a pluripotency program is reactivated in the neural crest after their specification.
    [Google Scholar]
  172. 172. 
    Zaret KS, Carroll JS. 2011. Pioneer transcription factors: establishing competence for gene expression. Genes Dev 25:212227–41
    [Google Scholar]
  173. 173. 
    Zhu Q, Song L, Peng G, Sun N, Chen J et al. 2014. The transcription factor Pou3f1 promotes neural fate commitment via activation of neural lineage genes and inhibition of external signaling pathways. eLife 3:e02224
    [Google Scholar]
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