The Neural Crest: A Remarkable Model System for Studying Development and Disease

  • Chaya KalcheimEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 1976)


Neural crest cells are the embryonic precursors of most neurons and all glia of the peripheral nervous system, pigment cells, some endocrine components, and connective tissue of the head, face, neck, and heart. Following induction, crest cells undergo an epithelial to mesenchymal transition that enables them to migrate along specific pathways culminating in their phenotypic differentiation. Researching this unique embryonic population has revealed important understandings of basic biological and developmental principles. These principles are likely to assist in clarifying the etiology and help in finding strategies for the treatment of neural crest diseases, collectively termed neurocristopathies. The progress achieved in neural crest research is made feasible thanks to the continuous development of species-specific in vivo and in vitro paradigms and more recently the possibility to produce neural crest cells and specific derivatives from embryonic or induced pluripotent stem cells. All of the above assist us in elucidating mechanisms that regulate neural crest development using state-of-the art cellular, molecular, and imaging approaches.

Key words

Cell migration Dorsal root ganglia Embryonic stem cells Epithelial-mesenchymal transition Induced pluripotent stem cells Melanocyte Neural tube PNS Schwann cell Sympathetic ganglia Vertebrate embryo 



I am grateful to Joel Yisraeli for critical reading of the manuscript. This work was supported by a grant from the Israel Science Foundation (#97/13) to C.K.


  1. 1.
    Kalcheim C (2000) Mechanisms of early neural crest development: from cell specification to migration. Int Rev Cytol 200:143–196CrossRefGoogle Scholar
  2. 2.
    Bronner ME (2012) Formation and migration of neural crest cells in the vertebrate embryo. Histochem Cell Biol 138(2):179–186. Scholar
  3. 3.
    Kalcheim C (2015) Epithelial-Mesenchymal transitions during neural crest and somite development. J Clin Med 5. Scholar
  4. 4.
    Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139(5):871–890. Scholar
  5. 5.
    Le Douarin NM, Kalcheim C (1999) The neural crest, 2nd edn. Cambridge University Press, New YorkCrossRefGoogle Scholar
  6. 6.
    Groves A, Bronner Fraser M (1999) Neural crest diversification. Curr Top Dev Biol 43:221–258CrossRefGoogle Scholar
  7. 7.
    Graham A, Begbie J, McGonnell I (2004) Significance of the cranial neural crest. Dev Dyn 229(1):5–13. Scholar
  8. 8.
    Noden DM (1978) The control of avian cephalic neural crest cytodifferentiation. I. Skeletal and connective tissues. Dev Biol 67:296–312CrossRefGoogle Scholar
  9. 9.
    Etchevers HC, Vincent C, Le Douarin M, Couly GF (2001) The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 128:1059–1068PubMedGoogle Scholar
  10. 10.
    Weston JA, Thiery JP (2015) Pentimento: neural crest and the origin of mesectoderm. Dev Biol 401(1):37–61. Scholar
  11. 11.
    Kulesa PM, Gammill LS (2010) Neural crest migration: patterns, phases and signals. Dev Biol 344(2):566–568. S0012-1606(10)00291-5 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Minoux M, Rijli FM (2010) Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development. Development 137(16):2605–2621. 137/16/2605 [pii]CrossRefPubMedGoogle Scholar
  13. 13.
    Kuo BR, Erickson CA (2011) Vagal neural crest cell migratory behavior: a transition between the cranial and trunk crest. Dev Dyn 240(9):2084–2100. Scholar
  14. 14.
    Kuo BR, Erickson CA (2010) Regional differences in neural crest morphogenesis. Cell Adhes Migr 4(4):567–585. 12890 [pii]CrossRefGoogle Scholar
  15. 15.
    Le Douarin NM (1982) The neural crest, 1st edn. Cambridge University Press, New YorkGoogle Scholar
  16. 16.
    Horstadius S (1950) The mechanics of sea urchin development. Annee Biol 26:381–398PubMedGoogle Scholar
  17. 17.
    Weston JA (1963) A radioautographic analysis of the migration and localization of trunk neural crest cells in the chick. Dev Biol 6:279–310CrossRefGoogle Scholar
  18. 18.
    Chibon P (1967) Nuclear labelling by tritiated thymidine of neural crest derivatives in the amphibian Urodele Pleurodeles waltlii Michah. J Embryol Exp Morphol 18:343–358PubMedGoogle Scholar
  19. 19.
    Le Douarin NM, Dieterlen-Lievre F (2013) How studies on the avian embryo have opened new avenues in the understanding of development: a view about the neural and hematopoietic systems. Develop Growth Differ 55(1):1–14. Scholar
  20. 20.
    Raible DW, Eisen JS (1994) Restriction of neural crest cell fate in the trunk of the embryonic zebrafish. Development 120:495–503PubMedGoogle Scholar
  21. 21.
    Raible DW, Eisen JS (1996) Regulative interactions in zebrafish neural crest. Development 122:501–507PubMedGoogle Scholar
  22. 22.
    Schilling TF, Kimmel CB (1994) Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120(3):483–494PubMedGoogle Scholar
  23. 23.
    Bronner-Fraser M, Fraser SE (1988) Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 335:161–164CrossRefGoogle Scholar
  24. 24.
    Serbedzija GN, Bronner-Fraser M, Fraser SE (1992) Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116:297–307PubMedGoogle Scholar
  25. 25.
    Krispin S, Nitzan E, Kassem Y, Kalcheim C (2010) Evidence for a dynamic spatiotemporal fate map and early fate restrictions of premigratory avian neural crest. Development 137:585–595. 137/4/585 [pii]CrossRefPubMedGoogle Scholar
  26. 26.
    Nakamura H, Funahashi J (2001) Introduction of DNA into chick embryos by in ovo electroporation. Methods 24(1):43–48. Scholar
  27. 27.
    Sato Y, Kasai T, Nakagawa S, Tanabe K, Watanabe T, Kawakami K, Takahashi Y (2007) Stable integration and conditional expression of electroporated transgenes in chicken embryos. Dev Biol 305:616–624. S0012-1606(07)00092-9 [pii]CrossRefPubMedGoogle Scholar
  28. 28.
    Ben-Yair R, Kalcheim C (2005) Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates. Development 132:689–701CrossRefGoogle Scholar
  29. 29.
    Rios AC, Denans N, Marcelle C (2010) Real-time observation of Wnt beta-catenin signaling in the chick embryo. Dev Dyn 239:346–353. Scholar
  30. 30.
    Applebaum M, Ben-Yair R, Kalcheim C (2014) Segregation of striated and smooth muscle lineages by a Notch-dependent regulatory network. BMC Biol 12:53. Scholar
  31. 31.
    Le Dreau G, Garcia-Campmany L, Rabadan MA, Ferronha T, Tozer S, Briscoe J, Marti E (2012) Canonical BMP7 activity is required for the generation of discrete neuronal populations in the dorsal spinal cord. Development 139:259–268. dev.074948 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Nitzan E, Avraham O, Kahane N, Ofek S, Kumar D, Kalcheim C (2016) Dynamics of BMP and Hes1/Hairy1 signaling in the dorsal neural tube underlies the transition from neural crest to definitive roof plate. BMC Biol 14:23. Scholar
  33. 33.
    Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70–71. Scholar
  34. 34.
    Danielian P, Muccino D, Rowitch D, Michael S, McMahon A (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr Biol 8:1323–1326CrossRefGoogle Scholar
  35. 35.
    Jiang XB, Rowitch DH, Soriano P, McMahon AP, Sucov HM (2000) Fate of the mammalian cardiac neural crest. Development 127:1607–1616PubMedPubMedCentralGoogle Scholar
  36. 36.
    Rios AC, Fu NY, Lindeman GJ, Visvader JE (2014) In situ identification of bipotent stem cells in the mammary gland. Nature 506:322–327. Scholar
  37. 37.
    Livet J, Weissman TA, Kang H, Draft RW, Lu J, Bennis RA, Sanes JR, Lichtman JW (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450(7166):56–62. Scholar
  38. 38.
    Baggiolini A, Varum S, Mateos JM, Bettosini D, John N, Bonalli M, Ziegler U, Dimou L, Clevers H, Furrer R, Sommer L (2015) Premigratory and migratory neural crest cells are multipotent in vivo. Cell Stem Cell 16(3):314–322. Scholar
  39. 39.
    Teillet MA, Kalcheim C, Le Douarin NM (1987) Formation of the dorsal root ganglia in the avian embryo: segmental origin and migratory behavior of neural crest progenitor cells. Dev Biol 120:329–347CrossRefGoogle Scholar
  40. 40.
    Yip JW (1986) Migratory pathways of sympathetic ganglioblasts and other neural crest derivatives in chick embryos. J Neurosci 6:3465–3473CrossRefGoogle Scholar
  41. 41.
    Kalcheim C (2011) Regulation of trunk myogenesis by the neural crest: a new facet of neural crest-somite interactions. Dev Cell 21:187–188. S1534-5807(11)00301-7 [pii]CrossRefPubMedGoogle Scholar
  42. 42.
    Borchin BE, Barberi T (2015) The use of human pluripotent stem cells for the in vitro derivation of cranial placodes and neural crest cells. Curr Top Dev Biol 111:497–514. Scholar
  43. 43.
    Le Douarin NM (1990) Cell lineage segregation during neural crest ontogeny. Ann N Y Acad Sci 599:131–140CrossRefGoogle Scholar
  44. 44.
    Le Douarin NM, Dupin E (2003) Multipotentiality of the neural crest. Curr Opin Genet Dev 13:529–536. S0959437X03001138 [pii]CrossRefGoogle Scholar
  45. 45.
    Rothman TP, Le Douarin NM, Fontaine-Perus JC, Gershon MD (1990) Developmental potential of neural crest-derived cells migrating from segments of developing quail bowel back-grafted into younger chick host embryos. Development 109:411–423PubMedGoogle Scholar
  46. 46.
    Le Lievre CS, Schweizer GG, Ziller CM, Le Douarin NM (1980) Restriction of developmental capabilities in neural crest cell derivatives as tested by in vivo transplantation experiments. Dev Biol 77:362–378CrossRefGoogle Scholar
  47. 47.
    Schweizer GG, Ayer-Le Lievre C, Le Douarin NM (1983) Restrictions of developmental capabilities in the dorsal root ganglia in the course of development. Cell Differ 13:191–200CrossRefGoogle Scholar
  48. 48.
    Nitzan E, Krispin S, Pfaltzgraff ER, Klar A, Labosky P, Kalcheim C (2013) A dynamic code of dorsal neural tube genes regulates the segregation between neurogenic and melanogenic neural crest cells. Development 140:2269–2279CrossRefGoogle Scholar
  49. 49.
    Raible DW, Eisen JS (1992) Spatiotemporal restriction of trunk neural crest cell lineage in the embryonic zebrafish. Soc Neurosci Abstr 18Google Scholar
  50. 50.
    Wakamatsu Y, Maynard TM, Weston JA (2000) Fate determination of neural crest cells by NOTCH-mediated lateral inhibition and asymmetrical cell division during gangliogenesis. Development 127:2811–2821PubMedGoogle Scholar
  51. 51.
    Shtukmaster S, Schier MC, Huber K, Krispin S, Kalcheim C, Unsicker K (2013) Sympathetic neurons and chromaffin cells share a common progenitor in the neural crest in vivo. Neural Dev 8:12. Scholar
  52. 52.
    Adameyko I, Lallemend F, Aquino JB, Pereira JA, Topilko P, Muller T, Fritz N, Beljajeva A, Mochii M, Liste I, Usoskin D, Suter U, Birchmeier C, Ernfors P (2009) Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 139:366–379. S0092-8674(09)01043-5 [pii]CrossRefPubMedGoogle Scholar
  53. 53.
    Theveneau E, Mayor R (2011) Collective cell migration of the cephalic neural crest: the art of integrating information. Genesis 49(4):164–176. Scholar
  54. 54.
    Strobl-Mazzulla PH, Bronner ME (2012) Epithelial to mesenchymal transition: new and old insights from the classical neural crest model. Semin Cancer Biol 22(5–6):411–416. Scholar
  55. 55.
    Theveneau E, Mayor R (2012) Neural crest delamination and migration: from epithelium-to-mesenchyme transition to collective cell migration. Dev Biol 366(1):34–54. Scholar
  56. 56.
    Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7(2):131–142. Scholar
  57. 57.
    Yang J, Weinberg RA (2008) Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14(6):818–829. Scholar
  58. 58.
    Sela-Donenfeld D, Kalcheim C (1999) Regulation of the onset of neural crest migration by coordinated activity of BMP4 and noggin in the dorsal neural tube. Development 126:4749–4762PubMedGoogle Scholar
  59. 59.
    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(21):5327–5339CrossRefGoogle Scholar
  60. 60.
    Burstyn-Cohen T, Kalcheim C (2002) Association between the cell cycle and neural crest delamination through specific regulation of G1/S transition. Dev Cell 3:383–395CrossRefGoogle Scholar
  61. 61.
    Shoval I, Ludwig A, Kalcheim C (2007) Antagonistic roles of full-length N-cadherin and its soluble BMP cleavage product in neural crest delamination. Development 134:491–501CrossRefGoogle Scholar
  62. 62.
    Groysman M, Shoval I, Kalcheim C (2008) A negative modulatory role for Rho and Rho-associated kinase signaling in delamination of neural crest cells. Neural Dev 3:27CrossRefGoogle Scholar
  63. 63.
    Shoval I, Kalcheim C (2012) Antagonistic activities of Rho and Rac GTPases underlie the transition from neural crest delamination to migration. Dev Dyn 241:1155–1168. Scholar
  64. 64.
    Perris R (1997) The extracellular matrix in neural crest-cell migration. Trends Neurosci 20:23–31CrossRefGoogle Scholar
  65. 65.
    Carmona-Fontaine C, Matthews H, Mayor R (2008) Directional cell migration in vivo: Wnt at the crest. Cell Adhes Migr 2(4):240–242. 6747 [pii]CrossRefGoogle Scholar
  66. 66.
    Carmona-Fontaine C, Matthews HK, Kuriyama S, Moreno M, Dunn GA, Parsons M, Stern CD, Mayor R (2008) Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 456(7224):957–961. nature07441 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Matthews HK, Marchant L, Carmona-Fontaine C, Kuriyama S, Larrain J, Holt MR, Parsons M, Mayor R (2008) Directional migration of neural crest cells in vivo is regulated by Syndecan-4/Rac1 and non-canonical Wnt signaling/RhoA. Development 135(10):1771–1780. dev.017350 [pii]CrossRefPubMedGoogle Scholar
  68. 68.
    Kasemeier-Kulesa JC, Kulesa PM, Lefcort F (2005) Imaging neural crest cell dynamics during formation of dorsal root ganglia and sympathetic ganglia. Development 132(2):235–245CrossRefGoogle Scholar
  69. 69.
    Krull CE, Lansford R, Gale NW, Collazo A, Marcelle C, Yancopoulos GD, Fraser SE, Bronner Fraser M (1997) Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. Curr Biol 7:571–580CrossRefGoogle Scholar
  70. 70.
    Kuriyama S, Theveneau E, Benedetto A, Parsons M, Tanaka M, Charras G, Kabla A, Mayor R (2014) In vivo collective cell migration requires an LPAR2-dependent increase in tissue fluidity. J Cell Biol 206:113–127. Scholar
  71. 71.
    McLennan R, Schumacher LJ, Morrison JA, Teddy JM, Ridenour DA, Box AC, Semerad CL, Li H, McDowell W, Kay D, Maini PK, Baker RE, Kulesa PM (2015) Neural crest migration is driven by a few trailblazer cells with a unique molecular signature narrowly confined to the invasive front. Development 142(11):2014–2025. Scholar
  72. 72.
    Richardson J, Gauert A, Briones Montecinos L, Fanlo L, Alhashem ZM, Assar R, Marti E, Kabla A, Hartel S, Linker C (2016) Leader cells define directionality of trunk, but not cranial, neural crest cell migration. Cell Rep 15:2076–2088. Scholar
  73. 73.
    Kalcheim C, Goldstein R (1991) Segmentation of sensory and sympathetic ganglia: interaction between neural crest and somite cells. J Physiol Paris 85:110–117PubMedGoogle Scholar
  74. 74.
    Gammill LS, Roffers-Agarwal J (2010) Division of labor during trunk neural crest development. Dev Biol 344(2):555–565. S0012-1606(10)00239-3 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    De Bellard ME, Ching W, Gossler A, Bronner-Fraser M (2002) Disruption of segmental neural crest migration and ephrin expression in delta-1 null mice. Dev Biol 249(1):121–130CrossRefGoogle Scholar
  76. 76.
    Kuan CY, Tannahill D, Cook GM, Keynes RJ (2004) Somite polarity and segmental patterning of the peripheral nervous system. Mech Dev 121(9):1055–1068CrossRefGoogle Scholar
  77. 77.
    Debby-Brafman A, Burstyn-Cohen T, Klar A, Kalcheim C (1999) F-spondin is expressed in somite regions avoided by neural crest cells and mediates the inhibition of distinct somitic domains to neural crest migration. Neuron 22:475–488CrossRefGoogle Scholar
  78. 78.
    Wang HU, Anderson DJ (1997) Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth. Neuron 18:383–396CrossRefGoogle Scholar
  79. 79.
    Eickholt BJ, Mackenzie SL, Graham A, Walsh FS, Doherty P (1999) Evidence for collapsin-1 functioning in the control of neural crest migration in both trunk and hindbrain regions. Development 126:2181–2189PubMedGoogle Scholar
  80. 80.
    Schwarz Q, Maden CH, Vieira JM, Ruhrberg C (2009) Neuropilin 1 signaling guides neural crest cells to coordinate pathway choice with cell specification. Proc Natl Acad Sci U S A 106:6164–6169. 0811521106 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Schwarz Q, Vieira JM, Howard B, Eickholt BJ, Ruhrberg C (2008) Neuropilin 1 and 2 control cranial gangliogenesis and axon guidance through neural crest cells. Development 135(9):1605–1613. dev.015412 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Scarpa E, Mayor R (2016) Collective cell migration in development. J Cell Biol 212:143–155. Scholar
  83. 83.
    Basch ML, Bronner-Fraser M (2006) Neural crest inducing signals. Adv Exp Med Biol 589:24–31CrossRefGoogle Scholar
  84. 84.
    Basch ML, Bronner-Fraser M, Garcia-Castro MI (2006) Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 441(7090):218–222CrossRefGoogle Scholar
  85. 85.
    Stuhlmiller TJ, Garcia-Castro MI (2012) Current perspectives of the signaling pathways directing neural crest induction. Cell Mol Life Sci 69(22):3715–3737. Scholar
  86. 86.
    Selleck MA, Bronner-Fraser M (1995) Origins of the avian neural crest: the role of neural plate-epidermal interactions. Development 121(2):525–538PubMedGoogle Scholar
  87. 87.
    Loring JF, Erickson CA (1987) Neural crest cell migratory pathways in the trunk of the chick embryo. Dev Biol 121:220–236CrossRefGoogle Scholar
  88. 88.
    Sela-Donenfeld D, Kalcheim C (2000) Inhibition of noggin expression in the dorsal neural tube by somitogenesis: a mechanism for coordinating the timing of neural crest emigration. Development 127:4845–4854PubMedGoogle Scholar
  89. 89.
    Martinez-Morales PL, Diez del Corral R, Olivera-Martinez I, Quiroga AC, Das RM, Barbas JA, Storey KG, Morales AV (2011) FGF and retinoic acid activity gradients control the timing of neural crest cell emigration in the trunk. J Cell Biol 194:489–503. jcb.201011077 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Keynes R, Cook G, Davies J, Lumsden A, Norris W, Stern C (1990) Segmentation and the development of the vertebrate nervous system. J Physiol Paris 84(1):27–32PubMedGoogle Scholar
  91. 91.
    Fraser SE (1993) Neural development: segmentation moves to the fore. Curr Biol 3:787–789CrossRefGoogle Scholar
  92. 92.
    Keynes RJ, Stern CD (1988) Mechanisms of vertebrate segmentation. Development 103:413–429PubMedGoogle Scholar
  93. 93.
    Erickson CA, Duong TD, Tosney KW (1992) Descriptive and experimental analysis of the dispersion of neural crest cells along the dorsolateral path and their entry into ectoderm in the chick embryo. Dev Biol 151:251–272CrossRefGoogle Scholar
  94. 94.
    Jia L, Cheng L, Raper J (2005) Slit/Robo signaling is necessary to confine early neural crest cells to the ventral migratory pathway in the trunk. Dev Biol 282(2):411–421. S0012-1606(05)00191-0 [pii]CrossRefPubMedGoogle Scholar
  95. 95.
    Noden DM, Trainor PA (2005) Relations and interactions between cranial mesoderm and neural crest populations. J Anat 207(5):575–601. JOA473 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Schneider R, Helms J (2003) The cellular and molecular origins of beak morphology. Science 299:565–568CrossRefGoogle Scholar
  97. 97.
    Le Douarin NM, Creuzet S, Couly G, Dupin E (2004) Neural crest cell plasticity and its limits. Development 131(19):4637–4650. 131/19/4637 [pii]CrossRefPubMedGoogle Scholar
  98. 98.
    Graham A (2003) Development of the pharyngeal arches. Am J Med Genet A 119A(3):251–256. Scholar
  99. 99.
    Couly GF, Coltey PM, Le Douarin NM (1992) The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114:1–15PubMedGoogle Scholar
  100. 100.
    Cerny R, Lwigale P, Ericsson R, Meulemans D, Epperlein HH, Bronner-Fraser M (2004) Developmental origins and evolution of jaws: new interpretation of "maxillary" and “mandibular”. Dev Biol 276(1):225–236CrossRefGoogle Scholar
  101. 101.
    Köntges G, Lumsden A (1996) Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 122:3229–3242PubMedGoogle Scholar
  102. 102.
    Noden DM (1983) The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am J Anat 168:257–276CrossRefGoogle Scholar
  103. 103.
    Grammatopoulos GA, Bell E, Toole L, Lumsden A, Tucker AS (2000) Homeotic transformation of branchial arch identity after Hoxa2 overexpression. Development 127(24):5355–5365PubMedGoogle Scholar
  104. 104.
    Schilling TF, Kimmel CB (1997) Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. Development 124(15):2945–2960PubMedGoogle Scholar
  105. 105.
    Grenier J, Teillet MA, Grifone R, Kelly RG, Duprez D (2009) Relationship between neural crest cells and cranial mesoderm during head muscle development. PLoS One 4(2):e4381. Scholar
  106. 106.
    Rinon A, Lazar S, Marshall H, Buchmann-Moller S, Neufeld A, Elhanany-Tamir H, Taketo MM, Sommer L, Krumlauf R, Tzahor E (2007) Cranial neural crest cells regulate head muscle patterning and differentiation during vertebrate embryogenesis. Development 134(17):3065–3075. dev.002501 [pii]CrossRefPubMedGoogle Scholar
  107. 107.
    Sela-Donenfeld D, Kalcheim C (2002) Localized BMP4-noggin interactions generate the dynamic patterning of noggin expression in somites. Dev Biol 246:311–328CrossRefGoogle Scholar
  108. 108.
    Brill G, Kahane N, Carmeli C, Von Schack D, Barde Y-A, Kalcheim C (1995) Epithelial-mesenchymal conversion of dermatome progenitors requires neural tube-derived signals: characterization of the role of Neurotrophin-3. Development 121:2583–2594PubMedGoogle Scholar
  109. 109.
    Spence MS, Yip J, Erickson CA (1996) The dorsal neural tube organizes the dermamyotome and induces axial myocytes in the avian embryo. Development 122:231–241PubMedGoogle Scholar
  110. 110.
    Olivera-Martinez I, Thelu J, Teillet M, Dhouailly D (2001) Dorsal dermis development depends on a signal from the dorsal neural tube, which can be substituted by Wnt-1. Mech Dev 100(2):233–244CrossRefGoogle Scholar
  111. 111.
    Capdevila J, Tabin C, Johnson RL (1998) Control of dorsoventral somite patterning by Wnt-1 and beta-catenin. Dev Biol 193:182–194CrossRefGoogle Scholar
  112. 112.
    Ikeya M, Takada S (1998) Wnt signaling from the dorsal neural tube is required for the formation of the medial dermomyotome. Development 125:4969–4976PubMedGoogle Scholar
  113. 113.
    Schmidt M, Tanaka M, Munsterberg A (2000) Expression of (beta)-catenin in the developing chick myotome is regulated by myogenic signals. Development 127(19):4105–4113PubMedGoogle Scholar
  114. 114.
    Marcelle C, Stark MR, Bronner-Fraser M (1997) Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124:3955–3963PubMedGoogle Scholar
  115. 115.
    Rios AC, Serralbo O, Salgado D, Marcelle C (2011) Neural crest regulates myogenesis through the transient activation of NOTCH. Nature 473(7348):532–535. nature09970 [pii]CrossRefPubMedGoogle Scholar
  116. 116.
    Van Ho AH, Hayashi S, Brohl D, Aurade F, Rattenbach R, Relaix F (2011) Neural crest cell lineage restricts skeletal muscle progenitor cell differentiation through Neuregulin-ErbB3 signaling. Dev Cell 21:273–287CrossRefGoogle Scholar
  117. 117.
    Krispin S, Nitzan E, Kalcheim C (2010) The dorsal neural tube: a dynamic setting for cell fate decisions. Dev Neurobiol 70:796–812. Scholar
  118. 118.
    Kim YJ, Lim H, Li Z, Oh Y, Kovlyagina I, Choi IY, Dong X, Lee G (2014) Generation of multipotent induced neural crest by direct reprogramming of human postnatal fibroblasts with a single transcription factor. Cell Stem Cell 15:497–506. Scholar
  119. 119.
    Motohashi T, Watanabe N, Nishioka M, Nakatake Y, Yulan P, Mochizuki H, Kawamura Y, Ko MS, Goshima N, Kunisada T (2016) Gene array analysis of neural crest cells identifies transcription factors necessary for direct conversion of embryonic fibroblasts into neural crest cells. Biol Open 5:311–322. Scholar
  120. 120.
    Kim K, Ossipova O, Sokol SY (2015) Neural crest specification by inhibition of the ROCK/myosin II pathway. Stem Cells 33:674–685. Scholar
  121. 121.
    Huang M, Miller ML, McHenry LK, Zheng T, Zhen Q, Ilkhanizadeh S, Conklin BR, Bronner ME, Weiss WA (2016) Generating trunk neural crest from human pluripotent stem cells. Sci Rep 6:19727. Scholar
  122. 122.
    Demers CJ, Soundararajan P, Chennampally P, Cox GA, Briscoe J, Collins SD, Smith RL (2016) Development-on-chip: in vitro neural tube patterning with a microfluidic device. Development 143:1884–1892. Scholar
  123. 123.
    Lee G, Papapetrou EP, Kim H, Chambers SM, Tomishima MJ, Fasano CA, Ganat YM, Menon J, Shimizu F, Viale A, Tabar V, Sadelain M, Studer L (2009) Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 461:402–406. Scholar
  124. 124.
    Lee G, Ramirez CN, Kim H, Zeltner N, Liu B, Radu C, Bhinder B, Kim YJ, Choi IY, Mukherjee-Clavin B, Djaballah H, Studer L (2012) Large-scale screening using familial dysautonomia induced pluripotent stem cells identifies compounds that rescue IKBKAP expression. Nat Biotechnol 30:1244–1248. Scholar
  125. 125.
    Noack Watt K, Trainor P (2014) Neurocristopathies: the etiology and pathogenesis of disorders arising from defects in neural crest cell development. In: Neural crest cells: evolution, development and disease. Academic Press, Massachusetts, pp 361–394. Scholar

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Authors and Affiliations

  1. 1.Department of Medical Neurobiology, Institute of Medical Research Israel-Canada (IMRIC)Hebrew University-Hadassah Medical SchoolJerusalemIsrael
  2. 2.Edmond and Lily Safra Center for Brain Sciences (ELSC)Hebrew University-Hadassah Medical SchoolJerusalemIsrael

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