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

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Neural Crest Cells

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1976))

Abstract

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.

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References

  1. Kalcheim C (2000) Mechanisms of early neural crest development: from cell specification to migration. Int Rev Cytol 200:143–196

    Article  CAS  PubMed  Google Scholar 

  2. Bronner ME (2012) Formation and migration of neural crest cells in the vertebrate embryo. Histochem Cell Biol 138(2):179–186. https://doi.org/10.1007/s00418-012-0999-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kalcheim C (2015) Epithelial-Mesenchymal transitions during neural crest and somite development. J Clin Med 5. https://doi.org/10.3390/jcm5010001

    Article  PubMed Central  Google Scholar 

  4. Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139(5):871–890. https://doi.org/10.1016/j.cell.2009.11.007

    Article  CAS  PubMed  Google Scholar 

  5. Le Douarin NM, Kalcheim C (1999) The neural crest, 2nd edn. Cambridge University Press, New York

    Book  Google Scholar 

  6. Groves A, Bronner Fraser M (1999) Neural crest diversification. Curr Top Dev Biol 43:221–258

    Article  CAS  PubMed  Google Scholar 

  7. Graham A, Begbie J, McGonnell I (2004) Significance of the cranial neural crest. Dev Dyn 229(1):5–13. https://doi.org/10.1002/dvdy.10442

    Article  PubMed  Google Scholar 

  8. Noden DM (1978) The control of avian cephalic neural crest cytodifferentiation. I. Skeletal and connective tissues. Dev Biol 67:296–312

    Article  CAS  PubMed  Google Scholar 

  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 128:1059–1068

    CAS  PubMed  Google Scholar 

  10. Weston JA, Thiery JP (2015) Pentimento: neural crest and the origin of mesectoderm. Dev Biol 401(1):37–61. https://doi.org/10.1016/j.ydbio.2014.12.035

    Article  CAS  PubMed  Google Scholar 

  11. Kulesa PM, Gammill LS (2010) Neural crest migration: patterns, phases and signals. Dev Biol 344(2):566–568. https://doi.org/10.1016/j.ydbio.2010.05.005. S0012-1606(10)00291-5 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Minoux M, Rijli FM (2010) Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development. Development 137(16):2605–2621. https://doi.org/10.1242/dev.040048. 137/16/2605 [pii]

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1002/dvdy.22715

    Article  PubMed  PubMed Central  Google Scholar 

  14. Kuo BR, Erickson CA (2010) Regional differences in neural crest morphogenesis. Cell Adhes Migr 4(4):567–585. 12890 [pii]

    Article  Google Scholar 

  15. Le Douarin NM (1982) The neural crest, 1st edn. Cambridge University Press, New York

    Google Scholar 

  16. Horstadius S (1950) The mechanics of sea urchin development. Annee Biol 26:381–398

    CAS  PubMed  Google Scholar 

  17. Weston JA (1963) A radioautographic analysis of the migration and localization of trunk neural crest cells in the chick. Dev Biol 6:279–310

    Article  CAS  PubMed  Google Scholar 

  18. Chibon P (1967) Nuclear labelling by tritiated thymidine of neural crest derivatives in the amphibian Urodele Pleurodeles waltlii Michah. J Embryol Exp Morphol 18:343–358

    CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1111/dgd.12015

    Article  Google Scholar 

  20. Raible DW, Eisen JS (1994) Restriction of neural crest cell fate in the trunk of the embryonic zebrafish. Development 120:495–503

    CAS  PubMed  Google Scholar 

  21. Raible DW, Eisen JS (1996) Regulative interactions in zebrafish neural crest. Development 122:501–507

    CAS  PubMed  Google Scholar 

  22. Schilling TF, Kimmel CB (1994) Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120(3):483–494

    CAS  PubMed  Google Scholar 

  23. Bronner-Fraser M, Fraser SE (1988) Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 335:161–164

    Article  CAS  PubMed  Google Scholar 

  24. Serbedzija GN, Bronner-Fraser M, Fraser SE (1992) Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116:297–307

    CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1242/dev.041509. 137/4/585 [pii]

    Article  CAS  PubMed  Google Scholar 

  26. Nakamura H, Funahashi J (2001) Introduction of DNA into chick embryos by in ovo electroporation. Methods 24(1):43–48. https://doi.org/10.1006/meth.2001.1155

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1016/j.ydbio.2007.01.043. S0012-1606(07)00092-9 [pii]

    Article  CAS  PubMed  Google Scholar 

  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 132:689–701

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1002/dvdy.22174

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1186/PREACCEPT-5975531631281105

    Article  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1242/dev.074948. dev.074948 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1186/s12915-016-0245-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70–71. https://doi.org/10.1038/5007

    Article  CAS  PubMed  Google Scholar 

  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 8:1323–1326

    Article  CAS  PubMed  Google Scholar 

  35. Jiang XB, Rowitch DH, Soriano P, McMahon AP, Sucov HM (2000) Fate of the mammalian cardiac neural crest. Development 127:1607–1616

    CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1038/nature12948

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1038/nature06293

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1016/j.stem.2015.02.017

    Article  CAS  PubMed  Google Scholar 

  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 120:329–347

    Article  CAS  PubMed  Google Scholar 

  40. Yip JW (1986) Migratory pathways of sympathetic ganglioblasts and other neural crest derivatives in chick embryos. J Neurosci 6:3465–3473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1016/j.devcel.2011.07.009. S1534-5807(11)00301-7 [pii]

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1016/bs.ctdb.2014.11.015

    Article  PubMed  Google Scholar 

  43. Le Douarin NM (1990) Cell lineage segregation during neural crest ontogeny. Ann N Y Acad Sci 599:131–140

    Article  PubMed  Google Scholar 

  44. Le Douarin NM, Dupin E (2003) Multipotentiality of the neural crest. Curr Opin Genet Dev 13:529–536. S0959437X03001138 [pii]

    Article  PubMed  Google Scholar 

  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 109:411–423

    CAS  PubMed  Google Scholar 

  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 77:362–378

    Article  PubMed  Google Scholar 

  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 13:191–200

    Article  CAS  PubMed  Google Scholar 

  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 140:2269–2279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Raible DW, Eisen JS (1992) Spatiotemporal restriction of trunk neural crest cell lineage in the embryonic zebrafish. Soc Neurosci Abstr 18

    Google Scholar 

  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 127:2811–2821

    CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1186/1749-8104-8-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1016/j.cell.2009.07.049. S0092-8674(09)01043-5 [pii]

    Article  CAS  PubMed  Google Scholar 

  53. Theveneau E, Mayor R (2011) Collective cell migration of the cephalic neural crest: the art of integrating information. Genesis 49(4):164–176. https://doi.org/10.1002/dvg.20700

    Article  PubMed  Google Scholar 

  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. https://doi.org/10.1016/j.semcancer.2012.04.008

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1016/j.ydbio.2011.12.041

    Article  CAS  PubMed  Google Scholar 

  56. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7(2):131–142. https://doi.org/10.1038/nrm1835

    Article  CAS  PubMed  Google Scholar 

  57. Yang J, Weinberg RA (2008) Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14(6):818–829. https://doi.org/10.1016/j.devcel.2008.05.009

    Article  CAS  PubMed  Google Scholar 

  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 126:4749–4762

    CAS  PubMed  Google Scholar 

  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):5327–5339

    Article  CAS  PubMed  Google Scholar 

  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 3:383–395

    Article  CAS  PubMed  Google Scholar 

  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 134:491–501

    Article  CAS  PubMed  Google Scholar 

  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 3:27

    Article  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1002/dvdy.23799

    Article  CAS  PubMed  Google Scholar 

  64. Perris R (1997) The extracellular matrix in neural crest-cell migration. Trends Neurosci 20:23–31

    Article  CAS  PubMed  Google Scholar 

  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]

    Article  Google Scholar 

  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. https://doi.org/10.1038/nature07441. nature07441 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1242/dev.017350. dev.017350 [pii]

    Article  CAS  PubMed  Google Scholar 

  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):235–245

    Article  CAS  PubMed  Google Scholar 

  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 7:571–580

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1083/jcb.201402093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1242/dev.117507

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1016/j.celrep.2016.04.067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Kalcheim C, Goldstein R (1991) Segmentation of sensory and sympathetic ganglia: interaction between neural crest and somite cells. J Physiol Paris 85:110–117

    CAS  PubMed  Google Scholar 

  74. Gammill LS, Roffers-Agarwal J (2010) Division of labor during trunk neural crest development. Dev Biol 344(2):555–565. https://doi.org/10.1016/j.ydbio.2010.04.009. S0012-1606(10)00239-3 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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):121–130

    Article  PubMed  Google Scholar 

  76. Kuan CY, Tannahill D, Cook GM, Keynes RJ (2004) Somite polarity and segmental patterning of the peripheral nervous system. Mech Dev 121(9):1055–1068

    Article  PubMed  Google Scholar 

  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 22:475–488

    Article  CAS  PubMed  Google Scholar 

  78. Wang HU, Anderson DJ (1997) Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth. Neuron 18:383–396

    Article  CAS  PubMed  Google Scholar 

  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 126:2181–2189

    CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1073/pnas.0811521106. 0811521106 [pii]

    Article  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1242/dev.015412. dev.015412 [pii]

    Article  CAS  PubMed  Google Scholar 

  82. Scarpa E, Mayor R (2016) Collective cell migration in development. J Cell Biol 212:143–155. https://doi.org/10.1083/jcb.201508047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Basch ML, Bronner-Fraser M (2006) Neural crest inducing signals. Adv Exp Med Biol 589:24–31

    Article  CAS  PubMed  Google Scholar 

  84. Basch ML, Bronner-Fraser M, Garcia-Castro MI (2006) Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 441(7090):218–222

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1007/s00018-012-0991-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Selleck MA, Bronner-Fraser M (1995) Origins of the avian neural crest: the role of neural plate-epidermal interactions. Development 121(2):525–538

    CAS  PubMed  Google Scholar 

  87. Loring JF, Erickson CA (1987) Neural crest cell migratory pathways in the trunk of the chick embryo. Dev Biol 121:220–236

    Article  CAS  PubMed  Google Scholar 

  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 127:4845–4854

    CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1083/jcb.201011077. jcb.201011077 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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):27–32

    CAS  PubMed  Google Scholar 

  91. Fraser SE (1993) Neural development: segmentation moves to the fore. Curr Biol 3:787–789

    Article  CAS  PubMed  Google Scholar 

  92. Keynes RJ, Stern CD (1988) Mechanisms of vertebrate segmentation. Development 103:413–429

    CAS  PubMed  Google Scholar 

  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 151:251–272

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1016/j.ydbio.2005.03.021. S0012-1606(05)00191-0 [pii]

    Article  CAS  PubMed  Google Scholar 

  95. Noden DM, Trainor PA (2005) Relations and interactions between cranial mesoderm and neural crest populations. J Anat 207(5):575–601. https://doi.org/10.1111/j.1469-7580.2005.00473.x. JOA473 [pii]

    Article  PubMed  PubMed Central  Google Scholar 

  96. Schneider R, Helms J (2003) The cellular and molecular origins of beak morphology. Science 299:565–568

    Article  CAS  PubMed  Google Scholar 

  97. Le Douarin NM, Creuzet S, Couly G, Dupin E (2004) Neural crest cell plasticity and its limits. Development 131(19):4637–4650. https://doi.org/10.1242/dev.01350. 131/19/4637 [pii]

    Article  CAS  PubMed  Google Scholar 

  98. Graham A (2003) Development of the pharyngeal arches. Am J Med Genet A 119A(3):251–256. https://doi.org/10.1002/ajmg.a.10980

    Article  PubMed  Google Scholar 

  99. Couly GF, Coltey PM, Le Douarin NM (1992) The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114:1–15

    CAS  PubMed  Google Scholar 

  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):225–236

    Article  CAS  PubMed  Google Scholar 

  101. Köntges G, Lumsden A (1996) Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 122:3229–3242

    PubMed  Google Scholar 

  102. Noden DM (1983) The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am J Anat 168:257–276

    Article  CAS  PubMed  Google Scholar 

  103. Grammatopoulos GA, Bell E, Toole L, Lumsden A, Tucker AS (2000) Homeotic transformation of branchial arch identity after Hoxa2 overexpression. Development 127(24):5355–5365

    CAS  PubMed  Google Scholar 

  104. Schilling TF, Kimmel CB (1997) Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. Development 124(15):2945–2960

    CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1371/journal.pone.0004381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1242/dev.002501. dev.002501 [pii]

    Article  CAS  PubMed  Google Scholar 

  107. Sela-Donenfeld D, Kalcheim C (2002) Localized BMP4-noggin interactions generate the dynamic patterning of noggin expression in somites. Dev Biol 246:311–328

    Article  CAS  PubMed  Google Scholar 

  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 121:2583–2594

    CAS  PubMed  Google Scholar 

  109. Spence MS, Yip J, Erickson CA (1996) The dorsal neural tube organizes the dermamyotome and induces axial myocytes in the avian embryo. Development 122:231–241

    CAS  PubMed  Google Scholar 

  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):233–244

    Article  CAS  PubMed  Google Scholar 

  111. Capdevila J, Tabin C, Johnson RL (1998) Control of dorsoventral somite patterning by Wnt-1 and beta-catenin. Dev Biol 193:182–194

    Article  CAS  PubMed  Google Scholar 

  112. Ikeya M, Takada S (1998) Wnt signaling from the dorsal neural tube is required for the formation of the medial dermomyotome. Development 125:4969–4976

    CAS  PubMed  Google Scholar 

  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):4105–4113

    CAS  PubMed  Google Scholar 

  114. Marcelle C, Stark MR, Bronner-Fraser M (1997) Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124:3955–3963

    CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1038/nature09970. nature09970 [pii]

    Article  CAS  PubMed  Google Scholar 

  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 21:273–287

    Article  CAS  PubMed  Google Scholar 

  117. Krispin S, Nitzan E, Kalcheim C (2010) The dorsal neural tube: a dynamic setting for cell fate decisions. Dev Neurobiol 70:796–812. https://doi.org/10.1002/dneu.20826

    Article  PubMed  Google Scholar 

  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. https://doi.org/10.1016/j.stem.2014.07.013

    Article  CAS  PubMed  Google Scholar 

  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. https://doi.org/10.1242/bio.015735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Kim K, Ossipova O, Sokol SY (2015) Neural crest specification by inhibition of the ROCK/myosin II pathway. Stem Cells 33:674–685. https://doi.org/10.1002/stem.1877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1038/srep19727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1242/dev.126847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1038/nature08320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1038/nbt.2435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. https://doi.org/10.1016/B978-0-12-401730-6.00018-1

    Chapter  Google Scholar 

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Acknowledgments

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.

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Correspondence to Chaya Kalcheim .

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Kalcheim, C. (2019). The Neural Crest: A Remarkable Model System for Studying Development and Disease. In: Schwarz, Q., Wiszniak, S. (eds) Neural Crest Cells. Methods in Molecular Biology, vol 1976. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-9412-0_1

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