Advertisement

Melanoma pp 3-19 | Cite as

Developmental Biology of Melanocytes

  • Lukas SommerEmail author
Reference work entry

Abstract

Apart from embryonic stem cells (ESCs) in the blastocyst, neural crest stem cells (NCSCs) in vertebrate embryos represent the stem cell population in our body with the broadest developmental potential, generating most of the neurons and glia of the peripheral nervous system (PNS) as well as various nonneural cell types, such as smooth muscle cells in the outflow tract of the heart, craniofacial bone, and cartilage and, in particular, melanocytes in the skin. It is assumed that a third of all congenital birth defects are due to failures in neural crest development, illustrating the significance of this stem cell population. Moreover, processes underlying melanocyte development appear to be recapitulated, at least partially, during formation of melanoma, the most aggressive skin tumor. For instance, it has recently been shown that an embryonic NCSC gene expression signature is reactivated upon tumor initiation in a zebrafish model of melanoma, suggesting a functional involvement of a NCSC program in tumors originating from neural crest derivatives. Thus, to gain insights into melanoma biology, it is important to understand the mechanisms regulating NCSC and melanocyte development, as outlined in this chapter.

Keywords

Neural crest Neural crest stem cell Melanocyte Embryonic development Lineage specification Tumor cell of origin 

References

  1. 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 139:366–379PubMedCrossRefPubMedCentralGoogle Scholar
  2. Adameyko I, Lallemend F, Furlan A, Zinin N, Aranda S, Kitambi SS, Blanchart A, Favaro R, Nicolis S, Lubke M, Muller T, Birchmeier C, Suter U, Zaitoun I, Takahashi Y, Ernfors P (2012) Sox2 and Mitf cross-regulatory interactions consolidate progenitor and melanocyte lineages in the cranial neural crest. Development 139:397–410PubMedPubMedCentralCrossRefGoogle Scholar
  3. Aoki Y, Saint-Germain N, Gyda M, Magner-Fink E, Lee YH, Credidio C, Saint-Jeannet JP (2003) Sox10 regulates the development of neural crest-derived melanocytes in Xenopus. Dev Biol 259:19–33PubMedCrossRefPubMedCentralGoogle Scholar
  4. 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 16:314–322PubMedCrossRefPubMedCentralGoogle Scholar
  5. Baroffio A, Dupin E, LeDouarin NM (1988) Clone-forming ability and differentiation potential of migratory neural crest cells. Proc Natl Acad Sci U S A 85:5325–5329PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bejar J, Hong Y, Schartl M (2003) Mitf expression is sufficient to direct differentiation of medaka blastula derived stem cells to melanocytes. Development 130:6545–6553PubMedCrossRefPubMedCentralGoogle Scholar
  7. Boiko AD, Razorenova OV, van de Rijn M, Swetter SM, Johnson DL, Ly DP, Butler PD, Yang GP, Joshua B, Kaplan MJ, Longaker MT, Weissman IL (2010) Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271. Nature 466:133–137PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bondurand N, Kuhlbrodt K, Pingault V, Enderich J, Sajus M, Tommerup N, Warburg M, Hennekam RC, Read AP, Wegner M, Goossens M (1999) A molecular analysis of the yemenite deaf-blind hypopigmentation syndrome: SOX10 dysfunction causes different neurocristopathies. Hum Mol Genet 8:1785–1789PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bondurand N, Pingault V, Goerich DE, Lemort N, Sock E, Caignec CL, Wegner M, Goossens M (2000) Interaction among SOX10, PAX3 and MITF, three genes altered in Waardenburg syndrome. Hum Mol Genet 9:1907–1917PubMedCrossRefPubMedCentralGoogle Scholar
  10. Bondurand N, Natarajan D, Barlow A, Thapar N, Pachnis V (2006) Maintenance of mammalian enteric nervous system progenitors by SOX10 and endothelin 3 signalling. Development 133:2075–2086PubMedCrossRefPubMedCentralGoogle Scholar
  11. Britsch S, Goerich DE, Riethmacher D, Peirano RI, Rossner M, Nave KA, Birchmeier C, Wegner M (2001) The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev 15:66–78PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bronner M (2015) Confetti clarifies controversy: neural crest stem cells are multipotent. Cell Stem Cell 16:217–218PubMedCrossRefPubMedCentralGoogle Scholar
  13. Bronner-Fraser M, Fraser S (1988) Cell lineage analysis shows multipotentiality of some avian neural crest cells. Nature 335:161–164PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bronner-Fraser M, Fraser S (1989) Developmental potential of avian trunk neural crest cells in situ. Neuron 3:755–766PubMedCrossRefPubMedCentralGoogle Scholar
  15. Budi EH, Patterson LB, Parichy DM (2011) Post-embryonic nerve-associated precursors to adult pigment cells: genetic requirements and dynamics of morphogenesis and differentiation. PLoS Genet 7:e1002044PubMedPubMedCentralCrossRefGoogle Scholar
  16. Buitrago-Delgado E, Nordin K, Rao A, Geary L, LaBonne C (2015) NEURODEVELOPMENT. Shared regulatory programs suggest retention of blastula-stage potential in neural crest cells. Science 348:1332–1335PubMedPubMedCentralCrossRefGoogle Scholar
  17. Calloni GW, Le Douarin NM, Dupin E (2009) High frequency of cephalic neural crest cells shows coexistence of neurogenic, melanogenic, and osteogenic differentiation capacities. Proc Natl Acad Sci U S A 106:8947–8952PubMedPubMedCentralCrossRefGoogle Scholar
  18. Camp E, Lardelli M (2001) Tyrosinase gene expression in zebrafish embryos. Dev Genes Evol 211:150–153PubMedCrossRefPubMedCentralGoogle Scholar
  19. Cheung M, Chaboissier MC, Mynett A, Hirst E, Schedl A, Briscoe J (2005) The transcriptional control of trunk neural crest induction, survival, and delamination. Dev Cell 8:179–192PubMedCrossRefPubMedCentralGoogle Scholar
  20. Civenni G, Walter A, Kobert N, Mihic-Probst D, Zipser M, Belloni B, Seifert B, Moch H, Dummer R, van den Broek M, Sommer L (2011) Human CD271-positive melanoma stem cells associated with metastasis establish tumor heterogeneity and long-term growth. Cancer Res 71:3098–3109PubMedCrossRefPubMedCentralGoogle Scholar
  21. Cohen AM, Konigsberg IR (1975) A clonal approach to the problem of neural crest determination. Dev Biol 46:262–280PubMedCrossRefPubMedCentralGoogle Scholar
  22. Cooper CD, Raible DW (2009) Mechanisms for reaching the differentiated state: insights from neural crest-derived melanocytes. Semin Cell Dev Biol 20:105–110PubMedCrossRefPubMedCentralGoogle Scholar
  23. Curran K, Raible DW, Lister JA (2009) Foxd3 controls melanophore specification in the zebrafish neural crest by regulation of Mitf. Dev Biol 332:408–417PubMedPubMedCentralCrossRefGoogle Scholar
  24. Curran K, Lister JA, Kunkel GR, Prendergast A, Parichy DM, Raible DW (2010) Interplay between Foxd3 and Mitf regulates cell fate plasticity in the zebrafish neural crest. Dev Biol 344:107–118PubMedPubMedCentralCrossRefGoogle Scholar
  25. Damsky WE, Curley DP, Santhanakrishnan M, Rosenbaum LE, Platt JT, Gould Rothberg BE, Taketo MM, Dankort D, Rimm DL, McMahon M, Bosenberg M (2011) Beta-catenin signaling controls metastasis in Braf-activated Pten-deficient melanomas. Cancer Cell 20:741–754PubMedPubMedCentralCrossRefGoogle Scholar
  26. Delfino-Machin M, Chipperfield TR, Rodrigues FS, Kelsh RN (2007) The proliferating field of neural crest stem cells. Dev Dyn 236:3242–3254PubMedCrossRefPubMedCentralGoogle Scholar
  27. Delmas V, Beermann F, Martinozzi S, Carreira S, Ackermann J, Kumasaka M, Denat L, Goodall J, Luciani F, Viros A, Demirkan N, Bastian BC, Goding CR, Larue L (2007) Beta-catenin induces immortalization of melanocytes by suppressing p16INK4a expression and cooperates with N-Ras in melanoma development. Genes Dev 21:2923–2935PubMedPubMedCentralCrossRefGoogle Scholar
  28. Dorsky RI, Moon RT, Raible DW (1998) Control of neural crest cell fate by the Wnt signalling pathway. Nature 396:370–373PubMedCrossRefPubMedCentralGoogle Scholar
  29. Dorsky RI, Raible DW, Moon RT (2000) Direct regulation of nacre, a zebrafish MITF homolog required for pigment cell formation, by the Wnt pathway. Genes Dev 14:158–162PubMedPubMedCentralGoogle Scholar
  30. Dunn KJ, Williams BO, Li Y, Pavan WJ (2000) Neural crest-directed gene transfer demonstrates Wnt1 role in melanocyte expansion and differentiation during mouse development. Proc Natl Acad Sci U S A 97:10050–10055PubMedPubMedCentralCrossRefGoogle Scholar
  31. Dupin E, Sommer L (2012) Neural crest progenitors and stem cells: from early development to adulthood. Dev Biol 366:83–95PubMedCrossRefPubMedCentralGoogle Scholar
  32. Dupin E, Glavieux C, Vaigot P, Le Douarin NM (2000) Endothelin 3 induces the reversion of melanocytes to glia through a neural crest-derived glial-melanocytic progenitor. Proc Natl Acad Sci U S A 97:7882–7887PubMedPubMedCentralCrossRefGoogle Scholar
  33. Dupin E, Real C, Glavieux-Pardanaud C, Vaigot P, Le Douarin NM (2003) Reversal of developmental restrictions in neural crest lineages: transition from Schwann cells to glial-melanocytic precursors in vitro. Proc Natl Acad Sci U S A 100:5229–5233PubMedPubMedCentralCrossRefGoogle Scholar
  34. Dupin E, Calloni GW, Le Douarin NM (2010) The cephalic neural crest of amniote vertebrates is composed of a large majority of precursors endowed with neural, melanocytic, chondrogenic and osteogenic potentialities. Cell Cycle 9:238–249PubMedCrossRefPubMedCentralGoogle Scholar
  35. Dutton KA, Pauliny A, Lopes SS, Elworthy S, Carney TJ, Rauch J, Geisler R, Haffter P, Kelsh RN (2001) Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128:4113–4125PubMedPubMedCentralGoogle Scholar
  36. Elworthy S, Lister JA, Carney TJ, Raible DW, Kelsh RN (2003) Transcriptional regulation of mitfa accounts for the sox10 requirement in zebrafish melanophore development. Development 130:2809–2818PubMedCrossRefPubMedCentralGoogle Scholar
  37. Erickson CA, Duong ED, Tosney KW (1992) Descriptive and experimental analysis of the dispersion of neural crest cells along the dorso-lateral path and their entry into ectoderm in the chick embryo. Dev Biol 151:251–272PubMedCrossRefPubMedCentralGoogle Scholar
  38. Ernfors P (2010) Cellular origin and developmental mechanisms during the formation of skin melanocytes. Exp Cell Res 316:1397–1407PubMedCrossRefPubMedCentralGoogle Scholar
  39. Etchevers H (2011) Primary culture of chick, mouse or human neural crest cells. Nat Protoc 6:1568–1577PubMedCrossRefPubMedCentralGoogle Scholar
  40. Frank E, Sanes JR (1991) Lineage of neurons and glia in chick dorsal root ganglia: analysis in vivo with a recombinant retrovirus. Development 111:895–908PubMedPubMedCentralGoogle Scholar
  41. Fuchs S, Herzog D, Sumara G, Buchmann-Moller S, Civenni G, Wu X, Chrostek-Grashoff A, Suter U, Ricci R, Relvas JB, Brakebusch C, Sommer L (2009) Stage-specific control of neural crest stem cell proliferation by the small rho GTPases Cdc42 and Rac1. Cell Stem Cell 4:236–247PubMedCrossRefPubMedCentralGoogle Scholar
  42. Graham A, Koentges G, Lumsden A (1996) Neural crest apoptosis and the establishment of craniofacial pattern: an honorable death. Mol Cell Neurosci 8:76–83PubMedCrossRefPubMedCentralGoogle Scholar
  43. Hagedorn L, Suter U, Sommer L (1999) P0 and PMP22 mark a multipotent neural crest-derived cell type that displays community effects in response to TGF-ß family factors. Development 126:3781–3794PubMedPubMedCentralGoogle Scholar
  44. Hari L, Brault V, Kléber M, Lee HY, Ille F, Leimeroth R, Paratore C, Suter U, Kemler R, Sommer L (2002) Lineage-specific requirements of ß-catenin in neural crest development. J Cell Biol 159:867–880PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hari L, Miescher I, Shakhova O, Suter U, Chin L, Taketo M, Richardson WD, Kessaris N, Sommer L (2012) Temporal control of neural crest lineage generation by Wnt/beta-catenin signaling. Development 139:2107–2117PubMedCrossRefPubMedCentralGoogle Scholar
  46. Harris ML, Hall R, Erickson CA (2008) Directing pathfinding along the dorso-lateral path – the role of EDNRB2 and EphB2 in overcoming inhibition. Development 135:4113–4122PubMedCrossRefPubMedCentralGoogle Scholar
  47. Harris ML, Buac K, Shakhova O, Hakami RM, Wegner M, Sommer L, Pavan WJ (2013) A dual role for SOX10 in the maintenance of the postnatal melanocyte lineage and the differentiation of melanocyte stem cell progenitors. PLoS Genet 9:e1003644PubMedPubMedCentralCrossRefGoogle Scholar
  48. Henion PD, Weston JA (1997) Timing and pattern of cell fate restrictions in the neural crest lineage. Development 124:4351–4359PubMedPubMedCentralGoogle Scholar
  49. Hornyak TJ, Hayes DJ, Chiu LY, Ziff EB (2001) Transcription factors in melanocyte development: distinct roles for Pax-3 and Mitf. Mech Dev 101:47–59PubMedCrossRefPubMedCentralGoogle Scholar
  50. Hou L, Panthier JJ, Arnheiter H (2000) Signaling and transcriptional regulation in the neural crest-derived melanocyte lineage: interactions between KIT and MITF. Development 127:5379–5389PubMedPubMedCentralGoogle Scholar
  51. Hou L, Pavan WJ, Shin MK, Arnheiter H (2004) Cell-autonomous and cell non-autonomous signaling through endothelin receptor B during melanocyte development. Development 131:3239–3247PubMedCrossRefPubMedCentralGoogle Scholar
  52. Hou L, Arnheiter H, Pavan WJ (2006) Interspecies difference in the regulation of melanocyte development by SOX10 and MITF. Proc Natl Acad Sci U S A 103:9081–9085PubMedPubMedCentralCrossRefGoogle Scholar
  53. Ignatius MS, Moose HE, El-Hodiri HM, Henion PD (2008) colgate/hdac1 repression of foxd3 expression is required to permit mitfa-dependent melanogenesis. Dev Biol 313:568–583PubMedCrossRefPubMedCentralGoogle Scholar
  54. Jin EJ, Erickson CA, Takada S, Burrus LW (2001) Wnt and BMP signaling govern lineage segregation of melanocytes in the avian embryo. Dev Biol 233:22–37PubMedCrossRefPubMedCentralGoogle Scholar
  55. Kaufman CK, Mosimann C, Fan ZP, Yang S, Thomas AJ, Ablain J, Tan JL, Fogley RD, van Rooijen E, Hagedorn EJ, Ciarlo C, White RM, Matos DA, Puller AC, Santoriello C, Liao EC, Young RA, Zon LI (2016) A zebrafish melanoma model reveals emergence of neural crest identity during melanoma initiation. Science 351:aad2197PubMedPubMedCentralCrossRefGoogle Scholar
  56. Kim J, Lo L, Dormand E, Anderson DJ (2003) SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 38:17–31PubMedCrossRefPubMedCentralGoogle Scholar
  57. Kleber M, Sommer L (2004) Wnt signaling and the regulation of stem cell function. Curr Opin Cell Biol 16:681–687PubMedCrossRefPubMedCentralGoogle Scholar
  58. Kleber M, Lee HY, Wurdak H, Buchstaller J, Riccomagno MM, Ittner LM, Suter U, Epstein DJ, Sommer L (2005) Neural crest stem cell maintenance by combinatorial Wnt and BMP signaling. J Cell Biol 169:309–320PubMedPubMedCentralCrossRefGoogle Scholar
  59. Kos R, Reedy MV, Johnson RL, Erickson CA (2001) The winged-helix transcription factor FoxD3 is important for establishing the neural crest lineage and repressing melanogenesis in avian embryos. Development 128:1467–1479PubMedPubMedCentralGoogle Scholar
  60. Krauthammer M, Kong Y, Ha BH, Evans P, Bacchiocchi A, McCusker JP, Cheng E, Davis MJ, Goh G, Choi M, Ariyan S, Narayan D, Dutton-Regester K, Capatana A, Holman EC, Bosenberg M, Sznol M, Kluger HM, Brash DE, Stern DF, Materin MA, Lo RS, Mane S, Ma S, Kidd KK, Hayward NK, Lifton RP, Schlessinger J, Boggon TJ, Halaban R (2012) Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat Genet 44:1006–1014PubMedPubMedCentralCrossRefGoogle Scholar
  61. Krispin S, Nitzan E, Kalcheim C (2010a) The dorsal neural tube: a dynamic setting for cell fate decisions. Dev Neurobiol 70:796–812PubMedCrossRefPubMedCentralGoogle Scholar
  62. Krispin S, Nitzan E, Kassem Y, Kalcheim C (2010b) Evidence for a dynamic spatiotemporal fate map and early fate restrictions of premigratory avian neural crest. Development 137:585–595PubMedCrossRefPubMedCentralGoogle Scholar
  63. Kuhlbrodt K, Herbarth B, Sock E, Enderich J, Hermans-Borgmeyer I, Wegner M (1998) Cooperative function of POU proteins and SOX proteins in glial cells. J Biol Chem 273:16050–16057PubMedCrossRefPubMedCentralGoogle Scholar
  64. Lahav R, Dupin E, Lecoin L, Glavieux C, Champeval D, Ziller C, Le Douarin NM (1998) Endothelin 3 selectively promotes survival and proliferation of neural crest-derived glial and melanocytic precursors in vitro. Proc Natl Acad Sci U S A 95:14214–14219PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lavoie JF, Biernaskie JA, Chen Y, Bagli D, Alman B, Kaplan DR, Miller FD (2009) Skin-derived precursors differentiate into skeletogenic cell types and contribute to bone repair. Stem Cells Dev 18:893–906PubMedCrossRefPubMedCentralGoogle Scholar
  66. Le Douarin NM, Dupin E (2003) Multipotentiality of the neural crest. Curr Opin Genet Dev 13:529–536PubMedCrossRefPubMedCentralGoogle Scholar
  67. Le Douarin NM, Calloni GW, Dupin E (2008) The stem cells of the neural crest. Cell Cycle 7:1013–1019PubMedCrossRefPubMedCentralGoogle Scholar
  68. Lee HY, Kleber M, Hari L, Brault V, Suter U, Taketo MM, Kemler R, Sommer L (2004) Instructive role of Wnt/beta-catenin in sensory fate specification in neural crest stem cells. Science 303:1020–1023.  https://doi.org/10.1126/science.1091611CrossRefPubMedPubMedCentralGoogle Scholar
  69. Leone DP, Genoud S, Atanasoski S, Grausenburger R, Berger P, Metzger D, Macklin WB, Chambon P, Suter U (2003) Tamoxifen-inducible glia-specific Cre mice for somatic mutagenesis in oligodendrocytes and Schwann cells. Mol Cell Neurosci 22:430–440PubMedCrossRefPubMedCentralGoogle Scholar
  70. Levy C, Khaled M, Fisher DE (2006) MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol Med 12:406–414PubMedCrossRefPubMedCentralGoogle Scholar
  71. Lister JA, Robertson CP, Lepage T, Johnson SL, Raible DW (1999) nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126:3757–3767PubMedPubMedCentralGoogle Scholar
  72. Lister JA, Cooper C, Nguyen K, Modrell M, Grant K, Raible DW (2006) Zebrafish Foxd3 is required for development of a subset of neural crest derivatives. Dev Biol 290:92–104PubMedCrossRefPubMedCentralGoogle Scholar
  73. Mackenzie MA, Jordan SA, Budd PS, Jackson IJ (1997) Activation of the receptor tyrosine kinase Kit is required for the proliferation of melanoblasts in the mouse embryo. Dev Biol 192:99–107PubMedCrossRefPubMedCentralGoogle Scholar
  74. McKenzie IA, Biernaskie J, Toma JG, Midha R, Miller FD (2006) Skin-derived precursors generate myelinating Schwann cells for the injured and dysmyelinated nervous system. J Neurosci 26:6651–6660PubMedCrossRefPubMedCentralGoogle Scholar
  75. Mort RL, Jackson IJ, Patton EE (2015) The melanocyte lineage in development and disease. Development 142:1387PubMedPubMedCentralCrossRefGoogle Scholar
  76. Motohashi T, Yamanaka K, Chiba K, Aoki H, Kunisada T (2009) Unexpected multipotency of melanoblasts isolated from murine skin. Stem Cells 27:888–897PubMedCrossRefPubMedCentralGoogle Scholar
  77. Murakami T, Toda S, Fujimoto M, Ohtsuki M, Byers HR, Etoh T, Nakagawa H (2001) Constitutive activation of Wnt/beta-catenin signaling pathway in migration-active melanoma cells: role of LEF-1 in melanoma with increased metastatic potential. Biochem Biophys Res Commun 288:8–15PubMedCrossRefPubMedCentralGoogle Scholar
  78. Nishimura EK, Jordan SA, Oshima H, Yoshida H, Osawa M, Moriyama M, Jackson IJ, Barrandon Y, Miyachi Y, Nishikawa S (2002) Dominant role of the niche in melanocyte stem-cell fate determination. Nature 416:854–860PubMedCrossRefPubMedCentralGoogle Scholar
  79. Opdecamp K, Nakayama A, Nguyen MT, Hodgkinson CA, Pavan WJ, Arnheiter H (1997) Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor. Development 124:2377–2386PubMedPubMedCentralGoogle Scholar
  80. Opdecamp K, Kos L, Arnheiter H, Pavan WJ (1998) Endothelin signalling in the development of neural crest-derived melanocytes. Biochem Cell Biol 76:1093–1099PubMedCrossRefPubMedCentralGoogle Scholar
  81. Paratore C, Goerich DE, Suter U, Wegner M, Sommer L (2001) Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development 128:3949–3961PubMedPubMedCentralGoogle Scholar
  82. Pingault V, Bondurand N, Kuhlbrodt K, Goerich DE, Prehu MO, Puliti A, Herbarth B, Hermans-Borgmeyer I, Legius E, Matthijs G, Amiel J, Lyonnet S, Ceccherini I, Romeo G, Smith JC, Read AP, Wegner M, Goossens M (1998) SOX10 mutations in patients with Waardenburg-Hirschsprung disease. Nat Genet 18:171–173PubMedCrossRefPubMedCentralGoogle Scholar
  83. Pla P, Alberti C, Solov’eva O, Pasdar M, Kunisada T, Larue L (2005) Ednrb2 orients cell migration towards the dorso-lateral neural crest pathway and promotes melanocyte differentiation. Pigment Cell Res 18:181–187PubMedCrossRefPubMedCentralGoogle Scholar
  84. Plouhinec JL, Roche DD, Pegoraro C, Figueiredo AL, Maczkowiak F, Brunet LJ, Milet C, Vert JP, Pollet N, Harland RM, Monsoro-Burq AH (2014) Pax3 and Zic1 trigger the early neural crest gene regulatory network by the direct activation of multiple key neural crest specifiers. Dev Biol 386:461–472PubMedCrossRefPubMedCentralGoogle Scholar
  85. Potterf SB, Furumura M, Dunn KJ, Arnheiter H, Pavan WJ (2000) Transcription factor hierarchy in Waardenburg syndrome: regulation of MITF expression by SOX10 and PAX3. Hum Genet 107:1–6PubMedCrossRefPubMedCentralGoogle Scholar
  86. Prasad MS, Sauka-Spengler T, LaBonne C (2012) Induction of the neural crest state: control of stem cell attributes by gene regulatory, post-transcriptional and epigenetic interactions. Dev Biol 366:10–21PubMedPubMedCentralCrossRefGoogle Scholar
  87. Raible DW, Eisen JS (1994) Restriction of neural crest cell fate in the trunk of the embryonic zebrafish. Development 120:495–503PubMedPubMedCentralGoogle Scholar
  88. Raible DW, Wood A, Hodsdon W, Henion PD, Weston JA, Eisen JS (1992) Segregation and early dispersal of neural crest cells in the embryonic zebrafish. Dev Dyn 195:29–42PubMedCrossRefPubMedCentralGoogle Scholar
  89. Richardson MK, Sieber-Blum M (1993) Pluripotent neural crest cells in the developing skin of the quail embryo. Dev Biol 157:348–358PubMedCrossRefPubMedCentralGoogle Scholar
  90. Rizvi TA, Huang Y, Sidani A, Atit R, Largaespada DA, Boissy RE, Ratner N (2002) A novel cytokine pathway suppresses glial cell melanogenesis after injury to adult nerve. J Neurosci 22:9831–9840PubMedPubMedCentralCrossRefGoogle Scholar
  91. Saldana-Caboverde A, Kos L (2010) Roles of endothelin signaling in melanocyte development and melanoma. Pigment Cell Melanoma Res 23:160–170PubMedPubMedCentralCrossRefGoogle Scholar
  92. Serbedzija GN, Fraser SE, Bronner-Fraser M (1990) Pathways of trunk neural crest cell migration in the mouse embryo as revealed by vital dye labeling. Development 108:605–612PubMedPubMedCentralGoogle Scholar
  93. Serbedzija GN, Bronner-Fraser M, Fraser SE (1994) Developmental potential of trunk neural crest cells in the mouse. Development 120:1709–1718PubMedPubMedCentralGoogle Scholar
  94. Shah N, Groves A, Anderson DJ (1996) Alternative neural crest cell fates are instructively promoted by TGFß superfamily members. Cell 85:331–343PubMedCrossRefPubMedCentralGoogle Scholar
  95. Shakhova O, Sommer L (2010) Neural crest-derived stem cells. In: StemBook (ed) The stem cell research community. StemBook.  https://doi.org/10.3824/stembook.3821.3851.3821
  96. Shakhova O, Sommer L (2015) In vitro derivation of melanocytes from embryonic neural crest stem cells. Methods Mol BiolGoogle Scholar
  97. Shakhova O, Zingg D, Schaefer SM, Hari L, Civenni G, Blunschi J, Claudinot S, Okoniewski M, Beermann F, Mihic-Probst D, Moch H, Wegner M, Dummer R, Barrandon Y, Cinelli P, Sommer L (2012) Sox10 promotes the formation and maintenance of giant congenital naevi and melanoma. Nat Cell Biol 14:882–890PubMedCrossRefPubMedCentralGoogle Scholar
  98. Shakhova O, Cheng P, Mishra PJ, Zingg D, Schaefer SM, Debbache J, Hausel J, Matter C, Guo T, Davis S, Meltzer P, Mihic-Probst D, Moch H, Wegner M, Merlino G, Levesque MP, Dummer R, Santoro R, Cinelli P, Sommer L (2015) Antagonistic cross-regulation between Sox9 and Sox10 controls an anti-tumorigenic program in melanoma. PLoS Genet 11:e1004877PubMedPubMedCentralCrossRefGoogle Scholar
  99. Sherman L, Stocker KM, Morrison R, Ciment G (1993) Basic fibroblast growth factor (bFGF) acts intracellularly to cause the transdifferentiation of avian neural crest-derived Schwann cell precursors into melanocytes. Development 118:1313–1326PubMedPubMedCentralGoogle Scholar
  100. Shin MK, Levorse JM, Ingram RS, Tilghman SM (1999) The temporal requirement for endothelin receptor-B signalling during neural crest development. Nature 402:496–501CrossRefGoogle Scholar
  101. Sieber-Blum M, Cohen A (1980) Clonal analysis of quail neural crest cells: they are pluripotent and differentiate in vitro in the absence of non-neural crest cells. Dev Biol 80:96–106PubMedCrossRefPubMedCentralGoogle Scholar
  102. Simoes-Costa M, Bronner ME (2015) Establishing neural crest identity: a gene regulatory recipe. Development 142:242–257PubMedPubMedCentralCrossRefGoogle Scholar
  103. Smith A (2006) A glossary for stem-cell biology. Nature 441:1060CrossRefGoogle Scholar
  104. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, Barker N, Klein AM, van Rheenen J, Simons BD, Clevers H (2010) Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143:134–144PubMedCrossRefPubMedCentralGoogle Scholar
  105. Sommer L (2011) Generation of melanocytes from neural crest cells. Pigment Cell Melanoma Res 24:411–421PubMedCrossRefPubMedCentralGoogle Scholar
  106. Stemple DL, Anderson DJ (1992) Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71:973–985PubMedCrossRefPubMedCentralGoogle Scholar
  107. Stolt CC, Lommes P, Hillgartner S, Wegner M (2008) The transcription factor Sox5 modulates Sox10 function during melanocyte development. Nucleic Acids Res 36:5427–5440PubMedPubMedCentralCrossRefGoogle Scholar
  108. Tachibana M, Takeda K, Nobukuni Y, Urabe K, Long JE, Meyers KA, Aaronson SA, Miki T (1996) Ectopic expression of MITF, a gene for Waardenburg syndrome type 2, converts fibroblasts to cells with melanocyte characteristics. Nat Genet 14:50–54PubMedCrossRefPubMedCentralGoogle Scholar
  109. Takeda K, Yasumoto K, Takada R, Takada S, Watanabe K, Udono T, Saito H, Takahashi K, Shibahara S (2000) Induction of melanocyte-specific microphthalmia-associated transcription factor by Wnt-3a. J Biol Chem 275:14013–14016PubMedCrossRefPubMedCentralGoogle Scholar
  110. Taylor KM, Labonne C (2005) SoxE factors function equivalently during neural crest and inner ear development and their activity is regulated by SUMOylation. Dev Cell 9:593–603PubMedCrossRefPubMedCentralGoogle Scholar
  111. Teng L, Mundell NA, Frist AY, Wang Q, Labosky PA (2008) Requirement for Foxd3 in the maintenance of neural crest progenitors. Development 135:1615–1624PubMedPubMedCentralCrossRefGoogle Scholar
  112. Thomas AJ, Erickson CA (2008) The making of a melanocyte: the specification of melanoblasts from the neural crest. Pigment Cell Melanoma Res 21:598–610PubMedCrossRefPubMedCentralGoogle Scholar
  113. Thomas AJ, Erickson CA (2009) FOXD3 regulates the lineage switch between neural crest-derived glial cells and pigment cells by repressing MITF through a non-canonical mechanism. Development 136:1849–1858PubMedPubMedCentralCrossRefGoogle Scholar
  114. Van Keymeulen A, Lee MY, Ousset M, Brohee S, Rorive S, Giraddi RR, Wuidart A, Bouvencourt G, Dubois C, Salmon I, Sotiriou C, Phillips WA, Blanpain C (2015) Reactivation of multipotency by oncogenic PIK3CA induces breast tumour heterogeneity. Nature 525:119–123PubMedCrossRefPubMedCentralGoogle Scholar
  115. Wehrle-Haller B, Weston JA (1995) Soluble and cell-bound forms of steel factor activity play distinct roles in melanocyte precursor dispersal and survival on the lateral neural crest migration pathway. Development 121:731–742PubMedPubMedCentralGoogle Scholar
  116. Weston JA (1991) Sequential segregation and fate of developmentally restricted intermediate cell populations in the neural crest lineage. Curr Top Dev Biol 25:133–153PubMedCrossRefPubMedCentralGoogle Scholar
  117. Widlund HR, Horstmann MA, Price ER, Cui J, Lessnick SL, Wu M, He X, Fisher DE (2002) Beta-catenin-induced melanoma growth requires the downstream target Microphthalmia-associated transcription factor. J Cell Biol 158:1079–1087PubMedPubMedCentralCrossRefGoogle Scholar
  118. Wong CE, Paratore C, Dours-Zimmermann MT, Rochat A, Pietri T, Suter U, Zimmermann DR, Dufour S, Thiery JP, Meijer D, Beermann F, Barrandon Y, Sommer L (2006) Neural crest-derived cells with stem cell features can be traced back to multiple lineages in the adult skin. J Cell Biol 175:1005–1015PubMedPubMedCentralCrossRefGoogle Scholar
  119. Wong DJ, Liu H, Ridky TW, Cassarino D, Segal E, Chang HY (2008) Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2:333–344PubMedPubMedCentralCrossRefGoogle Scholar
  120. Zuidervaart W, Pavey S, van Nieuwpoort FA, Packer L, Out C, Maat W, Jager MJ, Gruis NA, Hayward NK (2007) Expression of Wnt5a and its downstream effector beta-catenin in uveal melanoma. Melanoma Res 17:380–386PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Stem Cell Biology, Institute of AnatomyUniversity of ZurichZurichSwitzerland

Section editors and affiliations

  • David E. Fisher
    • 1
  • Nick Hayward
    • 2
  • David C. Whiteman
    • 3
  • Keith T. Flaherty
    • 4
  • F. Stephen Hodi
    • 5
    • 6
  • Hensin Tsao
    • 7
    • 8
  • Glenn Merlino
    • 9
  1. 1.Department of Dermatology, Harvard/MGH Cutaneous Biology Research Center, and Melanoma Program, MGH Cancer CenterMassachusetts General Hospital, Harvard Medical SchoolBostonUSA
  2. 2.QIMR Berghofer Medical Research InstituteHerstonAustralia
  3. 3.QIMR Berghofer Medical Research InstituteHerstonAustralia
  4. 4.Henri and Belinda Termeer Center for Targeted TherapiesMGH Cancer CenterBostonUSA
  5. 5.FraminghamUSA
  6. 6.Department of Medicine, Brigham and Women's HospitalDana-Farber Cancer InstituteBostonUSA
  7. 7.AuburndaleUSA
  8. 8.Harvard-MIT Health Sciences and TechnologyCambridgeUSA
  9. 9.Center for Cancer ResearchNational Cancer InstituteBethesdaUSA

Personalised recommendations