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Glial versus melanocyte cell fate choice: Schwann cell precursors as a cellular origin of melanocytes

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Abstract

Melanocytes and Schwann cells are derived from the multipotent population of neural crest cells. Although both cell types were thought to be generated through completely distinct pathways and molecular processes, a recent study has revealed that these different cell types are intimately interconnected far beyond previously postulated limits in that they share a common post-neural crest progenitor, i.e. the Schwann cell precursor. This finding raises interesting questions about the lineage relationships of hitherto unrelated cell types such as melanocytes and Schwann cells, and may provide clinical insights into mechanisms of pigmentation disorders and for cancer involving Schwann cells and melanocytes.

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References

  1. Le Douarin NM, Creuzet S, Couly G, Dupin E (2004) Neural crest cell plasticity and its limits. Development 131:4637–4650

    Article  CAS  PubMed  Google Scholar 

  2. Sauka-Spengler T, Bronner-Fraser M (2008) A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol 9:557–568

    Article  CAS  PubMed  Google Scholar 

  3. Raible DW (2006) Development of the neural crest: achieving specificity in regulatory pathways. Curr Opin Cell Biol 18:698–703

    Article  CAS  PubMed  Google Scholar 

  4. 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

    Article  CAS  PubMed  Google Scholar 

  5. Jessen KR, Mirsky R (2005) The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6:671–682

    Article  CAS  PubMed  Google Scholar 

  6. Jessen KR, Brennan A, Morgan L, Mirsky R, Kent A, Hashimoto Y, Gavrilovic J (1994) The Schwann cell precursor and its fate: a study of cell death and differentiation during gliogenesis in rat embryonic nerves. Neuron 12:509–527

    Article  CAS  PubMed  Google Scholar 

  7. Meier C, Parmantier E, Brennan A, Mirsky R, Jessen KR (1999) Developing Schwann cells acquire the ability to survive without axons by establishing an autocrine circuit involving insulin-like growth factor, neurotrophin-3, and platelet-derived growth factor-BB. J Neurosci 19:3847–3859

    CAS  PubMed  Google Scholar 

  8. Woodhoo A, Sommer L (2008) Development of the Schwann cell lineage: from the neural crest to the myelinated nerve. Glia 56:1481–1490

    Article  PubMed  Google Scholar 

  9. Dong Z, Brennan A, Liu N, Yarden Y, Lefkowitz G, Mirsky R, Jessen KR (1995) Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15:585–596

    Article  CAS  PubMed  Google Scholar 

  10. Grinspan JB, Marchionni MA, Reeves M, Coulaloglou M, Scherer SS (1996) Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: neuregulin receptors and the role of neuregulins. J Neurosci 16:6107–6118

    CAS  PubMed  Google Scholar 

  11. Syroid DE, Maycox PR, Burrola PG, Liu N, Wen D, Lee KF, Lemke G, Kilpatrick TJ (1996) Cell death in the Schwann cell lineage and its regulation by neuregulin. Proc Natl Acad Sci USA 93:9229–9234

    Article  CAS  PubMed  Google Scholar 

  12. 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 15:66–78

    Article  CAS  PubMed  Google Scholar 

  13. Garratt AN, Voiculescu O, Topilko P, Charnay P, Birchmeier C (2000) A dual role of erbB2 in myelination and in expansion of the Schwann cell precursor pool. J Cell Biol 148:1035–1046

    Article  CAS  PubMed  Google Scholar 

  14. Garratt AN, Britsch S, Birchmeier C (2000) Neuregulin, a factor with many functions in the life of a Schwann cell. Bioessays 22:987–996

    Article  CAS  PubMed  Google Scholar 

  15. Morrissey TK, Levi AD, Nuijens A, Sliwkowski MX, Bunge RP (1995) Axon-induced mitogenesis of human Schwann cells involves heregulin and p185erbB2. Proc Natl Acad Sci USA 92:1431–1435

    Article  CAS  PubMed  Google Scholar 

  16. Levi AD, Bunge RP, Lofgren JA, Meima L, Hefti F, Nikolics K, Sliwkowski MX (1995) The influence of heregulins on human Schwann cell proliferation. J Neurosci 15:1329–1340

    CAS  PubMed  Google Scholar 

  17. Taveggia C, Zanazzi G, Petrylak A, Yano H, Rosenbluth J, Einheber S, Xu X, Esper RM, Loeb JA, Shrager P, Chao MV, Falls DL, Role L, Salzer JL (2005) Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47:681–694

    Article  CAS  PubMed  Google Scholar 

  18. Morris JK, Lin W, Hauser C, Marchuk Y, Getman D, Lee KF (1999) Rescue of the cardiac defect in ErbB2 mutant mice reveals essential roles of ErbB2 in peripheral nervous system development. Neuron 23:273–283

    Article  CAS  PubMed  Google Scholar 

  19. Riethmacher D, Sonnenberg-Riethmacher E, Brinkmann V, Yamaai T, Lewin GR, Birchmeier C (1997) Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 389:725–730

    Article  CAS  PubMed  Google Scholar 

  20. Woldeyesus MT, Britsch S, Riethmacher D, Xu L, Sonnenberg-Riethmacher E, Abou-Rebyeh F, Harvey R, Caroni P, Birchmeier C (1999) Peripheral nervous system defects in erbB2 mutants following genetic rescue of heart development. Genes Dev 13:2538–2548

    Article  CAS  PubMed  Google Scholar 

  21. Chen S, Rio C, Ji RR, Dikkes P, Coggeshall RE, Woolf CJ, Corfas G (2003) Disruption of ErbB receptor signaling in adult non-myelinating Schwann cells causes progressive sensory loss. Nat Neurosci 6:1186–1193

    Article  CAS  PubMed  Google Scholar 

  22. Louvi A, Artavanis-Tsakonas S (2006) Notch signalling in vertebrate neural development. Nat Rev Neurosci 7:93–102

    Article  CAS  PubMed  Google Scholar 

  23. 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 128:3949–3961

    CAS  PubMed  Google Scholar 

  24. Shah NM, Marchionni MA, Isaacs I, Stroobant P, Anderson DJ (1994) Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77:349–360

    Article  CAS  PubMed  Google Scholar 

  25. 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 

  26. Kubu CJ, Orimoto K, Morrison SJ, Weinmaster G, Anderson DJ, Verdi JM (2002) Developmental changes in Notch1 and numb expression mediated by local cell-cell interactions underlie progressively increasing delta sensitivity in neural crest stem cells. Dev Biol 244:199–214

    Article  CAS  PubMed  Google Scholar 

  27. Morrison SJ, Perez SE, Qiao Z, Verdi JM, Hicks C, Weinmaster G, Anderson DJ (2000) Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101:499–510

    Article  CAS  PubMed  Google Scholar 

  28. Taylor MK, Yeager K, Morrison SJ (2007) Physiological Notch signaling promotes gliogenesis in the developing peripheral and central nervous systems. Development 134:2435–2447

    Article  CAS  PubMed  Google Scholar 

  29. Woodhoo A, Alonso MB, Droggiti A, Turmaine M, D’Antonio M, Parkinson DB, Wilton DK, Al-Shawi R, Simons P, Shen J, Guillemot F, Radtke F, Meijer D, Feltri ML, Wrabetz L, Mirsky R, Jessen KR (2009) Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat Neurosci 12:839–847

    Article  CAS  PubMed  Google Scholar 

  30. Erickson CA (1993) From the crest to the periphery: control of pigment cell migration and lineage segregation. Pigment Cell Res 6:336–347

    Article  CAS  PubMed  Google Scholar 

  31. Bronner ME, Cohen AM (1979) Migratory patterns of cloned neural crest melanocytes injected into host chicken embryos. Proc Natl Acad Sci USA 76:1843–1847

    Article  CAS  PubMed  Google Scholar 

  32. Johnston MC (1966) A radioautographic study of the migration and fate of cranial neural crest cells in the chick embryo. Anat Rec 156:143–155

    Article  CAS  PubMed  Google Scholar 

  33. Le Douarin N (1973) A biological cell labeling technique and its use in experimental embryology. Dev Biol 30:217–222

    Article  CAS  PubMed  Google Scholar 

  34. 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 192:99–107

    Article  CAS  PubMed  Google Scholar 

  35. Rawles ME (1947) Some observations on the developmental properties of the presumptive hind-limb area of the chick. Anat Rec 99:648

    CAS  PubMed  Google Scholar 

  36. 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 106:809–816

    CAS  PubMed  Google Scholar 

  37. Serbedzija GN, Fraser SE, Bronner-Fraser M (1990) Pathways of trunk neural crest cell migration in the mouse embryo as revealed by vital dye labelling. Development 108:605–612

    CAS  PubMed  Google Scholar 

  38. 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 

  39. Collazo A, Bronner-Fraser M, Fraser SE (1993) Vital dye labelling of Xenopus laevis trunk neural crest reveals multipotency and novel pathways of migration. Development 118:363–376

    CAS  PubMed  Google Scholar 

  40. 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 136:1849–1858

    Article  CAS  PubMed  Google Scholar 

  41. Niwa T, Mochii M, Nakamura A, Shiojiri N (2002) Plumage pigmentation and expression of its regulatory genes during quail development—histochemical analysis using Bh (black at hatch) mutants. Mech Dev 118:139–146

    Article  CAS  PubMed  Google Scholar 

  42. Wilkie AL, Jordan SA, Jackson IJ (2002) Neural crest progenitors of the melanocyte lineage: coat colour patterns revisited. Development 129:3349–3357

    CAS  PubMed  Google Scholar 

  43. Yang CT, Johnson SL (2006) Small molecule-induced ablation and subsequent regeneration of larval zebrafish melanocytes. Development 133:3563–3573

    Article  CAS  PubMed  Google Scholar 

  44. Hultman KA, Budi EH, Teasley DC, Gottlieb AY, Parichy DM, Johnson SL (2009) Defects in ErbB-dependent establishment of adult melanocyte stem cells reveal independent origins for embryonic and regeneration melanocytes. PLoS Genet 5:e1000544

    Article  PubMed  CAS  Google Scholar 

  45. Goodrich H, Nichols R (1931) The development and the regeneration of the color pattern in Brachydanio rerio. J Morphol 52:513–523

    Article  Google Scholar 

  46. O’Reilly-Pol T, Johnson SL (2009) Melanocyte regeneration reveals mechanisms of adult stem cell regulation. Semin Cell Dev Biol 20:117–124

    Article  PubMed  CAS  Google Scholar 

  47. Yang CT, Sengelmann RD, Johnson SL (2004) Larval melanocyte regeneration following laser ablation in zebrafish. J Invest Dermatol 123:924–929

    Article  CAS  PubMed  Google Scholar 

  48. Rawls JF, Johnson SL (2000) Zebrafish kit mutation reveals primary and secondary regulation of melanocyte development during fin stripe regeneration. Development 127:3715–3724

    CAS  PubMed  Google Scholar 

  49. Ide H, Akira E (1988) Differentiation and transdifferentiation of amphibian chromatophores. Prog Clin Biol Res 256:35–48

    CAS  PubMed  Google Scholar 

  50. Thibaudeau G, Holder S (1998) Cellular plasticity among axolotl neural crest-derived pigment cell lineages. Pigment Cell Res 11:38–44

    Article  CAS  PubMed  Google Scholar 

  51. Pickart MA, Sivasubbu S, Nielsen AL, Shriram S, King RA, Ekker SC (2004) Functional genomics tools for the analysis of zebrafish pigment. Pigment Cell Res 17:461–470

    Article  CAS  PubMed  Google Scholar 

  52. Rawls JF, Mellgren EM, Johnson SL (2001) How the zebrafish gets its stripes. Dev Biol 240:301–314

    Article  CAS  PubMed  Google Scholar 

  53. Lang MR, Patterson LB, Gordon TN, Johnson SL, Parichy DM (2009) Basonuclin-2 requirements for zebrafish adult pigment pattern development and female fertility. PLoS Genet 5:e1000744

    Article  PubMed  CAS  Google Scholar 

  54. Budi EH, Patterson LB, Parichy DM (2008) Embryonic requirements for ErbB signaling in neural crest development and adult pigment pattern formation. Development 135:2603–2614

    Article  CAS  PubMed  Google Scholar 

  55. Lyons DA, Pogoda HM, Voas MG, Woods IG, Diamond B, Nix R, Arana N, Jacobs J, Talbot WS (2005) erbb3 and erbb2 are essential for Schwann cell migration and myelination in zebrafish. Curr Biol 15:513–524

    Article  CAS  PubMed  Google Scholar 

  56. Thomas AJ, Erickson CA (2008) The making of a melanocyte: the specification of melanoblasts from the neural crest. Pigment Cell Melanoma Res 21:598–610

    Article  CAS  PubMed  Google Scholar 

  57. Goulding MD, Chalepakis G, Deutsch U, Erselius JR, Gruss P (1991) Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J 10:1135–1147

    CAS  PubMed  Google Scholar 

  58. Tremblay P, Kessel M, Gruss P (1995) A transgenic neuroanatomical marker identifies cranial neural crest deficiencies associated with the Pax3 mutant Splotch. Dev Biol 171:317–329

    Article  CAS  PubMed  Google Scholar 

  59. Hornyak TJ, Hayes DJ, Chiu LY, Ziff EB (2001) Transcription factors in melanocyte development: distinct roles for Pax-3 and Mitf. Mech Dev 101:47–59

    Article  CAS  PubMed  Google Scholar 

  60. Levy C, Khaled M, Fisher DE (2006) MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol Med 12:406–414

    Article  CAS  PubMed  Google Scholar 

  61. Steingrimsson E, Copeland NG, Jenkins NA (2004) Melanocytes and the microphthalmia transcription factor network. Annu Rev Genet 38:365–411

    Article  CAS  PubMed  Google Scholar 

  62. 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 124:2377–2386

    CAS  PubMed  Google Scholar 

  63. Planque N, Raposo G, Leconte L, Anezo O, Martin P, Saule S (2004) Microphthalmia transcription factor induces both retinal pigmented epithelium and neural crest melanocytes from neuroretina cells. J Biol Chem 279:41911–41917

    Article  CAS  PubMed  Google Scholar 

  64. Planque N, Turque N, Opdecamp K, Bailly M, Martin P, Saule S (1999) Expression of the microphthalmia-associated basic helix-loop–helix leucine zipper transcription factor Mi in avian neuroretina cells induces a pigmented phenotype. Cell Growth Differ 10:525–536

    CAS  PubMed  Google Scholar 

  65. 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 14:50–54

    Article  CAS  PubMed  Google Scholar 

  66. Lee M, Goodall J, Verastegui C, Ballotti R, Goding CR (2000) Direct regulation of the Microphthalmia promoter by Sox10 links Waardenburg-Shah syndrome (WS4)-associated hypopigmentation and deafness to WS2. J Biol Chem 275:37978–37983

    Article  CAS  PubMed  Google Scholar 

  67. Verastegui C, Bille K, Ortonne JP, Ballotti R (2000) Regulation of the microphthalmia-associated transcription factor gene by the Waardenburg syndrome type 4 gene, SOX10. J Biol Chem 275:30757–30760

    Article  CAS  PubMed  Google Scholar 

  68. Schreiner S, Cossais F, Fischer K, Scholz S, Bosl MR, Holtmann B, Sendtner M, Wegner M (2007) Hypomorphic Sox10 alleles reveal novel protein functions and unravel developmental differences in glial lineages. Development 134:3271–3281

    Article  CAS  PubMed  Google Scholar 

  69. Hou L, Arnheiter H, Pavan WJ (2006) Interspecies difference in the regulation of melanocyte development by SOX10 and MITF. Proc Natl Acad Sci USA 103:9081–9085

    Article  CAS  PubMed  Google Scholar 

  70. Potterf SB, Mollaaghababa R, Hou L, Southard-Smith EM, Hornyak TJ, Arnheiter H, Pavan WJ (2001) Analysis of SOX10 function in neural crest-derived melanocyte development: SOX10-dependent transcriptional control of dopachrome tautomerase. Dev Biol 237:245–257

    Article  CAS  PubMed  Google Scholar 

  71. Kim J, Lo L, Dormand E, Anderson DJ (2003) SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 38:17–31

    Article  CAS  PubMed  Google Scholar 

  72. Peirano RI, Goerich DE, Riethmacher D, Wegner M (2000) Protein zero gene expression is regulated by the glial transcription factor Sox10. Mol Cell Biol 20:3198–3209

    Article  CAS  PubMed  Google Scholar 

  73. Wu J, Saint-Jeannet JP, Klein PS (2003) Wnt-frizzled signaling in neural crest formation. Trends Neurosci 26:40–45

    Article  CAS  PubMed  Google Scholar 

  74. Dorsky RI, Moon RT, Raible DW (1998) Control of neural crest cell fate by the Wnt signalling pathway. Nature 396:370–373

    Article  CAS  PubMed  Google Scholar 

  75. Hari L, Brault V, Kleber M, Lee HY, Ille F, Leimeroth R, Paratore C, Suter U, Kemler R, Sommer L (2002) Lineage-specific requirements of beta-catenin in neural crest development. J Cell Biol 159:867–880

    Article  CAS  PubMed  Google Scholar 

  76. Jin EJ, Erickson CA, Takada S, Burrus LW (2001) Wnt and BMP signaling govern lineage segregation of melanocytes in the avian embryo. Dev Biol 233:22–37

    Article  CAS  PubMed  Google Scholar 

  77. Ikeya M, Lee SM, Johnson JE, McMahon AP, Takada S (1997) Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389:966–970

    Article  CAS  PubMed  Google Scholar 

  78. Moon RT, Bowerman B, Boutros M, Perrimon N (2002) The promise and perils of Wnt signaling through beta-catenin. Science 296:1644–1646

    Article  CAS  PubMed  Google Scholar 

  79. 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 14:158–162

    CAS  PubMed  Google Scholar 

  80. 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 275:14013–14016

    Article  CAS  PubMed  Google Scholar 

  81. Bernex F, De Sepulveda P, Kress C, Elbaz C, Delouis C, Panthier JJ (1996) Spatial and temporal patterns of c-kit-expressing cells in WlacZ/+ and WlacZ/WlacZ mouse embryos. Development 122:3023–3033

    CAS  PubMed  Google Scholar 

  82. Kluppel M, Nagle DL, Bucan M, Bernstein A (1997) Long-range genomic rearrangements upstream of Kit dysregulate the developmental pattern of Kit expression in W57 and Wbanded mice and interfere with distinct steps in melanocyte development. Development 124:65–77

    CAS  PubMed  Google Scholar 

  83. Manova K, Bachvarova RF (1991) Expression of c-kit encoded at the W locus of mice in developing embryonic germ cells and presumptive melanoblasts. Dev Biol 146:312–324

    Article  CAS  PubMed  Google Scholar 

  84. Yoshida H, Kunisada T, Kusakabe M, Nishikawa S, Nishikawa SI (1996) Distinct stages of melanocyte differentiation revealed by analysis of nonuniform pigmentation patterns. Development 122:1207–1214

    CAS  PubMed  Google Scholar 

  85. Hou L, Panthier JJ, Arnheiter H (2000) Signaling and transcriptional regulation in the neural crest-derived melanocyte lineage: interactions between KIT and MITF. Development 127:5379–5389

    CAS  PubMed  Google Scholar 

  86. Kunisada T, Yoshida H, Yamazaki H, Miyamoto A, Hemmi H, Nishimura E, Shultz LD, Nishikawa S, Hayashi S (1998) Transgene expression of steel factor in the basal layer of epidermis promotes survival, proliferation, differentiation and migration of melanocyte precursors. Development 125:2915–2923

    CAS  PubMed  Google Scholar 

  87. 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 121:731–742

    CAS  PubMed  Google Scholar 

  88. Nishikawa S, Kusakabe M, Yoshinaga K, Ogawa M, Hayashi S, Kunisada T, Era T, Sakakura T (1991) In utero manipulation of coat color formation by a monoclonal anti-c-kit antibody: two distinct waves of c-kit-dependency during melanocyte development. EMBO J 10:2111–2118

    CAS  PubMed  Google Scholar 

  89. Okura M, Maeda H, Nishikawa S, Mizoguchi M (1995) Effects of monoclonal anti-c-kit antibody (ACK2) on melanocytes in newborn mice. J Invest Dermatol 105:322–328

    Article  CAS  PubMed  Google Scholar 

  90. Baynash AG, Hosoda K, Giaid A, Richardson JA, Emoto N, Hammer RE, Yanagisawa M (1994) Interaction of endothelin-3 with endothelin-B receptor is essential for development of epidermal melanocytes and enteric neurons. Cell 79:1277–1285

    Article  CAS  PubMed  Google Scholar 

  91. Puffenberger EG, Hosoda K, Washington SS, Nakao K, deWit D, Yanagisawa M, Chakravart A (1994) A missense mutation of the endothelin-B receptor gene in multigenic Hirschsprung’s disease. Cell 79:1257–1266

    Article  CAS  PubMed  Google Scholar 

  92. Reid K, Turnley AM, Maxwell GD, Kurihara Y, Kurihara H, Bartlett PF, Murphy M (1996) Multiple roles for endothelin in melanocyte development: regulation of progenitor number and stimulation of differentiation. Development 122:3911–3919

    CAS  PubMed  Google Scholar 

  93. Shin MK, Levorse JM, Ingram RS, Tilghman SM (1999) The temporal requirement for endothelin receptor-B signalling during neural crest development. Nature 402:496–501

    Article  CAS  PubMed  Google Scholar 

  94. Lee HO, Levorse JM, Shin MK (2003) The endothelin receptor-B is required for the migration of neural crest-derived melanocyte and enteric neuron precursors. Dev Biol 259:162–175

    Article  CAS  PubMed  Google Scholar 

  95. Brennan A, Dean CH, Zhang AL, Cass DT, Mirsky R, Jessen KR (2000) Endothelins control the timing of Schwann cell generation in vitro and in vivo. Dev Biol 227:545–557

    Article  CAS  PubMed  Google Scholar 

  96. 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 USA 95:14214–14219

    Article  CAS  PubMed  Google Scholar 

  97. 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 USA 100:5229–5233

    Article  CAS  PubMed  Google Scholar 

  98. Nataf V, Le Douarin NM (2000) Induction of melanogenesis by tetradecanoylphorbol-13 acetate and endothelin 3 in embryonic avian peripheral nerve cultures. Pigment Cell Res 13:172–178

    Article  CAS  PubMed  Google Scholar 

  99. Ciment G, Glimelius B, Nelson DM, Weston JA (1986) Reversal of a developmental restriction in neural crest-derived cells of avian embryos by a phorbol ester drug. Dev Biol 118:392–398

    Article  CAS  PubMed  Google Scholar 

  100. Nichols DH, Kaplan RA, Weston JA (1977) Melanogenesis in cultures of peripheral nervous tissue. II. Environmental factors determining the fate of pigment-forming cells. Dev Biol 60:226–237

    Article  CAS  PubMed  Google Scholar 

  101. Nichols DH, Weston JA (1977) Melanogenesis in cultures of peripheral nervous tissue. I. The origin and prospective fate of cells giving rise to melanocytes. Dev Biol 60:217–225

    Article  CAS  PubMed  Google Scholar 

  102. 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 118:1313–1326

    CAS  PubMed  Google Scholar 

  103. 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 USA 97:7882–7887

    Article  CAS  PubMed  Google Scholar 

  104. Dupin E, Le Douarin NM (2003) Development of melanocyte precursors from the vertebrate neural crest. Oncogene 22:3016–3023

    Article  CAS  PubMed  Google Scholar 

  105. Trentin A, Glavieux-Pardanaud C, Le Douarin NM, Dupin E (2004) Self-renewal capacity is a widespread property of various types of neural crest precursor cells. Proc Natl Acad Sci USA 101:4495–4500

    Article  CAS  PubMed  Google Scholar 

  106. Real C, Glavieux-Pardanaud C, Vaigot P, Le-Douarin N, Dupin E (2005) The instability of the neural crest phenotypes: Schwann cells can differentiate into myofibroblasts. Int J Dev Biol 49:151–159

    Article  CAS  PubMed  Google Scholar 

  107. Real C, Glavieux-Pardanaud C, Le Douarin NM, Dupin E (2006) Clonally cultured differentiated pigment cells can dedifferentiate and generate multipotent progenitors with self-renewing potential. Dev Biol 300:656–669

    Article  CAS  PubMed  Google Scholar 

  108. Jaegle M, Ghazvini M, Mandemakers W, Piirsoo M, Driegen S, Levavasseur F, Raghoenath S, Grosveld F, Meijer D (2003) The POU proteins Brn-2 and Oct-6 share important functions in Schwann cell development. Genes Dev 17:1380–1391

    Article  CAS  PubMed  Google Scholar 

  109. Joseph NM, Mukouyama YS, Mosher JT, Jaegle M, Crone SA, Dormand EL, Lee KF, Meijer D, Anderson DJ, Morrison SJ (2004) Neural crest stem cells undergo multilineage differentiation in developing peripheral nerves to generate endoneurial fibroblasts in addition to Schwann cells. Development 131:5599–5612

    Article  CAS  PubMed  Google Scholar 

  110. Sutton J, Costa R, Klug M, Field L, Xu D, Largaespada DA, Fletcher CF, Jenkins NA, Copeland NG, Klemsz M, Hromas R (1996) Genesis, a winged helix transcriptional repressor with expression restricted to embryonic stem cells. J Biol Chem 271:23126–23133

    Article  CAS  PubMed  Google Scholar 

  111. Dottori M, Gross MK, Labosky P, Goulding M (2001) The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate. Development 128:4127–4138

    CAS  PubMed  Google Scholar 

  112. 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 128:1467–1479

    CAS  PubMed  Google Scholar 

  113. Curran K, Raible DW, Lister JA (2009) Foxd3 controls melanophore specification in the zebrafish neural crest by regulation of Mitf. Dev Biol 332:408–417

    Article  CAS  PubMed  Google Scholar 

  114. Hanna LA, Foreman RK, Tarasenko IA, Kessler DS, Labosky PA (2002) Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes Dev 16:2650–2661

    Article  CAS  PubMed  Google Scholar 

  115. Xu D, Yoder M, Sutton J, Hromas R (1998) Forced expression of Genesis, a winged helix transcriptional repressor isolated from embryonic stem cells, blocks granulocytic differentiation of 32D myeloid cells. Leukemia 12:207–212

    Article  CAS  PubMed  Google Scholar 

  116. Bardin AJ, Perdigoto CN, Southall TD, Brand AH, Schweisguth F (2010) Transcriptional control of stem cell maintenance in the Drosophila intestine. Development 137:705–714

    Article  CAS  PubMed  Google Scholar 

  117. Dejosez M, Krumenacker JS, Zitur LJ, Passeri M, Chu LF, Songyang Z, Thomson JA, Zwaka TP (2008) Ronin is essential for embryogenesis and the pluripotency of mouse embryonic stem cells. Cell 133:1162–1174

    Article  CAS  PubMed  Google Scholar 

  118. Jepsen K, Solum D, Zhou T, McEvilly RJ, Kim HJ, Glass CK, Hermanson O, Rosenfeld MG (2007) SMRT-mediated repression of an H3K27 demethylase in progression from neural stem cell to neuron. Nature 450:415–419

    Article  CAS  PubMed  Google Scholar 

  119. Pietersen AM, van Lohuizen M (2008) Stem cell regulation by polycomb repressors: postponing commitment. Curr Opin Cell Biol 20:201–207

    Article  CAS  PubMed  Google Scholar 

  120. Yu HS (2002) Melanocyte destruction and repigmentation in vitiligo: a model for nerve cell damage and regrowth. J Biomed Sci 9:564–573

    Article  CAS  PubMed  Google Scholar 

  121. Koga M (1977) Vitiligo: a new classification and therapy. Br J Dermatol 97:255–261

    Article  CAS  PubMed  Google Scholar 

  122. Westphal FL, de Campos JR, Ribas J, de Lima LC, Lima Netto JC, da Silva MS, Westphal DC (2009) Skin depigmentation: could it be a complication caused by thoracic sympathectomy? Ann Thorac Surg 88:e42–43

    Article  PubMed  Google Scholar 

  123. Long TF, Liu L, He L, Shen LD, Gu H, Yang Z, Tu Y, Ruan RH, Liu Y (2010) Androgen, estrogen and progesterone receptors in acquired bilateral nevus of Ota-like macules. Pigment Cell Melanoma Res 23:144–146

    Article  CAS  PubMed  Google Scholar 

  124. Patterson CR, Acland K, Khooshabeh R (2009) Cutaneous malignant melanoma arising in an acquired naevus of Ota. Australas J Dermatol 50:294–296

    Article  PubMed  Google Scholar 

  125. Luo XY, Xu AE, Li JC, Guan CP (2009) Naevus of Ota associated with segmental vitiligo: a case report. J Eur Acad Dermatol Venereol 24:611–612

    Article  PubMed  Google Scholar 

  126. Hussein MR (2008) Extracutaneous malignant melanomas. Cancer Invest 26:516–534

    Article  PubMed  Google Scholar 

  127. Reddy CE, Panda NK, Vaiphei K, Powari M (2003) Pigmented vagal paraganglioma. J Laryngol Otol 117:584–587

    Article  PubMed  Google Scholar 

  128. Kaehler KC, Russo PA, Katenkamp D, Kreusch T, Neuber K, Schwarz T, Hauschild A (2008) Melanocytic schwannoma of the cutaneous and subcutaneous tissues: three cases and a review of the literature. Melanoma Res 18:438–442

    Article  PubMed  Google Scholar 

  129. Mautner VF, Friedrich RE, von Deimling A, Hagel C, Korf B, Knofel MT, Wenzel R, Funsterer C (2003) Malignant peripheral nerve sheath tumours in neurofibromatosis type 1: MRI supports the diagnosis of malignant plexiform neurofibroma. Neuroradiology 45:618–625

    Article  CAS  PubMed  Google Scholar 

  130. De Schepper S, Boucneau J, Lambert J, Messiaen L, Naeyaert JM (2005) Pigment cell-related manifestations in neurofibromatosis type 1: an overview. Pigment Cell Res 18:13–24

    Article  PubMed  CAS  Google Scholar 

  131. Guillot B, Dalac S, Delaunay M, Baccard M, Chevrant-Breton J, Dereure O, Machet L, Sassolas B, Zeller J, Bernard P, Bedane C, Wolkenstein P (2004) Cutaneous malignant melanoma and neurofibromatosis type 1. Melanoma Res 14:159–163

    Article  PubMed  Google Scholar 

  132. Rubben A, Bausch B, Nikkels A (2006) Somatic deletion of the NF1 gene in a neurofibromatosis type 1-associated malignant melanoma demonstrated by digital PCR. Mol Cancer 5:36

    Article  PubMed  CAS  Google Scholar 

  133. Maertens O, De Schepper S, Vandesompele J, Brems H, Heyns I, Janssens S, Speleman F, Legius E, Messiaen L (2007) Molecular dissection of isolated disease features in mosaic neurofibromatosis type 1. Am J Hum Genet 81:243–251

    Article  CAS  PubMed  Google Scholar 

  134. Le LQ, Shipman T, Burns DK, Parada LF (2009) Cell of origin and microenvironment contribution for NF1-associated dermal neurofibromas. Cell Stem Cell 4:453–463

    Article  CAS  PubMed  Google Scholar 

  135. Wu J, Williams JP, Rizvi TA, Kordich JJ, Witte D, Meijer D, Stemmer-Rachamimov AO, Cancelas JA, Ratner N (2008) Plexiform and dermal neurofibromas and pigmentation are caused by Nf1 loss in desert hedgehog-expressing cells. Cancer Cell 13:105–116

    Article  CAS  PubMed  Google Scholar 

  136. Zheng H, Chang L, Patel N, Yang J, Lowe L, Burns DK, Zhu Y (2008) Induction of abnormal proliferation by nonmyelinating Schwann cells triggers neurofibroma formation. Cancer Cell 13:117–128

    Article  CAS  PubMed  Google Scholar 

  137. Joseph NM, Mosher JT, Buchstaller J, Snider P, McKeever PE, Lim M, Conway SJ, Parada LF, Zhu Y, Morrison SJ (2008) The loss of Nf1 transiently promotes self-renewal but not tumorigenesis by neural crest stem cells. Cancer Cell 13:129–140

    Article  CAS  PubMed  Google Scholar 

  138. Jeffery WR (2006) Ascidian neural crest-like cells: phylogenetic distribution, relationship to larval complexity, and pigment cell fate. J Exp Zool B Mol Dev Evol 306:470–480

    Article  PubMed  CAS  Google Scholar 

  139. Jeffery WR (2007) Chordate ancestry of the neural crest: new insights from ascidians. Semin Cell Dev Biol 18:481–491

    Article  CAS  PubMed  Google Scholar 

  140. Jeffery WR, Strickler AG, Yamamoto Y (2004) Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 431:696–699

    Article  CAS  PubMed  Google Scholar 

  141. Northcutt RG, Gans C (1983) The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Q Rev Biol 58:1–28

    Article  CAS  PubMed  Google Scholar 

  142. Donoghue PC, Graham A, Kelsh RN (2008) The origin and evolution of the neural crest. Bioessays 30:530–541

    Article  PubMed  Google Scholar 

  143. Wicht H, Lacalli T (2005) The nervous system of amphioxus: structure, development, and evolutionary significance. Can J Zool 83:122–150

    Article  Google Scholar 

  144. Stach T (2008) Chordate phylogeny and evolution: a not so simple three-taxon problem. J Zool 276:117–141

    Article  Google Scholar 

  145. Kuratani S, Ueki T, Aizawa S, Hirano S (1997) Peripheral development of cranial nerves in a cyclostome, Lampetra japonica: morphological distribution of nerve branches and the vertebrate body plan. J Comp Neurol 384:483–500

    Article  CAS  PubMed  Google Scholar 

  146. Whiting MF, Bradler S, Maxwell T (2003) Loss and recovery of wings in stick insects. Nature 421:264–267

    Article  CAS  PubMed  Google Scholar 

  147. 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 22:9831–9840

    CAS  PubMed  Google Scholar 

  148. 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 175:1005–1015

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Patrik Ernfors and Ruani Fernando for critical reading of the manuscript. We also thank Anastasia Ermolaeva and Maria Golubeva for helping us with design of the figures. I. Adameyko was supported by the Swedish Medical Research Council. F. Lallemend was supported by the Swedish Medical Research Council and the European Union.

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  1. Unit of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Karolinska Institute, Scheeles väg 1-A1-plan2, 171 77, Stockholm, Sweden

    Igor Adameyko & Francois Lallemend

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  1. Igor Adameyko
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  2. Francois Lallemend
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Correspondence to Igor Adameyko or Francois Lallemend.

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Adameyko, I., Lallemend, F. Glial versus melanocyte cell fate choice: Schwann cell precursors as a cellular origin of melanocytes. Cell. Mol. Life Sci. 67, 3037–3055 (2010). https://doi.org/10.1007/s00018-010-0390-y

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  • DOI: https://doi.org/10.1007/s00018-010-0390-y

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