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Cell Diversification During Neural Crest Ontogeny: The Neural Crest Stem Cells

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Perspectives of Stem Cells

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Abstract

The neural crest (NC) is a transitory ectodermal structure that forms in the vertebrate embryo at the junction between the presumptive CNS and epidermis. As it is at the origin of very diverse (neural and non-neural) cell types in adult tissues, the NC has attracted for long the interest of developmental biologists and is a valuable model to investigate stem cell biology. Here we review a number of data mainly provided by in vitro single cell culture experiments, which led to characterizing multipotent stem cells and progenitors in the NC cells (NCC) that undergo migration during embryogenesis. We focus on one striking property of the cephalic NCC, i.e., the capacity to yield chondrocytes and bone-forming cells in addition to skin melanocytes and nerve cells of the peripheral nervous system (PNS). We also emphasize the role of environmental cues in ensuring the survival and directing the differentiation of these progenitors in their various sites of homing. Finally we also include recent advances that uncover stem cell properties of NC-derived cells in the adult body. On one hand, differentiated cell types of NC origin are prone to dedifferentiate, as shown by in vitro experiments; on the other hand, undifferentiated multipotent NCC persist in many tissues and organs. These findings suggest that a diversity of NC-derived cells could be mobilized to function as stem cells in adult tissue repair.

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Abbreviations

ET3:

endothelin-3

NC:

neural crest

NCC:

neural crest cell(s)

NF:

neural fold

PNS:

peripheral nervous system

Shh:

Sonic Hedgehog

References

  • Ahlgren SC, Bronner-Fraser M (1999) Inhibition of sonic hedgehog signaling in vivo results in craniofacial neural crest cell death. Curr Biol 9:1304–1314.

    Article  CAS  PubMed  Google Scholar 

  • Baroffio A, Dupin E, Le Douarin NM (1988) Clone-forming ability and differentiation potential of migratory neural crest cells. Proc Natl Acad Sci USA 85:5325–5329.

    Article  CAS  PubMed  Google Scholar 

  • Baroffio A, Dupin E, Le Douarin NM (1991) Common precursors for neural and mesectodermal derivatives in the cephalic neural crest. Development 112:301–305.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Biernaskie J, Sparling JS, Liu J, Shannon CP, Plemel JR, Xie Y, Miller FD, Tetzlaff W (2007) Skin-derived precursors generate myelinating Schwann cells that promote remyelination and functional recovery after contusion spinal cord injury. J Neurosci 27:9545–9559.

    Article  CAS  PubMed  Google Scholar 

  • Billon N, Iannarelli P, Monteiro MC, Glavieux-Pardanaud C, Richardson WD, Kessaris N, Dani C, Dupin E (2007) The generation of adipocytes by the neural crest. Development 134:2283–2292.

    Article  CAS  PubMed  Google Scholar 

  • Blau HM, Brazelton TR, Weimann JM (2001) The evolving concept of a stem cell: entity or function?. Cell 105:829–841.

    Article  CAS  PubMed  Google Scholar 

  • Calloni GW, Glavieux-Pardanaud C, Le Douarin NM, Dupin E (2007) Sonic Hedgehog promotes the development of multipotent neural crest progenitors endowed with both mesenchymal and neural potentials. Proc Natl Acad Sci USA 104:19879–19884.

    Article  CAS  PubMed  Google Scholar 

  • 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 USA 106:8947–8952.

    Article  CAS  PubMed  Google Scholar 

  • Carmona-Fontaine C, Acuna G, Ellwanger K, Niehrs C, Mayor R (2007) Neural crests are actively precluded from the anterior neural fold by a novel inhibitory mechanism dependent on Dickkopf1 secreted by the prechordal mesoderm. Dev Biol 309:208–221.

    Article  CAS  PubMed  Google Scholar 

  • Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA (1996) Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383:407–413.

    Article  CAS  PubMed  Google Scholar 

  • Cohen AM, Konigsberg IR (1975) A clonal approach to the problem of neural crest determination. Dev Biol 46:262–280.

    Article  CAS  PubMed  Google Scholar 

  • Couly GF, Coltey PM, Le Douarin NM (1993) The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117:409–429.

    CAS  PubMed  Google Scholar 

  • Couly GF, Le Douarin NM (1985) Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev Biol 110:422–439.

    Article  CAS  PubMed  Google Scholar 

  • Duff RS, Langtimm CJ, Richardson MK, Sieber-Blum M (1991) In vitro clonal analysis of progenitor cell patterns in dorsal root and sympathetic ganglia of the quail embryo. Dev Biol 147:451–459.

    Article  CAS  PubMed  Google Scholar 

  • Dupin E (1984) Cell division in the ciliary ganglion of quail embryos in situ and after back-transplantation into the neural crest migration pathways of chick embryos. Dev Biol 105:288–299.

    Article  CAS  PubMed  Google Scholar 

  • Dupin E, Baroffio A, Dulac C, Cameron-Curry P, Le Douarin NM (1990) Schwann-cell differentiation in clonal cultures of the neural crest, as evidenced by the anti-Schwann cell myelin protein monoclonal antibody. Proc Natl Acad Sci USA 87:1119–1123.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Dupin E, Le Douarin NM (1995) Retinoic acid promotes the differentiation of adrenergic cells and melanocytes in quail neural crest cultures. Dev Biol 168:529–548.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Eguchi G, Kodama R (1993) Transdifferentiation. Curr Opin Cell Biol 5:1023–1028.

    Article  CAS  PubMed  Google Scholar 

  • Fernandes KJ, McKenzie IA, Mill P, Smith KM, Akhavan M, Barnabe-Heider F, Biernaskie J, Junek A, Kobayashi NR, Toma JG, Kaplan DR, Labosky PA, Rafuse V, Hui CC, Miller FD (2004) A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 6:1082–1093.

    Article  CAS  PubMed  Google Scholar 

  • Furshpan EJ, MacLeish PR, O‘Lague PH, Potter DD (1976) Chemical transmission between rat sympathetic neurons and cardiac myocytes developing in microcultures: evidence for cholinergic, adrenergic, and dual-function neurons. Proc Natl Acad Sci USA 73:4225–4229.

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Castro MI, Marcelle C, Bronner-Fraser M (2002) Ectodermal Wnt function as a neural crest inducer. Science 297:848–851.

    CAS  PubMed  Google Scholar 

  • Gershon MD (1999) Endothelin and the development of the enteric nervous system. Clin Exp Pharmacol Physiol 26:985–988.

    Article  CAS  PubMed  Google Scholar 

  • Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A, DenBesten P, Robey PG, Shi S (2002) Stem cell properties of human dental pulp stem cells. J Dent Res 81:531–535.

    Article  CAS  PubMed  Google Scholar 

  • Gronthos S, Mankani M, Brahim J, Robey PG, Shi S (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 97:13625–13630.

    Article  CAS  PubMed  Google Scholar 

  • 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-beta family factors. Development 126:3781–3794.

    CAS  PubMed  Google Scholar 

  • Hong CS, Saint-Jeannet JP (2007) The activity of Pax3 and Zic1 regulates three distinct cell fates at the neural plate border. Mol Biol Cell 18:2192–2202.

    Article  CAS  PubMed  Google Scholar 

  • Ito K, Sieber-Blum M (1991) In vitro clonal analysis of quail cardiac neural crest development. Dev Biol 148:95–106.

    Article  CAS  PubMed  Google Scholar 

  • Ito K, Sieber-Blum M (1993) Pluripotent and developmentally restricted neural-crest-derived cells in posterior visceral arches. Dev Biol 156:191–200.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 169:309–320.

    Article  CAS  PubMed  Google Scholar 

  • Kruger GM, Mosher JT, Bixby S, Joseph N, Iwashita T, Morrison SJ (2002) Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 35:657–669.

    Article  CAS  PubMed  Google Scholar 

  • Kuriyama S, Mayor R (2008) Molecular analysis of neural crest migration. Philos Trans R Soc Lond B Biol Sci 363:1349–1362.

    Article  PubMed  Google Scholar 

  • LaBonne C, Bronner-Fraser M (1998) Neural crest induction in Xenopus: evidence for a two-signal model. Development 125:2403–2414.

    CAS  PubMed  Google Scholar 

  • 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 

  • Lahav R, Ziller C, Dupin E, Le Douarin NM (1996) Endothelin 3 promotes neural crest cell proliferation and mediates a vast increase in melanocyte number in culture. Proc Natl Acad Sci USA 93:3892–3897.

    Article  CAS  PubMed  Google Scholar 

  • 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 18:893–906.

    Article  Google Scholar 

  • Le Douarin N (1982) The Neural Crest. Cambridge University Press, Cambridge.

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Le Douarin N, Kalcheim C (1999) The Neural Crest, 2nd edn. Cambridge University Press, Cambridge; New York.

    Google Scholar 

  • Le Lievre CS, Le Douarin NM (1982) The early development of cranial sensory ganglia and the potentialities of their component cells studied in quail-chick chimeras. Dev Biol 94:291–310.

    Article  Google Scholar 

  • Le Lièvre CS (1978) Participation of neural crest-derived cells in the genesis of the skull in birds. J Embryol Exp Morphol 47:17–37.

    PubMed  Google Scholar 

  • Lecoin L, Sakurai T, Ngo MT, Abe Y, Yanagisawa M, Le Douarin NM (1998) Cloning and characterization of a novel endothelin receptor subtype in the avian class. Proc Natl Acad Sci USA 95:3024–3029.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Li HY, Say EH, Zhou XF (2007) Isolation and characterization of neural crest progenitors from adult dorsal root ganglia. Stem Cells 25:2053–2065.

    Article  CAS  PubMed  Google Scholar 

  • Marchant L, Linker C, Ruiz P, Guerrero N, Mayor R (1998) The inductive properties of mesoderm suggest that the neural crest cells are specified by a BMP gradient. Dev Biol 198:319–329.

    CAS  PubMed  Google Scholar 

  • Mayor R, Guerrero N, Martinez C (1997) Role of FGF and noggin in neural crest induction. Dev Biol 189:1–12.

    Article  CAS  PubMed  Google Scholar 

  • Mayor R, Morgan R, Sargent MG (1995) Induction of the prospective neural crest of Xenopus. Development 121:767–777.

    CAS  PubMed  Google Scholar 

  • McCallion AS, Chakravarti A (2001) EDNRB/EDN3 and Hirschsprung disease type II. Pigment Cell Res 14:161–169.

    Article  CAS  PubMed  Google Scholar 

  • 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 26:6651–6660.

    Article  CAS  PubMed  Google Scholar 

  • Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S (2003) SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 100:5807–5812.

    Article  CAS  PubMed  Google Scholar 

  • Monsoro-Burq AH, Fletcher RB, Harland RM (2003) Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. Development 130:3111–3124.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Morrison SJ, White PM, Zock C, Anderson DJ (1999) Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96:737–749.

    Article  CAS  PubMed  Google Scholar 

  • Nagoshi N, Shibata S, Kubota Y, Nakamura M, Nagai Y, Satoh E, Morikawa S, Okada Y, Mabuchi Y, Katoh H, Okada S, Fukuda K, Suda T, Matsuzaki Y, Toyama Y, Okano H (2008) Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell 2:392–403.

    Article  CAS  PubMed  Google Scholar 

  • Nataf V, Grapin-Botton A, Champeval D, Amemiya A, Yanagisawa M, Le Douarin NM (1998) The expression patterns of endothelin-A receptor and endothelin 1 in the avian embryo. Mech Dev 75:145–149.

    Article  CAS  PubMed  Google Scholar 

  • Nataf V, Lecoin L, Eichmann A, Le Douarin NM (1996) Endothelin-B receptor is expressed by neural crest cells in the avian embryo. Proc Natl Acad Sci USA 93:9645–9650.

    Article  CAS  PubMed  Google Scholar 

  • 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 416:854–860.

    Article  CAS  PubMed  Google Scholar 

  • Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448:313–317.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Pardal R, Ortega-Saenz P, Duran R, Lopez-Barneo J (2007) Glia-like stem cells sustain physiologic neurogenesis in the adult mammalian carotid body. Cell 131:364–377.

    Article  CAS  PubMed  Google Scholar 

  • Patterson PH, Chun LL (1977) The induction of acetylcholine synthesis in primary cultures of dissociated rat sympathetic neurons. II. Developmental aspects. Dev Biol 60:473–481.

    Article  CAS  PubMed  Google Scholar 

  • Platt JB (1893) Ectodermic origin of the cartilage of the head. Anat Anz 8:506–509.

    Google Scholar 

  • Rao MS, Anderson DJ (1997) Immortalization and controlled in vitro differentiation of murine multipotent neural crest stem cells. J Neurobiol 32:722–746.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • Sato T, Sasai N, Sasai Y (2005) Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development 132:2355–2363.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Sauka-Spengler T, Meulemans D, Jones M, Bronner-Fraser M (2007) Ancient evolutionary origin of the neural crest gene regulatory network. Dev Cell 13:405–420.

    Article  CAS  PubMed  Google Scholar 

  • Schweizer G, Ayer-Le Lievre C, Le Douarin NM (1983) Restrictions of developmental capacities in the dorsal root ganglia during the course of development. Cell Differ 13:191–200.

    Article  CAS  PubMed  Google Scholar 

  • Sextier-Sainte-Claire Deville F, Ziller C, Le Douarin N (1992) Developmental potentialities of cells derived from the truncal neural crest in clonal cultures. Brain Res Dev Brain Res 66:1–10.

    CAS  PubMed  Google Scholar 

  • Sextier-Sainte-Claire Deville F, Ziller C, Le Douarin NM (1994) Developmental potentials of enteric neural crest-derived cells in clonal and mass cultures. Dev Biol 163:141–151.

    Article  CAS  PubMed  Google Scholar 

  • Shah NM, Groves AK, Anderson DJ (1996) Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85:331–343.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Sieber-Blum M (1989) Commitment of neural crest cells to the sensory neuron lineage. Science 243:1608–1611.

    Article  CAS  PubMed  Google Scholar 

  • Sieber-Blum M (1991) Role of the neurotrophic factors BDNF and NGF in the commitment of pluripotent neural crest cells. Neuron 6:949–955.

    Article  CAS  PubMed  Google Scholar 

  • Sieber-Blum M, Cohen AM (1980) Clonal analysis of quail neural crest cells: they are pluripotent and differentiate in vitro in the absence of noncrest cells. Dev Biol 80:96–106.

    Article  CAS  PubMed  Google Scholar 

  • Sieber-Blum M, Grim M (2004) The adult hair follicle: cradle for pluripotent neural crest stem cells. Birth Defects Res Part C Embryo Today 72:162–172.

    Article  CAS  Google Scholar 

  • Sieber-Blum M, Grim M, Hu YF, Szeder V (2004) Pluripotent neural crest stem cells in the adult hair follicle. Dev Dyn 231:258–269.

    Article  CAS  PubMed  Google Scholar 

  • Sieber-Blum M, Schnell L, Grim M, Hu YF, Schneider R, Schwab ME (2006) Characterization of epidermal neural crest stem cell (EPI-NCSC) grafts in the lesioned spinal cord. Mol Cell Neurosci 32:67–81.

    Article  CAS  PubMed  Google Scholar 

  • Sommer L (2006) Growth factors regulating neural crest cell fate decisions. Adv Exp Med Biol 589:197–205.

    Article  CAS  PubMed  Google Scholar 

  • Stemple DL, Anderson DJ (1992) Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71:973–985.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676.

    Article  CAS  PubMed  Google Scholar 

  • Toma JG, Akhavan M, Fernandes KJ, Barnabe-Heider F, Sadikot A, Kaplan DR, Miller FD (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3:778–784.

    Article  CAS  PubMed  Google Scholar 

  • Toma JG, McKenzie IA, Bagli D, Miller FD (2005) Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23:727–737.

    Article  CAS  PubMed  Google Scholar 

  • Tomita Y, Matsumura K, Wakamatsu Y, Matsuzaki Y, Shibuya I, Kawaguchi H, Ieda M, Kanakubo S, Shimazaki T, Ogawa S, Osumi N, Okano H, Fukuda K (2005) Cardiac neural crest cells contribute to the dormant multipotent stem cell in the mammalian heart. J Cell Biol 170:1135–1146.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • Yoshida S, Shimmura S, Nagoshi N, Fukuda K, Matsuzaki Y, Okano H, Tsubota K (2006) Isolation of multipotent neural crest-derived stem cells from the adult mouse cornea. Stem Cells 24:2714–2722.

    Article  CAS  PubMed  Google Scholar 

  • Youn YH, Feng J, Tessarollo L, Ito K, Sieber-Blum M (2003) Neural crest stem cell and cardiac endothelium defects in the TrkC null mouse. Mol Cell Neurosci 24:160–170.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge the support of the Centre National de la Recherche Scientifique, Foundation Bettencourt Schueller and Association pour la Recherche contre le Cancer. G.W.C. was recipient of a post-doctoral fellowship from ARC.

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Authors and Affiliations

  1. CNRS UPR2197 Laboratoire Développement, Evolution et Plasticité du Système Nerveux, Institut de Neurobiologie Alfred Fessard, 91198, Gif-sur-Yvette, France

    Elisabeth Dupin, Giordano W. Calloni & Nicole M. Le Douarin

  2. Departamento de Biologia Celular, Embriologia e Genètica, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Florianópolis, Brazil

    Giordano W. Calloni

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  1. Elisabeth Dupin
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  2. Giordano W. Calloni
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  3. Nicole M. Le Douarin
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Correspondence to Elisabeth Dupin .

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  1. Inst. Química, Universidade de São Paulo, Av. Prof. Lineu Prestes 748, São Paulo, 05508-900, Brazil

    Henning Ulrich

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Dupin, E., Calloni, G.W., Le Douarin, N.M. (2010). Cell Diversification During Neural Crest Ontogeny: The Neural Crest Stem Cells. In: Ulrich, H. (eds) Perspectives of Stem Cells. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3375-8_4

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