Functional neurons and melanocytes induced from immortal lines of postnatal neural crest-like stem cells

FASEB Journal

Volumn 23, Issue 9, 2009, Pages 3179-3192

  Sviderskaya, Elena V ^a   Easty, David J ^a,e   Lawrence, Mark A ^a   Sánchez, Daniel P ^b,f   Negulyaev, Yuri A ^c   Patel, Ricken H ^a   Anand, Praveen ^d   Korchev, Yuri E ^b   Bennett, Dorothy C ^a  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c INSTITUTE OF CYTOLOGY   (Russian Federation)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY COLLEGE DUBLIN   (Ireland)

^f Cinvestav Unidad Monterrey   (Mexico)

Author keywords

Chondrocyte; Determination; Differentiation; Melanoma; Schwann cell

Indexed keywords

EPHRIN RECEPTOR; PIGMENT; VANILLOID RECEPTOR 1; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CARTILAGE CELL; CELL IMMORTALIZATION; CELL STRUCTURE; CONNECTIVE TISSUE; EPIDERMIS; GENE EXPRESSION; HISTOCHEMISTRY; IMMUNOCYTOCHEMISTRY; MELANOCYTE; MOUSE; NERVE CELL; NEURAL CREST; NEURAL STEM CELL; NEWBORN; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; SCHWANN CELL; SENSORY NERVE CELL;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL SEPARATION; CHONDROCYTES; GENE EXPRESSION PROFILING; MELANOCYTES; MICE; NEURONS; PLURIPOTENT STEM CELLS; SCHWANN CELLS; SKIN; STEM CELLS;

EID: 70349339634     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-123596     Document Type: Article

References (69)

1. Le Douarin, N. M., and Kalcheim, C. (1999) The Neural Crest, Cambridge University Press, New York
2. Sieber-Blum, M. (2000) Factors controlling lineage specification in the neural crest. Int. Rev. Cytol. 197, 1-33
3. Joseph, N. M., Mukouyama, Y. S., Mosher, J. T., Jaegle, M., Crone, S. A., Dormand, E. L., Lee, K. F., Meijer, D., Anderson, D. J., and Morrison, S. J. (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 (Pubitemid 39625204)
4. Real, C., Glavieux-Pardanaud, C., Le Douarin, N. M., and Dupin, E. (2006) Clonally cultured differentiated pigment cells can dedifferentiate and generate multipotent progenitors with self-renewing potential. Dev. Biol. 300, 656-669 (Pubitemid 44909110)
5. Sieber-Blum, M., and Cohen, A. M. (1980) Clonal analysis of quail neural crest cells: they are pluripotent and differentiate in the absence of noncrest cells. Dev. Biol. 80, 96-106 (Pubitemid 11165707)
6. Huszar, D., Sharpe, A., and Jaenisch, R. (1991) Migration and proliferation of cultured neural crest cells in W mutant neural crest chimeras. Development 112, 131-141
7. Opdecamp, K., Nakayama, A., Nguyen, M. T. T., Hodgkinson, C., Pavan, W. J., and Arnheiter, H. (1997) Melanocyte development in vivo and in neural crest cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor. Development 124, 2377-2386 (Pubitemid 27309737)
8. Dunn, K. J., Williams, B. O., Li, Y., and Pavan, W. J. (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, 10050-10055 (Pubitemid 30680853)
9. Teng, L., and Labosky, P. A. (2006) Neural crest stem cells. Adv. Exp. Med. Biol. 589, 206-212
10. Kawa, Y., Ito, M., Ono, H., Asano, M., Takano, N., Ooka, S., Watabe, H., Hosaka, E., Baba, T., Kubota, Y., and Mizoguchi, M. (2000) Stem cell factor and/or endothelin-3 dependent immortal melanoblast and melanocyte populations derived from mouse neural crest cells. Pigment Cell Res. 13(Supp. 8), 73-80
11. Jessen, K. R., and Mirsky, R. (2002) Signals that determine Schwann cell identity. J. Anat. 200, 367-376
12. Le Douarin, N. M., Creuzet, S., Couly, G., and Dupin, E. (2004) Neural crest cell plasticity and its limits. Development 131, 4637-4650 (Pubitemid 39433452)
13. Bennett, D. C., and Lamoreux, M. L. (2003) The color loci of mice - a genetic century. Pigment Cell Res. 16, 333-344
14. Vance, K. W., and Goding, C. R. (2004) The transcription network regulating melanocyte development and melanoma. Pigment Cell Res. 17, 318-325 (Pubitemid 38993061)
15. Cheung, M., Chaboissier, M. C., Mynett, A., Hirst, E., Schedl, A., and Briscoe, J. (2005) The transcriptional control of trunk neural crest induction, survival, and delamination. Dev. Cell 8, 179-192 (Pubitemid 40197735)
16. Hagedorn, L., Suter, U., and Sommer, L. (1999) P0 and PMP22 mark a multipotent neural crest-derived cell type that displays community effects in response to TGF-β family factors. Development 126, 3781-3794 (Pubitemid 29440477)
17. Kruger, G. M., Mosher, J. T., Bixby, S., Joseph, N., Iwashita, T., and Morrison, S. J. (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 (Pubitemid 35223026)
18. Sieber-Blum, M., Grim, M., Hu, Y. F., and Szeder, V. (2004) Pluripotent neural crest stem cells in the adult hair follicle. Dev. Dyn. 231, 258-269 (Pubitemid 39238052)
19. Fernandes, K. J., McKenzie, I. A., Mill, P., Smith, K. M., Akhavan, M., Barnabe-Heider, F., Biernaskie, J., Junek, A., Kobayashi, N. R., Toma, J. G., Kaplan, D. R., Labosky, P. A., Rafuse, V., Hui, C. C., and Miller, F. D. (2004) A dermal niche for multipotent adult skin-derived precursor cells. Nat. Cell Biol. 6, 1082-1093 (Pubitemid 39468009)
20. Yu, H., Fang, D., Kumar, S. M., Li, L., Nguyen, T. K., Acs, G., Herlyn, M., and Xu, X. (2006) Isolation of a novel population of multipotent adult stem cells from human hair follicles. Am. J. Pathol. 168, 1879-1888 (Pubitemid 43825308)
21. Wong, C., Paratore, C., Dours-Zimmermann, M., Rochat, A., Pietri, T., Suter, U., Zimmermann, D., Dufour, S., Thiery, J., Meijer, D., Beermann, F., Barrandon, Y., and 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 (Pubitemid 44969205)
22. Bader, C. R., Bertrand, D., Dupin, E., and Kato, A. C. (1983) Development of electrical membrane properties in cultured avian neural crest. Nature 305, 808-810
23. Rheinwald, J. G., and Green, H. (1975) Formation of a keratinizing epithelium in culture by a cloned cell line derived from a teratoma. Cell 6, 317-330
24. Sviderskaya, E. V., Wakeling, W. F., and Bennett, D. C. (1995) A cloned, immortal line of murine melanoblasts inducible to differentiate to melanocytes. Development 121, 1547-1557
25. Bennett, D. C., Cooper, P. J., Dexter, T. J., Devlin, L. M., Heasman, J., and Nester, B. (1989) Cloned mouse melanocyte lines carrying the germline mutations albino and brown: complementation in culture. Development 105, 379-385 (Pubitemid 19053284)
26. Sviderskaya, E. V., Easty, D. J., and Bennett, D. C. (1998) Impaired growth and differentiation of diploid but not immortal melanoblasts from endothelin receptor B mutant (piebald) mice. Dev. Dyn. 213, 452-463
27. Hirobe, T. (1992) Basic fibroblast growth factor stimulates the sustained proliferation of mouse epidermal melanoblasts in a serum-free medium in the presence of dibutyryl cyclic AMP and keratinocytes. Development 114, 435-445
28. Halaban, R., and Alfano, F. D. (1984) Selective elimination of fibroblasts from cultures of normal human melanocytes. In Vitro Cell. Dev. Biol. 20, 447-450 (Pubitemid 15184812)
29. Spanakis, E., Lamina, P., and Bennett, D. C. (1992) Effects of the developmental colour mutations silver and recessive spotting on proliferation of diploid and immortal mouse melanocytes in culture. Development 114, 675-680
30. Sviderskaya, E. V., Bennett, D. C., Ho, L., Bailin, T., Lee, S. T., and Spritz, R. A. (1997) Complementation of hypopigmentation in p-mutant (pink-eyed dilution) mouse melanocytes by normal human P cDNA, and defective complementation by OCA2 mutant sequences. J. Invest. Dermatol. 108, 30-34 (Pubitemid 27019839)
31. Sviderskaya, E. V., Novak, E. K., Swank, R. T., and Bennett, D. C. (1998) The murine misty mutation: phenotypic effects on melanocytes, platelets and brown fat. Genetics 148, 381-390
32. Smith, G. D., Gunthorpe, M. J., Kelsell, R. E., Hayes, P. D., Reilly, P., Facer, P., Wright, J. E., Jerman, J. C., Walhin, J. P., Ooi, L., Egerton, J., Charles, K. J., Smart, D., Randall, A. D., Anand, P., and Davis, J. B. (2002) TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418, 186-190 (Pubitemid 34773773)
33. Shu, S. Y., Ju, G., and Fan, L. Z. (1988) The glucose oxidase- DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci. Lett. 85, 169-171 (Pubitemid 18048772)
34. Easty, D. J., Mitchell, P. J., Patel, K., Florenes, V. A., Spritz, R. A., and Bennett, D. C. (1997) Loss of expression of receptor tyrosine kinase family genes PTK7 and SEK in metastatic melanoma. Int. J. Cancer 71, 1061-1065 (Pubitemid 27252891)
35. Coste, B., Osorio, N., Padilla, F., Crest, M., and Delmas, P. (2004) Gating and modulation of presumptive NaV1.9 channels in enteric and spinal sensory neurons. Mol. Cell. Neurosci. 26, 123-134 (Pubitemid 38581028)
36. Maruyama, H., Yamamoto, M., Matsutomi, T., Zheng, T., Nakata, Y., Wood, J. N., and Ogata, N. (2004) Electrophysiological characterization of the tetrodotoxin-resistant Na+ channel, Na(v)1.9, in mouse dorsal root ganglion neurons. Plügers Arch. 449, 76-87 (Pubitemid 39506358)
37. Ito, K., and Takeuchi, T. (1984) The differentiation in vitro of the neural crest cells of the mouse embryo. J. Embryol. Exp. Morphol. 84, 49-62 (Pubitemid 15162500)
38. Ink4a in melanocyte senescence and differentiation. J. Natl. Cancer Inst. 94, 446-454
39. Ono, H., Kawa, Y., Asano, M., Ito, M., Takano, A., Kubota, Y., Matsumoto, J., and Mizoguchi, M. (1998) Development of melanocyte progenitors in murine Steel mutant neural crest explants cultured with stem cell factor, endothelin-3, or TPA. Pigment Cell Res. 11, 291-298 (Pubitemid 128533542)
40. Hornyak, T. J., Hayes, D. J., and Ziff, E. B. (2000) Cell-density- dependent regulation of expression and glycosylation of dopachrome tautomerase/tyrosinase-related protein-2. J. Invest. Dermatol. 115, 106-112
41. Sviderskaya, E. V., Hill, S. P., Balachandar, D., Barsh, G. S., and Bennett, D. C. (2001) Agouti signaling protein and other factors modulating differentiation and proliferation of immortal melanoblasts. Dev. Dyn. 221, 373-379 (Pubitemid 32685651)
42. Chi, N., and Epstein, J. A. (2002) Getting your Pax straight: Pax proteins in development and disease. Trends Genet. 18, 41-47 (Pubitemid 34031857)
43. Sánchez-Martín, M., Pérez-Losada, J., Rodríguez-García, A., González-Sánchez, B., Korf, B. R., Kuster, W., Moss, C., Spritz, R. A., and Sánchez-García, I. (2003) Deletion of the SLUG (SNAI2) gene results in human piebaldism. Am. J. Med. Genet. A 122, 125-132
44. Eisen, T., Easty, D. J., Bennett, D. C., and Goding, C. R. (1995) The POU domain transcription factor Brn-2: elevated expression in malignant melanoma and regulation of melanocytespecific gene expression. Oncogene 11, 2157-2164
45. Cook, A. L., Donatien, P. D., Smith, A. G., Murphy, M., Jones, M. K., Herlyn, M., Bennett, D. C., Leonard, J. H., and Sturm, R. A. (2003) Human melanoblasts in culture: expression of BRN2 and synergistic regulation by fibroblast growth factor-2, stem cell factor, and endothelin-3. J. Invest. Dermatol. 121, 1150-1159 (Pubitemid 37430986)
46. Schilham, M. W., Oosterwegel, M. A., Moerer, P., Ya, J., de Boer, P. A., van de Wetering, M., Verbeek, S., Lamers, W. H., Kruisbeek, A. M., Cumano, A., and Clevers, H. (1996) Defects in cardiac outflow tract formation and pro-B-lymphocyte expansion in mice lacking Sox-4. Nature 380, 711-714 (Pubitemid 26125470)
47. Carreira, S., Dexter, T. J., Yavuzer, U., Easty, D. J., and Goding, C. R. (1998) Brachyury-related transcription factor Tbx2 and repression of the melanocyte-specific TRP-1 promoter. Mol. Cell. Biol. 18, 5099-5108 (Pubitemid 28388093)
48. Shioda, T., Fenner, M. H., and Isselbacher, K. J. (1996) msg1, a novel melanocyte-specific gene, encodes a nuclear protein and is associated with pigmentation. Proc. Natl. Acad. Sci. U. S. A. 93, 12298-12303 (Pubitemid 26367137)
49. Easty, D. J., and Bennett, D. C. (2000) Protein tyrosine kinases in malignant melanoma. Melanoma Res. 10, 401-411
50. Swope, V. B., Medrano, E. E., Smalara, D., and Abdel-Malek, Z. A. (1995) Long-term proliferation of human melanocytes is supported by the physiologic mitogens α-melanotropin, endothelin-1 and basic fibroblast growth factor. Exp. Cell. Res. 217, 453-459
51. Shah, N. M., Groves, A. K., and Anderson, D. J. (1996) Alternative neural crest cell fates are instructively promoted by TGFβ superfamily members. Cell 85, 331-343
52. Shah, N. M., Marchionni, M. A., Isaacs, I., Stroobant, P., and Anderson, D. J. (1994) Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77, 349-360 (Pubitemid 24145196)
53. Dong, Z., Brennan, A., Liu, N., Yarden, Y., Lefkowitz, G., Mirsky, R., and Jessen, K. R. (1995) Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15, 585-596
54. Konieczny, S. F., and Emerson, C. P. (1984) 5-Azacytidine induction of stable mesodermal stem cell lineages from 10T1/2 cells: evidence for regulatory genes controlling determination. Cell 38, 791-800
55. Zhang, J. M., Hoffmann, R., and Sieber-Blum, M. (1997) Mitogenic and anti-proliferative signals for neural crest cells and the neurogenic action of TGF-β1. Dev. Dyn. 208, 375-386 (Pubitemid 27114290)
56. Lentz, S. I., Knudson, C. M., Korsmeyer, S. J., and Snider, W. D. (1999) Neurotrophins support the development of diverse sensory axon morphologies. J. Neurosci. 19, 1038-1048
57. LeMaster, A. M., Krimm, R. F., Davis, B. M., Noel, T., Forbes, M. E., Johnson, J. E., and Albers, K. M. (1999) Overexpression of brain-derived neurotrophic factor enhances sensory innervation and selectively increases neuron number. J. Neurosci. 19, 5919-5931 (Pubitemid 29327927)
58. Dhaka, A., Viswanath, V., and Patapoutian, A. (2006) TRP ion channels and temperature sensation. Annu. Rev. Neurosci. 29, 135-161 (Pubitemid 44476842)
59. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., and Julius, D. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824 (Pubitemid 27462969)
60. Bandell, M., Story, G. M., Hwang, S. W., Viswanath, V., Eid, S. R., Petrus, M. J., Earley, T. J., and Patapoutian, A. (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41, 849-857 (Pubitemid 38429729)
61. Cummins, T. R., Dib-Hajj, S. D., Black, J. A., Akopian, A. N., Wood, J. N., and Waxman, S. G. (1999) A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J. Neurosci. 19, RC43
62. Nishimura, E. K., Jordan, S. A., Oshima, H., Yoshida, H., Osawa, M., Moriyama, M., Jackson, I. J., Barrandon, Y., Miyachi, Y., and Nishikawa, S. (2002) Dominant role of the niche in melanocyte stem-cell fate determination. Nature 416, 854-860 (Pubitemid 34453742)
63. Soriano, P. (1997) The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites. Development 124, 2691-2700
64. Poliakov, A., Cotrina, M., and Wilkinson, D. G. (2004) Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly. Dev. Cell 7, 465-480 (Pubitemid 39341833)
65. Houghton, A. N., Eisinger, M., Albino, A. P., Cairncross, J. G., and Old, L. J. (1982) Surface antigens of melanocytes and melanomas: markers of melanoma differentiation and melanoma subsets. J. Exp. Med. 156, 1755-1766 (Pubitemid 13167419)
66. Weerda, H. G., Gamberger, T. I., Siegner, A., Gjuric, M., and Tamm, E. R. (1998) Effects of transforming growth factor-beta1 and basic fibroblast growth factor on proliferation of cell cultures derived from human vestibular nerve schwannoma. Acta Otolaryngol. 118, 337-343 (Pubitemid 28273173)
67. Baker, M. D. (2002) Electrophysiology of mammalian Schwann cells. Prog. Biophys. Mol. Biol. 78, 83-103
68. Rush, A. M., Cummins, T. R., and Waxman, S. G. (2007) Multiple sodium channels and their roles in electrogenesis within dorsal root ganglion neurons. J. Physiol. 579, 1-14
69. Bassi, M. T., Incerti, B., Easty, D. J., Sviderskaya, E. V., and Ballabio, A. (1996) Cloning of the murine homolog of the ocular albinism type 1 (OA1) gene: sequence, genomic structure, and expression analysis in pigment cells. Genome Res. 6, 880-885