Two distinct types of mouse melanocyte: Differential signaling requirement for the maintenance of non-cutaneous and dermal versus epidermal melanocytes

Development

Volumn 136, Issue 15, 2009, Pages 2511-2521

  Aoki, Hitomi ^a   Yamada, Yasuhiro ^a   Hara, Akira ^a   Kunisada, Takahiro ^a  

^a GIFU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

c KIT; Endothelin; HGF; KITL; Melanocytes; Mouse

Indexed keywords

CYTOKERATIN 14; ENDOTHELIN 3; SCATTER FACTOR; STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EPIDERMIS; EPIDERMIS CELL; HAIR FOLLICLE; MELANOCYTE; MOUSE; NEWBORN; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SKIN CELL;

ANIMALS; CORNEA; DERMIS; ENDOTHELIN-3; EPIDERMIS; FLOW CYTOMETRY; HARDERIAN GLAND; HEPATOCYTE GROWTH FACTOR; MELANOCYTES; MICE; MICE, TRANSGENIC; MUTATION; OLIGOPEPTIDES; PHENOTYPE; PIGMENTATION; PIPERIDINES; PROTO-ONCOGENE PROTEINS C-KIT; SIGNAL TRANSDUCTION; STEM CELL FACTOR; STEM CELLS;

MUS MUSCULUS;

EID: 69049101216     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.037168     Document Type: Article

References (62)

1. Aoki, H., Motohashi, T., Yoshimura, N., Yamazaki, H., Yamane, T., Panthier, J. J. and Kunisada, T. (2005). Cooperative and indispensable roles of endothelin 3 and KIT signalings in melanocyte development. Dev. Dyn. 233, 407-417.
2. Aoki, H., Yoshida, H., Hara, A., Suzuki, T. and Kunisada, T. (2008a). Transplantation of melanocytes into iris: method for iris repigmentation. Transplantation 85, 492-494.
3. Aoki, H., Hara, A., Motohashi, T., Chem, H. and Kunisada, T. (2008b). Iris as a recipient tissue for pigment cells: organized in vivo differentiation of melanocytes and pigmented epithelium derived from embryonic stem cells in vitro. Dev. Dyn. 237, 2394-2404.
4. Aoki, H., Hara, A., Niwa, M., Motohashi, T., Suzuki, T. and Kunisada, T. (2008c). Transplantation of cells from eye-like structures differentiated from embryonic stem cells in vitro and in vivo regeneration of retinal ganglion-like cells. Graefes. Arch. Clin. Exp. Ophthalmol. 246, 255-265.
5. Aubin-Houzelstein, G., Djian-Zaouche, J., Bernex, F., Gadin, S., Delmas, V., Larue, L. and Panthier, J. J. (2008). Melanoblasts' proper location and timed differentiation depend on Notch/RBP-J signaling in postnatal hair follicles. J. Invest. Dermatol. 128, 2686-2695.
6. Barsh, G. and Cotsarelis, G. (2007). How hair gets its pigment. Cell 130, 779-781.
7. Baynash, A. G., Hosoda, K., Giaid, A., Richardson, J. A., Emoto, N., Hammer, R. E. and 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.
8. Boissy, R. E. (1999). Extracutaneous melanocytes. In The Pigmentary System (ed. J. J. Nordlund., R. E. Boissy., V. J. Hearing., R. A. King and J. P. Ortone), pp. 59-72. New York: Oxford University Press.
9. Botchkareva, N. V., Khlgatian, M., Longley, B. J., Botchkarev, V. A. and Gilchrest, B. A. (2001). SCF/c-kit signaling is required for cyclic regeneration of the hair pigmentation unit. FASEB J. 15, 645-658.
10. Cable, J., Jackson, I. J. and Steel, K. P. (1995). Mutations at the W locus affect survival of neural crest-derived melanocytes in the mouse. Mech. Dev. 50, 139-150.
11. Dorsky, R. I., Raible, D. W. and Moon, R. T. (2000). Direct regulation of nacre, a zebrafish MITF homolog required for pigment cell formation, by the Wnt pathway. Genes Dev. 14, 158-162.
12. Fitch, K. R., McGowan, K. A., van Raamsdonk, C. D., Fuchs, H., Lee, D., Puech, A., Hérault, Y., Threadgill, D. W., Hrabé de Angelis, M. and Barsh, G. S. (2003). Genetics of dark skin in mice. Genes Dev. 17, 214-228.
13. Geissler, E. N., Ryan, M. A. and Housman, D. E. (1988). The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell 55, 185-192.
14. Guyonneau, L., Murisier, F., Rossier, A., Moulin, A. and Beermann, F. (2004). Melanocytes and pigmentation are affected in dopachrome tautomerase knockout mice. Mol. Cell. Biol. 24, 3396-3403.
15. Hall, B. K. (1999). The Neural Crest in Development and Evolution. New York: Springer.
16. Hodgkinson, C. A., Moore, K. J., Nakayama, A., Steingrimsson, E., Copeland, N. G., Jenkins, N. A. and Arnheiter, H. (1993). Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic-helix-loop-helix-zipper protein. Cell 74, 395-404.
17. Hosoda, K., Hammer, R. E., Richardson, J. A., Baynash, A. G., Cheung, J. C., Giaid, A. and Yanagisawa, M. (1994). Targeted and natural (piebald-lethal) mutations of endothelin-B receptor gene produce megacolon associated with spotted coat color in mice. Cell 79, 1267-1276.
18. Ikeya, M., Lee, S. M., Johnson, J. E., McMahon, A. P. and Takada, S. (1997). Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389, 966-970.
19. Inoue-Narita, T., Hamada, K., Sasaki, T., Hatakeyama, S., Fujita, S., Kawahara, K., Sasaki, M., Kishimoto, H., Eguchi, S., Kojima, I. et al. (2008). Pten deficiency in melanocytes results in resistance to hair graying and susceptibility to carcinogen-induced melanomagenesis. Cancer Res. 68, 5760-5768.
20. Kawamoto, S., Niwa, H., Tashiro, F., Sano, S., Kondoh, G., Takeda, J., Tabayashi, K. and Miyazaki, J. (2000). A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett. 470, 263-268.
21. Kos, L., Aronzon, A., Takayama, H., Maina, F., Ponzetto, C., Merlino, G. and Pavan, W. (1999). Hepatocyte growth factor/scatter factor-MET signaling in neural crest-derived melanocyte development. Pigment Cell Res. 12, 13-21.
22. Kunisada, T., Yoshida, H., Ogawa, M., Shultz, D. L. and Nishikawa, S. I. (1996). Characterization and isolation of melanocyte progenitors from mouse embryos. Dev. Growth Differ. 38, 87-97.
23. Kunisada, T., Yoshida, H., Yamazaki, H., Miyamoto, A., Hemmi, H., Nishimura, E., Shultz, L. D., Nishikawa, S. and 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.
24. Kunisada, T., Yamazaki, H., Hirobe, T., Kamei, S., Omoteno, M., Tagaya, H., Hemmi, H., Koshimizu, U., Nakamura, T. and Hayashi, S. I. (2000). Keratinocyte expression of transgenic hepatocyte growth factor affects melanocyte development, leading to dermal melanocytosis. Mech. Dev. 94, 67-78.
25. Le Douarin, N. M. and Kalcheim, C. (1999). The Neural Crest, 2nd edn. New York: Cambridge University Press.
26. Lister, J. A., Robertson, C. P., Lepage, T., Johnson, S. L. and Raible, D. W. (1999). nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126, 3757-3767.
27. Mackenzie, M. A., Jordan, S. A., Budd, P. S. and Jackson, I. J. (1997). Activation of the receptor tyrosine kinase Kit is required for the proliferation of melanoblasts in the mouse embryo. Dev. Biol. 192, 99-107.
28. Mak, S. S., Moriyama, M., Nishioka, E., Osawa, M. and Nishikawa, S. (2006). Indispensable role of Bcl2 in the development of the melanocyte stem cell. Dev. Biol. 291, 144-153.
29. McGill, G. G., Horstmann, M., Widlund, H. R., Du, J., Motyckova, G., Nishimura, E. K., Lin, Y. L., Ramaswamy, S., Avery, W., Ding, H. F. et al. (2002). Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell 109, 707-718.
30. McGill, G. G., Haq, R., Nishimura, E. K. and Fisher, D. E. (2006). c-Met expression is regulated by Mitf in the melanocyte lineage. J. Biol. Chem. 281, 10365-10373.
31. McGowan, K. A., Li, J. Z., Park, C. Y., Beaudry, V., Tabor, H. K., Sabnis, A. J., Zhang, W., Fuchs, H., de Angelis, M. H., Myers, R. M. et al. (2008). Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects. Nat. Genet. 40, 963-970.
32. Moriyama, M., Osawa, M., Mak, S. S., Ohtsuka, T., Yamamoto, N., Han, H., Delmas, V., Kageyama, R., Beermann, F., Larue, L. et al. (2006). Notch signaling via Hes1 transcription factor maintains survival of melanoblasts and melanocyte stem cells. J. Cell Biol. 173, 333-339.
33. Motohashi, T., Aoki, H., Chiba, K., Yoshimura, N. and Kunisada, T. (2007). Multipotent cell fate of neural crest-like cells derived from embryonic stem cells. Stem Cells 25, 402-410.
34. Nakayama, A., Nguyen, M. T., Chen, C. C., Opdecamp, K., Hodgkinson, C. A. and Arnheiter, H. (1998). Mutations in microphthalmia, the mouse homolog of the human deafness gene MITF, affect neuroepithelial and neural crest-derived melanocytes differently. Mech. Dev. 70, 155-166.
35. Nishikawa, S., Kusakabe, M., Yoshinaga, K., Ogawa, M., Hayashi, S., Kunisada, T., Era, T., Sakakura, T. and Nishikawa, S. (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.
36. 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.
37. Nishimura, E. K., Granter, S. R. and Fisher, D. E. (2005). Mechanisms of hair graying: incomplete melanocyte stem cell maintenance in the niche. Science 307, 720-724.
38. Opdecamp, K., Nakayama, A., Nguyen, M. T., Hodgkinson, C. A., Pavan, W. J. and 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.
39. Osawa, M. and Fisher, D. E. (2008). Notch and melanocytes: diverse outcomes from a single signal. J. Invest. Dermatol. 128, 2571-2574.
40. Osawa, M., Egawa, G., Mak, S. S., Moriyama, M., Freter, R., Yonetani, S., Beermann, F. and Nishikawa, S. (2005). Molecular characterization of melanocyte stem cells in their niche. Development 132, 5589-5599.
41. Pavan, W. J. and Tilghman, S. M. (1994). Piebald lethal (sl) acts early to disrupt the development of neural crest-derived melanocytes. Proc. Natl. Acad. Sci. USA 91, 7159-7163.
42. Pingault, V., Bondurand, N., Kuhlbrodt, K., Goerich, D. E., Préhu, M. O., Puliti, A., Herbarth, B., Hermans-Borgmeyer, I., Legius, E., Matthijs, G. et al. (1998). SOX10 mutations in patients with Waardenburg-Hirschsprung disease. Nat. Genet. 18, 171-173.
43. Potterf, S. B., Furumura, M., Dunn, K. J., Arnheiter, H. and Pavan, W. J. (2000). Transcription factor hierarchy in Waardenburg syndrome: regulation of MITF expression by SOX10 and PAX3. Hum. Genet. 107, 1-6.
44. Sarin, K. Y. and Artandi, S. E. (2007). Aging, graying and loss of melanocyte stem cells. Stem Cell Rev. 3, 212-217.
45. Schouwey, K., Delmas, V., Larue, L., Zimber-Strobl, U., Strobl, L. J., Radtke, F. and Beermann, F. (2007). Notch1 and Notch2 receptors influence progressive hair graying in a dose-dependent manner. Dev. Dyn. 236, 282-289.
46. Shin, M. K., Levorse, J. M., Ingram, R. S. and Tilghman, S. M. (1999). The temporal requirement for endothelin receptor-B signalling during neural crest development. Nature 402, 496-501.
47. Southard-Smith, E. M., Kos, L. and Pavan, W. J. (1998). Sox10 mutation disrupts neural crest development in Dom Hirschsprung mouse model. Nat. Genet. 18, 60-64.
48. Steinman, R. M., Pack, M. and Inaba, K. (1997). Dendritic cell development and maturation. Adv. Exp. Med. Biol. 417, 1-6.
49. Tosaki, H., Kunisada, T., Motohashi, T., Aoki, H., Yoshida, H. and Kitajima, Y. (2006). Mice transgenic for Kit(V620A): recapitulation of piebaldism but not progressive depigmentation seen in humans with this mutation. J. Invest. Dermatol. 126, 1111-1118.
50. Van Raamsdonk, C. D., Fitch, K. R., Fuchs, H., de Angelis, M. H. and Barsh, G. S. (2004). Effects of G-protein mutations on skin color. Nat. Genet. 36, 961-968.
51. Van Raamsdonk, C. D., Bezrookove, V., Green, G., Bauer, J., Gaugler, L., O'Brien, J. M., Simpson, E. M., Barsh, G. S., Bastian, B. C. (2009). Frequent somatic mutations of GNAQ in uveal melanoma and blue naevi. Nature 457, 599-602.
52. Watanabe, A., Takeda, K., Ploplis, B. and Tachibana, M. (1998). Epistatic relationship between Waardenburg syndrome genes MITF and PAX3. Nat. Genet. 18, 283-286.
53. Wehrle-Haller, B. and Weston, J. A. (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.
54. Weiner, L., Han, R., Scicchitano, B. M., Li, J., Hasegawa, K., Grossi, M., Lee, D. and Brissette, J. L. (2007). Dedicated epithelial recipient cells determine pigmentation patterns. Cell 130, 932-942.
55. Yamane, T., Hayashi, S., Mizoguchi, M., Yamazaki, H. and Kunisada, T. (1999). Derivation of melanocytes from embryonic stem cells in culture. Dev. Dyn. 216, 450-458.
56. Yamazaki, H., Sakata, E., Yamane, T., Yanagisawa, A., Abe, K., Yamamura, K., Hayashi, S. and Kunisada, T. (2005). Presence and distribution of neural crest-derived cells in the murine developing thymus and their potential for differentiation. Int. Immunol. 17, 549-558.
57. Yonetani, S., Moriyama, M., Nishigori, C., Osawa, M. and Nishikawa, S. (2008). In vitro expansion of immature melanoblasts and their ability to repopulate melanocyte stem cells in the hair follicle. J. Invest. Dermatol. 128, 408-420.
58. Yoshida, H., Nishikawa, S.-I., Okamura, H., Sakakura, T. and Kusakabe, M. (1993). The role of c-kit proto-oncogene during melanocyte development in mouse. In vivo approach by the in utero microinjection of anti-c-kit antibody. Dev. Growth Differ. 35, 209-220.
59. Yoshida, H., Kunisada, T., Kusakabe, M., Nishikawa, S. and Nishikawa, S. I. (1996a). Distinct stages of melanocyte differentiation revealed by analysis of nonuniform pigmentation patterns. Development 122, 1207-1214.
60. Yoshida, H., Hayashi, S., Shultz, L. D., Yamamura, K., Nishikawa, S., Nishikawa, S. and Kunisada, T. (1996b). Neural and skin cell-specific expression pattern conferred by steel factor regulatory sequence in transgenic mice. Dev. Dyn. 207, 222-232.
61. Yoshida, H., Kunisada, T., Grimm, T., Nishimura, E. K., Nishioka, E. and Nishikawa, S. I. (2001). Melanocyte migration and survival controlled by SCF/c-kit expression. J. Investig. Dermatol. Symp. Proc. 6, 1-5.
62. Zembowicz, A. and Mihm, M. C. (2004). Dermal dendritic melanocytic proliferations: an update. Histopathology 45, 433-451.