Functionally distinct melanocyte populations revealed by reconstitution of hair follicles in mice

Pigment Cell and Melanoma Research

Volumn 24, Issue 1, 2011, Pages 125-135

  Aoki, Hitomi ^a   Hara, Akira ^a   Motohashi, Tsutomu ^a   Osawa, Masatake ^b   Kunisada, Takahiro ^a  

^a GIFU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Cell lineage; Endothelin3; Hair reconstitution assay; Kit; Melanocytes

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CELL LINEAGE; CELL POPULATION; CHIMERA; CONTROLLED STUDY; DERMIS; EPIDERMIS; HAIR COLOR; HAIR FOLLICLE; HAIR FOLLICLE RECONSTITUTION; KERATINOCYTE; MALE; MELANOCYTE; MOUSE; NONHUMAN; TISSUE REGENERATION;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL ASSAY; CHIMERA; DERMIS; ENDOTHELIN-3; HAIR FOLLICLE; HUMANS; KERATIN-14; MELANOCYTES; MICE; MICE, TRANSGENIC; SKIN PIGMENTATION;

MUS;

EID: 78651462653     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/j.1755-148X.2010.00801.x     Document Type: Article

References (44)

1. Adameyko, I., Lallemend, F., Aquino, J.B. et al. (2009). Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 139, 366-379.
2. Alexeev, V., and Yoon, K. (2006). Distinctive role of the cKit receptor tyrosine kinase signaling in mammalian melanocytes. J. Invest. Dermatol. 126, 1102-1110.
3. 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.
4. 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.
5. 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.
6. Aoki, H., Yamada, Y., Hara, A., and Kunisada, T. (2009). Two distinct types of mouse melanocyte: differential signaling requirement for the maintenance of non-cutaneous and dermal versus epidermal melanocytes. Development 136, 2511-2521.
7. 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.
8. Hall, B.K. (2009). The Neural Crest and Neural Crest Cells in Vertebrate Development and Evolution. (New York: Springer-Verlag).
9. Hirobe, T. (1984). Histochemical survey of the distribution of the epidermal melanoblasts and melanocytes in the mouse during fetal and postnatal periods. Anat Rec. 208, 589-594.
10. Jackson, I.J. (1993). Molecular genetics. Colour-coded switches. Nature 362, 587-588.
11. Jeon, S., Kim, N.H., Kim, J.Y., and Lee, A.Y. (2009). Stem cell factor induces ERM proteins phosphorylation through PI3K activation to mediate melanocyte proliferation and migration. Pigment Cell Melanoma Res. 22, 77-85.
12. Kamimura, J., Lee, D., Baden, H.P., Brissette, J., and Dotto, G.P. (1997). Primary mouse keratinocyte cultures contain hair follicle progenitor cells with multiple differentiation potential. J. Invest. Dermatol. 109, 534-540.
13. 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.
14. Kelsh, R.N., Harris, M.L., Colanesi, S., and Erickson, C.A. (2009). Stripes and belly-spots - a review of pigment cell morphogenesis in vertebrates. Semin. Cell Dev. Biol. 20, 90-104.
15. Kishimoto, J., Ehama, R., Wu, L., Jiang, S., Jiang, N., and Burgeson, R.E. (1999). Selective activation of the versican promoter by epithelial-mesenchymal interactions during hair follicle development. Proc. Natl Acad. Sci. U S A 96, 7336-7341.
16. Kopan, R., Lee, J., Lin, M.H., Syder, A.J., Kesterson, J., Crutchfield, N., Li, C.R., Wu, W., Books, J., and Gordon, J.I. (2002). Genetic mosaic analysis indicates that the bulb region of coat hair follicles contains a resident population of several active multipotent epithelial lineage progenitors. Dev. Biol. 242, 44-57.
17. 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.
18. 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.
19. Le Douarin, N.M., and Kalcheim, C. (1999). The Neural Crest, 2nd edn. (New York: Cambridge University Press).
20. Li, L., Fukunaga-Kalabis, M., Yu, H., Xu, X., Kong, J., Lee, J.T., and Herlyn, M. (2010). Human dermal stem cells differentiate into functional epidermal melanocytes. J. Cell Sci. 123, 853-860.
21. Lichti, U., Weinberg, W.C., Goodman, L., Ledbetter, S., Dooley, T., Morgan, D., and Yuspa, S.H. (1993). In vivo regulation of murine hair growth: insights from grafting defined cell populations onto nude mice. J. Invest. Dermatol. 101, 124S-129S.
22. 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.
23. Mayer, T.C., and Fishbane, J.L. (1972). Mesoderm-ectoderm interaction in the production of the agouti pigmentation pattern in mice. Genetics 71, 297-303.
24. Monroy, A., and Moscona, A.A. (1979). Introductory Concepts in Developmental Biology. (Chicago: University of Chicago Press).
25. Moscona, A. (1961). Rotation-mediated histogenetic aggregation of dissociated cells. A quantifiable approach to cell interactions in vitro. Exp. Cell Res. 22, 455-475.
26. Nagai, T., Ibata, K., Park, E.S., Kubota, M., Mikoshiba, K., and Miyawaki, A. (2002). A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90.
27. Nishimura, E.K., Yoshida, H., Kunisada, T., and Nishikawa, S.I. (1999). Regulation of E- and P-cadherin expression correlated with melanocyte migration and diversification. Dev. Biol. 215, 155-166.
28. 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.
29. Ollmann, M.M., Wilson, B.D., Yang, Y.K., Kerns, J.A., Chen, Y., Gantz, I., and Barsh, G.S. (1997). Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science 278, 135-138.
30. 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.
31. Oshima, H., Rochat, A., Kedzia, C., Kobayashi, K., and Barrandon, Y. (2001). Morphogenesis and renewal of hair follicles from adult multipotent stem cells. Cell 104, 233-245.
32. Potten, C.S. (1970). Radiation depigmentation of mouse hair: effect of the hair growth cycle on the sensitivity. J. Invest. Dermatol. 55, 410-418.
33. Randall, V.A., Jenner, T.J., Hibberts, N.A., De Oliveira, I.O., and Vafaee, T. (2008). Stem cell factor/c-Kit signalling in normal and androgenetic alopecia hair follicles. J. Endocrinol. 197, 11-23.
34. Tang, A., Eller, M.S., Hara, M., Yaar, M., Hirohashi, S., and Gilchrest, B.A. (1994). E-cadherin is the major mediator of human melanocyte adhesion to keratinocytes in vitro. J. Cell Sci. 107, 983-992.
35. 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.
36. th Annual Meeting of the JSPCR, Nagoya, Japan. Pigment Cell Res. 15, 472.
37. Uehara, S., Kawasaki, A., and Yamamoto, H. (2009). Classic versus non-classic: a survival Kit for life in the skin. Pigment Cell Melanoma Res. 22, 706-708.
38. Wehrle-Haller, B., and Weston, J.A. (1997). Receptor tyrosine kinase-dependent neural crest migration in response to differentially localized growth factors. Bioessays 19, 337-345.
39. Yajima, I., and Larue, L. (2008). The location of heart melanocytes is specified and the level of pigmentation in the heart may correlate with coat color. Pigment Cell Melanoma Res. 21, 471-476.
40. 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.
41. 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.
42. Yoshida, H., Kunisada, T., Kusakabe, M., Nishikawa, S., and Nishikawa, S.I. (1996a). Distinct stages of melanocyte differentiation revealed by anlaysis of nonuniform pigmentation patterns. Development 122, 1207-1214.
43. 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.
44. Zheng, Y., Du, X., Wang, W., Boucher, M., Parimoo, S., and Stenn, K. (2005). Organogenesis from dissociated cells: generation of mature cycling hair follicles from skin-derived cells. J. Invest. Dermatol. 124, 867-876.