Melanocyte stem cells: A melanocyte reservoir in hair follicles for hair and skin pigmentation

Pigment Cell and Melanoma Research

Volumn 24, Issue 3, 2011, Pages 401-410

  Nishimura, Emi K ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Aging; Bulge area; Hair follicles; Hair greying; Melanocyte stem cells; Melanocytes; Stem cell niche; Subbulge area

Indexed keywords

CELL MARKER;

AGING; ARTICLE; CELL MATURATION; CELL POPULATION; CELL REGENERATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; EPIDERMIS; GERM CELL; HAIR COLOR; HAIR FOLLICLE; HUMAN; MELANOCYTE; NONHUMAN; SKIN PIGMENTATION; STEM CELL;

ANIMALS; HAIR FOLLICLE; HUMANS; MELANINS; MELANOCYTES; MICE; SKIN PIGMENTATION; STEM CELLS;

MAMMALIA;

EID: 79956042667     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/j.1755-148X.2011.00855.x     Document Type: Article

References (55)

1. Amoh, Y., Yang, M., Li, L., Reynoso, J., Bouvet, M., Moossa, A.R., Katsuoka, K., and Hoffman, R.M. (2005). Nestin-linked green fluorescent protein transgenic nude mouse for imaging human tumor angiogenesis. Cancer Res. 65, 5352-5357.
2. Bennett, D.C., and Lamoreux, M.L. (2003). The color loci of mice - a genetic century. Pigment Cell Res. 16, 333-344.
3. Bosenberg, M., Muthusamy, V., Curley, D.P., Wang, Z., Hobbs, C., Nelson, B., Nogueira, C., Horner 2nd, J.W., Depinho, R., and Chin, L. (2006). Characterization of melanocyte-specific inducible Cre recombinase transgenic mice. Genesis 44, 262-267.
4. 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.
5. Commo, S., and Bernard, B.A. (2000). Melanocyte subpopulation turnover during the human hair cycle: an immunohistochemical study. Pigment Cell Res. 13, 253-259.
6. Coolidge, W.D. (1925). High voltage cathode rays outside the generating tube. Science 62, 441-442.
7. Cotsarelis, G. (2006). Epithelial stem cells: a folliculocentric view. J. Invest. Dermatol. 126, 1459-1468.
8. Cui, J., Shen, L.Y., and Wang, G.C. (1991). Role of hair follicles in the repigmentation of vitiligo. J. Invest. Dermatol. 97, 410-416.
9. Delmas, V., Martinozzi, S., Bourgeois, Y., Holzenberger, M., and Larue, L. (2003). Cre-mediated recombination in the skin melanocyte lineage. Genesis 36, 73-80.
10. Du, J., Miller, A.J., Widlund, H.R., Horstmann, M.A., Ramaswamy, S., and Fisher, D.E. (2003). MLANA/MART1 and SILV/PMEL17/GP100 are transcriptionally regulated by MITF in melanocytes and melanoma. Am. J. Pathol. 163, 333-343.
11. Freter, R., Osawa, M., and Nishikawa, S. (2010). Adult stem cells exhibit global suppression of RNA polymerase II serine-2 phosphorylation. Stem Cells 28, 1571-1580.
12. Fuchs, E. (2007). Scratching the surface of skin development. Nature 445, 834-842.
13. Hall, P.A., and Watt, F.M. (1989). Stem cells: the generation and maintenance of cellular diversity. Development 106, 619-633.
14. Hasty, P., Campisi, J., Hoeijmakers, J., Van Steeg, H., and Vijg, J. (2003). Aging and genome maintenance: lessons from the mouse? Science 299, 1355-1359.
15. Horikawa, T., Norris, D.A., Johnson, T.W., Zekman, T., Dunscomb, N., Bennion, S.D., Jackson, R.L., and Morelli, J.G. (1996). DOPA-negative melanocytes in the outer root sheath of human hair follicles express premelanosomal antigens but not a melanosomal antigen or the melanosome-associated glycoproteins tyrosinase, TRP-1, and TRP-2. J. Invest. Dermatol. 106, 28-35.
16. Keough, E.V., and Walsh, R.J. (1965). Rate of graying of human hair. Nature 207, 877-878.
17. Kubic, J.D., Young, K.P., Plummer, R.S., Ludvik, A.E., and Lang, D. (2008). Pigmentation PAX-ways: the role of Pax3 in melanogenesis, melanocyte stem cell maintenance, and disease. Pigment Cell Melanoma Res. 21, 627-645.
18. 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.
19. 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.
20. Loeffler, M., and Potten, S.C. (1997). Stem cells and cellular pedigrees - a conceptual introduction. In Stem Cells, S.C. Potten, ed. (London: Academic Press), pp. 5-6.
21. Mak, S.S., Moriyama, M., Nishioka, E., Osawa, M., and Nishikawa, S.I. (2006). Indispensable role of Bcl2 in the development of the melanocyte stem cell. Dev. Biol. 291, 144-153.
22. Martin, G.M. (2005). Genetic modulation of senescent phenotypes in Homo sapiens. Cell 120, 523-532.
23. Mayer, T.C. (1973). The migratory pathway of neural crest cells into the skin of mouse embryos. Dev. Biol. 34, 39-46.
24. Moriyama, M., Osawa, M., Mak, S.S. et al. (2006). Notch signaling via Hes1 transcription factor maintains survival of melanoblasts and melanocyte stem cells. J. Cell Biol. 173, 333-339.
25. Motohashi, T., Yamanaka, K., Chiba, K., Aoki, H., and Kunisada, T. (2009). Unexpected multipotency of melanoblasts isolated from murine skin. Stem Cells 27, 888-897.
26. Narisawa, Y., Kohda, H., and Tanaka, T. (1997). Three-dimensional demonstration of melanocyte distribution of human hair follicles: special reference to the bulge area. Acta Derm. Venereol. 77, 97-101.
27. Nishikawa, S., and Osawa, M. (2007). Generating quiescent stem cells. Pigment Cell Res. 20, 263-270.
28. 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.
29. 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.
30. 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.
31. Nishimura, E.K., Suzuki, M., Igras, V., Du, J., Lonning, S., Miyachi, Y., Roes, J., Beermann, F., and Fisher, D.E. (2010). Key roles for transforming growth factor beta in melanocyte stem cell maintenance. Cell Stem Cell 6, 130-140.
32. Ortonne, J.P., and Nordlund, J.J. (1998). Mechanisms that cause abnormal skin color. In The Pigmenrary System, J.J. Nordlund, R. Boissy, V.J. Hearing, R. King, and J.P. Ortonne, eds. (New York: Oxford University Press), pp. 489-502.
33. Ortonne, J.P., Schmitt, D., and Thivolet, J. (1980). PUVA-induced repigmentation of vitiligo: scanning electron microscopy of hair follicles. J. Invest. Dermatol. 74, 40-42.
34. 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.
35. Potten, C.S., and Loeffler, M. (1990). Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110, 1001-1020.
36. 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.
37. Shukla, R.C. (1969). The origin of Langerhans' cell from the melanocyte. Acta Anat. (Basel) 73, 372-388.
38. Silver, A.F., Chase, H.B., and Potten, C.S. (1968). Melanocyte precursor cells in the hair follicle germ during the dormat stage (telogen). Experientia 25, 299-301.
39. Silvers, W.K. (1979). The Coat Colours of Mice. A Model for Gene Action and Interaction (New York: Springer-Verlag).
40. Slominski, A., Paus, R., Plonka, P., Chakraborty, A., Maurer, M., Pruski, D., and Lukiewicz, S. (1994). Melanogenesis during the anagen-catagen-telogen transformation of the murine hair cycle. J. Invest. Dermatol. 102, 862-869.
41. Slominski, A., Wortsman, J., Plonka, P.M., Schallreuter, K.U., Paus, R., and Tobin, D.J. (2005). Hair follicle pigmentation. J. Invest. Dermatol. 124, 13-21.
42. Staricco, M.D. (1959). Amelanotic melanocytes in the outer root sheeth of the human hair follicle. J. Invest. Dermatol. 33, 295-297.
43. Staricco, R.G. (1963). Amelanotic melanocytes in the outer sheath of the human hair follicle and their role in the repigmentation of regenerated epidermis. Ann. N Y Acad. Sci. 100, 239-255.
44. Sugiyama, S. (1979). Mode of redifferentiation and melanogenesis of melanocytes in mouse hair follicles. An ultrastructural and cytochemical study. J. Ultrastruct. Res. 67, 40-54.
45. Tanimura, S., Tadokoro, Y., Inomata, K. et al. (2011). Hair follicle stem cells provide a functional niche for melanocyte stem cells. Cell Stem Cell, 8, 177-187.
46. Tobin, D.J., and Paus, R. (2001). Graying: gerontobiology of the hair follicle pigmentary unit. Exp. Gerontol. 36, 29-54.
47. Tobin, D.J., Colen, S.R., and Bystryn, J.C. (1995). Isolation and long-term culture of human hair-follicle melanocytes. J. Invest. Dermatol. 104, 86-89.
48. Tobin, D.J., Hagen, E., Botchkarev, V.A., and Paus, R. (1998). Do hair bulb melanocytes undergo apoptosis during hair follicle regression (catagen)? J. Invest. Dermatol. 111, 941-947.
49. Tobin, D.J., Slominski, A., Botchkarev, V., and Paus, R. (1999). The fate of hair follicle melanocytes during the hair growth cycle. J. Invest. Dermatol. Symp. Proc. 4, 323-332.
50. Toma, J.G., Akhavan, M., Fernandes, K.J., Barnabe-Heider, F., Sadikot, A., Kaplan, D.R., and Miller, F.D. (2001). Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat. Cell Biol. 3, 778-784.
51. Toma, J.G., Mckenzie, I.A., Bagli, D., and Miller, F.D. (2005). Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23, 727-737.
52. Trentin, A., Glavieux-Pardanaud, C., Le Douarin, N.M., and 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.
53. Van Den Bossche, K., Naeyaert, J.M., and Lambert, J. (2006). The quest for the mechanism of melanin transfer. Traffic 7, 769-778.
54. Wong, C.E., Paratore, C., Dours-Zimmermann, M.T. et al. (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.
55. Yajima, I., Belloir, E., Bourgeois, Y., Kumasaka, M., Delmas, V., and Larue, L. (2006). Spatiotemporal gene control by the Cre-ERT2 system in melanocytes. Genesis 44, 34-43.