Dual origin of melanocytes defined by Sox1 expression and their region-specific distribution in mammalian skin

Development Growth and Differentiation

Volumn 55, Issue 2, 2013, Pages 270-281

  Yoshimura, Naoko ^a   Motohashi, Tsutomu ^a   Aoki, Hitomi ^a   Tezuka, Ken Ichi ^a   Watanabe, Natsuki ^a   Wakaoka, Takanori ^a   Era, Takumi ^b   Kunisada, Takahiro ^a  

^a GIFU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Cre recombinase; Hair follicle; K14; Melanocyte lineage tracing; Neural crest; Sox1

Indexed keywords

CRE RECOMBINASE; TRANSCRIPTION FACTOR SOX1;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; EPIDERMIS CELL; MELANOCYTE; MOUSE; NEURAL CREST CELL; NEUROEPITHELIUM; NONHUMAN; PROTEIN EXPRESSION;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; EPIDERMIS; IMMUNOHISTOCHEMISTRY; LUMINESCENT PROTEINS; MELANOCYTES; MICE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; NEURAL CREST; NEUROEPITHELIAL CELLS; SCHWANN CELLS; SKIN; SOXB1 TRANSCRIPTION FACTORS;

MAMMALIA; MUS; VERTEBRATA;

EID: 84873460220     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/dgd.12034     Document Type: Article

References (49)

1. Abitua, P. B., Wagner, E., Navarrete, I. A. & Levine, M. 2012. Identification of a rudimentary neural crest in a non-vertebrate chordate. Nature 492, 104-107.
2. Adameyko, I., Lallemend, F., Aquino, J. B., Pereira, J. A., Topilko, P., Muller, T., Fritz, N., Beljajeva, A., Mochii, M., Liste, I., Usoskin, D., Suter, U., Birchmeier, C. & Ernfors, P. 2009. Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 139, 366-379.
3. Baker, C. V. & Bronner-Fraser, M. 1997. The origins of the neural crest. Part II: an evolutionary perspective. Mech. Dev. 69, 13-29.
4. Breau, M. A., Pietri, T., Stemmler, M. P., Thiery, J. P. & Weston, J. A. 2008. A nonneural epithelial domain of embryonic cranial neural folds gives rise to ectomesenchyme. Proc. Natl Acad. Sci. USA 105, 7750-7755.
5. Bronner-Frazer, M. 1995. Origins and developmental potential of the neural crest. Exp. Cell Res. 218, 405-417.
6. Budi, E. H., Patterson, L. B. & Parichy, D. M. 2008. Embryonic requirements for ErbB signaling in neural crest development and adult pigment pattern formation. Development 135, 2603-2614.
7. Catala, M., Ziller, C., Lapointe, F. & Le Douarin, N. M. 2000. The developmental potentials of the caudalmost part of the neural crest are restricted to melanocytes and glia. Mech. Dev. 95, 77-87.
8. Chan, W. Y. & Tam, P. P. L. 1988. A morphological and experimental study of the mesencephalic neural crest cells in the embryo using wheat germ aggulutinin-gold conjugates as the cell marker. Development 102, 427-442.
9. Corbo, J. C., Erives, A., Di Gregorio, A., Chang, A. & Levine, M. 1997. Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate. Development 124, 2335-2344.
10. Danielian, P. S., Muccino, D., Rowitch, D. H., Michael, S. K. & McMahon, A. P. 1998. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 24, 1323-1326.
11. Davis, R. L. & Kirschner, M. W. 2000. The fate of cells in the tailbud of Xenopus laevis. Development 127, 255-267.
12. Echelard, Y., Vassileva, G. & McMahon, A. P. 1994. Cis-acting regulatory sequences governing Wnt-1 expression in the developing mouse CNS. Development 120, 2213-2224.
13. Erickson, C. A. 1993. From the crest to the periphery: control of pigment cell migration and lineage segregation. Pigment Cell Res. 6, 336-347.
14. Griffith, C. M., Wiley, M. J. & Sanders, E. J. 1992. The vertebrate tail bud: three germ layers from one tissue. Anat. Embryol. (Berl) 185, 101-113.
15. Hall, B. K. 2009. The Neural Crest and Neural Crest Cells in Vertebrate Development and Evolution. New York: Springer.
16. Holland, L. Z. & Holland, N. D. 2001. Evolution of neural crest and placodes: amphioxus as a model for the ancestral vertebrate? J. Anat. 199, 85-98.
17. Hultman, K. A., Budi, E. H., Teasley, D. C., Gottlieb, A. Y., Parichy, D. M. & Johnson, S. L. 2009. Defects in ErbB-dependent establishment of adult melanocyte stem cells reveal independent origins for embryonic and regeneration melanocytes. PLoS Genet. 5, e1000544.
18. Jeffery, W. R., Strickler, A. G. & Yamamoto, Y. 2004. Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 431, 696-699.
19. Kanki, J. P. & Ho, R. K. 1997. The development of the posterior body in zebrafish. Development 124, 881-893.
20. Kunisada, T., Yoshida, H., Ogawa, M., Shultz, D. L. & Nishikawa, S. I. 1996. Characterization and isolation of melanocyte progenitors from mouse embryos. Dev. Growth Differ. 38, 87-97.
21. Langeland, J. A., Tomsa, J. M., Jackman, W. R. Jr & Kimmel, C. B. 1998. An amphioxus snail gene: expression in paraxial mesoderm and neural plate suggests a conserved role in patterning the chordate embryo. Dev. Genes Evol. 208, 569-577.
22. Le Douarin, N. M. & Kalcheim, C. 1999. The Neural Crest, 2nd edn. New York: Cambridge University Press.
23. Liem, K. F. Jr, Tremml, G., Roelink, H. & Jessell, T. M. 1995. Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969-979.
24. Mackenzie, M. A., Jordan, S. A., Budd, P. S. & 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.
25. Morales, A. V., Barbas, J. A. & Nieto, M. A. 2005. How to become neural crest: from segregation to delamination. Semin. Cell Dev. Biol. 16, 655-662.
26. Morrison, S. J., White, P. M., Zock, C. & Anderson, D. J. 1999. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96, 737-749.
27. Motohashi, T., Aoki, H., Chiba, K., Yoshimura, N. & Kunisada, T. 2007. Multipotent cell fate of neural crest-like cells derived from embryonic stem cells. Stem Cells 25, 402-410.
28. Motohashi, T., Yamanaka, K., Chiba, K., Aoki, H. & Kunisada, T. 2009. Unexpected multipotency of melanoblasts isolated from murine skin. Stem Cells 27, 888-897.
29. Motohashi, T., Yamanaka, K., Chiba, K., Miyajima, K., Aoki, H., Hirobe, T. & Kunisada, T. 2011. Neural crest cells retain their capability for multipotential differentiation even after lineage-restricted stages. Dev. Dyn. 240, 1681-1693.
30. Nakagawa, S. & Takeichi, M. 1998. Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 125, 2963-2971.
31. Nishimura, E. K., Jordan, S. A., Oshima, H., Yoshida, H., Osawa, M., Moriyama, M., Jackson, I. J., Barrandon, Y., Miyachi, Y. & Nishikawa, S. 2002. Dominant role of the niche in melanocyte stem-cell fate determination. Nature 416, 854-860.
32. Nordlund, J., Boissy, R. E., Hearing, V. J., King, R. A., Oetting, W. S. & Ortonne, J.-P. ed. 2006. The Pigmentary System. Chichester: Wiley-Blackwell.
33. Osumi-Yamashita, N., Ninomiya, Y., Doi, H. & Eto, K. 1994. The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontnasal mass of mouse embryos. Dev. Biol. 164, 409-419.
34. Pavan, W. J. & 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.
35. Pevny, L. H., Sockanathan, S., Placzek, M. & Lovell-Badge, R. 1998. A role for SOX1 in neural determination. Development 125, 1967-1978.
36. Serbedzija, G. N., Fraser, S. E. & Bronner-Fraser, M. 1990. Pathways of trunk neural crest cell migration in the mouse embryo as revealed by vital dye labelling. Development 108, 605-612.
37. Serbedzija, G. N., Bronner-Fraser, M. & Fraser, S. E. 1992. Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116, 297-307.
38. Serbedzija, G. N., Bronner-Fraser, M. & Fraser, S. E. 1994. Developmental potential of trunk neural crest cells in the mouse. Development 120, 1709-1718.
39. Sieber-Blum, M., Grim, M., Hu, Y. F. & Szeder, V. 2004. Pluripotent neural crest stem cells in the adult hair follicle. Dev. Dyn. 231, 258-269.
40. Stone, J. R. & Hall, B. K. 2004. Latent homologues for the neural crest as an evolutionary novelty. Evol. Dev. 6, 123-129.
41. Srinivas, S., Watanabe, T., Lin, C. S., William, C. M., Tanabe, Y., Jessell, T. M. & Costantini, F. 2001. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4.
42. Takashima, Y., Era, T., Nakao, K., Kondo, S., Kasuga, M., Smith, A. G. & Nishikawa, S. 2007. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 129, 1377-1388.
43. Tsukamoto, K., Jackson, I. J., Urabe, K., Montague, P. M. & Hearing, V. J. 1992. A second tyrosinase-related protein, TRP-2, is a melanogenic enzyme termed DOPAchrome tautomerase. EMBO J. 11, 519-526.
44. Uehara, S., Kawasaki, A. & Yamamoto, H. 2009. Classic versus non-classic; a survival Kit for life in the skin. Pigment Cell Melanoma Res. 22, 706-708.
45. Vasioukhin, V., Degenstein, L., Wise, B. & Fuchs, E. 1999. The magical touch: Genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc. Natl Acad. Sci. USA 96, 8551-8556.
46. Wehrle-Haller, B. & 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.
47. Wilkie, A. L., Jordan, S. A. & Jackson, I. J. 2002. Neural crest progenitors of the melanocyte lineage: coat colour patterns revisited. Development 129, 3349-3357.
48. Wilson, Y. M., Richards, K. L., Ford-Perriss, M. L., Panthier, J. J. & Murphy, M. 2004. Neural crest cell lineage segregation in the mouse neural tube. Development 131, 6153-6162.
49. Yamane, T., Hayashi, S., Mizoguchi, M., Yamazaki, H. & Kunisada, T. 1999. Derivation of melanocytes from embryonic stem cells in culture. Dev. Dyn. 216, 450-458.