The chemokine SDF-1/CXCL12 regulates the migration of melanocyte progenitors in mouse hair follicles

Differentiation

Volumn 77, Issue 4, 2009, Pages 395-411

  Belmadani, Abdelhak ^a   Jung, Hosung ^a   Ren, Dongjun ^a   Miller, Richard J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

CXCR4 receptors; Melanocyte precursors; Melanocytes; Migration; SDF 1

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; NESTIN; PLERIXAFOR; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR SOX10;

ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EPIDERMIS; FLUORESCENCE ACTIVATED CELL SORTING; HAIR FOLLICLE; HAIR GROWTH; MELANOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; CELL MOVEMENT; CHEMOKINE CXCL12; GREEN FLUORESCENT PROTEINS; HAIR FOLLICLE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERMEDIATE FILAMENT PROTEINS; INTRAMOLECULAR OXIDOREDUCTASES; LIGANDS; MELANOCYTES; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS;

MUS; MUS MUSCULUS;

EID: 61649113459     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2008.10.015     Document Type: Article

References (81)

1. Amoh Y., Li L., Campillo R., Kawahara K., Katsuoka K., Penman S., and Hoffman R.M. Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Proc. Natl. Acad. Sci. USA 102 (2005) 17734-17738
2. Amoh Y., Li L., Katsuoka K., Penman S., and Hoffman R.M. Multipotent nestin-positive, keratin-negative hair-follicle bulge stem cells can form neurons. Proc. Natl. Acad. Sci. USA 102 (2005) 5530-5534
3. Bagri A., Gurney T., He X., Zou Y.R., Littman D.R., Tessier-Lavigne M., and Pleasure S.J. The chemokine SDF1 regulates migration of dentate granule cells. Development 129 (2002) 4249-4260
4. Belmadani A., Tran P.B., Ren D., Assimacopoulos S., Grove E.A., and Miller R.J. The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J. Neurosci. 25 (2005) 3995-4003
5. Belmadani A., Tran P.B., Ren D., and Miller R.J. Chemokines regulate the migration of neural progenitors to sites of neuroinflammation. J. Neurosci. 26 (2006) 3182-3191
6. Bhattacharyya B.J., Banisadr G., Jung H., Ren D., Cronshaw D.G., Zou Y., and Miller R.J. The chemokine stromal cell-derived factor-1 regulates GABAergic inputs to neural progenitors in the postnatal dentate gyrus. J. Neurosci. 28 (2008) 6720-6730
7. Blanpain C., Lowry W.E., Geoghegan A., Polak L., and Fuchs E. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118 (2004) 635-648
8. Botchkareva N.V., Khlgatian M., Longley B.J., Botchkarev V.A., and Gilchrest B.A. SCF/c-kit signaling is required for cyclic regeneration of the hair pigmentation unit. Faseb J 15 (2001) 645-658
9. Botchkareva N.V., Botchkarev V.A., and Gilchrest B.A. Fate of melanocytes during development of the hair follicle pigmentary unit. J. Invest. Dermatol. Symp. Proc. 8 (2003) 76-79
10. Capela A., and Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35 (2002) 865-875
11. Chalasani S.H., Baribaud F., Coughlan C.M., Sunshine M.J., Lee V.M., Doms R.W., Littman D.R., and Raper J.A. The chemokine stromal cell-derived factor-1 promotes the survival of embryonic retinal ganglion cells. J. Neurosci. 23 (2003) 4601-4612
12. Claudinot S., Nicolas M., Oshima H., Rochat A., and Barrandon Y. Long-term renewal of hair follicles from clonogenic multipotent stem cells. Proc. Natl. Acad. Sci. USA 102 (2005) 14677-14682
13. 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. 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 (2003) 1150-1159
14. Cotsarelis G., Sun T.T., and Lavker R.M. Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61 (1990) 1329-1337
15. De Bellard M.E., Ching W., Gossler A., and Bronner-Fraser M. Disruption of segmental neural crest migration and ephrin expression in delta-1 null mice. Dev. Biol. 249 (2002) 121-130
16. Fuchs E. Epidermal differentiation and keratin gene expression. J. Cell Sci. Suppl. 17 (1993) 197-208
17. Fuchs E., Merrill B.J., Jamora C., and DasGupta R. At the roots of a never-ending cycle. Dev. Cell 1 (2001) 13-25
18. Hakami R.M., Hou L., Baxter L.L., Loftus S.K., Southard-Smith E.M., Incao A., Cheng J., and Pavan W.J. Genetic evidence does not support direct regulation of EDNRB by SOX10 in migratory neural crest and the melanocyte lineage. Mech. Dev. 123 (2006) 124-134
19. Hardy M.H. The secret life of the hair follicle. Trends Genet. 8 (1992) 55-61
20. Hirobe T. 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 (1992) 435-445
21. Hirobe T. Structure and function of melanocytes: microscopic morphology and cell biology of mouse melanocytes in the epidermis and hair follicle. Histol. Histopathol. 10 (1995) 223-237
22. Hirobe T., and Abe H. The slaty mutation affects the morphology and maturation of melanosomes in the mouse melanocytes. Pigment Cell Res. 19 (2006) 454-459
23. Hirobe T., Osawa M., and Nishikawa S. Steel factor controls the proliferation and differentiation of neonatal mouse epidermal melanocytes in culture. Pigment Cell Res. 16 (2003) 644-655
24. Hou L., Panthier J.J., and Arnheiter H. Signaling and transcriptional regulation in the neural crest-derived melanocyte lineage: interactions between KIT and MITF. Development 127 (2000) 5379-5389
25. Imokawa G., Kobayasi T., and Miyagishi M. Intracellular signaling mechanisms leading to synergistic effects of endothelin-1 and stem cell factor on proliferation of cultured human melanocytes. Cross-talk via trans-activation of the tyrosine kinase c-kit receptor. J. Biol. Chem. 275 (2000) 33321-33328
26. Ito M., Kawa Y., Ono H., Okura M., Baba T., Kubota Y., Nishikawa S.I., and Mizoguchi M. Removal of stem cell factor or addition of monoclonal anti-c-kit antibody induces apoptosis in murine melanocyte precursors. J. Invest. Dermatol. 112 (1999) 796-801
27. Jiao Z., Mollaaghababa R., Pavan W.J., Antonellis A., Green E.D., and Hornyak T.J. Direct interaction of Sox10 with the promoter of murine dopachrome tautomerase (Dct) and synergistic activation of Dct expression with Mitf. Pigment Cell Res. 17 (2004) 352-362
28. Jordan S.A., and Jackson I.J. A late wave of melanoblast differentiation and rostrocaudal migration revealed in patch and rump-white embryos. Mech. Dev. 92 (2000) 135-143
29. Jordan S.A., and Jackson I.J. MGF (KIT ligand) is a chemokinetic factor for melanoblast migration into hair follicles. Dev. Biol. 225 (2000) 424-436
30. Kawabata K., Ujikawa M., Egawa T., Kawamoto H., Tachibana K., Iizasa H., Katsura Y., Kishimoto T., and Nagasawa T. A cell-autonomous requirement for CXCR4 in long-term lymphoid and myeloid reconstitution. Proc. Natl. Acad. Sci. USA 96 (1999) 5663-5667
31. Kuhlbrodt K., Schmidt C., Sock E., Pingault V., Bondurand N., Goossens M., and Wegner M. Functional analysis of Sox10 mutations found in human Waardenburg-Hirschsprung patients. J. Biol. Chem. 273 (1998) 23033-23038
32. Kunisada K., Hirota H., Fujio Y., Matsui H., Tani Y., Yamauchi-Takihara K., and Kishimoto T. Activation of JAK-STAT and MAP kinases by leukemia inhibitory factor through gp130 in cardiac myocytes. Circulation 94 (1996) 2626-2632
33. Kunisada T., Yoshida H., Yamazaki H., Miyamoto A., Hemmi H., Nishimura E., Shultz L.D., Nishikawa S., and Hayashi S. Transgene expression of steel factor in the basal layer of epidermis promotes survival, proliferation, differentiation and migration of melanocyte precursors. Development 125 (1998) 2915-2923
34. Le Douarin N.M., and Dupin E. Cell lineage analysis in neural crest ontogeny. J. Neurobiol. 24 (1993) 146-161
35. Lee E.C., Yu D., Martinez de Velasco J., Tessarollo L., Swing D.A., Court D.L., Jenkins N.A., and Copeland N.G. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73 (2001) 56-65
36. Li L., Mignone J., Yang M., Matic M., Penman S., Enikolopov G., and Hoffman R.M. Nestin expression in hair follicle sheath progenitor cells. Proc. Natl. Acad. Sci. USA 100 (2003) 9958-9961
37. Lu M., Grove E.A., and Miller R.J. Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc. Natl. Acad. Sci. USA 99 (2002) 7090-7095
38. Ma Q., Jones D., Borghesani P.R., Segal R.A., Nagasawa T., Kishimoto T., Bronson R.T., and Springer T.A. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. USA 95 (1998) 9448-9453
39. Mackenzie M.A., Jordan S.A., Budd P.S., and Jackson I.J. Activation of the receptor tyrosine kinase kit is required for the proliferation of melanoblasts in the mouse embryo. Dev. Biol. 192 (1997) 99-107
40. Mayer T.C. The migratory pathway of neural crest cells into the skin of mouse embryos. Dev. Biol. 34 (1973) 39-46
41. McGrath K.E., Koniski A.D., Maltby K.M., McGann J.K., and Palis J. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev. Biol. 213 (1999) 442-456
42. Mikkola M.L., and Millar S.E. The mammary bud as a skin appendage: unique and shared aspects of development. J. Mammary Gland Biol. Neoplasia 11 (2006) 187-203
43. Mollaaghababa R., and Pavan W.J. The importance of having your SOX on: role of SOX10 in the development of neural crest-derived melanocytes and glia. Oncogene 22 (2003) 3024-3034
44. Morris R.J., and Potten C.S. Highly persistent label-retaining cells in the hair follicles of mice and their fate following induction of anagen. J. Invest. Dermatol. 112 (1999) 470-475
45. Muller A., Homey B., Soto H., Ge N., Catron D., Buchanan M.E., McClanahan T., Murphy E., Yuan W., Wagner S.N., Barrera J.L., Mohar A., Verastegui E., and Zlotnik A. Involvement of chemokine receptors in breast cancer metastasis. Nature 410 (2001) 50-56
46. Nagasawa T., Nakajima T., Tachibana K., Iizasa H., Bleul C.C., Yoshie O., Matsushima K., Yoshida N., Springer T.A., and Kishimoto T. Molecular cloning and characterization of a murine pre-B-cell growth-stimulating factor/stromal cell-derived factor 1 receptor, a murine homolog of the human immunodeficiency virus 1 entry coreceptor fusin. Proc. Natl. Acad. Sci. USA 93 (1996) 14726-14729
47. Nakayama A., Nguyen M.T., Chen C.C., Opdecamp K., Hodgkinson C.A., and Arnheiter H. Mutations in microphthalmia, the mouse homolog of the human deafness gene MITF, affect neuroepithelial and neural crest-derived melanocytes differently. Mech. Dev. 70 (1998) 155-166
48. Nelson W.G., and Sun T.T. The 50- and 58-kdalton keratin classes as molecular markers for stratified squamous epithelia: cell culture studies. J. Cell Biol. 97 (1983) 244-251
49. Nishikawa S., Kusakabe M., Yoshinaga K., Ogawa M., Hayashi S., Kunisada T., Era T., Sakakura T., and Nishikawa S. 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 (1991) 2111-2118
50. Nishimura E.K., Yoshida H., Kunisada T., and Nishikawa S.I. Regulation of E- and P-cadherin expression correlated with melanocyte migration and diversification. Dev. Biol. 215 (1999) 155-166
51. Nishimura E.K., Jordan S.A., Oshima H., Yoshida H., Osawa M., Moriyama M., Jackson I.J., Barrandon Y., Miyachi Y., and Nishikawa S. Dominant role of the niche in melanocyte stem-cell fate determination. Nature 416 (2002) 854-860
52. Opdecamp K., Nakayama A., Nguyen M.T., Hodgkinson C.A., Pavan W.J., and Arnheiter H. Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor. Development 124 (1997) 2377-2386
53. Oro A.E., and Scott M.P. Splitting hairs: dissecting roles of signaling systems in epidermal development. Cell 95 (1998) 575-578
54. Osawa M., Egawa G., Mak S.S., Moriyama M., Freter R., Yonetani S., Beermann F., and Nishikawa S. Molecular characterization of melanocyte stem cells in their niche. Development 132 (2005) 5589-5599
55. Oshima H., Rochat A., Kedzia C., Kobayashi K., and Barrandon Y. Morphogenesis and renewal of hair follicles from adult multipotent stem cells. Cell 104 (2001) 233-245
56. Panaretto B.A. Gene expression of potential morphogens during hair follicle and tooth formation: a review. Reprod. Fertil. Dev. 5 (1993) 345-360
57. Peters E.M., Tobin D.J., Botchkareva N., Maurer M., and Paus R. Migration of melanoblasts into the developing murine hair follicle is accompanied by transient c-kit expression. J. Histochem. Cytochem. 50 (2002) 751-766
58. Potter S.B., Mollaaghababa R., Hou L., Southard-Smith E.M., Hornyak T.J., Arnheiter H., and Pavan W.J. Analysis of SOX10 function in neural crest-derived melanocyte development: SOX10-dependent transcriptional control of dopachrome tautomerase. Dev. Biol. 237 (2001) 245-257
59. Pujol F., Kitabgi P., and Boudin H. The chemokine SDF-1 differentially regulates axonal elongation and branching in hippocampal neurons. J. Cell Sci. 118 (2005) 1071-1080
60. Sawada S., Gowrishankar K., Kitamura R., Suzuki M., Suzuki G., Tahara S., and Koito A. Disturbed CD4+ T cell homeostasis and in vitro HIV-1 susceptibility in transgenic mice expressing T cell line-tropic HIV-1 receptors. J. Exp. Med. 187 (1998) 1439-1449
61. Sieber-Blum M., and Grim M. The adult hair follicle: cradle for pluripotent neural crest stem cells. Birth Defects. Res. C Embryo Today 72 (2004) 162-172
62. Sieber-Blum M., Grim M., Hu Y.F., and Szeder V. Pluripotent neural crest stem cells in the adult hair follicle. Dev. Dyn. 231 (2004) 258-269
63. Sieber-Blum M., Schnell L., Grim M., Hu Y.F., Schneider R., and Schwab M.E. Characterization of epidermal neural crest stem cell (EPI-NCSC) grafts in the lesioned spinal cord. Mol. Cell Neurosci. 32 (2006) 67-81
64. Slominski A., and Paus R. Melanogenesis is coupled to murine anagen: toward new concepts for the role of melanocytes and the regulation of melanogenesis in hair growth. J. Invest. Dermatol. 101 (1993) 90S-97S
65. Stenn K.S., and Paus R. Controls of hair follicle cycling. Physiol. Rev. 81 (2001) 449-494
66. Stumm R.K., Zhou C., Ara T., Lazarini F., Dubois-Dalcq M., Nagasawa T., Hollt V., and Schulz S. CXCR4 regulates interneuron migration in the developing neocortex. J. Neurosci. 23 (2003) 5123-5130
67. Tachibana K., Hirota S., Iizasa H., Yoshida H., Kawabata K., Kataoka Y., Kitamura Y., Matsushima K., Yoshida N., Nishikawa S., Kishimoto T., and Nagasawa T. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393 (1998) 591-594
68. Tamura A., Halaban R., Moellmann G., Cowan J.M., Lerner M.R., and Lerner A.B. Normal murine melanocytes in culture. In Vitro Cell Dev. Biol. 23 (1987) 519-522
69. Taylor G., Lehrer M.S., Jensen P.J., Sun T.T., and Lavker R.M. Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 102 (2000) 451-461
70. Tobin D.J., Hagen E., Botchkarev V.A., and Paus R. Do hair bulb melanocytes undergo apoptosis during hair follicle regression (catagen)?. J. Invest. Dermatol. 111 (1998) 941-947
71. Tran P.B., and Miller R.J. Chemokine receptors in the brain: a developing story. J. Comp. Neurol. 457 (2003) 1-6
72. Tran P.B., and Miller R.J. HIV-1, chemokines and neurogenesis. Neurotox Res. 8 (2005) 149-158
73. Tran P.B., Ren D., Veldhouse T.J., and Miller R.J. Chemokine receptors are expressed widely by embryonic and adult neural progenitor cells. J. Neurosci. Res. 76 (2004) 20-34
74. Tran P.B., Banisadr G., Ren D., Chenn A., and Miller R.J. Chemokine receptor expression by neural progenitor cells in neurogenic regions of mouse brain. J. Comp. Neurol. 500 (2007) 1007-1033
75. Wehrle-Haller B., and Weston J.A. 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 (1995) 731-742
76. Wilson C., Cotsarelis G., Wei Z.G., Fryer E., Margolis-Fryer J., Ostead M., Tokarek R., Sun T.T., and Lavker R.M. Cells within the bulge region of mouse hair follicle transiently proliferate during early anagen: heterogeneity and functional differences of various hair cycles. Differentiation 55 (1994) 127-136
77. Wong C.E., Paratore C., Dours-Zimmermann M.T., Rochat A., Pietri T., Suter U., Zimmermann D.R., Dufour S., Thiery J.P., Meijer D., Beermann F., Barrandon Y., and Sommer L. Neural crest-derived cells with stem cell features can be traced back to multiple lineages in the adult skin. J. Cell Biol. 175 (2006) 1005-1015
78. Yoshida H., Kunisada T., Kusakabe M., Nishikawa S., and Nishikawa S.I. Distinct stages of melanocyte differentiation revealed by anlaysis of nonuniform pigmentation patterns. Development 122 (1996) 1207-1214
79. Yoshida S., Shimmura S., Nagoshi N., Fukuda K., Matsuzaki Y., Okano H., and Tsubota K. Isolation of multipotent neural crest-derived stem cells from the adult mouse cornea. Stem Cells 24 (2006) 2714-2722
80. Zicha D., Dunn G., and Jones G. Analyzing chemotaxis using the Dunn direct-viewing chamber. Methods Mol. Biol. 75 (1997) 449-457
81. Zou Y.R., Kottmann A.H., Kuroda M., Taniuchi I., and Littman D.R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393 (1998) 595-599