Revisiting epidermal melanocytes: Regulation of their survival, proliferation, and function in human skin

Melanoma Development: Molecular Biology, Genetics and Clinical Application

Volumn , Issue , 2017, Pages 7-38

  Abdel Malek, Zalfa A ^a   Swope, Viki B ^a   Indra, Arup ^b,c,d  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON STATE UNIVERSITY   (United States)

^d OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85008965875     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-319-41319-8_2     Document Type: Chapter

References (188)

1. Abdel-Malek Z, Swope VB, Pallas J, Krug K, Nordlund JJ (1992) Mitogenic, melanogenic and cAMP responses of cultured neonatal human melanocytes to commonly used mitogens. J Cell Physiol 150:416-425
2. Abdel-Malek Z, Swope V, Collins C, Boissy R, Zhao H, Nordlund J (1993) Contribution of melanogenic proteins to the heterogeneous pigmentation of human melanocytes. J Cell Sci 106:1323-1331
3. Abdel-Malek Z, Swope VB, Suzuki I, Akcali C, Harriger MD, Boyce ST, Urabe K, Hearing VJ (1995) Mitogenic and melanogenic stimulation of normal human melanocytes by melanotropic peptides. Proc Natl Acad Sci U S A 92:1789-1793
4. Abdel-Malek ZA, Kadekaro AL, Kavanagh RJ, Todorovic A, Koikov LN, Mcnulty JC, Jackson PJ, Milhauser GL, Schwemberger S, Babcock G et al (2006) Melanoma prevention strategy based on using tetrapeptide alpha-MSH analogs that protect human melanocytes from UV-induced damage and cytotoxicity. FASEB J 20:1561-1563
5. Abdel-Malek ZA, Ruwe A, Kavanagh-Starner R, Kadekaro AL, Swope V, Haskell-Luevano C, Koikov L, Knittel JJ (2009) alpha-MSH tripeptide analogs activate the melanocortin 1 receptor and reduce UV-induced DNA damage in human melanocytes. Pigment Cell Melanoma Res 22:635-644
6. Arad S, Konnikov N, Goukassian DA, Gilchrest BA (2006) T-oligos augment UV-induced protective responses in human skin. FASEB J 20:1895-1897
7. Barnetson RS, Ooi TK, Zhuang L, Halliday GM, Reid CM, Walker PC, Humphrey SM, Kleinig MJ (2006) [Nle4-D-Phe7]-alpha-melanocyte-stimulating hormone significantly increased pigmentation and decreased UV damage in fair-skinned Caucasian volunteers. J Invest Dermatol 126:1869-1878
8. Berking C, Takemoto R, Satyamoorthy K, Elenitsas R, Herlyn M (2001) Basic fibroblast growth factor and ultraviolet B transform melanocytes in human skin. Am J Pathol 158:943-953
9. Berking C, Takemoto R, Satyamoorthy K, Shirakawa T, Eskandarpour M, Hansson J, Vanbelle PA, Elder DE, Herlyn M (2004) Induction of melanoma phenotypes in human skin by growth factors and ultraviolet B. Cancer Res 64:807-811
10. Bohm M, Moellmann G, Cheng E, Alvarez-Franco M, Wagner S, Sassone-Corsi P, Halaban R (1995) Identification of p90RSK as the probable CREB-Ser133 kinase in human melanocytes. Cell Growth Differ 6:291-302
11. Bohm M, Wolff I, Scholzen TE, Robinson SJ, Healy E, Luger TA, Schwarz T, Schwarz A (2005) alpha-Melanocyte-stimulating hormone protects from ultraviolet radiation-induced apoptosis and DNA damage. J Biol Chem 280:5795-5802
12. Botchkarev VA, Yaar M, Peters EM, Raychaudhuri SP, Botchkareva NV, Marconi A, Raychaudhuri SK, Paus R, Pincelli C (2006) Neurotrophins in skin biology and pathology. J Invest Dermatol 126:1719-1727
13. Box NF, Wyeth JR, O’gorman LE, Martin NG, Sturm RA (1997) Characterization of melanocyte stimulating hormone receptor variant alleles in twins with red hair. Hum Mol Genet 6:1891-1897
14. Box NF, Duffy DL, Irving RE, Russell A, Chen W, Griffiths LR, Parsons PG, Green AC, Sturm RA (2001) Melanocortin-1 receptor genotype is a risk factor for basal and squamous cell carcinoma. J Invest Dermatol 116:224-229
15. Brash DE, Rudolph JA, Simon JA, Lin A, Mckenna GJ, Baden HP, Halperin AJ, Pontén JN (1991) A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc Natl Acad Sci U S A 88:10124-10128
16. Brito FC, Kos L (2008) Timeline and distribution of melanocyte precursors in the mouse heart. Pigment Cell Melanoma Res 21:464-470
17. Bronner-Fraser M (1993) Neural development: crest destiny. Curr Biol CB 3:201-203
18. Buac K, Xu M, Cronin J, Weeraratna AT, Hewitt SM, Pavan WJ (2009) NRG1/ERBB3 signaling in melanocyte development and melanoma: inhibition of differentiation and promotion of proliferation. Pigment Cell Melanoma Res 22:773-784
19. Bustamante J, Bredeston L, Malanga G, Mordoh J (1993) Role of melanin as a scavenger of active oxygen species. Pigment Cell Res 6:348-353
20. Candille SI, Kaelin CB, Cattanach BM, Yu B, Thompson DA, Nix MA, Kerns JA, Schmutz SM, Millhauser GL, Barsh GS (2007) A {beta}-defensin mutation causes black coat color in domestic dogs. Science Sciencexpress, www.sciencexpress.org. 18 Oct 2007. 10.1126/science.1147880
21. Chakraborty AK, Funasaka Y, Slominski A, Ermak G, Hwang J, Pawelek JM, Ichihashi M (1996) Production and release of proopiomelanocortin (POMC) derived peptides by human melanocytes and keratinocytes in culture: regulation by ultraviolet B. Biochim Biophys Acta 1313:130-138
22. Cheli Y, Ohanna M, Ballotti R, Bertolotto C (2009) Fifteen-year quest for microphthalmia-associated transcription factor target genes. Pigment Cell Melanoma Res 23:27-40
23. Chhajlani V, Wikberg JES (1992) Molecular cloning and expression of the human melanocyte stimulating hormone receptor cDNA. FEBS Lett 309:417-420
24. Choi W, Kolbe L, Hearing VJ (2012) Characterization of the bioactive motif of neuregulin-1, a fibroblast-derived paracrine factor that regulates constitutive color and the function of melanocytes in human skin. Pigment Cell Melanoma Res 25:477-481
25. Choi W, Wolber R, Gerwat W, Mann T, Batzer J, Smuda C, Liu H, Kolbe L, Hearing VJ (2010) The fibroblast-derived paracrine factor neuregulin-1 has a novel role in regulating the constitutive color and melanocyte function in human skin. J Cell Sci 123:3102-3111
26. Chouinard N, Valerie K, Rouabhia M, Huot J (2002) UVB-mediated activation of p38 mitogen-activated protein kinase enhances resistance of normal human keratinocytes to apoptosis by stabilizing cytoplasmic p53. Biochem J 365:133-145
27. Coleman DJ, Garcia G, Hyter S, Jang HS, Chagani S, Liang X, Larue L, Ganguli-Indra G, Indra AK (2014) Retinoid-X-receptors (alpha/beta) in melanocytes modulate innate immune responses and differentially regulate cell survival following UV irradiation. PLoS Genet 10:e1004321
28. Corre S, Primot A, Sviderskaya E, Bennett DC, Vaulont S, Goding CR, Galibert MD (2004) UV-induced expression of key component of the tanning process, the POMC and MC1R genes, is dependent on the p-38-activated upstream stimulating factor-1 (USF-1). J Biol Chem 279:51226-51233
29. Corre S, Mekideche K, Adamski H, Mosser J, Watier E, Galibert MD (2006) In vivo and ex vivo UV-induced analysis of pigmentation gene expressions. J Invest Dermatol 126:916-918
30. Cui R, Widlund HR, Feige E, Lin JY, Wilensky DL, Igras VE, D’orazio J, Fung CY, Schanbacher CF, Granter SR et al (2007) Central role of p53 in the suntan response and pathologic hyperpigmentation. Cell 128:853-864
31. D’orazio JA, Nobuhisa T, Cui R, Arya M, Spry M, Wakamatsu K, Igras V, Kunisada T, Granter SR, Nishimura EK et al (2006) Topical drug rescue strategy and skin protection based on the role of Mc1r in UV-induced tanning. Nature 443:340-344
32. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W et al (2002) Mutations of the BRAF gene in human cancer. Nature 417:949-954
33. Demenais F, Mohamdi H, Chaudru V, Goldstein AM, Newton Bishop JA, Bishop DT, Kanetsky PA, Hayward NK, Gillanders E, Elder DE et al (2010) Association of MC1R variants and host phenotypes with melanoma risk in CDKN2A mutation carriers: a GenoMEL study. J Natl Cancer Inst 102:1568-1583
34. Demunter A, De Wolf-Peeters C, Degreef H, Stas M, Van Den Oord JJ (2001) Expression of the endothelin-B receptor in pigment cell lesions of the skin. Evidence for its role as tumor progression marker in malignant melanoma. Evidence for its role as tumor progression marker in malignant melanoma 438:485-491
35. Denecker G, Vandamme N, Akay O, Koludrovic D, Taminau J, Lemeire K, Gheldof A, De Craene B, Van Gele M, Brochez L et al (2014) Identification of a ZEB2-MITF-ZEB1 transcriptional network that controls melanogenesis and melanoma progression. Cell Death Differ 21:1250-1261
36. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399:601-605
37. Duval C, Regnier M, Schmidt R (2001) Distinct melanogenic response of human melanocytes in mono-culture, in co-culture with keratinocytes and in reconstructed epidermis, to UV exposure. Pigment Cell Res 14:348-355
38. Eckert RL, Crish JF, Robinson NA (1997) The epidermal keratinocyte as a model for the study of gene regulation and cell differentiation. Physiol Rev 77:397-424
39. Eisinger M, Marko O (1982) Selective proliferation of normal human melanocytes in vitro in the presence of phorbol ester and cholera toxin. Proc Natl Acad Sci U S A 79:2018-2022
40. Epstein JH (1983) Photocarcinogenesis, skin cancer and aging. J Am Acad Dermatol 9:487-502
41. Fuchs SY, Tappin I, Ronai Z (2000) Stability of the ATF2 transcription factor is regulated by phosphorylation and dephosphorylation. J Biol Chem 275:12560-12564
42. Funasaka Y, Sato H, Chakraborty AK, Ohashi A, Chrousos GP, Ichihashi M (1999) Expression of proopiomelanocortin, corticotropin-releasing hormone (CRH), and CRH receptor in melanoma cells, nevus cells, and normal human melanocytes. J Investig Dermatol Symp Proc 4:105-109
43. Galibert MD, Boucontet L, Goding CR, Meo T (1997) Recognition of the E-C4 element from the C4 complement gene promoter by the upstream stimulatory factor-1 transcription factor. J Immunol 159:6176-6183
44. Garcia-Borron JC, Sanchez-Laorden BL, Jimenez-Cervantes C (2005) Melanocortin-1 receptor structure and functional regulation. Pigment Cell Res 18:393-410
45. Garcia-Borron JC, Abdel-Malek Z, Jimenez-Cervantes C (2014) MC1R, the cAMP pathway, and the response to solar UV: extending the horizon beyond pigmentation. Pigment Cell Melanoma Res 27:699-720
46. Giebel LB, Spritz RA (1991) Mutation of the KIT (mast/stem cell growth factor receptor) proto-oncogene in human piebaldism. Proc Natl Acad Sci U S A 88:8696-8699
47. Gilchrest BA, Rogers GS (1993) Photoaging. In: Lim HW, Soter NA (eds) Clinical photomedicine. Marcel Dekker, Inc., New York, pp 95-111
48. Gilchrest BA, Eller MS, Geller AC, Yaar M (1999) The pathogenesis of melanoma induced by ultraviolet radiation. N Engl J Med 340:1341-1348
49. Gledhill K, Rhodes LE, Brownrigg M, Haylett AK, Masoodi M, Thody AJ, Nicolaou A, Tobin DJ (2010) Prostaglandin-E2 is produced by adult human epidermal melanocytes in response to UVB in a melanogenesis-independent manner. Pigment Cell Melanoma Res 23:394-403
50. Goldgeier MH, Klein LE, Klein-Angerer S, Moellmann G, Nordlund JJ (1984) The distribution of melanocytes in the leptomeninges of the human brain. J Invest Dermatol 82:235-238
51. Gordon PR, Mansur CP, Gilchrest BA (1989) Regulation of human melanocyte growth, dendricity, and melanization by keratinocyte derived factors. J Invest Dermatol 92:565-572
52. Grichnik JM, Burch JA, Burchette J, Shea CR (1998) The SCF/KIT pathway plays a critical role in the control of normal human melanocyte homeostasis. J Invest Dermatol 111:233-238
53. Guo H, Yang K, Deng F, Xing Y, Li Y, Lian X, Yang T (2012a) Wnt3a inhibits proliferation but promotes melanogenesis of melan-a cells. Int J Mol Med 30:636-642
54. Guo H, Yang K, Deng F, Ye J, Xing Y, Li Y, Lian X, Yang T (2012b) Wnt3a promotes melanin synthesis of mouse hair follicle melanocytes. Biochem Biophys Res Commun 420:799-804
55. Haass NK, Herlyn M (2005) Normal human melanocyte homeostasis as a paradigm for understanding melanoma. J Investig Dermatol Symp Proc 10:153-163
56. Halaban R, Langdon R, Birchall N, Cuono C, Baird A, Scott G, Moellmann G, Mcguire J (1988) Basic fibroblast growth factor from human keratinocytes is a natural mitogen for melanocytes. J Cell Biol 107:1611-1619
57. Halder RM, Bridgeman-Shah S (1995) Skin cancer in African Americans. Cancer 75:667-673
58. Harder J, Bartels J, Christophers E, Schroder JM (2001) Isolation and characterization of human beta -defensin-3, a novel human inducible peptide antibiotic. J Biol Chem 276:5707-5713
59. Hauser JE, Kadekaro AL, Kavanagh RJ, Wakamatsu K, Terzieva S, Schwemberger S, Babcock G, Rao MB, Ito S, Abdel-Malek ZA (2006) Melanin content and MC1R function independently affect UVR-induced DNA damage in cultured human melanocytes. Pigment Cell Res 19:303-314
60. Hayakawa J, Mittal S, Wang Y, Korkmaz KS, Adamson E, English C, Ohmichi M, Mcclelland M, Mercola D (2004) Identification of promoters bound by c-Jun/ATF2 during rapid large-scale gene activation following genotoxic stress. Mol Cell 16:521-535
61. Hearing VJ (2005) Biogenesis of pigment granules: a sensitive way to regulate melanocyte function. J Dermatol Sci 37:3-14
62. Hemesath TJ, Price ER, Takemoto C, Badalian T, Fisher DE (1998) MAP kinase links the transcription factor microphthalmia to c-kit signalling in melanocytes. Nature 391:298-301
63. Hennessy A, Oh C, Diffey B, Wakamatsu K, Ito S, Rees J (2005) Eumelanin and pheomelanin concentrations in human epidermis before and after UVB irradiation. Pigment Cell Res 18:220-223
64. Herraiz C, Journe F, Abdel-Malek Z, Ghanem G, Jimenez-Cervantes C, Garcia-Borron JC (2011) Signaling from the human melanocortin 1 receptor to ERK1 and ERK2 mitogen-activated protein kinases involves transactivation of cKIT. Mol Endocrinol 25:138-156
65. Hirobe T, Takeuchi T (1977) Induction of melanogenesis in the epidermal melanoblasts of newborn mouse by MSH. J Embryol Exp Morphol 37:79-90
66. Horikawa T, Norris DA, Yohn JJ, Zekman T, Travers JB, Morelli JG (1995) Melanocyte mitogens induce both melanocyte chemokinesis and chemotaxis. J Invest Dermatol 104:256-259
67. Huang C, Ma W-Y, Maxinert A, Sun Y, Dong Z (1999) p38 Kinase mediates UV-induced phosphorylation of p53 protein at serine 389. J Biol Chem 274:12229-12235
68. Hunt G, Kyne S, Wakamatsu K, Ito S, Thody AJ (1995) Nle4DPhe7 α-melanocyte-stimulating hormone increases the eumelanin:phaeomelanin ratio in cultured human melanocytes. J Invest Dermatol 104:83-85
69. Hyter S, Coleman DJ, Ganguli-Indra G, Merrill GF, Ma S, Yanagisawa M, Indra AK (2013) Endothelin-1 is a transcriptional target of p53 in epidermal keratinocytes and regulates ultraviolet-induced melanocyte homeostasis. Pigment Cell Melanoma Res 26:247-258
70. Im S, Moro O, Peng F, Medrano EE, Cornelius J, Babcock G, Nordlund J, Abdel-Malek Z (1998a) Activation of the cyclic AMP pathway by α-melanotropin mediates the response of human melanocytes to ultraviolet B radiation. Cancer Res 58:47-54
71. Im S, Moro O, Peng F, Medrano EE, Cornelius J, Babcock G, Nordlund JJ, Abdel-Malek ZA (1998b) Activation of the cyclic AMP pathway by alpha-melanotropin mediates the response of human melanocytes to ultraviolet B radiation. Cancer Res 58:47-54
72. Imokawa G, Yada Y, Miyagishi M (1992) Endothelins secreted from human keratinocytes are intrinsic mitogens for human melanocytes. J Biol Chem 267:24675-24680
73. Imokawa G, Yada Y, Morisaki N, Kimura M (1998) Biological characterization of human fibroblast-derived mitogenic factors for human melanocytes. Biochem J 330:1235-1239
74. Ito S, Wakamatsu K (2003) Quantitative analysis of eumelanin and pheomelanin in humans, mice and other animals: a comparative review. Pigment Cell Res 16(5):523-531
75. Jamal S, Schneider RJ (2002) UV-induction of keratinocyte endothelin-1 downregulates E-cadherin in melanocytes and melanoma cells. J Clin Invest 110:443-452
76. Jarrett SG, Horrell EM, Christian PA, Vanover JC, Boulanger MC, Zou Y, D’orazio JA (2014) PKA-mediated phosphorylation of ATR promotes recruitment of XPA to UV-induced DNA damage. Mol Cell 54:999-1011
77. Jarrett SG, Wolf Horrell EM, Boulanger MC, D’orazio JA (2015) Defining the contribution of MC1R physiological ligands to ATR phosphorylation at Ser435, a predictor of DNA repair in melanocytes. J Invest Dermatol 135:3086-3095
78. Jimbow K, Fitzpatrick TB (1975) Changes in distribution patterns of cytoplasmic filaments in human melanocytes during ultraviolet-mediated melanin pigmentation. J Cell Biol 65:481-488
79. Kadekaro AL, Kavanagh R, Kanto H, Terzieva S, Hauser J, Kobayashi N, Schwemberger S, Cornelius J, Babcock G, Shertzer HG et al (2005) alpha-Melanocortin and endothelin-1 activate antiapoptotic pathways and reduce DNA damage in human melanocytes. Cancer Res 65:4292-4299
80. Kadekaro AL, Leachman S, Kavanagh RJ, Swope V, Cassidy P, Supp D, Sartor M, Schwemberger S, Babcock G, Wakamatsu K et al (2010) Melanocortin 1 receptor genotype: an important determinant of the damage response of melanocytes to ultraviolet radiation. FASEB J 24:3850-3860
81. Kauser S, Schallreuter KU, Thody AJ, Gummer C, Tobin DJ (2003) Regulation of human epidermal melanocyte biology by beta-endorphin. J Invest Dermatol 120:1073-1080
82. Kennedy C, Ter Huurne J, Berkhout M, Gruis N, Bastiaens M, Bergman W, Willemze R, Bouwes Bavinck JN (2001) Melanocortin 1 receptor (MC1R) gene variants are associated with an increased risk for cutaneous melanoma which is largely independent of skin type and hair color. J Invest Dermatol 117:294-300
83. Khaled M, Levy C, Fisher DE (2010) Control of melanocyte differentiation by a MITF-PDE4D3 homeostatic circuit. Genes Dev 24:2276-2281
84. Khlgatian MK, Hadshiew IM, Asawanonda P, Yaar M, Eller MS, Fujita M, Norris DA, Gilchrest BA (2002) Tyrosinase gene expression is regulated by p53. J Invest Dermatol 118:126-132
85. Kim JY, Shin JY, Kim MR, Hann SK, Oh SH (2012) siRNA-mediated knock-down of COX-2 in melanocytes suppresses melanogenesis. Exp Dermatol 21:420-425
86. Kim YI, Park SW, Shin MK, Lee MH (2015) Activin suppresses LPS-induced toll-like receptor, cytokine and inducible nitric oxide synthase expression in normal melanocytes by inhibiting NFĸB and MAPK pathway activation. Int J Mol Med 1165-1172
87. Kobayashi N, Nakagawa A, Muramatsu T, Yamashina Y, Shirai T, Hashimoto MW, Ishigaki Y, Ohnishi T, Mori T (1998) Supranuclear melanin caps reduce ultraviolet induced DNA photoproducts in human epidermis. J Invest Dermatol 110:806-810
88. Kock A, Schwarz T, Kirnbauer R, Urbanski A, Perry P, Ansel JC, Luger TA (1990) Human keratinocytes are a source for tumor necrosis factor α: evidence for synthesis and release upon stimulation with endotoxin or ultraviolet light. J Exp Med 172:1609-1614
89. Kokot A, Metze D, Mouchet N, Galibert MD, Schiller M, Luger TA, Bohm M (2009) Alpha-melanocyte-stimulating hormone counteracts the suppressive effect of UVB on Nrf2 and Nrf-dependent gene expression in human skin. Endocrinology 150:3197-3206
90. Krivosheya D, Tapia L, Levinson JN, Huang K, Kang Y, Hines R, Ting AK, Craig AM, Mei L, Bamji SX et al (2008) ErbB4-neuregulin signaling modulates synapse development and dendritic arborization through distinct mechanisms. J Biol Chem 283:32944-32956
91. Krude H, Biebermann H, Luck W, Horn R, Brabant G, Gruters A (1998) Severe early-onset obesity, adrenal insufficiency and red hair pigmentation caused by POMC mutations in humans. Nat Genet 19:155-157
92. Kupper TS, Chua AO, Flood P, Mcguire J, Gubler U (1987) Interleukin 1 gene expression in cultured human keratinocytes is augmented by ultraviolet irradiation. J Clin Invest 80:430-436
93. Landi MT, Kanetsky PA, Tsang S, Gold B, Munroe D, Rebbeck T, Swoyer J, Ter-Minassian M, Hedayati M, Grossman L et al (2005) MC1R, ASIP, and DNA repair in sporadic and familial melanoma in a Mediterranean population. J Natl Cancer Inst 97:998-1007
94. Levine N, Sheftel SN, Eytan T, Dorr RT, Hadley ME, Weinrach JC, Ertl GA, Toth K, Hruby VJ (1991) Induction of skin tanning by the subcutaneous administration of a potent synthetic melanotropin. JAMA 266:2730-2736
95. Levy C, Khaled M, Robinson KC, Veguilla RA, Chen PH, Yokoyama S, Makino E, Lu J, Larue L, Beermann F et al (2010) Lineage-specific transcriptional regulation of DICER by MITF in melanocytes. Cell 141:994-1005
96. Li G, Satyamoorthy K, Herlyn M (2001) N-cadherin-mediated intercellular interactions promote survival and migration of melanoma cells. Cancer Res 61:3819-3825
97. Lim HW, Grimes PE, Agbai O, Hamzavi I, Henderson M, Haddican M, Linkner RV, Lebwohl M (2015) Afamelanotide and narrowband UV-B phototherapy for the treatment of vitiligo: a randomized multicenter trial. JAMA Dermatol 151:42-50
98. Liu Z-G, Baskaran R, Lea-Chou ET, Wood LD, Chen Y, Karin M, Wang JYJ (1996) Three distinct signalling responses by murine fibroblasts to genotoxic stress. Nature 384:273-276
99. Lubbe J, Reichel M, Burg G, Kleihues P (1994) Absence of p53 gene mutations in cutaneous melanoma. J Invest Dermatol 102:819-821
100. Ma HJ, Ma HY, Yang Y, Li PC, Zi SX, Jia CY, Chen R (2014) alpha-Melanocyte stimulating hormone (MSH) and prostaglandin E2 (PGE2) drive melanosome transfer by promoting filopodia delivery and shedding spheroid granules: evidences from atomic force microscopy observation. J Dermatol Sci 76:222-230
101. Marconi A, Terracina M, Fila C, Franchi J, Bonte F, Romagnoli G, Maurelli R, Failla CM, Dumas M, Pincelli C (2003) Expression and function of neurotrophins and their receptors in cultured human keratinocytes. J Invest Dermatol 121:1515-1521
102. Maresca V, Flori E, Bellei B, Aspite N, Kovacs D, Picardo M (2010) MC1R stimulation by alpha-MSH induces catalase and promotes its re-distribution to the cell periphery and dendrites. Pigment Cell Melanoma Res 23:263-275
103. Marrot L, Belaidi JP, Jones C, Perez P, Meunier JR (2005) Molecular responses to stress induced in normal human caucasian melanocytes in culture by exposure to simulated solar UV. Photochem Photobiol 81:367-375
104. Matsumoto K, Tajima H, Nakamura T (1991) Hepatocyte growth factor is a potent stimulator of human melanocyte DNA synthesis and growth. Biochem Biophys Res Commun 176:45-51
105. Mcgill GG, Horstmann M, Widlund HR, Du J, Motyckova G, Nishimura EK, 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
106. Mcgowan KA, Li JZ, Park CY, Beaudry V, Tabor HK, Sabnis AJ, Zhang W, Fuchs H, De Angelis MH, Myers RM et al (2008) Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects. Nat Genet 40:963-970
107. Medrano EE, Im S, Yang F, Abdel-Malek Z (1995) UVB light induces G1 arrest in human melanocytes by prolonged inhibition of pRb phosphorylation associated with long term expression of the protein p21Waf-1/SDI/Cip-1 protein. Cancer Res 55:4047-4052
108. Mitra D, Luo X, Morgan A, Wang J, Hoang MP, Lo J, Guerrero CR, Lennerz JK, Mihm MC, Wargo JA et al (2012) An ultraviolet-radiation-independent pathway to melanoma carcinogenesis in the red hair/fair skin background. Nature 491:449-453
109. Morelli JG, Yohn JJ, Lyons MB, Murphy RC, Norris DA (1989) Leukotrienes C4 and D4 as potent mitogens for cultured human melanocytes. J Invest Dermatol 93:719-722
110. Mountjoy KG, Robbins LS, Mortrud MT, Cone RD (1992) The cloning of a family of genes that encode the melanocortin receptors. Science 257:1248-1251
111. Murase D, Hachiya A, Amano Y, Ohuchi A, Kitahara T, Takema Y (2009) The essential role of p53 in hyperpigmentation of the skin via regulation of paracrine melanogenic cytokine receptor signaling. J Biol Chem 284:4343-4353
112. Newton Bishop JA, Bishop DT (2005) The genetics of susceptibility to cutaneous melanoma. Drugs Today (Barc) 41:193-203
113. Nicolaou A, Estdale SE, Tsatmali M, Herrero DP, Thody AJ (2004) Prostaglandin production by melanocytic cells and the effect of alpha-melanocyte stimulating hormone. FEBS Lett 570:223-226
114. Nudi M, Ouimette JF, Drouin J (2005) Bone morphogenic protein (Smad)-mediated repression of proopiomelanocortin transcription by interference with Pitx/Tpit activity. Mol Endocrinol 19:1329-1342
115. Nylander K, Bourdon J-C, Bray SE, Gibbs NK, Kay R, Hart I, Hall PA (2000) Transcriptional activation of tyrosinase and TRP-1 by p53 links UV irradiation to the protective tanning response. J Pathol 190:39-46
116. Ono K, Han J (2000) The p38 signal transduction pathway. Activation and function. Activation and function 12:1-13
117. Otsuka T, Takayama H, Sharp R, Celli G, Larochelle WJ, Bottaro DP, Ellmore N, Vieira W, Owens JW, Anver M et al (1998) c-Met autocrine activation induces development of malignant melanoma and acquisition of the metastatic phenotype. Cancer Res 58:5157-5167
118. Palmer JS, Duffy DL, Box NF, Aitken JF, O’gorman LE, Green AC, Hayward NK, Martin NG, Sturm RA (2000) Melanocortin-1 receptor polymorphisms and risk of melanoma: is the association explained solely by pigmentation phenotype? Am J Hum Genet 66:176-186
119. Park HY, Wu C, Yaar M, Stachur CM, Kosmadaki M, Gilchrest BA (2009) Role of BMP-4 and its signaling pathways in cultured human melanocytes. Int J Cell Biol 2009:750482
120. Pasterkamp RJ, Peschon JJ, Spriggs MK, Kolodkin AL (2003) Semaphorin 7A promotes axon outgrowth through integrins and MAPKs. Nature 424:398-405
121. Pathak MA (1991) Ultraviolet radiation and the development of non-melanoma and melanoma skin cancer: clinical and experimental evidence. Skin Pharmacol 4(Suppl 1):85-94
122. Pathak MA, Jimbow K, Fitzpatrick T (1980) Photobiology of pigment cell. In: Seiji M (ed) Phenotypic expression in pigment cells. University of Tokyo Press, Tokyo, pp 655-670
123. Pawelek J, Wong G, Sansone M, Morowitz J (1973) Molecular biology of pigment cells: molecular controls in mammalian pigmentation. Yale J Biol Med 46:430-443
124. Pittelkow MR, Shipley GD (1989) Serum-free culture of normal human melanocytes: growth kinetics and growth factor requirements. J Cell Physiol 140:565-576
125. Plettenberg A, Ballaun C, Pammer J, Mildner M, Strunk D, Weninger W, Tschachler E (1995) Human melanocytes and melanoma cells constitutively express the bcl-2 proto-oncogene in situ and in cell culture. Am J Pathol 146:651-659
126. Premi S, Wallisch S, Mano CM, Weiner AB, Bacchiocchi A, Wakamatsu K, Bechara EJ, Halaban R, Douki T, Brash DE (2015) Photochemistry. Chemiexcitation of melanin derivatives induces DNA photoproducts long after UV exposure. Chemiexcitation of melanin derivatives induces DNA photoproducts long after UV exposure 347:842-847
127. Price ER, Horstmann MA, Wells AG, Weilbaecher KN, Takemoto CM, Landis MW, Fisher DE (1998) α-Melanocyte-stimulating hormone signaling regulates expression of microphthalmia, a gene deficient in Waardenburg syndrome. J Biol Chem 273:33042-33047
128. Puffenberger EG, Hosoda K, Washington SS, Nakao K, Dewit D, Yanagisawa M, Chakravarti A (1994) A missense mutation of the endothelin-B receptor gene in multigenic Hirschsprung’s disease. Cell 79:1257-1266
129. Quevedo WC Jr, Szabo G, Virks J (1969) Influence of age and UV on the population of DOPA-positive melanocytes in human skin. J Invest Dermatol 52:287-290
130. Robbins LS, Nadeau JH, Johnson KR, Kelly MA, Roselli-Rehfuss L, Baack E, Mountjoy KG, Cone RD (1993) Pigmentation phenotypes of variant extension locus alleles result from point mutations that alter MSH receptor function. Cell 72:827-834
131. Rokos H, Beazley WD, Schallreuter KU (2002) Oxidative stress in vitiligo: photo-oxidation of pterins produces H(2)O(2) and pterin-6-carboxylic acid. Biochem Biophys Res Commun 292:805-811
132. Romero-Graillet C, Aberdam E, Biagoli N, Massabni W, Ortonne JP, Ballotti R (1996) Ultraviolet B radiation acts through the nitric oxide and cGMP signal transduction pathway to stimulate melanogenesis in human melanocytes. J Biol Chem 271:28052-28056
133. Romero-Graillet C, Aberdam E, Clement M, Ortonne JP, Ballotti R (1997) Nitric oxide produced by ultraviolet-irradiated keratinocytes stimulates melanogenesis. J Clin Invest 99:635-642
134. Rosette C, Karin M (1996) Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 274:1194-1197
135. Sakai C, Ollmann M, Kobayashi T, Abdel-Malek Z, Muller J, Vieira WD, Imokawa G, Barsh GS, Hearing VJ (1997) Modulation of murine melanocyte function in vitro by agouti signal protein. EMBO J 16:3544-3552
136. Sato Y, Takahashi H (1998) Molecular cloning and expression of murine homologue of semaphorin K1 gene. Biochim Biophys Acta 1443:419-422
137. Scott G, Deng A, Rodriguez-Burford C, Seiberg M, Han R, Babiarz L, Grizzle W, Bell W, Pentland A (2001) Protease-activated receptor 2, a receptor involved in melanosome transfer, is upregulated in human skin by ultraviolet irradiation. J Invest Dermatol 117:1412-1420
138. Scott MC, Wakamatsu K, Ito S, Kadekaro AL, Kobayashi N, Groden J, Kavanagh R, Takakuwa T, Virador V, Hearing VJ et al (2002) Human melanocortin 1 receptor variants, receptor function and melanocyte response to UV radiation. J Cell Sci 115:2349-2355
139. Scott G, Leopardi S, Parker L, Babiarz L, Seiberg M, Han R (2003) The proteinase-activated receptor-2 mediates phagocytosis in a Rho-dependent manner in human keratinocytes. J Invest Dermatol 121:529-541
140. Scott G, Jacobs S, Leopardi S, Anthony FA, Learn D, Malaviya R, Pentland A (2005) Effects of PGF2alpha on human melanocytes and regulation of the FP receptor by ultraviolet radiation. Exp Cell Res 304:407-416
141. Scott GA, Mcclelland LA, Fricke AF (2008) Semaphorin 7a promotes spreading and dendricity in human melanocytes through beta1-integrins. J Invest Dermatol 128:151-161
142. Seiberg M, Paine C, Sharlow E, Costanzo M, Andrade-Gordon P, Eisinger M, Shapiro SS (2000) The protease-activated receptor-2 regulates pigmentation via keratinocyte-melanocyte interactions. Exp Cell Res 254:25-32
143. Sharov AA, Fessing M, Atoyan R, Sharova TY, Haskell-Luevano C, Weiner L, Funa K, Brissette JL, Gilchrest BA, Botchkarev VA (2005) Bone morphogenetic protein (BMP) signaling controls hair pigmentation by means of cross-talk with the melanocortin receptor-1 pathway. Proc Natl Acad Sci U S A 102:93-98
144. Siracusa LD (1994) The agouti gene: turned on to yellow. Trends Genet 10:423-428
145. Slominski A (1998) Identification of beta-endorphin, alpha-MSH and ACTH peptides in cultured human melanocytes, melanoma and squamous cell carcinoma cells by RP-HPLC. Exp Dermatol 7:213-216
146. Slominski A, Ermak G, Hwang J, Chakraborty A, Mazurkiewicz JE, Mihm M (1995) Proopiomelanocortin, corticotropin releasing hormone and corticotropin releasing hormone receptor genes are expressed in human skin. FEBS Lett 374:113-116
147. Slominski A, Zbytek B, Szczesniewski A, Semak I, Kaminski J, Sweatman T, Wortsman J (2005) CRH stimulation of corticosteroids production in melanocytes is mediated by ACTH. Am J Physiol Endocrinol Metab 288:E701-E706
148. Smit NPM, Vink AA, Kolb RM, Steenwinkel M-JST, Van Den Berg PTM, Van Nieuwpoort F, Roza L, Pavel S (2001) Melanin offers protection against induction of cyclobutane pyrimidine dimers and 6-4 photoproducts by UVB in cultured human melanocytes. Photochem Photobiol 74:424-430
149. Smith R, Healy E, Siddiqui S, Flanagan N, Steijlen PM, Rosdahl I, Jacques JP, Rogers S, Turner R, Jackson IJ et al (1998) Melanocortin 1 receptor variants in Irish population. J Invest Dermatol 111:119-122
150. Smith AG, Luk N, Newton RA, Roberts DW, Sturm RA, Muscat GE (2008) Melanocortin-1 receptor signaling markedly induces the expression of the NR4A nuclear receptor subgroup in melanocytic cells. J Biol Chem 283:12564-12570
151. Song X, Mosby N, Yang J, Xu A, Abdel-Malek Z, Kadekaro AL (2009) alpha-MSH activates immediate defense responses to UV-induced oxidative stress in human melanocytes. Pigment Cell Melanoma Res 22:809-818
152. Sosman JA, Margolin KA (2009) Inside life of melanoma cell signaling, molecular insights, and therapeutic targets. Curr Oncol Rep 11:405-411
153. Starner RJ, Mcclelland L, Abdel-Malek Z, Fricke A, Scott G (2010) PGE(2) is a UVR-inducible autocrine factor for human melanocytes that stimulates tyrosinase activation. Exp Dermatol 19:682-684
154. Stefanato CM, Yaar M, Bhawan J, Phillips TJ, Kosmadaki MG, Botchkarev V, Gilchrest BA (2003) Modulations of nerve growth factor and Bcl-2 in ultraviolet-irradiated human epidermis. J Cutan Pathol 30:351-357
155. Steingrimsson E, Copeland NG, Jenkins NA (2004) Melanocytes and the microphthalmia transcription factor network. Annu Rev Genet 38:365-411
156. Stratigos AJ, Dimisianos G, Nikolaou V, Poulou M, Sypsa V, Stefanaki I, Papadopoulos O, Polydorou D, Plaka M, Christofidou E et al (2006) Melanocortin receptor-1 gene polymorphisms and the risk of cutaneous melanoma in a low-risk southern European population. J Invest Dermatol 126:1842-1849
157. Suzuki I, Cone R, Im S, Nordlund J, Abdel-Malek Z (1996) Binding of melanotropic hormones to the melanocortin receptor MC1R on human melanocytes stimulates proliferation and melanogenesis. Endocrinology 137:1627-1633
158. Suzuki I, Tada A, Ollmann MM, Barsh GS, Im S, Lamoreux ML, Hearing VJ, Nordlund J, Abdel-Malek ZA (1997) Agouti signaling protein inhibits melanogenesis and the response of human melanocytes to α-melanotropin. J Invest Dermatol 108:838-842
159. Suzuki I, Kato T, Motokawa T, Tomita Y, Nakamura E, Katagiri T (2002) Increase of pro-opiomelanocortin mRNA prior to tyrosinase, tyrosinase-related protein 1, dopachrome tautomerase, Pmel-17/gp100, and P-protein mRNA in human skin after ultraviolet B irradiation. J Invest Dermatol 118:73-78
160. Swope V, Alexander C, Starner R, Schwemberger S, Babcock G, Abdel-Malek ZA (2014) Significance of the melanocortin 1 receptor in the DNA damage response of human melanocytes to ultraviolet radiation. Pigment Cell Melanoma Res 27:601-610
161. Swope VB, Abdel-Malek ZA, Kassem L, Nordlund JJ (1991) Interleukins 1α and 6 and tumor necrosis factor-α are paracrine inhibitors of human melanocyte proliferation and melanogenesis. J Invest Dermatol 96:180-185
162. Swope VB, Sauder DN, Mckenzie RC, Sramkoski RM, Krug KA, Babcock GF, Nordlund JJ, Abdel-Malek ZA (1994) Synthesis of interleukin-1α and β by normal human melanocytes. J Invest Dermatol 102:749-753
163. Swope VB, Medrano EE, Smalara D, Abdel-Malek Z (1995a) Long-term proliferation of human melanocytes is supported by the physiologic mitogens α-melanotropin, endothelin-1, and basic fibroblast growth factor. Exp Cell Res 217:453-459
164. Swope VB, Medrano EE, Smalara D, Abdel-Malek ZA (1995b) Long-term proliferation of human melanocytes is supported by the physiologic mitogens alpha-melanotropin, endothelin-1, and basic fibroblast growth factor. Exp Cell Res 217:453-459
165. Swope VB, Jameson JA, Mcfarland KL, Supp DM, Miller WE, Mcgraw DW, Patel MA, Nix MA, Millhauser GL, Babcock GF et al (2012) Defining MC1R regulation in human melanocytes by its agonist alpha-melanocortin and antagonists agouti signaling protein and beta-defensin 3. J Invest Dermatol 132(9):2255-2262
166. Szabo G (1954) The number of melanocytes in human epidermis. Br Med J 1:1016-1017
167. Tachibana M (1999) Sound needs sound melanocytes to be heard. Pigment Cell Res 12:344-354
168. Tada A, Suzuki I, Im S, Davis MB, Cornelius J, Babcock G, Nordlund JJ, Abdel-Malek ZA (1998a) Endothelin-1 is a paracrine growth factor that modulates melanogenesis of human melanocytes and participates in their responses to ultraviolet radiation. Cell Growth Differ Mol Biol J Am Assoc Cancer Res 9:575-584
169. Tada A, Suzuki I, Im S, Davis MB, Cornelius J, Babcock G, Nordlund JJ, Abdel-Malek ZA (1998b) Endothelin-1 is a paracrine growth factor that modulates melanogenesis of human melanocytes and participates in their responses to ultraviolet radiation. Cell Growth Differ 9:575-584
170. Tada A, Pereira E, Beitner Johnson D, Kavanagh R, Abdel-Malek ZA (2002) Mitogen and ultraviolet-B-induced signaling pathways in normal human melanocytes. J Invest Dermatol 118:316-322
171. Tadokoro T, Kobayashi N, Zmudzka BZ, Ito S, Wakamatsu K, Yamaguchi Y, Korossy KS, Miller SA, Beer JZ, Hearing VJ (2003) UV-induced DNA damage and melanin content in human skin differing in racial/ethnic origin. FASEB J 17:1177-1179
172. Tamagnone L, Artigiani S, Chen H, He Z, Ming GI, Song H, Chedotal A, Winberg ML, Goodman CS, Poo M et al (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99:71-80
173. Thody AJ, Ridley K, Penny RJ, Chalmers R, Fisher C, Shuster S (1983) MSH peptides are present in mammalian skin. Peptides 4:813-816
174. Tsatmali M, Graham A, Szatkowski D, Ancans J, Manning P, Mcneil CJ, Graham AM, Thody AJ (2000) α-Melanocyte-stimulating hormone modulates nitric oxide production in melanocytes. J Invest Dermatol 114:520-526
175. Von Koschembahr AM, Swope VB, Starner RJ, Abdel-Malek ZA (2015) Endothelin-1 protects human melanocytes from UV-induced DNA damage by activating JNK and p38 signaling pathways. Exp Dermatol 24:269-274
176. Wakamatsu K, Graham A, Cook D, Thody AJ (1997) Characterization of ACTH peptides in human skin and their activation of the melanocortin-1 receptor. Pigment Cell Res 10:288-297
177. Wakamatsu K, Kavanagh R, Kadekaro AL, Terzieva S, Strum RA, Leachman S, Abdel-Malek ZA, Ito S (2006) Diversity of pigmentation in cultured human melanocytes is due to differences in the type as well as quantity of melanin. Pigment Cell Res 19:154-162
178. Wang Z, Coleman DJ, Bajaj G, Liang X, Ganguli-Indra G, Indra AK (2011) RXRalpha ablation in epidermal keratinocytes enhances UVR-induced DNA damage, apoptosis, and proliferation of keratinocytes and melanocytes. J Invest Dermatol 131(1):177-187
179. Wu M, Hemesath T, Takemoto CM, Horstmann MA, Wells AG, Price ER, Fisher DZ, Fisher DE (2000) c-Kit triggers dual phosphorylations, which couple activation and degradation of the essential melanocyte factor Mi. Genes Dev 14:301-312
180. Yaar M, Grossman K, Eller M, Gilchrest BA (1991) Evidence for nerve growth factor-mediated paracrine effects in human epidermis. J Cell Biol 115:821-828
181. Yaar M, Eller MS, Dibenedetto P, Reenstra WR, Zhai S, Mcquiad T, Archambault M, Gilchrest BA (1994) The trk family of receptors mediates nerve growth factor and neurotrophin-3 effects in melanocytes. J Clin Invest 94:1550-1562
182. Yaar M, Wu C, Park HY, Panova I, Schutz G, Gilchrest BA (2006) Bone morphogenetic protein-4, a novel modulator of melanogenesis. J Biol Chem 281:25307-25314
183. Yada Y, Higuchi K, Imokawa G (1991) Effects of endothelins on signal transduction and proliferation in human melanocytes. J Biol Chem 266:18352-18357
184. Yajima I, 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
185. Yazdani U, Terman JR (2006) The semaphorins. Genome Biol 7:211
186. Yohn JJ, Morelli JG, Walchak SJ, Rundell KB, Norris DA, Zamora MR (1993) Cultured human keratinocytes synthesize and secrete endothelin-1. J Invest Dermatol 100:23-26
187. Zayed AA, Khorshied MM, Hussein MF (2015) Inducible nitric oxide synthase promoter polymorphism: a molecular susceptibility marker for vitiligo in Egyptians. Int J Dermatol 54:675-679
188. Zhai S, Yaar M, Doyle S, Gilchrest B (1996) Nerve growth factor rescues pigment cells from ultaviolet-induced apoptosis by upregulating BCL-2 levels. Exp Cell Res 224:335-343