Cyclic AMP a key messenger in the regulation of skin pigmentation

Pigment Cell Research

Volumn 13, Issue 2, 2000, Pages 60-69

  Buscà, Roser ^a   Ballotti, Robert ^a  

^a INSERM   (France)

Author keywords

MSH; MAPK; Melanogenesis; MITF

Indexed keywords

CYCLIC AMP;

ANIMAL; HUMAN; METABOLISM; PHYSIOLOGY; REVIEW; SECOND MESSENGER; SKIN PIGMENTATION;

ANIMALS; CYCLIC AMP; HUMANS; SECOND MESSENGER SYSTEMS; SKIN PIGMENTATION;

ANIMALIA;

EID: 0034127724     PISSN: 08935785     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-0749.2000.130203.x     Document Type: Review

References (87)

1. Fitzpatrick TB, Szabo G, Seiji M, Quevedo WC. Biology of the melanin pigmentary system. In: Fitzpatrick TB. Dermatology in General Medicine. New York: Academic Press; 1979. pp. 131-163
2. Le Douarin N. The neural crest. Cambridge: Cambridge university Press; 1982
3. Hearing VJ. Biochemical control of melanogenesis and melanosomal organization. J Invest Dermatol 1999;4:24-28
4. Brilliant MH, Barsh GS. Anatomy of pigment cell genes acting at a cellular level. In: Nordlund JJ, Boissy RE, Hearing VJ, King RA, Ortonne J-P. The Pigmentary System. Oxford: Oxford University Press; 1998. pp. 217-229
5. Barsh GS. Genetics of pigmentation: From fancy genes to complex traits. Trends Genet 1996;12:299-305
6. Siegrist W, Willard DH, Wilkison WO, Eberle AN. Agouti protein inhibits growth of B16 melanoma cells in vitro by acting through melanocortin receptors. Biochem Biophys Res Commun 1996;218:171-175
7. Suzuki I, Tada A, Ollmann MM, Barsh GS, Im S, Lamoreux ML, Hearing VJ, Nordlund JJ, Abdel-Malek ZA. Agouti signaling protein inhibits melanogenesis and the response of human melanocytes to alpha-melanotropin. J Invest Dermatol 1997;108:838-842
8. y) mutation explained by deletion of a maternally expressed gene and the simultaneous production of agouti fusion RNAs. Development 1994;120:1695-1708
9. Lamerson CL, Nordlund JJ. Pigmentary Changes in Addison's disease with adrenal insufficiency. In: Nordlund JJ, Boissy RE, Hearing VJ, King RA, Ortonne J-P. The pigmentary system. Oxford: Oxford University Press; 1998. pp. 875-877
10. Pears JS, Jung RT, Bartlett W, Browning MC, Kenicer K, Thody AJ. A case of skin hyperpigmentation due to alpha-MSH hypersecretion. Br J Dermatol 1992;126:286-289
11. Valverde P, Healy E, Jackson I, Rees J, Thody A. Variants of the melanocyte-stimulating hormone receptor gene are associated with red hair and fair skin in humans. Nat Genet 1995;11:328-330
12. Krude H, Biebermann H, Luck W, Horn R, Brabant G, Gruters A. Severe early-onset obesity, adrenal insufficiency and red hair pigmentation caused by POMC mutations in humans. Nat Genet 1998;19:155-157
13. Lerner AB, McGuire JS. Effect of α and β melanocyte stimulating hormone on the skin colour of the man. Nature 1961;189:176-179
14. Levine N, Sheftel SN, Eytan T, Dorr RT, Hadley ME, Weinrach JC, Ertl GA, Toth K, McGee DL, Hruby VJ. Induction of skin tanning by subcutaneous administration of a potent synthetic melanotropin. J Am Med Assoc 1991;226:2730-2736
15. Abdel-Malek Z, Swope V, Suzuki I, Akcali C, Harriger M, Boyce S, Urabe K, Hearing VJ. Mitogenic and melanogenic stimulation of normal human melanocytes by melanotropic peptides. Proc Natl Acad Sci USA 1995;92:1789-1793
16. Englaro W, Rezzonico R, Durand-Clément M, Lallemand D, Ortonne JP, Ballotti R. Mitogen-activated protein kinase pathway and AP-1 are activated during cAMP-induced melanogenesis in B-16 melanoma cells. J Biol Chem 1995;270:24315-24320
17. Hearing VJ, Tsukamoto K. Enzymatic control of pigmentation in mammals. FASEB J 1991;5:2902-2909
18. Allan AE, Archambault M, Messana E, Gilchrest BA. Topically applied diacylglycerols increase pigmentation in guinea pig skin. J Invest Dermatol 1995;105:687-692
19. Lowe C, Goodman-Lowe G. Suntanning in hammerhead sharks. Nature 1996;383:677
20. Romero-Graillet C, Aberdam E, Clement M, Ortonne J-P, Ballotti R. Nitric oxide produced by ultraviolet-irradiated keratinocytes stimulates melanogenesis. J Clin Invest 1997;99:1-8
21. Abdel-Malek Z, Swope VB, Smalara D, Babcock G, Dawes S, Nordlund JJ. Analysis of the UV-induced melanogenesis and growth arrest of human melanocytes. Pigment Cell Res 1994;7:326-33222.
22. Friedmann PS, Gilchrest BA. Ultraviolet radiation directly induces pigment production by cultured human melanocytes. J Cell Physiol 1987;133:88-94
23. Aberdam E, Roméro C, Ortonne J-P. Repeated UVB irradiations do not have the same potential to promote stimulation of melanogenesis in cultured normal human melanocytes. J Cell Sci 1993;106:1015-1022
24. Gilchrest BA, Park HY, Eller MS, Yaar M. Mechanisms of ultraviolet light-induced pigmentation. Photochem Photobiol 1996;93:1-10
25. Nishizuka Y. Studies and perspectives of protein kinase C. Science 1986;233:305-312
26. Friedmann PS, Wren F, MacNeil S. Alpha-MSH causes a small rise in cAMP but has no effect on basal or ultraviolet-stimulated melanogenesis in human melanocytes. Brit J Dermatol 1990;123:145-151
27. Park HY, Perez JM, Laursen R, Hara M, Gilchrest BA. Protein kinase C-beta activates tyrosinase by phosphorylating serine residues in its cytoplasmic domain. J Biol Chem 1999;274:16470-16478
28. Bertolotto C, Bille K, Ortonne J-P, Ballotti R. In B16 melanoma cells, the inhibition of melanogenesis by TPA results from PKC activation and diminution of microphthalmia binding to the M-box of the tyrosinase promoter. Oncogene 1998;16:1665-1670
29. Romero-Graillet C, Aberdam E, Biagoli N, Massabni W, Ortonne J-P, Ballotti R. Ultraviolet B radiation acts through the nitric oxide and cGMP signal transduction pathway to stimulate melanogenesis in human melanocytes. J Biol Chem 1996;271:28052-28056
30. Eller MS, Maeda T, Magnoni C, Atwal D, Gilchrest BA. Enhancement of DNA repair in human skin cells by thymidine dinucleotides: Evidence for a p53-mediated mammalian SOS response. Proc Natl Acad Sci USA 1997;94:12627-12632
31. Gordon PR, Mansur CP, Gilchrest BA. Regulation of human melanocyte growth, dendricity, and melanization by keratinocyte derived factors. J Invest Dermatol 1989;92:565-572
32. Abdel-Malek ZA, Swope BV, Amornsiripanitch N, Nordlund JJ. In vitro modulation of proliferation and melanization of S91 melanoma cells by prostaelandins. Cancer Res 1987;47:3141-3146
33. 7α-MSH affect morphology, tyrosinase activity and melanogenesis in cultured human melanocytes. J Cell Science 1994;107:205-211
34. Hara M, Yaar M, Gilchrest BA. Endothelin-1 of keratinocyte origin is a mediator of melanocyte dendricity. J Invest Dermatol 1995;105:744-748
35. Yohn JJ, Morelli JG, Walchack SJ, Rundell KB, Norris DA, Zamora MR. Cultured human keranocytes synthesize and secreted endothelin-1. J Invest Dermatol 1993;100:23-26
36. Swope VB, Abdel-Malek ZA, Sauder DN, Nordlund JJ. A new role for epidermal cell-derived thymocyte activating factor/IL-1 as an antagonist for distinct epidermal cell function. J Immunol 1989;142:1943-1949
37. Köck A, Schauer E, Luger TA. The human melanocyte is an immunocompetent epidermal cell: Production of immunomodulating cytokines. Arch Derm Res 1991;283:56
38. Kameyama K, Tanaka S, Ishida Y, Hearing VJ. Interferons modulate the expression of hormone receptors on the surface of murine melanoma cells. J Clin Invest 1989;83:213-221
39. Halaban R, Langdon R, Birchall N, Cuono C, Baird A, Scott G, Moellmann G, McGuire J. Basic fibroblast growth factor from human keratinocytes is a natural mitogen for melanocytes. J Cell Biol 1988;107:1611-1619
40. Hunt G, Donatien PD, Lunec J, Todd C, Kyne S, Thody AJ. Cultured human melanocytes respond to MSH peptides and ACTH. Pigment Cell Res 1994;7:217-221
41. Wakamatsu K, Graham A, Cook D, Thody A. Characterisation of ACTH peptides in human skin and their activation of themelanocortin-1 receptor. Pigment Cell Res 1997;10:288-297
42. Chakraborty A, Pawelek J. MSH receptors in immortalized human epidermal keratinocytes: A potential mechanism for coordinate regulation of the epidermal-melanin unit. J Cell Physiol 1993;157:344-350
43. Aberdam E, Mari B, Auberger P, Ortonne J-P, Ballotti R. UVB control of melanogenesis via regulation of neutral endopeptidase (NEP), the enzyme responsible for the degradation of alpha-MSH. Pigment Cell Res 1999;Suppl 7:116
44. Roesler WJ, Park EA, McFie PJ. Characterization of CCAAT/ enhancer-binding protein alpha as a cyclic AMP-responsive nuclear regulator. J Biol Chem 1998;273:14950-14957
45. Karin M. Signal transduction from the cell surface to the nucleus through the phosphorylation of transcription factors. Curr Opin Cell Biol 1994;6:415-424
46. Bertolotto C, Bille K, Ortonne J-P, Ballotti R. Regulation of tyrosinase gene expression by cAMP in B16 melanoma cells involves two CATGTG motifs surrounding the TATA box: Implication of the microphthalmia gene product. J Cell Biol 1996;134:747-755
47. Bertolotto C, Buscà R, Abbe P, Bille K, Aberdam E, Ortonne J-P, Ballotti R. Different cis-acting elements are involved in the regulation of TRP1 and TRP2 promoter activities by cyclic AMP: Pivotal role of M boxes (GTCATGTGCT) and of microphthalmia. Mol Cell Biol 1998;18:694-702
48. Hodgkinson CA, Moore KJ, Nakayama A, Steingrimsson E, Copeland NG, Jenkins NA, Arnheiter H. Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic-helix-loop-helix-zipper protein. Cell 1993;74:395-404
49. Steingrimsson E, Moore KJ, Lamoreux ML. Ferré-D'Amaré AR, Burley SK, Zimring DCS, Skow LC, Hodgkinson CA, Arnheiter H, Copeland NG, Jenkins NA. Molecular basis of mouse microphthalmia (mi) mutations helps explain their developmental and phenotypic consequences. Nat Genet 1994;8:256-263
50. Marks SC, Walker DG. The hematogenous origin o osteoclasts: Experimental evidence from osteopetrotic (microphthalmic) mice treated with spleen cells from beige mouse donors. Am J Anat 1981;161:1-10
51. Stechschulte DJ. Effect of the mi allele on mast cells, basophils, natural killer cells, and osteoclasts in C57B1/6J. J Cell Physiol 1987;132:565-570
52. Tachibana M, Perez-Jurado LA, Nakayama A, Hodgkinson CA, Li X, Schneider M, Miki T, Fex J, Francke U, Arnheiter H. Cloning of MITF, the human homolog of the mouse microphthalmia gene and assignment to chromosome 3p14.1-p12.3. Hum Mol Genet 1994;3:553-557
53. Tassabehji M, Newton VE, Read AP. MITF gene mutations in patients with type 2 Waardenburg syndrome. Nat Genet 1994;8:251-255
54. Waardenburg PJ. A new syndrome combining developmental anomalies of eyelids, eyebrows and nose root with pigmentary defects of the iris and head hair and with congenital deafness. Am J Hum Genet 1951;3:195-253
55. Beckmann H, Kadesch T. The leucine zipper of TFE3 dictates helix-loop-helix dimerization specificity. Genes Dev 1991;5:1057-1066
56. Ferré-D'Amaré AR, Prendergast GC, Ziff EB, Burley SK. Recognition by Max of its cognate DNA through a dimeric b/HLH/Z domain. Nature 1993;363:38-45
57. Fisher DE, Carr CS, Parent LA, Sharp PA, TFEB has DNA-binding and oligomerization properties of a unique helix-loop-helix/leucine-zipper family. Genes Dev 1991;5:2342-2352
58. Carr CS, Sharp PA. A helix-loop-helix protein related to the immunoglobulin E-box binding protein. Mol Cell Biol 1990;10:4384-4388
59. Zhao GQ, Zhao Q, Shou X, Mattei MG, DeCorombrugghe B. TFEC, a basic helix-loop-helix protein, forms heterodimers with TFE3 and inhibits TFE3-dependent transcription activation. Mol Cell Biol 1993;13:4505-4512
60. Bertolotto C, Abbe P, Hemesath TJ, Bille K, Ortonne J-P, Ballotti R. Microphthalmia gene product as a signal transducer in cAMP-induced differentiation of melanocytes. J Cell Biol 1998;142:827-835
61. Eisen T, Easty DJ, Bennett DC, Goding CR. The POU domain transcription factor Brn-2: Elevated expression in malignant melanoma and regulation of melanocyte-specific gene expression. Oncogene 1995;11:2157-2164
62. Verastegui C, Bertolotto C, Bille K, Abbe P, Ortonne J-P, Ballotti R. TFE3 and TFEB as transcriptional activators of tyrosinase and TRP1 genes. Pig Cell Res 1999:Suppl 7:144
63. Carreira S, Dexter TJ, Yavuzer U, Easty DJ, Goding CR. Brachyury-related transcription factor Tbx2 and repression of the melanocyte-specific TRP-1 promoter. Mol Cell Biol 1998;18:5099-5108
64. Epstein DJ, Vekemans M, Gros P. Splotch (Sp2h), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3. Cell 1991;67:767-774
65. Galibert MD, Yavuzer U, Dexter J, Goding CR. Pax3 and regulation of the melanocyte-specific tyrosinase-related protein-1 promoter. J Biol Chem 1999;274:26894-26900
66. Tassabehji M, Read AP, Newton VE, Harris R, Balling R, Gruss P, Strachan T. Waardenburg's syndrome patients have mutation in the human homologue of the pax-3 paired box gene. Nature 1992;355:635-636
67. Watanabe A, Takeda K, Ploplis B, Tachibana M. Epistatic relationship between Waardenburg syndrome genes MITF and PAX3. Nat Genet 1998;18:283-286
68. Southard-Smith EM, Kos L, Pavan WS. Sox10 mutation disrupts neural crest development in Dom Hirschsprung mouse model. Nat Gene 1998;18:60-64
69. Pingault V, Bondurand N, Kuhlbrodt K, Goerich D, Préhu MO, Puliti A, Legius E, Matthijs G, Amiel J, Lyonnet S, Ceccherini I, Romeo G, Smith G, Read A, Wegner M, Goossens M. SOX 10 mutations in patients with Waardenburg-Hirschsprung disease. Nature Genet 1998;18:171-173
70. Potterf SB, Furumura M, Dunn J, Arnheiter H. Regulation of MITF gene expression by SOX10. Pigment Cell Res 1999;Suppl 7:46
71. Sakai C, Ollmann M, Kobayashi T, Abdel-Malek Z, Muller J, Vieira WD, Imokawa G, Barsh GS, Hearing VJ. Modulation of murine melanocyte function in vitro by agouti signal protein. EMBO J 1997;16:3544-3552
72. Aberdam E, Bertolotto C, Sviderskaya EV, de Thillot V, Hemesath TJ, Fisher DE, Bennett DC, Ortonne J-P, Ballotti R. Involvement of microphthalmia in the inhibition of melanocyte lineage differentiation and of melanogenesis by agouti signal protein. J Biol Chem 1998;273:19560-19565
73. Furumura M, Sakai C, Potterf SB, Vieira WD, Barsh GS, Hearing VJ. Characterization of genes modulated during pheomelanogenesis using differential display. Proc Natl Acad Sci USA 1998;95:7374-7378
74. Furumura M, Potterf SB, Kazumoto T, Matzunaga J, Hearing VJ. Involvement of ubiquitinous transcription factors (ITF2 and E2A) in the regulation of melanogenic gene expression. Pigment Cell Res 1999;Suppl 7:32
75. Kimura K, Hattori S, Kabuyama Y, Shizawa Y, Takayanagi J, Nakamura S, Toki S, Matsuda Y, Onodera K, Fukui Y. Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase. J Biol Chem 1994;269:18961-18967
76. S6-kinase pathway induces B16 melanoma cell differentiation. J Biol Chem 1996;271:31824-31830
77. Buscà R, Bertolotto C, Abbe P, Englaro W, Ishizaki T, Narumiya S, Boquet P, Ortonne J-P, Ballotti R. Inhibition of Rho is required for cAMP-induced melanoma cell differentiation. Mol Biol Cell 1998;9:1367-1378
78. Ridley AJ, Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and stress fibers in response to growth factors. Cell 1992;70:389-399
79. Robinson MJ, Cobb MH. Mitogen-activated protein kinase pathways. Curr Opin Cell Biol 1997;9:180-186
80. Morrison DK, Cutler Jr RE. The Complexity of Raf-1 Regulation. Curr Opin Cell Biol 1997;9:174-179
81. Buscà R, Abbe P, Mantoux F, Aberdam E, Eychene A, Ortonne J-P, Ballotti R. B-Raf mediates the cAMP activation of MAPK in B16 melanoma cells. Pigment Cell Res 1999;Suppl 7:106
82. Frodin M, Peraldi P, Van Obberghen E. Cyclic AMP activates the mitogen-activated protein kinase cascade in PC12 cells. J Biol Chem 1994;269:6207-6214
83. Fleischman RA, Saltman D, Stastny V, Zneimer S. Deletion of the c-kit proto-oncogene in human developmental defect piebald trait. Proc Natl Acad Sci USA 1991;88:10885-10889
84. Hemesath TJ, Price ER, Takemoto C, Badalian T, Fisher DE. MAPK links microphthalmia to c-kit signaling in melanocytes. Nature 1998;391:298-301
85. Price ER, Ding HF, Badalian T, Bhattacharya S, Takemoto C, Yao TP. Lineage-specific signaling in melanocytes. C-kit stimulation recruits p300/CBP to microphthalmia. J Biol Chem 1998;273:17983-17986
86. Englaro W, Bertolotto C, Busca R, Brunet A, Pages G, Ortonne J-P, Ballotti R. Inhibition of the mitogen-activated protein kinase pathway triggers B16 melanoma cells differentiation. J Biol Chem 1998;273:1-5
87. Xu W, Gong L, Haddad MM, Bischof O, Campisi J, Yeh E, Medrano E. Regulation of microphthalmia-associated transcription factor MITF protein levels by association with the human ubiquitin-conjugating enzyme hUBC9. Pigment Cell Res 1999;Suppl 7:31