The pleiotropic roles of autophagy regulators in melanogenesis

Pigment Cell and Melanoma Research

Volumn 24, Issue 4, 2011, Pages 595-604

  Ho, Hsiang ^a   Ganesan, Anand K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Autophagy; Melanoma; Melanosome

Indexed keywords

MELANIN;

ARTICLE; AUTOPHAGY; BIOGENESIS; CELL MIGRATION; CELL ORGANELLE; EYE PROTECTION; FUNCTIONAL GENOMICS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LYSOSOME; MELANOGENESIS; MELANOSOME; NONHUMAN; PLEIOTROPY; PROTEIN SYNTHESIS; SKIN PROTECTION; STARVATION;

ANIMALS; AUTOPHAGY; BIOLOGICAL TRANSPORT; ENDOSOMES; HUMANS; MELANINS; MELANOSOMES; SIGNAL TRANSDUCTION;

MUS;

EID: 81155159651     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/j.1755-148X.2011.00889.x     Document Type: Article

References (93)

1. Abrahamsen, H., and Stenmark, H. (2010). Protein secretion: unconventional exit by exophagy. Curr. Biol. 20, R415-R418.
2. Bellei, B., Flori, E., Izzo, E., Maresca, V., and Picardo, M. (2008). GSK3beta inhibition promotes melanogenesis in mouse B16 melanoma cells and normal human melanocytes. Cell. Signal. 20, 1750-1761.
3. Bennett, D.C., and Lamoreux, M.L. (2003). The color loci of mice - a genetic century. Pigment Cell Res. 16, 333-344.
4. Berson, J.F., Theos, A.C., Harper, D.C., Tenza, D., Raposo, G., and Marks, M.S. (2003). Proprotein convertase cleavage liberates a fibrillogenic fragment of a resident glycoprotein to initiate melanosome biogenesis. J. Cell Biol. 161, 521-533.
5. Bodemann, B.O., Orvedahl, A., Cheng, T. et al. (2011). RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly. Cell 144, 253-267.
6. Boissy, R.E., Smyth, J.R. Jr, and Fite, K.V. (1983). Progressive cytologic changes during the development of delayed feather amelanosis and associated choroidal defects in the DAM chicken line. A vitiligo model. Am. J. Pathol. 111, 197-212.
7. Boissy, R.E., Moellmann, G., Trainer, A.T., Smyth, J.R. Jr, and Lerner, A.B. (1986). Delayed-amelanotic (DAM or Smyth) chicken: melanocyte dysfunction in vivo and in vitro. J. Invest. Dermatol. 86, 149-156.
8. Boissy, R.E., Beato, K.E., and Nordlund, J.J. (1991a). Dilated rough endoplasmic reticulum and premature death in melanocytes cultured from the vitiligo mouse. Am. J. Pathol. 138, 1511-1525.
9. Boissy, R.E., Liu, Y.Y., Medrano, E.E., and Nordlund, J.J. (1991b). Structural aberration of the rough endoplasmic reticulum and melanosome compartmentalization in long-term cultures of melanocytes from vitiligo patients. J. Invest. Dermatol. 97, 395-404.
10. Bomirski, A., Wrzolkowa, T., Arendarczyk, M., Bomirska, M., Kuklinska, E., Slominski, A., and Moellmann, G. (1987). Pathology and ultrastructural characteristics of a hypomelanotic variant of transplantable hamster melanoma with elevated tyrosinase activity. J. Invest. Dermatol. 89, 469-473.
11. Busca, R., Bertolotto, C., Ortonne, J.P., and Ballotti, R. (1996). Inhibition of the phosphatidylinositol 3-kinase/p70(S6)-kinase pathway induces B16 melanoma cell differentiation. J. Biol. Chem. 271, 31824-31830.
12. Cheli, Y., Ohanna, M., Ballotti, R., and Bertolotto, C. (2010). Fifteen-year quest for microphthalmia-associated transcription factor target genes. Pigment Cell Melanoma Res. 23, 27-40.
13. Chow, C.Y., Zhang, Y., Dowling, J.J. et al. (2007). Mutation of FIG 4 causes neurodegeneration in the pale tremor mouse and patients with CMT4J. Nature 448, 68-72.
14. Costin, G.E., and Hearing, V.J. (2007). Human skin pigmentation: melanocytes modulate skin color in response to stress. FASEB J. 21, 976-994.
15. Dove, S.K., Piper, R.C., Mcewen, R.K. et al. (2004). Svp1p defines a family of phosphatidylinositol 3, 5-bisphosphate effectors. EMBO J. 23, 1922-1933.
16. 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.
17. Efe, J.A., Botelho, R.J., and Emr, S.D. (2007). Atg18 regulates organelle morphology and Fab1 kinase activity independent of its membrane recruitment by phosphatidylinositol 3, 5-bisphosphate. Mol. Biol. Cell 18, 4232-4244.
18. Fader, C.M., and Colombo, M.I. (2009). Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ. 16, 70-78.
19. Ferguson, C.J., Lenk, G.M., and Meisler, M.H. (2009). Defective autophagy in neurons and astrocytes from mice deficient in PI(3, 5)P2. Hum. Mol. Genet. 18, 4868-4878.
20. Ferguson, C.J., Lenk, G.M., and Meisler, M.H. (2010). PtdIns(3, 5)P2 and autophagy in mouse models of neurodegeneration. Autophagy 6, 170-171.
21. Funderburk, S.F., Wang, Q.J., and Yue, Z. (2010). The Beclin 1-VPS34 complex - at the crossroads of autophagy and beyond. Trends Cell Biol. 20, 355-362.
22. Ganesan, A.K., Ho, H., Bodemann, B. et al. (2008). Genome-wide siRNA-based functional genomics of pigmentation identifies novel genes and pathways that impact melanogenesis in human cells. PLoS Genet. 4, e1000298.
23. Ganley, I.G., Lam Du, H., Wang, J., Ding, X., Chen, S., and Jiang, X. (2009). ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J. Biol. Chem. 284, 12297-12305.
24. Gautam, R., Novak, E.K., Tan, J., Wakamatsu, K., Ito, S., and Swank, R.T. (2006). Interaction of Hermansky-Pudlak Syndrome genes in the regulation of lysosome-related organelles. Traffic 7, 779-792.
25. Grasso, D., Ropolo, A., Lo Re, A., Boggio, V., Molejon, M.I., Iovanna, J.L., Gonzalez, C.D., Urrutia, R., and Vaccaro, M.I. (2011). Zymophagy, a novel selective autophagy pathway mediated by VMP1-USP9x-p62, prevents pancreatic cell death. J. Biol. Chem. 286, 8308-8324.
26. Grimes, P., Nordlund, J.J., Pandya, A.G., Taylor, S., Rendon, M., and Ortonne, J.P. (2006). Increasing our understanding of pigmentary disorders. J. Am. Acad. Dermatol. 54, S255-S261.
27. Guan, J., Stromhaug, P.E., George, M.D., Habibzadegah-Tari, P., Bevan, A., Dunn, W.A. Jr, and Klionsky, D.J. (2001). Cvt18/Gsa12 is required for cytoplasm-to-vacuole transport, pexophagy, and autophagy in Saccharomyces cerevisiae and Pichia pastoris. Mol. Biol. Cell 12, 3821-3838.
28. He, B., and Guo, W. (2009). The exocyst complex in polarized exocytosis. Curr. Opin. Cell Biol. 21, 537-542.
29. Hearing, V.J. (2005). Biogenesis of pigment granules: a sensitive way to regulate melanocyte function. J. Dermatol. Sci. 37, 3-14.
30. Ho, H., Kapadia, R., Al-Tahan, S., Ahmad, S., and Ganesan, A.K. (2011). WIPI1 coordinates melanogenic gene transcription and melanosome formation via TORC1 inhibition. J. Biol. Chem. 286, 12509-12523.
31. Hoashi, T., Watabe, H., Muller, J., Yamaguchi, Y., Vieira, W.D., and Hearing, V.J. (2005). MART-1 is required for the function of the melanosomal matrix protein PMEL17/GP100 and the maturation of melanosomes. J. Biol. Chem. 280, 14006-14016.
32. Hoekstra, H.E. (2006). Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 97, 222-234.
33. Huang, J., and Klionsky, D.J. (2007). Autophagy and human disease. Cell cycle 6, 1837-1849.
34. Huizing, M., Boissy, R.E., and Gahl, W.A. (2002). Hermansky-Pudlak syndrome: vesicle formation from yeast to man. Pigment Cell Res. 15, 405-419.
35. Hurbain, I., Geerts, W.J., Boudier, T., Marco, S., Verkleij, A.J., Marks, M.S., and Raposo, G. (2008). Electron tomography of early melanosomes: implications for melanogenesis and the generation of fibrillar amyloid sheets. Proc. Natl. Acad. Sci. U S A 105, 19726-19731.
36. Inoki, K., Corradetti, M.N., and Guan, K.L. (2005). Dysregulation of the TSC-mTOR pathway in human disease. Nat. Genet. 37, 19-24.
37. Jeffries, T.R., Dove, S.K., Michell, R.H., and Parker, P.J. (2004). PtdIns-specific MPR pathway association of a novel WD40 repeat protein, WIPI49. Mol. Biol. Cell 15, 2652-2663.
38. Jeong, T.J., Shin, M.K., Uhm, Y.K., Kim, H.J., Chung, J.H., and Lee, M.H. (2010). Association of UVRAG polymorphisms with susceptibility to non-segmental vitiligo in a Korean sample. Exp. Dermatol. 19, e323-e325.
39. Jimbow, K., Fitzpatrick, T.B., Szabo, G., and Hori, Y. (1975). Congenital circumscribed hypomelanosis: a characterization based on electron microscopic study of tuberous sclerosis, nevus depigmentosus, and piebaldism. J. Invest. Dermatol. 64, 50-62.
40. Jin, N., Chow, C.Y., Liu, L. et al. (2008). VAC14 nucleates a protein complex essential for the acute interconversion of PI3P and PI(3, 5)P(2) in yeast and mouse. EMBO J. 27, 3221-3234.
41. Jin, Y., Birlea, S.A., Fain, P.R. et al. (2010). Variant of TYR and autoimmunity susceptibility loci in generalized vitiligo. N. Engl. J. Med. 362, 1686-1697.
42. Jung, C.H., Jun, C.B., Ro, S.H., Kim, Y.M., Otto, N.M., Cao, J., Kundu, M., and Kim, D.H. (2009). ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell 20, 1992-2003.
43. Kang, R., Zeh, H.J., Lotze, M.T., and Tang, D. (2011). The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 18, 571-580.
44. Klionsky, D.J., Abeliovich, H., Agostinis, P. et al. (2008). Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-175.
45. Kwiatkowski, D.J. (2003). Rhebbing up mTOR: new insights on TSC1 and TSC2, and the pathogenesis of tuberous sclerosis. Cancer Biol. Ther. 2, 471-476.
46. Larue, L., Kumasaka, M., and Goding, C.R. (2003). Beta-catenin in the melanocyte lineage. Pigment Cell Res. 16, 312-317.
47. Lazova, R., and Pawelek, J.M. (2009). Why do melanomas get so dark? Exp. Dermatol. 18, 934-938.
48. Lazova, R., Klump, V., and Pawelek, J. (2010). Autophagy in cutaneous malignant melanoma. J. Cutan. Pathol. 37, 256-258.
49. Levine, B., and Kroemer, G. (2008). Autophagy in the pathogenesis of disease. Cell 132, 27-42.
50. Levy, C., Khaled, M., and Fisher, D.E. (2006). MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol. Med. 12, 406-414.
51. Liang, C., Lee, J.S., Inn, K.S. et al. (2008). Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat. Cell Biol. 10, 776-787.
52. Marino, G., Fernandez, A.F., Cabrera, S. et al. (2010). Autophagy is essential for mouse sense of balance. J. Clin. Invest. 120, 2331-2344.
53. Matsunaga, K., Noda, T., and Yoshimori, T. (2009). Binding Rubicon to cross the Rubicon. Autophagy 5, 876-877.
54. Meijer, A.J., and Codogno, P. (2011). Autophagy: regulation by energy sensing. Curr. Biol. 21, R227-R229.
55. Meyskens, F.L. Jr, Farmer, P., and Fruehauf, J.P. (2001). Redox regulation in human melanocytes and melanoma. Pigment Cell Res. 14, 148-154.
56. Miracco, C., Cevenini, G., Franchi, A. et al. (2010). Beclin 1 and LC3 autophagic gene expression in cutaneous melanocytic lesions. Hum. Pathol. 41, 503-512.
57. Mizushima, N. (2010). The role of the Atg1/ULK1 complex in autophagy regulation. Curr. Opin. Cell Biol. 22, 132-139.
58. Mizushima, N., Levine, B., Cuervo, A.M., and Klionsky, D.J. (2008). Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075.
59. Murthy, M., Garza, D., Scheller, R.H., and Schwarz, T.L. (2003). Mutations in the exocyst component Sec5 disrupt neuronal membrane traffic, but neurotransmitter release persists. Neuron 37, 433-447.
60. Ni-Komatsu, L., Tong, C., Chen, G., Brindzei, N., and Orlow, S.J. (2008). Identification of quinolines that inhibit melanogenesis by altering tyrosinase family trafficking. Mol. Pharmacol. 74, 1576-1586.
61. Obara, K., and Ohsumi, Y. (2008). Dynamics and function of PtdIns(3)P in autophagy. Autophagy 4, 952-954.
62. Ohguchi, K., Banno, Y., Nakagawa, Y., Akao, Y., and Nozawa, Y. (2005). Negative regulation of melanogenesis by phospholipase D1 through mTOR/p70 S6 kinase 1 signaling in mouse B16 melanoma cells. J. Cell. Physiol. 205, 444-451.
63. Okulicz, J.F., Shah, R.S., Schwartz, R.A., and Janniger, C.K. (2003). Oculocutaneous albinism. J. Eur. Acad. Dermatol. Venereol. 17, 251-256.
64. Price, E.R., Horstmann, M.A., Wells, A.G., Weilbaecher, K.N., Takemoto, C.M., Landis, M.W., and Fisher, D.E. (1998). Alpha-Melanocyte-stimulating hormone signaling regulates expression of microphthalmia, a gene deficient in Waardenburg syndrome. J. Biol. Chem. 273, 33042-33047.
65. Proikas-Cezanne, T., and Pfisterer, S.G. (2009). Assessing mammalian autophagy by WIPI-1/Atg18 puncta formation. Methods Enzymol. 452, 247-260.
66. Proikas-Cezanne, T., Waddell, S., Gaugel, A., Frickey, T., Lupas, A., and Nordheim, A. (2004). WIPI-1alpha (WIPI49), a member of the novel 7-bladed WIPI protein family, is aberrantly expressed in human cancer and is linked to starvation-induced autophagy. Oncogene 23, 9314-9325.
67. Proikas-Cezanne, T., Ruckerbauer, S., Stierhof, Y.D., Berg, C., and Nordheim, A. (2007). Human WIPI-1 puncta-formation: a novel assay to assess mammalian autophagy. FEBS Lett. 581, 3396-3404.
68. Raposo, G., and Marks, M.S. (2007). Melanosomes - dark organelles enlighten endosomal membrane transport. Nat. Rev. Mol. Cell Biol. 8, 786-797.
69. Raposo, G., Tenza, D., Murphy, D.M., Berson, J.F., and Marks, M.S. (2001). Distinct protein sorting and localization to premelanosomes, melanosomes, and lysosomes in pigmented melanocytic cells. J. Cell Biol. 152, 809-824.
70. Razi, M., Chan, E.Y., and Tooze, S.A. (2009). Early endosomes and endosomal coatomer are required for autophagy. J. Cell Biol. 185, 305-321.
71. Reggiori, F., Tucker, K.A., Stromhaug, P.E., and Klionsky, D.J. (2004). The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev. Cell 6, 79-90.
72. Rutherford, A.C., Traer, C., Wassmer, T., Pattni, K., Bujny, M.V., Carlton, J.G., Stenmark, H., and Cullen, P.J. (2006). The mammalian phosphatidylinositol 3-phosphate 5-kinase (PIKfyve) regulates endosome-to-TGN retrograde transport. J. Cell Sci. 119, 3944-3957.
73. Sakai, Y., Oku, M., Van Der Klei, I.J., and Kiel, J.A. (2006). Pexophagy: autophagic degradation of peroxisomes. Biochim. Biophys. Acta 1763, 1767-1775.
74. Sarangarajan, R., and Apte, S.P. (2005). Melanization and phagocytosis: implications for age related macular degeneration. Mol. Vis. 11, 482-490.
75. Shotelersuk, V., and Gahl, W.A. (1998). Hermansky-Pudlak syndrome: models for intracellular vesicle formation. Mol. Genet. Metab. 65, 85-96.
76. Slominski, A., Tobin, D.J., Shibahara, S., and Wortsman, J. (2004). Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol. Rev. 84, 1155-1228.
77. Smith, J.W., Koshoffer, A., Morris, R.E., and Boissy, R.E. (2005). Membranous complexes characteristic of melanocytes derived from patients with Hermansky-Pudlak syndrome type 1 are macroautophagosomal entities of the lysosomal compartment. Pigment Cell Res. (Sponsored by the European Society for Pigment Cell Research and the International Pigment Cell Society) 18, 417-426.
78. Stein, W.D. (1955). Ultra-violet absorption investigation of melanins. Nature 175, 472.
79. Steingrimsson, E., Copeland, N.G., and Jenkins, N.A. (2004). Melanocytes and the microphthalmia transcription factor network. Annu. Rev. Genet. 38, 365-411.
80. Sturm, R.A. (2009). Molecular genetics of human pigmentation diversity. Hum. Mol. Genet. 18, R9-R17.
81. Suzuki, K., Kirisako, T., Kamada, Y., Mizushima, N., Noda, T., and Ohsumi, Y. (2001). The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 20, 5971-5981.
82. Tanida, I. (2011). Autophagy basics. Microbiol. Immunol. 55, 1-11.
83. Tanida, I., Ueno, T., and Kominami, E. (2004). LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 36, 2503-2518.
84. Theos, A.C., Truschel, S.T., Raposo, G., and Marks, M.S. (2005). The Silver locus product Pmel17/gp100/Silv/ME20: controversial in name and in function. Pigment Cell Res. 18, 322-336.
85. Truschel, S.T., Simoes, S., Setty, S.R. et al. (2009). ESCRT-I function is required for Tyrp1 transport from early endosomes to the melanosome limiting membrane. Traffic 10, 1318-1336.
86. Van Den Boorn, J.G., Picavet, D.I., Van Swieten, P.F. et al. (2011). Skin-depigmenting agent monobenzone induces potent t-cell autoimmunity toward pigmented cells by tyrosinase haptenation and melanosome autophagy. J. Invest. Dermatol. 131, 1240-1245.
87. Wasmeier, C., Hume, A.N., Bolasco, G., and Seabra, M.C. (2008). Melanosomes at a glance. J. Cell Sci. 121, 3995-3999.
88. Xie, Z., and Klionsky, D.J. (2007). Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9, 1102-1109.
89. Yamaguchi, Y., and Hearing, V.J. (2009). Physiological factors that regulate skin pigmentation. Biofactors 35, 193-199.
90. Yamaguchi, Y., Brenner, M., and Hearing, V.J. (2007). The regulation of skin pigmentation. J. Biol. Chem. 282, 27557-27561.
91. Yorimitsu, T., and Klionsky, D.J. (2005). Autophagy: molecular machinery for self-eating. Cell Death Differ. 12(Suppl 2), 1542-1552.
92. Zecca, L., Zucca, F.A., Albertini, A., Rizzio, E., and Fariello, R.G. (2006). A proposed dual role of neuromelanin in the pathogenesis of Parkinson's disease. Neurology 67, S8-S11.
93. Zhong, Y., Wang, Q.J., Li, X., Yan, Y., Backer, J.M., Chait, B.T., Heintz, N., and Yue, Z. (2009). Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat. Cell Biol. 11, 468-476.