Bcl-2 family members: Essential players in skin cancer

Cancer Letters

Volumn 320, Issue 1, 2012, Pages 1-13

  Nys, Kris ^a   Agostinis, Patrizia ^a  

^a LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

Author keywords

Apoptosis; Bcl 2 family; Skin; Skin cancer; UVB

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; ANTINEOPLASTIC AGENT; BH3 PROTEIN; BORTEZOMIB; CARBOPLATIN; DACARBAZINE; DOCETAXEL; HEAT SHOCK PROTEIN 90; OBLIMERSEN; PACLITAXEL; PROTEIN BCL 2; PROTEIN MCL 1; TEMOZOLOMIDE; TW 37; UNCLASSIFIED DRUG;

APOPTOSIS; BLOOD TOXICITY; CANCER THERAPY; CUTANEOUS MALIGNANT MELANOMA; DRUG POTENTIATION; DRUG TARGETING; EPIDERMIS; HUMAN; HYPOXIA; KERATINOCYTE; MELANOCYTE; MELANOMA; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; SHORT SURVEY; SKIN CANCER; SKIN CARCINOGENESIS; SQUAMOUS CELL CARCINOMA; SUNBURN; TUMOR MICROENVIRONMENT; ULTRAVIOLET B RADIATION;

EID: 84859213556     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.01.031     Document Type: Review

References (158)

1. Lippens S., Denecker G., Ovaere P., Vandenabeele P., Declercq W. Death penalty for keratinocytes: apoptosis versus cornification. Cell Death Differ. 2005, 12(Suppl 2):1497-1508.
2. Houben E., De P.K., Rogiers V. A keratinocyte's course of life. Skin Pharmacol. Physiol 2007, 20:122-132.
3. Ernfors P. Cellular origin and developmental mechanisms during the formation of skin melanocytes. Exp. Cell Res. 2010, 316:1397-1407.
4. de Gruijl F.R., van Kranen H.J., Mullenders L.H. UV-induced DNA damage, repair, mutations and oncogenic pathways in skin cancer. J. Photochem. Photobiol. B 2001, 63:19-27.
5. Armstrong B.K., Kricker A. The epidemiology of UV induced skin cancer. J. Photochem. Photobiol. B 2001, 63:8-18.
6. Afaq F., Adhami V.M., Mukhtar H. Photochemoprevention of ultraviolet B signaling and photocarcinogenesis. Mutat. Res. 2005, 571:153-173.
7. Assefa Z., Van L.A., Garmyn M., Agostinis P. Ultraviolet radiation-induced apoptosis in keratinocytes: on the role of cytosolic factors. Biochim. Biophys. Acta 2005, 1755:90-106.
8. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
9. Lavrik I., Golks A., Krammer P.H. Death receptor signaling. J. Cell Sci. 2005, 118:265-267.
10. Green D.R. Apoptotic pathways: ten minutes to dead. Cell 2005, 121:671-674.
11. Garrido C., Galluzzi L., Brunet M., Puig P.E., Didelot C., Kroemer G. Mechanisms of cytochrome c release from mitochondria. Cell Death Differ. 2006, 13:1423-1433.
12. Tait S.W., Green D.R. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 2010, 11:621-632.
13. Sitailo L.A., Jerome-Morais A., Denning M.F. Mcl-1 functions as major epidermal survival protein required for proper keratinocyte differentiation. J. Invest. Dermatol. 2009, 129:1351-1360.
14. Motoyama N., Wang F., Roth K.A., Sawa H., Nakayama K., Nakayama K., Negishi I., Senju S., Zhang Q., Fujii S. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 1995, 267:1506-1510.
15. Rinkenberger J.L., Horning S., Klocke B., Roth K., Korsmeyer S.J. Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev. 2000, 14:23-27.
16. Kozopas K.M., Yang T., Buchan H.L., Zhou P., Craig R.W. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc. Natl. Acad. Sci. USA 1993, 90:3516-3520.
17. Pena J.C., Fuchs E., Thompson C.B. Bcl-x expression influences keratinocyte cell survival but not terminal differentiation. Cell Growth Differ. 1997, 8:619-629.
18. Zuliani T., Obriot H., Tual M., Lachman-Weber N., Dumas M., Formstecher P., Polakowska R., Ratinaud M.H. Variable Bax antigenicity is linked to keratinocyte position within epidermal strata and UV-induced apoptosis. Exp. Dermatol. 2008, 17:125-132.
19. Levy C., Khaled M., Fisher D.E. MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol. Med. 2006, 12:406-414.
20. Vachtenheim J., Borovansky J. "Transcription physiology" of pigment formation in melanocytes: central role of MITF. Exp. Dermatol. 2010, 19:617-627.
21. Hornyak T.J., Hayes D.J., Chiu L.Y., Ziff E.B. Transcription factors in melanocyte development: distinct roles for Pax-3 and Mitf. Mech. Dev. 2001, 101:47-59.
22. McGill G.G., Horstmann M., Widlund H.R., Du J., Motyckova G., Nishimura E.K., Lin Y.L., Ramaswamy S., Avery W., Ding H.F., Jordan S.A., Jackson I.J., Korsmeyer S.J., Golub T.R., Fisher D.E. Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell 2002, 109:707-718.
23. Veis D.J., Sorenson C.M., Shutter J.R., Korsmeyer S.J. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 1993, 75:229-240.
24. Nishimura E.K., Granter S.R., Fisher D.E. Mechanisms of hair graying: incomplete melanocyte stem cell maintenance in the niche. Science 2005, 307:720-724.
25. Hoek K.S., Goding C.R. Cancer stem cells versus phenotype-switching in melanoma. Pigm. Cell Melanoma Res. 2010, 23:746-759.
26. Herrlich P., Karin M., Weiss C. Supreme EnLIGHTenment: damage recognition and signaling in the mammalian UV response. Mol. Cell 2008, 29:279-290.
27. Kvam E., Tyrrell R.M. Induction of oxidative DNA base damage in human skin cells by UV and near visible radiation. Carcinogenesis 1997, 18:2379-2384.
28. Gross S., Knebel A., Tenev T., Neininger A., Gaestel M., Herrlich P., Bohmer F.D. Inactivation of protein-tyrosine phosphatases as mechanism of UV-induced signal transduction. J. Biol. Chem. 1999, 274:26378-26386.
29. Wang H., Kochevar I.E. Involvement of UVB-induced reactive oxygen species in TGF-beta biosynthesis and activation in keratinocytes. Free Radic. Biol. Med. 2005, 38:890-897.
30. Grossman D., Kim P.J., Blanc-Brude O.P., Brash D.E., Tognin S., Marchisio P.C., Altieri D.C. Transgenic expression of survivin in keratinocytes counteracts UVB-induced apoptosis and cooperates with loss of p53. J. Clin. Invest. 2001, 108:991-999.
31. Sitailo L.A., Tibudan S.S., Denning M.F. Activation of caspase-9 is required for UV-induced apoptosis of human keratinocytes. J. Biol. Chem. 2002, 277:19346-19352.
32. Bivik C.A., Larsson P.K., Kagedal K.M., Rosdahl I.K., Ollinger K.M. UVA/B-induced apoptosis in human melanocytes involves translocation of cathepsins and Bcl-2 family members. J. Invest. Dermatol. 2006, 126:1119-1127.
33. Bivik C., Rosdahl I., Ollinger K. Hsp70 protects against UVB induced apoptosis by preventing release of cathepsins and cytochrome c in human melanocytes. Carcinogenesis 2007, 28:537-544.
34. Rodriguez-Villanueva J., Greenhalgh D., Wang X.J., Bundman D., Cho S., Delehedde M., Roop D., McDonnell T.J. Human keratin-1. bcl-2 transgenic mice aberrantly express keratin 6, exhibit reduced sensitivity to keratinocyte cell death induction, and are susceptible to skin tumor formation. Oncogene 1998, 16:853-863.
35. Jost M., Gasparro F.P., Jensen P.J., Rodeck U. Keratinocyte apoptosis induced by ultraviolet B radiation and CD95 ligation - differential protection through epidermal growth factor receptor activation and Bcl-x(L) expression. J. Invest Dermatol. 2001, 116:860-866.
36. Takahashi H., Honma M., Ishida-Yamamoto A., Namikawa K., Miwa A., Okado H., Kiyama H., Iizuka H. In vitro and in vivo transfer of bcl-2 gene into keratinocytes suppresses UVB-induced apoptosis. Photochem. Photobiol. 2001, 74:579-586.
37. Assefa Z., Garmyn M., Vantieghem A., Declercq W., Vandenabeele P., Vandenheede J.R., Agostinis P. Ultraviolet B radiation-induced apoptosis in human keratinocytes: cytosolic activation of procaspase-8 and the role of Bcl-2. FEBS Lett. 2003, 540:125-132.
38. Naik E., Michalak E.M., Villunger A., Adams J.M., Strasser A. Ultraviolet radiation triggers apoptosis of fibroblasts and skin keratinocytes mainly via the BH3-only protein Noxa. J. Cell Biol. 2007, 176:415-424.
39. Knezevic D., Zhang W., Rochette P.J., Brash D.E. Bcl-2 is the target of a UV-inducible apoptosis switch and a node for UV signaling. Proc. Natl. Acad. Sci. USA 2007, 104:11286-11291.
40. Delehedde M., Cho S.H., Hamm R., Brisbay S., Ananthaswamy H.N., Kripke M., McDonnell T.J. Impact of Bcl-2 and Ha-ras on keratinocytes in organotypic culture. J. Invest. Dermatol. 2001, 116:366-373.
41. Taylor J.K., Zhang Q.Q., Monia B.P., Marcusson E.G., Dean N.M. Inhibition of Bcl-xL expression sensitizes normal human keratinocytes and epithelial cells to apoptotic stimuli. Oncogene 1999, 18:4495-4504.
42. Ren H., Fu K., Wang D., Mu C., Wang G. Oxidized DJ-1 interacts with the mitochondrial protein BCL-XL. J. Biol. Chem. 2011, 286:35308-35317.
43. Ploner C., Kofler R., Villunger A. Noxa: at the tip of the balance between life and death. Oncogene 2008, 27(Suppl. 1):S84-S92.
44. Nijhawan D., Fang M., Traer E., Zhong Q., Gao W., Du F., Wang X. Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev. 2003, 17:1475-1486.
45. Nys K., Van Laethem A., Michiels C., Rubio N., Piette J.G., Garmyn M., Agostinis P. A p38(MAPK)/HIF-1 pathway initiated by UVB irradiation is required to induce Noxa and apoptosis of human keratinocytes. J. Invest. Dermatol. 2010, 130:2269-2276.
46. Nakamura S., Takahashi H., Kinouchi M., Manabe A., Ishida-Yamamoto A., Hashimoto Y., Iizuka H. Differential phosphorylation of mitogen-activated protein kinase families by epidermal growth factor and ultraviolet B irradiation in SV40-transformed human keratinocytes. J. Dermatol. Sci. 2001, 25:139-149.
47. Van Laethem A., Nys K., Van Kelst S., Claerhout S., Ichijo H., Vandenheede J.R., Garmyn M., Agostinis P. Apoptosis signal regulating kinase-1 connects reactive oxygen species to p38 MAPK-induced mitochondrial apoptosis in UVB-irradiated human keratinocytes. Free Radical Biol. Med. 2006, 41:1361-1371.
48. Wu X., Deng Y. Bax and BH3-domain-only proteins in p53-mediated apoptosis. Front Biosci. 2002, 7:d151-d156.
49. Moll U.M., Wolff S., Speidel D., Deppert W. Transcription-independent pro-apoptotic functions of p53. Curr. Opin. Cell Biol. 2005, 17:631-636.
50. McKay B.C., Chen F., Perumalswami C.R., Zhang F., Ljungman M. The tumor suppressor p53 can both stimulate and inhibit ultraviolet light-induced apoptosis. Mol. Biol. Cell 2000, 11:2543-2551.
51. Brash D.E., Ziegler A., Jonason A.S., Simon J.A., Kunala S., Leffell D.J. Sunlight and sunburn in human skin cancer: p53, apoptosis, and tumor promotion. J. Invest. Dermatol. Symp. Proc. 1996, 1:136-142.
52. Chaturvedi V., Sitailo L.A., Qin J.Z., Bodner B., Denning M.F., Curry J., Zhang W., Brash D., Nickoloff B.J. Knockdown of p53 levels in human keratinocytes accelerates Mcl-1 and Bcl-x(L) reduction thereby enhancing UV-light induced apoptosis. Oncogene 2005, 24:5299-5312.
53. Zhang L., Hu J.J., Gong F. MG132 inhibition of proteasome blocks high-dose UV irradiation-induced apoptosis. Cell Cycle 2011, 10:3515-3518.
54. Wan Y.S., Wang Z.Q., Shao Y., Voorhees J.J., Fisher G.J. Ultraviolet irradiation activates PI 3-kinase/AKT survival pathway via EGF receptors in human skin in vivo. Int. J. Oncol. 2001, 18:461-466.
55. Ming M., Han W., Maddox J., Soltani K., Shea C.R., Freeman D.M., He Y.Y. UVB-induced ERK/AKT-dependent PTEN suppression promotes survival of epidermal keratinocytes. Oncogene 2010, 29:492-502.
56. Claerhout S., Decraene D., Van L.A., Van K.S., Agostinis P., Garmyn M. AKT delays the early-activated apoptotic pathway in UVB-irradiated keratinocytes via BAD translocation. J. Invest. Dermatol. 2007, 127:429-438.
57. Umeda J., Sano S., Kogawa K., Motoyama N., Yoshikawa K., Itami S., Kondoh G., Watanabe T., Takeda J. In vivo cooperation between Bcl-xL and the phosphoinositide 3-kinase-Akt signaling pathway for the protection of epidermal keratinocytes from apoptosis. FASEB J. 2003, 17:610-620.
58. Gillardon F., Moll I., Meyer M., Michaelidis T.M. Alterations in cell death and cell cycle progression in the UV-irradiated epidermis of bcl-2-deficient mice. Cell Death Differ. 1999, 6:55-60.
59. Bivik C., Ollinger K. JNK mediates UVB-induced apoptosis upstream lysosomal membrane permeabilization and Bcl-2 family proteins. Apoptosis 2008, 13:1111-1120.
60. Cirman T., Oresic K., Mazovec G.D., Turk V., Reed J.C., Myers R.M., Salvesen G.S., Turk B. Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J. Biol. Chem. 2004, 279:3578-3587.
61. Heinrich M., Neumeyer J., Jakob M., Hallas C., Tchikov V., Winoto-Morbach S., Wickel M., Schneider-Brachert W., Trauzold A., Hethke A., Schutze S. Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and -3 activation. Cell Death Differ. 2004, 11:550-563.
62. Bhoumik A., Ivanov V., Ronai Z. Activating transcription factor 2-derived peptides alter resistance of human tumor cell lines to ultraviolet irradiation and chemical treatment. Clin. Cancer Res. 2001, 7:331-342.
63. Mizutani Y., Hayashi N., Kawashima M., Imokawa G. A single UVB exposure increases the expression of functional KIT in human melanocytes by up-regulating MITF expression through the phosphorylation of p38/CREB. Arch. Dermatol. Res. 2010, 302:283-294.
64. Hornyak T.J., Jiang S., Guzman E.A., Scissors B.N., Tuchinda C., He H., Neville J.D., Strickland F.M. Mitf dosage as a primary determinant of melanocyte survival after ultraviolet irradiation. Pigm. Cell Melanoma Res. 2009, 22:307-318.
65. Shang J., Eberle J., Geilen C.C., Hossini A.M., Fecker L.F., Orfanos C.E., Tebbe B. The role of nuclear factor-kappa B and melanogenesis in tumor necrosis factor-alpha-induced apoptosis of normal human melanocytes. Skin Pharmacol. Appl. Skin Physiol. 2002, 15:321-329.
66. Terzian T., Torchia E.C., Dai D., Robinson S.E., Murao K., Stiegmann R.A., Gonzalez V., Boyle G.M., Powell M.B., Pollock P.M., Lozano G., Robinson W.A., Roop D.R., Box N.F. P53 prevents progression of nevi to melanoma predominantly through cell cycle regulation. Pigm. Cell Melanoma Res. 2010, 23:781-794.
67. Waster P.K., Ollinger K.M. Redox-dependent translocation of p53 to mitochondria or nucleus in human melanocytes after UVA- and UVB-induced apoptosis. J. Invest. Dermatol. 2009, 129:1769-1781.
68. Cui R., Widlund H.R., Feige E., Lin J.Y., Wilensky D.L., Igras V.E., D'Orazio J., Fung C.Y., Schanbacher C.F., Granter S.R., Fisher D.E. Central role of p53 in the suntan response and pathologic hyperpigmentation. Cell 2007, 128:853-864.
69. van den Oord J.J., Vandeghinste N., De L.M., De Wolf-Peeters C. Bcl-2 expression in human melanocytes and melanocytic tumors 1. Am. J. Pathol. 1994, 145:294-300.
70. Kim D.J., Kataoka K., Sano S., Connolly K., Kiguchi K., DiGiovanni J. Targeted disruption of Bcl-xL in mouse keratinocytes inhibits both UVB- and chemically induced skin carcinogenesis. Mol. Carcinog. 2009, 48:873-885.
71. Lee S., Chari N.S., Kim H.W., Wang X., Roop D.R., Cho S.H., DiGiovanni J., McDonnell T.J. Cooperation of Ha-ras and Bcl-2 during multistep skin carcinogenesis. Mol. Carcinog. 2007, 46:949-957.
72. Kim D.J., Angel J.M., Sano S., DiGiovanni J. Constitutive activation and targeted disruption of signal transducer and activator of transcription 3 (Stat3) in mouse epidermis reveal its critical role in UVB-induced skin carcinogenesis. Oncogene 2009, 28:950-960.
73. Chan K.S., Sano S., Kataoka K., Abel E., Carbajal S., Beltran L., Clifford J., Peavey M., Shen J., DiGiovanni J. Forced expression of a constitutively active form of Stat3 in mouse epidermis enhances malignant progression of skin tumors induced by two-stage carcinogenesis. Oncogene 2008, 27:1087-1094.
74. Rossiter H., Beissert S., Mayer C., Schon M.P., Wienrich B.G., Tschachler E., Kupper T.S. Targeted expression of bcl-2 to murine basal epidermal keratinocytes results in paradoxical retardation of ultraviolet- and chemical-induced tumorigenesis. Cancer Res. 2001, 61:3619-3626.
75. Schenkel J., Weiher H., Furstenberger G., Jager R. Suprabasal BCL-2 expression does not sensitize to chemically-induced skin cancer in transgenic mice. Anticancer Res. 2008, 28:2825-2829.
76. Bowen A.R., Hanks A.N., Allen S.M., Alexander A., Diedrich M.J., Grossman D. Apoptosis regulators and responses in human melanocytic and keratinocytic cells. J. Invest. Dermatol. 2003, 120:48-55.
77. Selzer E., Schlagbauer-Wadl H., Okamoto I., Pehamberger H., Potter R., Jansen B. Expression of Bcl-2 family members in human melanocytes, in melanoma metastases and in melanoma cell lines. Melanoma Res. 1998, 8:197-203.
78. Ma Y., Hendershot L.M. The role of the unfolded protein response in tumour development: friend or foe?. Nat. Rev. Cancer 2004, 4:966-977.
79. Hersey P., Zhang X.D. Adaptation to ER stress as a driver of malignancy and resistance to therapy in human melanoma. Pigm. Cell Melanoma Res. 2008, 21:358-367.
80. Dong L., Jiang C.C., Thorne R.F., Croft A., Yang F., Liu H., de Bock C.E., Hersey P., Zhang X.D. Ets-1 mediates upregulation of Mcl-1 downstream of XBP-1 in human melanoma cells upon ER stress. Oncogene 2011, 30:3716-3726.
81. Jiang C.C., Lucas K., very-Kiejda K.A., Wade M., deBock C.E., Thorne R.F., Allen J., Hersey P., Zhang X.D. Up-regulation of Mcl-1 is critical for survival of human melanoma cells upon endoplasmic reticulum stress. Cancer Res. 2008, 68:6708-6717.
82. Chen J., Zhang X., Lentz C., bi-Daoud M., Pare G.C., Yang X., Feilotter H.E., Tron V.A. miR-193b Regulates Mcl-1 in Melanoma. Am. J. Pathol. 2011, 179:2162-2168.
83. Hirobe T., Furuya R., Akiu S., Ifuku O., Fukuda M. Keratinocytes control the proliferation and differentiation of cultured epidermal melanocytes from ultraviolet radiation B-induced pigmented spots in the dorsal skin of hairless mice. Pigm. Cell Res. 2002, 15:391-399.
84. Hirobe T. Role of keratinocyte-derived factors involved in regulating the proliferation and differentiation of mammalian epidermal melanocytes. Pigm. Cell Res. 2005, 18:2-12.
85. Abdel-Malek Z.A., Kadekaro A.L., Swope V.B. Stepping up melanocytes to the challenge of UV exposure. Pigm. Cell Melanoma Res. 2010, 23:171-186.
86. Bivik C.A., Andersson E.B., Rosdahl I.K. Wavelength-specific effects on UVB-induced apoptosis in melanocytes. A study of Bcl-2/Bax expression and keratinocyte rescue effects. Melanoma Res. 2005, 15:7-13.
87. Imokawa G. Autocrine and paracrine regulation of melanocytes in human skin and in pigmentary disorders. Pigm. Cell Res. 2004, 17:96-110.
88. Kadekaro A.L., Kavanagh R., Kanto H., Terzieva S., Hauser J., Kobayashi N., Schwemberger S., Cornelius J., Babcock G., Shertzer H.G., Scott G., bdel-Malek Z.A. alpha-Melanocortin and endothelin-1 activate antiapoptotic pathways and reduce DNA damage in human melanocytes. Cancer Res. 2005, 65:4292-4299.
89. Hachiya A., Kobayashi A., Ohuchi A., Takema Y., Imokawa G. The paracrine role of stem cell factor/c-kit signaling in the activation of human melanocytes in ultraviolet-B-induced pigmentation. J. Invest. Dermatol. 2001, 116:578-586.
90. Stefanato C.M., Yaar M., Bhawan J., Phillips T.J., Kosmadaki M.G., Botchkarev V., Gilchrest B.A. Modulations of nerve growth factor and Bcl-2 in ultraviolet-irradiated human epidermis. J. Cutan. Pathol. 2003, 30:351-357.
91. Jiang X., Gurel O., Mendiaz E.A., Stearns G.W., Clogston C.L., Lu H.S., Osslund T.D., Syed R.S., Langley K.E., Hendrickson W.A. Structure of the active core of human stem cell factor and analysis of binding to its receptor kit. EMBO J. 2000, 19:3192-3203.
92. Ito M., Kawa Y., Ono H., Okura M., Baba T., Kubota Y., Nishikawa S.I., Mizoguchi M. Removal of stem cell factor or addition of monoclonal anti-c-KIT antibody induces apoptosis in murine melanocyte precursors. J. Invest. Dermatol. 1999, 112:796-801.
93. Hemesath T.J., Price E.R., Takemoto C., Badalian T., Fisher D.E. MAP kinase links the transcription factor microphthalmia to c-Kit signalling in melanocytes. Nature 1998, 391:298-301.
94. Phung B., Sun J., Schepsky A., Steingrimsson E., Ronnstrand L. C-KIT signaling depends on microphthalmia-associated transcription factor for effects on cell proliferation. PLoS One 2011, 6:e24064.
95. Kimura S., Kawakami T., Kawa Y., Soma Y., Kushimoto T., Nakamura M., Watabe H., Ooka S., Mizoguchi M. Bcl-2 reduced and fas activated by the inhibition of stem cell factor/KIT signaling in murine melanocyte precursors. J. Invest. Dermatol. 2005, 124:229-234.
96. Blume-Jensen P., Janknecht R., Hunter T. The kit receptor promotes cell survival via activation of PI 3-kinase and subsequent Akt-mediated phosphorylation of bad on Ser136. Curr. Biol. 1998, 8:779-782.
97. Zhai S., Yaar M., Doyle S.M., Gilchrest B.A. Nerve growth factor rescues pigment cells from ultraviolet-induced apoptosis by upregulating BCL-2 levels. Exp. Cell Res. 1996, 224:335-343.
98. Pincelli C., Marconi A. Autocrine nerve growth factor in human keratinocytes. J. Dermatol. Sci. 2000, 22:71-79.
99. Woodman S.E., Davies M.A. Targeting KIT in melanoma: a paradigm of molecular medicine and targeted therapeutics. Biochem. Pharmacol. 2010, 80:568-574.
100. Saldana-Caboverde A., Kos L. Roles of endothelin signaling in melanocyte development and melanoma. Pigm. Cell Melanoma Res. 2010, 23:160-170.
101. Boiko A.D., Razorenova O.V., van de R.M., Swetter S.M., Johnson D.L., Ly D.P., Butler P.D., Yang G.P., Joshua B., Kaplan M.J., Longaker M.T., Weissman I.L. Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271. Nature 2010, 466:133-137.
102. Evans S.M., Schrlau A.E., Chalian A.A., Zhang P., Koch C.J. Oxygen levels in normal and previously irradiated human skin as assessed by EF5 binding. J. Invest. Dermatol. 2006, 126:2596-2606.
103. Boutin A.T., Weidemann A., Fu Z., Mesropian L., Gradin K., Jamora C., Wiesener M., Eckardt K.U., Koch C.J., Ellies L.G., Haddad G., Haase V.H., Simon M.C., Poellinger L., Powell F.L., Johnson R.S. Epidermal sensing of oxygen is essential for systemic hypoxic response. Cell 2008, 133:223-234.
104. Bedogni B., Powell M.B. Skin hypoxia: a promoting environmental factor in melanomagenesis. Cell Cycle 2006, 5:1258-1261.
105. Nys K., Maes H., Dudek A.M., Agostinis P. Uncovering the role of hypoxia inducible factor-1alpha in skin carcinogenesis. Biochim. Biophys. Acta 1816, 2011:1-12.
106. Piret J.P., Mottet D., Raes M., Michiels C. Is HIF-1alpha a pro- or an anti-apoptotic protein?. Biochem. Pharmacol. 2002, 64:889-892.
107. Baek J.H., Jang J.E., Kang C.M., Chung H.Y., Kim N.D., Kim K.W. Hypoxia-induced VEGF enhances tumor survivability via suppression of serum deprivation-induced apoptosis. Oncogene 2000, 19:4621-4631.
108. Kothari S., Cizeau J., Millan-Ward E., Israels S.J., Bailes M., Ens K., Kirshenbaum L.A., Gibson S.B. BNIP3 plays a role in hypoxic cell death in human epithelial cells that is inhibited by growth factors EGF and IGF. Oncogene 2003, 22:4734-4744.
109. Kim J.Y., Ahn H.J., Ryu J.H., Suk K., Park J.H. BH3-only protein Noxa is a mediator of hypoxic cell death induced by hypoxia-inducible factor 1alpha. J. Exp. Med. 2004, 199:113-124.
110. Mizushima N., Levine B., Cuervo A.M., Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
111. Levine B., Klionsky D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 2004, 6:463-477.
112. White E., DiPaola R.S. The double-edged sword of autophagy modulation in cancer. Clin. Cancer Res. 2009, 15:5308-5316.
113. Morselli E., Galluzzi L., Kepp O., Vicencio J.M., Criollo A., Maiuri M.C., Kroemer G. Anti- and pro-tumor functions of autophagy. Biochim. Biophys. Acta 2009, 1793:1524-1532.
114. Zhang H., Bosch-Marce M., Shimoda L.A., Tan Y.S., Baek J.H., Wesley J.B., Gonzalez F.J., Semenza G.L. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J. Biol. Chem. 2008, 283:10892-10903.
115. Novak I., Kirkin V., McEwan D.G., Zhang J., Wild P., Rozenknop A., Rogov V., Lohr F., Popovic D., Occhipinti A., Reichert A.S., Terzic J., Dotsch V., Ney P.A., Dikic I. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010, 11:45-51.
116. Ding W.X., Ni H.M., Li M., Liao Y., Chen X., Stolz D.B., Dorn G.W., Yin X.M. Nix is critical to two distinct phases of mitophagy, reactive oxygen species-mediated autophagy induction and Parkin-ubiquitin-p62-mediated mitochondrial priming. J. Biol. Chem. 2010, 285:27879-27890.
117. Lazova R., Klump V., Pawelek J. Autophagy in cutaneous malignant melanoma. J. Cutan. Pathol. 2010, 37:256-268.
118. Ma X.H., Piao S., Wang D., McAfee Q.W., Nathanson K.L., Lum J.J., Li L.Z., Amaravadi R.K. Measurements of tumor cell autophagy predict invasiveness, resistance to chemotherapy, and survival in melanoma. Clin. Cancer Res. 2011, 17:3478-3489.
119. Claerhout S., Verschooten L., Van K.S., De V.R., Proby C., Agostinis P., Garmyn M. Concomitant inhibition of AKT and autophagy is required for efficient cisplatin-induced apoptosis of metastatic skin carcinoma. Int. J. Cancer 2010, 127:2790-2803.
120. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 2003, 3:721-732.
121. Giatromanolaki A., Sivridis E., Kouskoukis C., Gatter K.C., Harris A.L., Koukourakis M.I. Hypoxia-inducible factors 1alpha and 2alpha are related to vascular endothelial growth factor expression and a poorer prognosis in nodular malignant melanomas of the skin. Melanoma Res. 2003, 13:493-501.
122. Trisciuoglio D., Gabellini C., Desideri M., Ziparo E., Zupi G., Del B.D. Bcl-2 regulates HIF-1alpha protein stabilization in hypoxic melanoma cells via the molecular chaperone HSP90. PLoS One 2010, 5:e11772.
123. Patel M.P., Masood A., Patel P.S., Chanan-Khan A.A. Targeting the Bcl-2. Curr. Opin. Oncol. 2009, 21:516-523.
124. Neckers L., Ivy S.P. Heat shock protein 90. Curr. Opin. Oncol. 2003, 15:419-424.
125. Lining X., Uchi H., Hayashida S., Tsuji G., Kido M., Nakahara T., Takeuchi S., Takahara M., Moroi Y., Furue M. Expression of hypoxia-inducible factor-1alpha and hypoxia-inducible factor-2alpha with progression of keratinocytic neoplasms. J. Dermatol. Sci. 2009, 56:135-136.
126. Scortegagna M., Martin R.J., Kladney R.D., Neumann R.G., Arbeit J.M. Hypoxia-inducible factor-1alpha suppresses squamous carcinogenic progression and epithelial-mesenchymal transition. Cancer Res. 2009, 69:2638-2646.
127. Delehedde M., Cho S.H., Sarkiss M., Brisbay S., Davies M., El-Naggar A.K., McDonnell T.J. Altered expression of bcl-2 family member proteins in nonmelanoma skin cancer. Cancer 1999, 85:1514-1522.
128. Nagata M., Wada K., Nakajima A., Nakajima N., Kusayama M., Masuda T., Iida S., Okura M., Kogo M., Kamisaki Y. Role of myeloid cell leukemia-1 in cell growth of squamous cell carcinoma. J. Pharmacol. Sci. 2009, 110:344-353.
129. Decraene D., Agostinis P., Pupe A., De H.P., Garmyn M. Acute response of human skin to solar radiation: regulation and function of the p53 protein. J. Photochem. Photobiol. B 2001, 63:78-83.
130. Uribe P., Gonzalez S. Epidermal growth factor receptor (EGFR) and squamous cell carcinoma of the skin: molecular bases for EGFR-targeted therapy. Pathol. Res. Pract. 2011, 207:337-342.
131. Raisova M., Hossini A.M., Eberle J., Riebeling C., Wieder T., Sturm I., Daniel P.T., Orfanos C.E., Geilen C.C. The Bax/Bcl-2 ratio determines the susceptibility of human melanoma cells to CD95/Fas-mediated apoptosis. J. Invest. Dermatol. 2001, 117:333-340.
132. Karst A.M., Dai D.L., Martinka M., Li G. PUMA expression is significantly reduced in human cutaneous melanomas. Oncogene 2005, 24:1111-1116.
133. Eberle J., Kurbanov B.M., Hossini A.M., Trefzer U., Fecker L.F. Overcoming apoptosis deficiency of melanoma-hope for new therapeutic approaches. Drug Resist. Update 2007, 10:218-234.
134. Cartlidge R.A., Thomas G.R., Cagnol S., Jong K.A., Molton S.A., Finch A.J., McMahon M. Oncogenic BRAF(V600E) inhibits BIM expression to promote melanoma cell survival. Pigm. Cell Melanoma Res. 2008, 21:534-544.
135. Polzien L., Baljuls A., Albrecht M., Hekman M., Rapp U.R. BAD contributes to RAF-mediated proliferation and cooperates with B-RAF-V600E in cancer signaling. J. Biol. Chem. 2011, 286:17934-17944.
136. Wang Y.F., Jiang C.C., Kiejda K.A., Gillespie S., Zhang X.D., Hersey P. Apoptosis induction in human melanoma cells by inhibition of MEK is caspase-independent and mediated by the Bcl-2 family members PUMA, Bim, and Mcl-1. Clin. Cancer Res. 2007, 13:4934-4942.
137. Stahl J.M., Sharma A., Cheung M., Zimmerman M., Cheng J.Q., Bosenberg M.W., Kester M., Sandirasegarane L., Robertson G.P. Deregulated Akt3 activity promotes development of malignant melanoma. Cancer Res. 2004, 64:7002-7010.
138. dos Santos L.V., Carvalho A.L. Bcl-2 targeted-therapy for the treatment of head and neck squamous cell carcinoma. Recent Pat Anticancer Drug Discov. 2011, 6:45-57.
139. Ashimori N., Zeitlin B.D., Zhang Z., Warner K., Turkienicz I.M., Spalding A.C., Teknos T.N., Wang S., Nor J.E. TW-37, a small-molecule inhibitor of Bcl-2, mediates S-phase cell cycle arrest and suppresses head and neck tumor angiogenesis. Mol. Cancer Ther. 2009, 8:893-903.
140. Olie R.A., Hafner C., Kuttel R., Sigrist B., Willers J., Dummer R., Hall J., Stahel R.A., Zangemeister-Wittke U. Bcl-2 and bcl-xL antisense oligonucleotides induce apoptosis in melanoma cells of different clinical stages. J. Invest. Dermatol. 2002, 118:505-512.
141. Verhaegen M., Bauer J.A., Martin d.l., Wang V.G., Wolter K.G., Brenner J.C., Nikolovska-Coleska Z., Bengtson A., Nair R., Elder J.T., Van B.M., Carey T.E., Bradford C.R., Wang S., Soengas M.S. A novel BH3 mimetic reveals a mitogen-activated protein kinase-dependent mechanism of melanoma cell death controlled by p53 and reactive oxygen species. Cancer Res. 2006, 66:11348-11359.
142. Skoda C., Erovic B.M., Wachek V., Vormittag L., Wrba F., Martinek H., Heiduschka G., Kloimstein P., Selzer E., Thurnher D. Down-regulation of Mcl-1 with antisense technology alters the effect of various cytotoxic agents used in treatment of squamous cell carcinoma of the head and neck. Oncol. Rep. 2008, 19:1499-1503.
143. Jansen B., Schlagbauer-Wadl H., Brown B.D., Bryan R.N., van E.A., Muller M., Wolff K., Eichler H.G., Pehamberger H. bcl-2 antisense therapy chemosensitizes human melanoma in SCID mice. Nat. Med. 1998, 4:232-234.
144. Jansen B., Wacheck V., Heere-Ress E., Schlagbauer-Wadl H., Hoeller C., Lucas T., Hoermann M., Hollenstein U., Wolff K., Pehamberger H. Chemosensitisation of malignant melanoma by BCL2 antisense therapy. Lancet 2000, 356:1728-1733.
145. Keuling A.M., Felton K.E., Parker A.A., Akbari M., Andrew S.E., Tron V.A. RNA silencing of Mcl-1 enhances ABT-737-mediated apoptosis in melanoma: role for a caspase-8-dependent pathway. PLoS One 2009, 4:e6651.
146. Hassan M., Alaoui A., Feyen O., Mirmohammadsadegh A., Essmann F., Tannapfel A., Gulbins E., Schulze-Osthoff K., Hengge U.R. The BH3-only member Noxa causes apoptosis in melanoma cells by multiple pathways. Oncogene 2008, 27:4557-4568.
147. Lucas K.M., Mohana-Kumaran N., Lau D.T., Zhang X.D., Hersey P., Huang D., Weninger W., Haas N.K., Allen J.D. Modulation of Noxa and Mcl-1 as a strategy for sensitizing melanoma cells to the BH3-mimetic ABT-737. Clin. Cancer Res. 2011.
148. Fernandez Y., Verhaegen M., Miller T.P., Rush J.L., Steiner P., Opipari A.W., Lowe S.W., Soengas M.S. Differential regulation of noxa in normal melanocytes and melanoma cells by proteasome inhibition: therapeutic implications. Cancer Res. 2005, 65:6294-6304.
149. Qin J.Z., Ziffra J., Stennett L., Bodner B., Bonish B.K., Chaturvedi V., Bennett F., Pollock P.M., Trent J.M., Hendrix M.J., Rizzo P., Miele L., Nickoloff B.J. Proteasome inhibitors trigger NOXA-mediated apoptosis in melanoma and myeloma cells. Cancer Res. 2005, 65:6282-6293.
150. Li C., Li R., Grandis J.R., Johnson D.E. Bortezomib induces apoptosis via Bim and Bik up-regulation and synergizes with cisplatin in the killing of head and neck squamous cell carcinoma cells. Mol. Cancer Ther. 2008, 7:1647-1655.
151. Fribley A.M., Evenchik B., Zeng Q., Park B.K., Guan J.Y., Zhang H., Hale T.J., Soengas M.S., Kaufman R.J., Wang C.Y. Proteasome inhibitor PS-341 induces apoptosis in cisplatin-resistant squamous cell carcinoma cells by induction of Noxa. J. Biol. Chem. 2006, 281:31440-31447.
152. Fennell D.A., Chacko A., Mutti L. BCL-2 family regulation by the 20S proteasome inhibitor bortezomib. Oncogene 2008, 27:1189-1197.
153. Richardson P.G., Mitsiades C., Schlossman R., Ghobrial I., Hideshima T., Munshi N., Anderson K.C. Bortezomib in the front-line treatment of multiple myeloma. Expert Rev. Anticancer Ther. 2008, 8:1053-1072.
154. Qin J.Z., Xin H., Sitailo L.A., Denning M.F., Nickoloff B.J. Enhanced killing of melanoma cells by simultaneously targeting Mcl-1 and NOXA. Cancer Res. 2006, 66:9636-9645.
155. Wolter K.G., Verhaegen M., Fernandez Y., Nikolovska-Coleska Z., Riblett M., de la Vega C.M., Wang S., Soengas M.S. Therapeutic window for melanoma treatment provided by selective effects of the proteasome on Bcl-2 proteins. Cell Death Differ. 2007, 14:1605-1616.
156. Faivre S., Djelloul S., Raymond E. New paradigms in anticancer therapy: targeting multiple signaling pathways with kinase inhibitors. Semin. Oncol. 2006, 33:407-420.
157. Liu R., Liu D., Xing M. The Akt inhibitor MK2206 synergizes, but perifosine antagonizes, the BRAFV600E inhibitor PLX4032 and the MEK1/2 inhibitor AZD6244 in the inhibition of thyroid cancer cells. J. Clin. Endocrinol. Metab. 2011.
158. Bonilla-Hernan M.G., Miranda-Carus M.E., Martin-Mola E. New drugs beyond biologics in rheumatoid arthritis: the kinase inhibitors. Rheumatology (Oxford) 2011, 50:1542-1550.