Mad dogs, Englishmen and apoptosis: The role of cell death in UV-induced skin cancer

Apoptosis

Volumn 8, Issue 4, 2003, Pages 315-325

  Guzman, E ^a,b   Langowski, J L ^a,b   Owen Schaub, Laurie ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c 1274 Webber Hall ^*  (United States)

Author keywords

Apoptosis; Fas; Fas ligand; Immune suppression; Ultraviolet; UV induced skin cancer

Indexed keywords

FAS ANTIGEN; FAS LIGAND; TUMOR NECROSIS FACTOR RECEPTOR;

APOPTOSIS; CANCER GROWTH; DOG; ETHNIC GROUP; HUMAN; IMMUNITY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SHORT SURVEY; SIGNAL TRANSDUCTION; SKIN CANCER; SKIN CARCINOGENESIS; SUN EXPOSURE; SUNBURN; ULTRAVIOLET RADIATION;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; DNA DAMAGE; FAS LIGAND PROTEIN; HUMANS; MEMBRANE GLYCOPROTEINS; MITOCHONDRIA; RECEPTORS, TUMOR NECROSIS FACTOR; SKIN NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

CANIS FAMILIARIS;

EID: 0043169570     PISSN: 13608185     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1024112231953     Document Type: Short Survey

References (103)

1. Fisher MS, Kripke ML. Systemic alteration induced in mice by ultraviolet light irradiation and its relationship to ultraviolet carcinogenesis. Proc Natl Acad Sci USA 1977; 74: 1688-1692.
2. Frankel DH, Hanusa BH, Zitelli JA. New primary nonmelanoma skin cancer in patients with a history of squamous cell carcinoma of the skin. Implications and recommendations for follow-up. J Am Acad Dermatol 1992; 26: 720-726.
3. Kahn HS, Tatham LM, Patel AV, Thun MJ, Heath Jr. CW. Increased cancer mortality following a history of nonmelanoma skin cancer. Jama 1998; 280: 910-912.
4. Tyrrell RM. Ultraviolet radiation and free radical damage to skin. Biochem Soc Symp 1995; 61: 47-53.
5. Ziegler A, Leffell DJ, Kunala S, et al. Mutation hotspots due to sunlight in the p53 gene of nonmelanoma skin cancers. Proc Natl Acad Sci USA 1993; 90: 4216-4220.
6. Parrish JA, Jaenicke KF, Anderson RR. Erythema and melanogenesis action spectra of normal human skin. Photochem Photobiol 1982; 36: 187-191.
7. Drobetsky EA, Turcotte J, Chateauneuf A. A role for ultraviolet A in solar mutagenesis. Proc Natl Acad Sci USA 1995; 92: 2350-2354.
8. Cleaver JE, Bootsma D. Xeroderma pigmentosum: Biochemical and genetic characteristics. Annu Rev Genet 1975; 9: 19-38.
9. Kraemer KH, Lee MM, Scotto J. Xeroderma pigmentosum: Cutaneous, ocular, and neurological abnormalities in 830 published cases. Arch Dermatol 1987; 123: 241-250.
10. Brash DE. UV mutagenic photoproducts in Escherichia coli and human cells: A molecular genetics perspective on human skin cancer. Photochem Photobiol 1988; 48: 59-66.
11. Cadet J, Anselmino C, Douki T, Voituriez L. Photochemistry of nucleic acids in cells. J Photochem Photobiol B 1992; 15: 277-298.
12. Tang MS, Hrncir J, Mitchell D, Ross J, Clarkson J. The relative cytotoxicity and mutagenicity of cyclobutane pyrimidine dimers and (6-4) photoproducts in Escherichia coli cells. Mutat Res 1986; 161: 9-17.
13. You YH, Lee DH, Yoon YH, Nakajima S, Yasui A, Pfeifer GP. Cyclobutane pyrimidine dimers are responsible for the vast majority of mutations induced by UVB irradiation in mammalian cells. J Biol Chem 2001; 276: 44688-44694.
14. Kanjilal S, Perceall WE, Cummings KK, Kripke ML, Ananthaswamy HN. High frequency of p53 mutations in ultraviolet radiation-induced murine skin tumors: Evidence of strand bias and tumor heterogeneity. Cancer Res 1993; 53: 2961-2964.
15. Kripke ML, Cox PA, Alas LG, Yarosh DB. Pyrimidine dimers in DNA initiate systemic immunosuppression in UV-irradiated mice. Proc Natl Acad Sci USA 1992; 89: 7516-7520.
16. Vink AA, Strickland FM, Bucana C, et al. Localization of DNA damage and its role in altered antigen-presenting cell function in ultraviolet-irradiated mice. J Exp Med 1996; 183: 1491-1500.
17. Wolf P, Yarosh DB, Kripke ML. Effects of sunscreens and a DNA excision repair enzyme on ultraviolet radiation-induced inflammation, immune suppression, and cyclobutane pyrimidine dimer formation in mice. J Invest Dermatol 1993; 101: 523-527.
18. Wolf P, Cox P, Yarosh DB, Kripke ML. Sunscreens and T4N5 liposomes differ in their ability to protect against ultraviolet-induced sunburn cell formation, alterations of dendritic epidermal cells, and local suppression of contact hypersensitivity. J Invest Dermatol 1995; 104: 287-292.
19. Vink AA, Moodycliffe AM, Shreedhar V, et al. The inhibition of antigen-presenting activity of dendritic cells resulting from UV irradiation of murine skin is restored by in vitro photorepair of cyclobutane pyrimidine dimers. Proc Natl Acad Sci USA 1997; 94: 5255-5260.
20. Brash DE, Rudolph JA, Simon JA, et al. A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc Natl Acad Sci USA 1992; 88: 10124-10128.
21. Zhan Q, Carrier F, Fornance Jr. AJ. Induction of cellular p53 activity by DNA-damaging agents and growth arrest. Mol Cell Biol 1993; 13: 4242-4250.
22. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997; 88: 323-331.
23. Smith ML, Chen IT, Zhan Q, O'Connor PM, Fornace Jr. AJ. Involvement of the p53 tumor suppressor in repair of u.v.-type DNA damage. Oncogene 1995; 10: 1053-1059.
24. Ziegler A, Jonason AS, Leffell DJ, et al. Sunburn and p53 in the onset of skin cancer. Nature 1994; 372: 773-776.
25. Hill LL, Ouhtit A, Loughlin SM, Kripke ML, Ananthaswamy HN, Owen-Schaub LB. Fas ligand: A sensor for DNA damage critical in skin cancer etiology. Science 1999; 285: 898-900.
26. Li G, Ho VC, Berean K, Tron VA. Ultraviolet radiation induction of squamous cell carcinomas in p53 transgenic mice. Cancer Res 1995; 55: 2070-2074.
27. Li G, Tron V, Ho V. Induction of squamous cell carcinoma in p53-deficient mice after ultraviolet irradiation. J Invest Dermatol 1998; 110: 72-75.
28. Campbell C, Quinn AG, Ro YS, Angus B, Rees JL. p53 mutations are common and early events that precede tumor invasion in squamous cell neoplasia of the skin. J Invest Dermatol 1993; 100: 746-748.
29. Lacour JP. Carcinogenesis of basal cell carcinomas: Genetics and molecular mechanisms. Br J Dermatol 2002; 146(Suppl 61): 17-19.
30. Ichiki H, Sakurada H, Kamo N, Takahashi TA, Sekiguchi S. Generation of active oxygens, cell deformation and membrane potential changes upon UV-B irradiation in human blood cells. Biol Pharm Bull 1994; 17: 1065-1069.
31. Renzing J, Hansen S, Lane DP. Oxidative stress is involved in the activation of p53. J Cell Sci 1996; 109: 1105-1112.
32. Aragane Y, Kulms D, Metze D, et al. Ultraviolet light induces apoptosis via direct activation of CD95 (Fas/APO-1) independently of its ligand CD95L. J Cell Biol 1998; 140: 171-182.
33. Sheikh MS, Antinore MJ, Huang Y, Fournance Hr AJ. Ultraviolet-irradiation-induced apoptosis is mediated via ligand independent activation of tumor necrosis factor receptor 1. Oncogene 1998; 17: 2555-2563.
34. Zanke BW, Boudreau K, Rubie E, et al. The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat. Curr Biol 1996; 6: 606-613.
35. Tournier C, Hess P, Yang DD, et al. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 2000; 288: 870-874.
36. Muller M, Wilder S, Bannasch D, et al. p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J Exp Med 1998; 188: 2033-2045.
37. Kibitel J, Hejmadi V, Alas L, O'Connor A, Sutherland BM, Yarosh DB. UV-DNA damage in mouse and human cells induces the expression of tumor necrosis factor alpha. Photochem Photobiol 1998; 67: 541-546.
38. Bennett M, MacDonald K, Chan SW, Luzio J, Simari R, Weissberg P. Cell surface trafficking of Fas: A rapid mechanism of p53-mediated apoptosis. Science 1998; 282: 290-293.
39. Owen-Schaub LB, Zhang W, Cusack JC, et al. Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol Cell Biol 1995; 15: 3032-3040.
40. Ouhtit A, Gorny A, Muller HK, Hill LL, Owen-Schaub L, Ananthaswamy HN. Loss of Fas-ligand expression in mouse keratinocytes during UV carcinogenesis. Am J Pathol 2000; 157: 1975-1981.
41. Washio F, Ueda M, Ito A, Ichihashi M. Higher susceptibility to apoptosis following ultraviolet B irradiation of xeroderma pigmentosum fibroblasts is accompanied by upregulation of p53 and downregulation of bcl-2. Br J Dermatol 1999; 140: 1031-1037.
42. Adrain C, Creagh EM, Martin SJ. Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. Embo J 2001; 20: 6627-6636.
43. Ekert PG, Silke J, Hawkins CJ, Verhagen AM, Vaux DL. DIABLO promotes apoptosis by removing MIHA/XIAP from processed caspase 9. J Cell Biol 2001; 152: 483-490.
44. Sitailo L, Tibudan SS, Denning MF. Activation of caspase-9 is required for UV-induced apoptosis of human keratinocytes. J Biol Chem 2002; 277: 19346-19352.
45. Zhuang L, Wang B, Shinder GA, Shivji GM, Mak TW, Sauder DN. TNF receptor p55 plays a pivotal role in murine keratinocyte apoptosis induced by ultraviolet B irradiation. J Immunol 1999; 162: 1440-1447.
46. Miyasita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995; 80: 293-299.
47. Miyashita T, Harigai M, Hanada M, Reed JC. Identification of a p53 dependent negative response element in the bcl-2 gene. CancerRes 1994; 54: 3131-3135.
48. French LE, Hahne M, Viard I, et al. Fas and Fas ligand in embryos and adult mice: Ligand expression in several immune-privileged tissues and coexpression in adult tissues characterized by apoptotic cell turnover. J Cell Biol 1996; 133: 335-343.
49. Munsch D, Watanabe-Fukunaga R, Bourdon JC, et al. Human and mouse Fas (APO-1/CD95) death receptor genes each contain a p53-responsive element that is activated by p53 mutants unable to induce apoptosis. J Biol Chem 2000; 275: 3867-3872.
50. Filipowicz E, Adegboyega P, Sanchez RL, Gatalica Z. Expression of CD95 (Fas) in sun-exposed human skin and cutaneous carcinomas. Cancer 2002; 94: 814-819.
51. Gutierrez-Steil C, Wrone-Smith T, Sun X, Krueger JG, Coven T, Nickoloff BJ. Sunlight-induced basal cell carcinoma tumor cells and ultraviolet-B-irradiated psoriatic plaques express Fas ligand (CD95L). J Clin Invest 1998; 101: 33-39.
52. Bullani RR, Wehrli P, Viard-Leveugle I, et al. Frequent downregulation of Fas (CD95) expression and function in melanoma. Melanoma Res 2002; 12: 263-270.
53. Soubrane C, Mouawad R, Antoine EC, Verola O, Gil-Delgado M, Khayat D. A comparative study of Fas and Fas-ligand expression during melanoma progression. Br J Dermatol 2000; 143: 307-312.
54. Ivanov VN, Bhoumik A, Krasilnikov M, et al. Cooperation between STAT3 and c-jun suppresses Fas transcription. Molecular Cell 2001; 7: 517-528.
55. Cheng J, Zhou T, Liu C, et al. Protection from Fas-mediated apoptosis by a soluble form of the Fas molecule. Science 1994; 263: 1759-1762.
56. Casino I, Fiucci G, Papoff G, Ruberti G. Three functional forms of the human apoptosis-inducing Fas molecule are produced by alternative splicing. J Immunol 1995; 154: 2706-2713.
57. Redondo P, Solano T, Vazquez B, Bauza A, Idoate M. Fas and Fas ligand: Expression and soluble circulating levels in cutaneous malignant melanoma. British J Dermatol 2002; 147: 80-86.
58. Ugurel S, Rappl G, Tilgen W, Reinhold U. Increased soluble CD95 (sFas/CD95) serum level correlates with poor prognosis in melanoma patients. Clin Cancer Res 2001; 7: 1282-1286.
59. Maeda T, Hao C, Tron VA. Ultraviolet light (UV) regulation of TNF family decoy receptors DcR2 and DcR3 in human keratinocytes. J Curan Med Surg 2001; 5: 294-298.
60. Nagata S. Apoptosis by death factor. Cell 1997; 88: 355-365.
61. Orlinick JR, Elkon KB, Chao MV. Separate domains of the human fas ligand dictate self-association and receptor binding. J Biol Chem 1997; 272: 32221-32229.
62. Chinnaiyan A, O'Rourke K, Tewari M, Dixit VM. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 1995; 81: 505-512.
63. Salvesen GS, Dixit VM. Caspases: Intracellular signaling by proteolysis. Cell 1997; 91: 443-446.
64. Irmler M, Thome M, Hahne M, et al. Inhibition of death receptor signals by cellular FLIP. Nature 1997; 388: 190-195.
65. Bullani RR, Huard B, Viard-Leveugle I, et al. Selective expression of FLIP in malignant melanocytic skin lesions. J Invest Dermatol 2001; 117: 360-364.
66. Shin MS, Park WS, Kim SY, et al. Alterations of Fas (Apo-1/CD95) gene in cutaneous malignant melanoma. Am J Pathol 1999;154:1785-1791.
67. Lee SH, Shin MS, Kim HS, et al. Somatic mutations of Fas (Apo-1/CD95) gene in cutaneous squamous cell carcinoma arising from a burn scar. J Invest Dermatol 2000; 114: 122-126.
68. Deveraux QL, Reed JC. IAP family proteins - Suppressors of apoptosis. Genes Dev 1999; 13: 239-252.
69. Chen G, Goeddel DV. TNF-R1 signaling: A beautiful pathway. Science 2002; 296: 1634-1635.
70. Gupta S. A decision between life and death during TNF-alpha-induced signaling. J Clin Immunol 2002; 22: 185-194.
71. Kock A, Schwartz T, Kirnbauer R, et al. Human keratinocytes are a source for human tumor necrosis factor alpha: Evidence for synthesis and release upon stimulation with endotoxin or ultraviolet light. J Exp Med 1990; 172: 1609-1614.
72. Yoshikawa T, Streilein JW. Genetic basis of the effects of ultraviolet light B on cutaneous immunity. Evidence that polymorphism at the Tnfa and Lps loci governs susceptibility. Immunogenetics 1990; 32: 398-405.
73. Niizeki H, Naruse T, Hecker KH, et al. Polymorphisms in the tumor necrosis factor (TNF) genes are associated with susceptibility to effects of ultraviolet-B radiation on induction of contact hypersensitivity. Tissue Antigens 2001; 58: 369-378.
74. Moore RJ, Owens DM, Stamp G, et al. Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat Med 1999; 5: 828-831.
75. Kondo S, Wang B, Fujisawa H, et al. Effect of gene-targeted mutation in TNF receptor (p55) on contact hypersensitivity and ultraviolet B-induced immunosuppression. J Immunol 1995; 155: 3801-3805.
76. Amerio P, Toto P, Feliciani C, et al. Rethinking the role of tumour necrosis factor-alpha in ultraviolet (UV) B-induced immunosuppression: Altered immune response in UV-irradiated TNFR1R2 gene-targeted mutant mice. Br J Dermatol 2001; 144:952-957.
77. Kripke ML. Antigenicity of murine skin tumors induced by ultraviolet light. J Natl Cancer Inst 1974; 53: 1333-1336.
78. Kripke ML. Ultraviolet radiation and immunology: Something new under the sun - Presidential address. Cancer Res 1994; 54: 6102-6105.
79. Yoshikawa T, Rae V, Bruins-Slot W, Van den Berg JW, Taylor JR, Streilien JW. Susceptibility to effects of UVB radiation as a risk factor for skin cancer in humans. J Invest Dermatol 1990; 95: 530-536.
80. Streilien JW, Taylor JR, Vincek V, et al. Relationship between ultraviolet radiation-induced immunosuppression and carcinogenesis (Review). J Invest Dermatol 1994; 103: 107S-111S.
81. Cockburn IT, Krupp P. The risk of neoplasms in patients treated with cyclosporine A. J Autoimmun 1989; 2: 723-731.
82. Kinlen LJ, Sheil AG, Peto J, Doll R. Collaborative United Kingdom Australasian study of cancer in patients treated with immunosuppressive drugs. Br Med J 1979; 2: 1461-1466.
83. Boyle J, MacKie RM, Briggs JD, Junor BJ, Atichison TC. Cancer, warts, and sunshine in renal transplant patients. A case-control study. Lancet 1984; 1: 702-705.
84. Kim TY, Kripke ML, Ullrich SE. Immunosuppression by factors released from UV-irradiated epidermal cells: Selective effects on the generation of contact and delayed hypersensitivity after exposure to UVA or UVB radiation. J Invest Dermatol 1990; 94: 26-32.
85. Moodycliffe AM, Bucana CD, Kripke ML, Norval M, Ullrich SE. Differential effects of a monoclonal antibody to cis-urocanic acid on the suppression of delayed and contact hypersensitivity following ultraviolet irradiation. J Immunol 1996; 157: 2891-2899.
86. Noonan FP, Hoffman HA. Susceptibility to immunosuppression by ultraviolet B radiation in the mouse. Immunogenetics 1994; 39: 29-39.
87. Hill LL, Shreedhar VK, Kripke ML, Owen-Schaub LB. A critical role for Fas ligand in the active suppression of systemic immune responses by ultraviolet radiation. J Exp Med 1999; 189: 1285-1294.
88. Watanabe T, Yoshida M, Shirai Y, et al. Administration of an antigen at a high dose generates regulatory CD4+ T cells expressing CD95 ligand and secreting IL-4 in the liver. J Immunol 2002; 168: 2188-2199.
89. Rivas JM, Ullrich SE. The role of IL-4, IL-10, and TNF-alpha in the immune suppression induced by ultraviolet radiation. J Leukoc Biol 1994; 56: 769-775.
90. Nishigori C, Yarosh DB, Ullrich SE, et al. Evidence that DNA damage triggers interleukin 10 cytokine production in UV-irradiated murine keratinocytes. Proc Natl Acad Sci USA 1996; 93: 10354-10359.
91. Rodriguez-Villanueva J, Greenhalgh D, Wang XJ, et al. 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.
92. Cho SH, Delehedde M, Rodriguez-Villanueva J, Brisbay S, McDonnell TJ. Bax gene disruption alters the epidermal response to ultraviolet irradiation and in vivo induced skin carcinogenesis. Int J Mol Med 2001; 7: 235-241.
93. Jiang W, Ananthaswamy HN, Muller HK, Kripke ML. p53 protects against skin cancer induction by UV-B radiation. Oncogene 1999; 18: 4247-4253.
94. Jiang W, Ananthaswamy HN, Muller HK, et al. UV irradiation augments lymphoid malignancies in mice with one functional copy of wild-type p53. Proc Natl Acad Sci USA 2001; 98: 9790-9795.
95. Cho S, O'Connor SL, McDonnell TJ. Evidence that nucleotide excision repair is attenuated in bax-deficient mammalian cells following ultraviolet irradiation. Exp Cell Res 2002; 278: 158-165.
96. Grossman D, Kim PJ, Blanc-Brude OP, et al. Transgenic expression of survivin in keratinocytes counteracts UV-B induced apoptosis and cooperates with loss of p53. J Clin Invest 2001; 108: 991-999.
97. Allen SM, Florell SR, Hanks AN, et al. Survivin expression in mouse skin prevents papilloma regression and promotes chemical-induced tumor progression. Cancer Res 2003; 63: 567-572.
98. Gradilone A, Gazzaniga P, Ribuffo D, et al. Survivin, bcl-2, bax, and bcl-X gene expression in sentinel lymph nodes from melanoma patients. J Clin Oncol 2003; 21: 306-312.
99. Lo Muzio L, Staibano S, Pannone G, et al. Expression of the apoptosis inhibitor survivin in aggressive squamous cell carcinoma. Exp Mol Pathol 2002; 70: 249-254.
100. Kanter-Lewensohn L, Hedblad MA, Wejde J, Larsson O. Immunohistochemical markers for distinguishing Spitz nevi from malignant melanomas. Mod Pathol 1997; 10: 917-920.
101. Morales-Ducret CR, van de Rijn M, LeBrun DP, Smoller BR. bcl-2 expression in primary malignancies of the skin. Arch Dermatol 1995; 131: 909-912.
102. Cerroni L, Kerl H. Aberrant bcl-2 protein expression provides a possible mechanism of neoplastic cell growth in cutaneous basal-cell carcinoma. J Cutan Pathol 1994; 21: 398-403.
103. Zhang W, Remenyik E, Zelterman D, Brash DE, Wikonkal NM. Escaping the stem cell compartment: Sustained UVB exposure allows p53-mutant keratinocytes to colonize adjacent epidermal proliferating units without incurring additional mutations. Proc Natl Acad Sci USA 2001; 98: 13948-13953.