The sunburn cell revisited: An update on mechanistic aspects

Photochemical and Photobiological Sciences

Volumn 1, Issue 6, 2002, Pages 365-377

  Sheehan, John M ^a   Young, Antony R ^a  

^a ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; APOPTOSIS; DNA DAMAGE; EPIDERMIS; GENETICS; HUMAN; METABOLISM; PATHOLOGY; REVIEW; SUNBURN; CELL NUCLEUS; CELL STIMULATION; CELL TYPE; CYTOPLASM; EOSINOPHIL; EPIDERMIS CELL; MAMMAL CELL; MEMBRANE BINDING; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RADIATION EXPOSURE; REGULATORY MECHANISM; SKIN; ULTRAVIOLET A RADIATION; ULTRAVIOLET B RADIATION; ULTRAVIOLET C RADIATION;

ANIMALS; APOPTOSIS; DNA DAMAGE; EPIDERMIS; HUMANS; SUNBURN;

CASPASE; INHIBITOR OF APOPTOSIS PROTEIN; MEMBRANE RECEPTOR; PROTEIN P53; PSORALEN;

MAMMALIA;

EID: 0041909920     PISSN: 1474905X     EISSN: 14749092     Source Type: Journal    
DOI: 10.1039/b108291d     Document Type: Article

References (190)

1. A. R. Young The sunburn cell Photodermatology 1987 4 127-134.
2. F. Daniels D. Brophy W. Lobitz Histochemical responses of human skin following ultraviolet irradiation J. Invest. Dermatol. 1961 37 351-357.
3. A. Woodcock I. A. Magnus The sunburn cell in mouse skin: preliminary quantitative studies on its production Br. J. Dermatol. 1976 95 459-468.
4. W. Lever and G. Schaumburg-Lever, Histopathology of the skin, J. B. Lippincott Company, Philadelphia, 1975.
5. M. Garmyn J. D. Ribaya-Mercado R. M. Russel J. Bhawan B. A. Gilchrest Effect of beta-carotene supplementation on the human sunburn reaction Exp. Dermatol. 1995 4 104-111.
6. B. A. Gilchrest N. A. Soter J. S. Stoff M. C. Mihm, Jr. The human sunburn reaction: histologic and biochemical studies J. Am. Acad. Dermatol. 1981 5 411-422.
7. L. Kanerva Electron microscopic observations of dyskeratosis, apoptosis, colloid bodies and fibrillar degeneration after skin irritation with dithranol J. Cutaneous Pathol. 1990 17 37-44.
8. K. Danno T. Horio S. Imamura Infrared radiation suppresses ultraviolet B-induced sunburn-cell formation Arch. Dermatol. Res. 1992 284 92-94.
9. K. Hanada R. W. Gange M. J. Connor Effect of glutathione depletion on sunburn cell formation in the hairless mouse J. Invest. Dermatol. 1991 96 838-840.
10. K. Hanada D. Sawamura K. Tamai T. Baba I. Hashimoto T. Muramatsu N. Miura A. Naganuma Novel function of metallothionein in photoprotection: metallothionein-null mouse exhibits reduced tolerance against ultraviolet B injury in the skin J. Invest. Dermatol. 1998 111 582-585.
11. Y. Miyachi T. Horio S. Imamura Sunburn cell formation is prevented by scavenging oxygen intermediates Clin. Exp. Dermatol. 1983 8 305-310.
12. A. R. Young I. A. Magnus An action spectrum for 8-MOP induced sunburn cells in mammalian epidermis Br. J. Dermatol. 1981 104 541-548.
13. K. Iwasaki M. Izawa M. Mihara UV-induced apoptosis in rat skin J. Dermatol. Sci. 1996 12 31-35.
14. K. Danno T. Horio Formation of UV-induced apoptosis relates to the cell cycle Br. J. Dermatol. 1982 107 423-428.
15. Y. Aragane D. Kulms D. Metze G. Wilkes B. Pöppelmann T. A. Luger T. Schwarz Ultraviolet light induces apoptosis via direct activation of CD95 (Fas/APO-1) independently of its ligand CD95L J. Cell Biol. 1998 140 171-182.
16. T. Baba H. Nakano K. Tamai D. Sawamura K. Hanada I. Hashimoto Y. Arima Inhibitory effect of beta-thujaplicin on ultraviolet B-induced apoptosis in mouse keratinocytes J. Invest. Dermatol. 1998 110 24-28.
17. J. F. Kerr Shrinkage necrosis: a distinct mode of cellular death J. Pathol. 1971 105 13-20.
18. B. E. Johnson G. Mandell F. Daniels, Jr. Melanin and cellular reactions to ultraviolet radiation Nature (London), New Biol. 1972 235 147-149.
19. M. Kumakiri K. Hashimoto I. Willis Biologic changes due to long-wave ultraviolet irradiation on human skin: ultrastructural study J. Invest. Dermatol. 1977 69 392-400.
20. I. Willis L. Cylus UVA erythema in skin: is it a sunburn? J. Invest. Dermatol. 1977 68 128-129.
21. R. Rosario G. J. Mark J. A. Parrish M. C. Mihm, Jr. Histological changes produced in skin by equally erythemogenic doses of UV-A, UV-B, UV-C and UV-A with psoralens Br. J. Dermatol. 1979 101 299-308.
22. R. Lavker K. Kaidbey The spectral dependence for UVA-induced cumulative damage in human skin J. Invest. Dermatol. 1997 108 17-21.
23. Y. P. Lu Y. R. Lou P. Yen D. Mitchell M. T. Huang A. H. Conney Time course for early adaptive responses to ultraviolet B light in the epidermis of SKH-1 mice Cancer Res. 1999 59 4591-4602.
24. J. I. Youn R. W. Gange D. Maytum J. A. Parrish Effect of hypoxia on sunburn cell formation and inflammation induced by ultraviolet radiation Photodermatology 1988 5 252-256.
25. Y. Yasui T. Hirone Action spectrum for bergamot-oil phototoxicity measured by sunburn cell counting J. Dermatol. 1994 21 319-322.
26. M. Weil M. D. Jacobson H. S. Coles T. J. Davies R. L. Gardner K. D. Raff M. C. Raff Constitutive expression of the machinery for programmed cell death J. Cell Biol. 1996 133 1053-1059.
27. M. Weil M. C. Raff V. M. Braga Caspase activation in the terminal differentiation of human epidermal keratinocytes Curr. Biol. 1999 9 361-364.
28. H. Steller J. M. Abrams M. E. Grether K. White Programmed cell death in Drosophila Philos. Trans. R. Soc. London, Ser. B 1994 345 247-250.
29. K. White M. E. Grether J. M. Abrams L. Young K. Farrell H. Steller Genetic control of programmed cell death in Drosophila [see comments] Science 1994 264 677-683.
30. M. Irmler K. Hofmann D. Vaux J. Tschopp Direct physical interaction between the Caenorhabditis elegans ‘death proteins’ CED-3 and CED-4 FEBS Lett. 1997 406 189-190.
31. H. R. Horvitz S. Shaham M. O. Hengartner The genetics of programmed cell death in the nematode Caenorhabditis elegans Cold Spring Harbor Symp. Quant. Biol. 1994 59 377-385.
32. A. Sugimoto P. D. Friesen J. H. Rothman Baculovirus p35 prevents developmentally programmed cell death and rescues a ced-9 mutant in the nematode Caenorhabditis elegans EMBO J. 1994 13 2023-2028.
33. A. Ziegler D. J. Leffell S. Kunala H. W. Sharma M. Gailani J. A. Simon A. J. Halperin H. P. Baden P. E. Shapiro A. E. Bale Mutation hotspots due to sunlight in the p53 gene of nonmelanoma skin cancers Proc. Natl. Acad. Sci. U. S. A. 1993 90 4216-4220.
34. G. Murphy A. R. Young H. C. Wulf D. Kulms T. Schwarz The molecular determinants of sunburn cell formation Exp. Dermatol. 2001 1 155-160.
35. S. W. Muchmore M. Sattler H. Liang R. P. Meadows J. E. Harlan H. S. Yoon D. Nettesheim B. S. Chang C. B. Thompson S. L. Wong S. L. Ng S. W. Fesik X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death Nature 1996 381 335-341.
36. J. D. de F. A. Prins D. Y. Mason J. C. Reed O. G. van P. M. Kluin Subcellular localization of the bcl-2 protein in malignant and normal lymphoid cells Cancer Res. 1994 54 256-260.
37. D. Hockenbery G. Nunez C. Milliman R. D. Schreiber S. J. Korsmeyer Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death Nature 1990 348 334-336.
38. S. Krajewski S. Tanaka S. Takayama M. J. Schibler W. Fenton J. C. Reed Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes Cancer Res. 1993 53 4701-4714.
39. M. Nguyen D. G. Millar V. W. Yong S. J. Korsmeyer G. C. Shore Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence J. Biol. Chem. 1993 268 25265-25268.
40. I. S. Goping A. Gross J. N. Lavoie M. Nguyen R. Jemmerson K. Roth S. J. Korsmeyer G. C. Shore Regulated targeting of BAX to mitochondria J. Cell Biol. 1998 143 207-215.
41. A. Gross J. Jockel M. C. Wei S. J. Korsmeyer Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis EMBO J. 1998 17 3878-3885.
42. I. Martinou M. Missotten P. A. Fernandez R. Sadoul J. C. Martinou Bax and Bak proteins require caspase activity to trigger apoptosis in sympathetic neurons Neuroreport 1998 9 15-19.
43. J. Yang X. Liu K. Bhalla C. N. Kim A. M. Ibrado J. Cai T. I. Peng D. P. Jones X. Wang Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked [see comments] Science 1997 275 1129-1132.
44. D. M. Finucane E. Bossy-Wetzel N. J. Waterhouse T. G. Cotter D. R. Green Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL J. Biol. Chem. 1999 274 2225-2233.
45. C. Prives P. A. Hall The p53 pathway J. Pathol. 1999 187 112-126.
46. A. J. Levine p53, the cellular gatekeeper for growth and division Cell 1997 88 323-331.
47. M. L. Agarwal W. R. Taylor M. V. Chernov O. B. Chernova G. R. Stark The p53 network J. Biol. Chem. 1998 273 1-4.
48. W. S. El-Deiry S. E. Kern J. A. Pietenpol K. W. Kinzler B. Vogelstein Definition of a consensus binding site for p53 Nature Genetics 1992 1 45-49.
49. N. M. Wikonkal D. E. Brash Ultraviolet radiation induced signiature mutations in photocarcinogenesis J. Invest. Dermatol. Symp. Proc. 1999 4 6-10.
50. A. Ziegler A. S. Jonason D. J. Leffell J. A. Simon H. W. Sharma J. Kimmelman L. Remington T. Jacks D. E. Brash Sunburn and p53 in the onset of skin cancer [see comments] Nature 1994 372 773-776.
51. K. Danno T. Horio Sunburn cell: factors involved in its formation Photochem. Photobiol. 1987 45 683-690.
52. D. E. Brash A. Ziegler A. S. Jonason J. A. Simon S. Kunala D. J. Leffell Sunlight and sunburn in human skin cancer: p53, apoptosis, and tumor promotion J. Invest. Dermatol. Symp. Proc. 1996 1 136-142.
53. H. Ananthaswamy C. Conti A. Ouhtit A. Gorny P. Khaskina p53 mutations in UV-induced skin tumors from XPC-deficient mice Photochem. Photobiol. 1999 3S.
54. F. Washio M. Ueda A. Ito M. Ichihashi 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.
55. G. Li V. C. Ho p53-dependent DNA repair and apoptosis respond differently to high- and low-dose ultraviolet radiation Br. J. Dermatol. 1998 139 3-10.
56. J. W. Harper G. R. Adami N. Wei K. Keyomarsi S. J. Elledge The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases Cell 1993 75 805-816.
57. E. R. McDonald G. S. Wu T. Waldman W. S. El-Deiry Repair Defect in p21 WAF1/CIP1 -/- human cancer cells Cancer Res. 1996 56 2250-2255.
58. G. Li D. L. Mitchell V. C. Ho J. C. Reed V. A. Tron Decreased DNA repair but normal apoptosis in ultraviolet-irradiated skin of p53-transgenic mice Am. J. Pathol. 1996 148 1113-1123.
59. P. Wehrli I. Viard R. Bullani J. Tschopp L. E. French Death receptors in cutaneous biology and disease J. Invest. Dermatol. 2000 115 141-148.
60. L. A. Tartaglia T. M. Ayres G. H. Wong D. V. Goeddel A novel domain within the 55 kd TNF receptor signals cell death Cell 1993 74 845-853.
61. M. E. Peter P. H. Krammer Mechanisms of CD95 (APO-1/Fas)-mediated apoptosis Curr. Opin. Immunol. 1998 10 545-551.
62. K. Sayama S. Yonehara Y. Watanabe Y. Miki Expression of Fas antigen on keratinocytes in vivo and induction of apoptosis in cultured keratinocytes J. Invest. Dermatol. 1994 103 330-334.
63. H. Matsue H. Kobayashi T. Hosokawa T. Akitaya A. Ohkawara Keratinocytes constitutively express the Fas antigen that mediates apoptosis in IFN gamma-treated cultured keratinocytes Arch. Dermatol. Res. 1995 287 315-320.
64. A. Kaptein M. Jansen G. Dilaver J. Kitson L. Dash E. Wang M. J. Owen J. L. Bodmer J. Tschopp S. N. Farrow Studies on the interaction between TWEAK and the death receptor WSL-1/TRAMP (DR3) FEBS Lett. 2000 485 135-141.
65. M. S. Shin H. S. Kim S. H. Lee W. S. Park S. Y. Kim J. Y. Park J. H. Lee S. K. Lee S. N. Lee S. S. Jung J. Y. Han H. Kim J. Y. Lee N. J. Yoo Mutations of tumor necrosis factor-related apoptosis-inducing ligand receptor 1 (TRAIL-R1) and receptor 2 (TRAIL-R2) genes in metastatic breast cancers Cancer Res. 2001 61 4942-4946.
66. M. S. Sheikh T. F. Burns Y. Huang G. S. Wu S. Amundson K. S. Brooks A. J. Fornace, Jr. W. S. el Deiry p53-dependent and -independent regulation of the death receptor KILLER/DR5 gene expression in response to genotoxic stress and tumor necrosis factor alpha Cancer Res. 1998 58 1593-1598.
67. M. A. Degli-Esposti W. C. Dougall P. J. Smolak J. Y. Waugh C. A. Smith R. G. Goodwin The novel receptor TRAIL-R4 induces NF-kappaB and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain Immunity 1997 7 813-820.
68. F. Bachmann S. A. Buechner M. Wernli S. Strebel P. Erb Ultraviolet light downregulates CD95 ligand and TRAIL receptor expression facilitating actinic keratosis and squamous cell carcinoma formation J. Invest. Dermatol. 2001 117 59-66.
69. B. R. Wong R. Josien S. Y. Lee B. Sauter H. L. Li R. M. Steinman Y. Choi TRANCE (tumor necrosis factor [TNF]-related activation-induced cytokine), a new TNF family member predominantly expressed in T cells, is a dendritic cell-specific survival factor J. Exp. Med. 1997 186 2075-2080.
70. C. Rosette M. Karin Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors Science 1996 274 1194-1197.
71. D. Kulms B. Poppelmann D. Yarosh T. A. Luger J. Krutmann T. Schwarz Nuclear and cell membrane effects contribute independently to the induction of apoptosis in human cells exposed to UVB radiation Proc. Natl. Acad. Sci. U. S. A. 1999 96 7974-7979.
72. E. S. Alnemri Mammalian cell death proteases: a family of highly conserved aspartate specific cysteine proteases J. Cell. Biochem. 1997 64 33-42.
73. G. Nunez M. A. Benedict Y. Hu N. Inohara Caspases: the proteases of the apoptotic pathway Oncogene 1998 17 3237-3245.
74. A. Ashkenazi V. M. Dixit Death receptors: signaling and modulation Science 1998 281 1305-1308.
75. M. MacFarlane M. Ahmad S. M. Srinivasula A. Fernandes G. M. Cohen E. S. Alnemri Identification and molecular cloning of two novel receptors for the cytotoxic ligand TRAIL J. Biol. Chem. 1997 272 25417-25420.
76. G. Kothny-Wilkes D. Kulms T. A. Luger M. Kubin T. Schwarz Interleukin-1 protects transformed keratinocytes from tumor necrosis factor-related apoptosis-inducing ligand- and CD95-induced apoptosis but not from ultraviolet radiation-induced apoptosis J. Biol. Chem. 1999 274 28916-28921.
77. A. Schwarz K. Mahnke T. A. Luger T. Schwarz Pentoxifylline reduces the formation of sunburn cells Exp. Dermatol. 1997 6 1-5.
78. L. Eckhart W. Declercq J. Ban M. Rendl B. Lengauer C. Mayer S. Lippens P. Vandenabeele E. Tschachler Terminal differentiation of human keratinocytes and stratum corneum formation is associated with caspase-14 activation J. Invest. Dermatol. 2000 115 1148-1151.
79. K. Miwa M. Asano R. Horai Y. Iwakura S. Nagata T. Suda Caspase 1-independent IL-1beta release and inflammation induced by the apoptosis inducer Fas ligand Nature Medicine 1998 4 1287-1292.
80. W. Chen H. G. Wang S. M. Srinivasula E. S. Alnemri N. R. Cooper B cell apoptosis triggered by antigen receptor ligation proceeds via a novel caspase-dependent pathway J. Immunol. 1999 163 2483-2491.
81. K. Samejima S. Tone T. J. Kottke M. Enari H. Sakahira C. A. Cooke Durrieu L. M. Martins S. Nagata S. H. Kaufmann W. C. Earnshaw Transition from caspase-dependent to caspase-independent mechanisms at the onset of apoptotic execution J. Cell Biol. 1998 143 225-239.
82. D. D. Mosser A. W. Caron L. Bourget C. Denis-Larose B. Massie Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis Mol. Cell. Biol. 1997 17 5317-5327.
83. N. M. Robertson J. Zangrilli T. Fernandes-Alnemri P. D. Friesen G. Litwack E. S. Alnemri Baculovirus P35 inhibits the glucocorticoid-mediated pathway of cell death Cancer Res. 1997 57 43-47.
84. A. Vantieghem Z. Assefa P. Vandenabeele W. Declercq S. Courtois J. R. Vandenheede W. Merlevede W. P. de P. Agostinis Hypericin-induced photosensitization of HeLa cells leads to apoptosis or necrosis. Involvement of cytochrome c and procaspase-3 activation in the mechanism of apoptosis FEBS Lett. 1998 440 19-24.
85. S. Kamada M. Washida J. Hasegawa H. Kusano Y. Funahashi Y. Tsujimoto Involvement of caspase-4(-like) protease in Fas-mediated apoptotic pathway Oncogene 1997 15 285-290.
86. A. Krippner-Heidenreich R. V. Talanian R. Sekul R. Kraft H. Thole H. Ottleben B. Luscher Targeting of the transcription factor Max during apoptosis: phosphorylation-regulated cleavage by caspase-5 at an unusual glutamic acid residue in position P1 Biochem. J. 2001 358 705-715.
87. T. E. Allsopp J. McLuckie L. E. Kerr M. Macleod J. Sharkey J. S. Kelly Caspase 6 activity initiates caspase 3 activation in cerebellar granule cell apoptosis Cell Death Differ. 2000 7 984-993.
88. M. Germain E. B. Affar D. D’Amours V. M. Dixit G. S. Salvesen G. G. Poirier Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7 J. Biol. Chem. 1999 274 28379-28384.
89. M. Ahmad S. M. Srinivasula R. Hegde R. Mukattash T. Fernandes-Alnemri E. S. Alnemri Identification and characterization of murine caspase-14, a new member of the caspase family Cancer Res. 1998 58 5201-5205.
90. H. Li H. Zhu C. J. Xu J. Yuan Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis Cell 1998 94 491-501.
91. X. Luo I. Budihardjo H. Zou C. Slaughter X. Wang Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors Cell 1998 94 481-490.
92. H. Zou Y. Li X. Liu X. Wang An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9 J. Biol. Chem. 1999 274 11549-11556.
93. S. B. Bratton G. Walker S. M. Srinivasula X. M. Sun M. Butterworth E. S. Alnemri G. M. Cohen Recruitment, activation and retention of caspases-9 and -3 by Apaf-1 apoptosome and associated XIAP complexes EMBO J. 2001 20 998-1009.
94. T. Fernandes-Alnemri R. C. Armstrong J. Krebs S. M. Srinivasula L. Wang F. Bullrich L. C. Fritz J. A. Trapani K. J. Tomaselli G. Litwack E. S. Alnemri In vitro activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains Proc. Natl. Acad. Sci. U. S. A. 1996 93 7464-7469.
95. J. Lee J. Hur P. Lee J. Y. Kim N. Cho S. Y. Kim H. Kim M. S. Lee K. Suk Dual role of inflammatory stimuli in activation-induced cell death of mouse microglial cells. Initiation of two separate apoptotic pathways via induction of interferon regulatory factor-1 and caspase-11 J. Biol. Chem. 2001 276 32956-32965.
96. S. J. Kang S. Wang H. Hara E. P. Peterson S. Namura S. Amin-Hanjani Z. Huang A. Srinivasan K. J. Tomaselli N. A. Thornberry M. A. Moskowitz J. Yuan Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions J. Cell Biol. 2000 149 613-622.
97. S. Wang M. Miura Y. K. Jung H. Zhu E. Li J. Yuan Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE Cell 1998 92 501-509.
98. T. Nakagawa J. Yuan Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis J. Cell Biol. 2000 150 887-894.
99. T. Nakagawa H. Zhu N. Morishima E. Li J. Xu B. A. Yankner J. Yuan Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta Nature 2000 403 98-103.
100. T. Yoneda K. Imaizumi K. Oono D. Yui F. Gomi T. Katayama M. Tohyama Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress J. Biol. Chem. 2001 276 13935-13940.
101. V. Bitko S. Barik An endoplasmic reticulum-specific stress-activated caspase (caspase-12) is implicated in the apoptosis of A549 epithelial cells by respiratory syncytial virus J. Cell. Biochem. 2001 80 441-454.
102. E. W. Humke J. Ni V. M. Dixit ERICE, a novel FLICE-activatable caspase J. Biol. Chem. 1998 273 15702-15707.
103. M. K. Kuechle H. M. Predd P. Fleckman B. A. Dale R. B. Presland Caspase-14, a keratinocyte specific caspase: mRNA splice variants and expression pattern in embryonic and adult mouse Cell Death Differ. 2001 8 868-870.
104. S. Lippens M. Kockx M. Knaapen L. Mortier R. Polakowska A. Verheyen M. Garmyn A. Zwijsen P. Formstecher D. Huylebroeck P. Vandenabeele W. Declercq Epidermal differentiation does not involve the pro-apoptotic executioner caspases, but is associated with caspase-14 induction and processing Cell Death Differ. 2000 7 1218-1224.
105. L. Eckhart W. Declercq J. Ban M. Rendl B. Lengauer C. Mayer S. Lippens P. Vandenabeele E. Tschachler Terminal differentiation of human keratinocytes and stratum corneum formation is associated with caspase-14 activation J. Invest. Dermatol. 2000 115 1148-1151.
106. L. Eckhart J. Ban H. Fischer E. Tschachler Caspase-14: analysis of gene structure and mRNA expression during keratinocyte differentiation Biochem. Biophys. Res. Commun. 2000 277 655-659.
107. S. Hu S. J. Snipas C. Vincenz G. Salvesen V. M. Dixit Caspase-14 is a novel developmentally regulated protease J. Biol. Chem. 1998 273 29648-29653.
108. C. M. Van de G. Van Loo S. Pype W. Van Criekinge d. b. Van I. F. Molemans W. Fiers W. Declercq P. Vandenabeele Identification of a new caspase homologue: caspase-14 Cell Death Differ. 1998 5 838-846.
109. J. F. Krebs R. C. Armstrong A. Srinivasan T. Aja A. M. Wong A. Aboy R. Sayers B. Pham T. Vu K. Hoang D. S. Karanewsky C. Leist A. Schmitz J. C. Wu K. J. Tomaselli L. C. Fritz Activation of membrane-associated procaspase-3 is regulated by Bcl-2 J. Cell Biol. 1999 144 915-926.
110. M. Mancini D. W. Nicholson S. Roy N. A. Thornberry E. P. Peterson L. A Casciola-Rosen A. Rosen The caspase-3 precursor has a cytosolic and mitochondrial distribution: implications for apoptotic signaling J. Cell Biol. 1998 140 1485-1495.
111. N. E. Crook R. J. Clem L. K. Miller An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif J. Virol. 1993 67 2168-2174.
112. Q. L. Deveraux H. R. Stennicke G. S. Salvesen J. C. Reed Endogenous inhibitors of caspases J. Clin. Immunol. 1999 19 388-398.
113. M. Rothe M. G. Pan W. J. Henzel T. M. Ayres D. V. Goeddel The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins Cell 1995 83 1243-1252.
114. C. S. Duckett V. E. Nava R. W. Gedrich R. J. Clem J. L. Van Dongen M. C. Gilfillan H. Shiels J. M. Hardwick C. B. Thompson A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors EMBO J. 1996 15 2685-2694.
115. P. Liston N. Roy K. Tamai C. Lefebvre S. Baird G. Cherton-Horvat R. Farahani M. McLean J. E. Ikeda A. MacKenzie R. G. Korneluk Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes Nature 1996 379 349-353.
116. G. Ambrosini C. Adida D. C. Altieri A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma Nature Medicine 1997 3 917-921.
117. N. Roy Q. L. Deveraux R. Takahashi G. S. Salvesen J. C. Reed The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases EMBO J. 1997 16 6914-6925.
118. I. Tamm Y. Wang E. Sausville D. A. Scudiero N. Vigna T. Oltersdorf J. C. Reed IAP-family protein survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs Cancer Res. 1998 58 5315-5320.
119. H. R. Stennicke G. S. Salvesen Biochemical characteristics of caspases-3, -6, -7, and -8 J. Biol. Chem. 1997 272 25719-25723.
120. G. Ambrosini C. Adida G. Sirugo D. C. Altieri Induction of apoptosis and inhibition of cell proliferation by survivin gene targeting J. Biol. Chem. 1998 273 11177-11182.
121. M. L. Lo S. Staibano G. Pannone M. D. Mignogna A. Mariggio G. Salvatore P. Chieffi D. Tramontano G. De Rosa D. C. Altieri Expression of the apoptosis inhibitor survivin in aggressive squamous cell carcinoma Exp. Mol. Pathol. 2001 70 249-254.
122. D. Grossman P. J. Kim J. S. Schechner D. C. Altieri Inhibition of melanoma tumor growth in vivo by survivin targeting Proc. Natl. Acad. Sci. U. S. A. 2001 98 635-640.
123. C. Du M. Fang Y. Li L. Li X. Wang Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition Cell 2000 102 33-42.
124. A. M. Verhagen P. G. Ekert M. Pakusch J. Silke L. M. Connolly G. E. Reid R. L. Moritz R. J. Simpson D. L. Vaux Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins Cell 2000 102 43-53.
125. V. A. Fadok D. R. Voelker P. A. Campbell J. J. Cohen D. L. Bratton P. M. Henson Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages J. Immunol. 1992 148 2207-2216.
126. W. Maruyama S. Irie T. A. Sato Morphological changes in the nucleus and actin cytoskeleton in the process of Fas-induced apoptosis in Jurkat T cells Histochem. J. 2000 32 495-503.
127. E. Bonanno M. Ruzittu E. C. Carla M. R. Montinari P. Pagliara L. Dini Cell shape and organelle modification in apoptotic U937 cells Eur. J. Histochem. 2000 44 237-246.
128. G. Bonelli M. C. Sacchi G. Barbiero F. Duranti G. Goglio D. C. Verdun J. S. Amenta M. Piacentini C. Tacchetti F. M. Baccino Apoptosis of L929 cells by etoposide: a quantitative and kinetic approach Exp. Cell Res. 1996 228 292-305.
129. Y. Zhao M. Wu Y. Shen Z. Zhai Analysis of nuclear apoptotic process in a cell-free system Cell. Mol. Life Sci. 2001 58 298-306.
130. G. M. Cohen X. M. Sun R. T. Snowden D. Dinsdale D. N. Skilleter Key morphological features of apoptosis may occur in the absence of internucleosomal DNA fragmentation Biochem. J. 1992 286 331-334.
131. Y. Liu J. M. Cousin J. Hughes D. J. Van J. R. Seckl C. Haslett I. Dransfield J. Savill A. G. Rossi Glucocorticoids promote nonphlogistic phagocytosis of apoptotic leukocytes J. Immunol. 1999 162 3639-3646.
132. M. D. Navazo L. Daviet J. Savill Y. Ren L. L. Leung J. L. McGregor Identification of a domain (155–183) on CD36 implicated in the phagocytosis of apoptotic neutrophils J. Biol. Chem. 1996 271 15381-15385.
133. P. Nicotera M. Leist E. Fava L. Berliocchi C. Volbracht Energy requirement for caspase activation and neuronal cell death Brain Pathol. 2000 10 276-282.
134. F. Gillardon I. Moll M. Meyer T. M. Michaelidis 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.
135. T. L. Deckwerth E. M. Johnson, Jr. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor J. Cell Biol. 1993 123 1207-1222.
136. G. Kroemer N. Zamzami S. A. Susin Mitochondrial control of apoptosis Immunol. Today 1997 18 44-51.
137. P. X. Petit S. A. Susin N. Zamzami B. Mignotte G. Kroemer Mitochondria and programmed cell death: back to the future FEBS Lett. 1996 396 7-13.
138. P. Bernardi V. Petronilli The permeability transition pore as a mitochondrial calcium release channel: a critical appraisal J. Bioenerg. Biomembr. 1996 28 131-138.
139. N. Zamzami S. A. Susin P. Marchetti T. Hirsch I. Gomez-Monterrey M. Castedo G. Kroemer Mitochondrial control of nuclear apoptosis [see comments] J. Exp. Med. 1996 183 1533-1544.
140. M. Zoratti I. Szabo The mitochondrial permeability transition Biochim. Biophys. Acta 1995 1241 139-176.
141. S. A. Susin N. Zamzami G. Kroemer Mitochondria as regulators of apoptosis: doubt no more Biochim. Biophys. Acta 1998 1366 151-165.
142. F. Ichas L. S. Jouaville J. P. Mazat Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals Cell 1997 89 1145-1153.
143. X. Liu C. N. Kim J. Yang R. Jemmerson X. Wang Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome, c Cell 1996 86 147-157.
144. E. Bossy-Wetzel D. D. Newmeyer D. R. Green Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization EMBO J. 1998 17 37-49.
145. C. Purring-Koch G. McLendon Cytochrome c binding to Apaf-1: the effects of dATP and ionic strength Proc. Natl. Acad. Sci. U. S. A. 2000 97 11928-11931.
146. A. Saleh S. M. Srinivasula S. Acharya R. Fishel E. S. Alnemri Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation J. Biol. Chem. 1999 274 17941-17945.
147. H. Wiseman B. Halliwell Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer Biochem. J. 1996 313 17-29.
148. M. Higuchi T. Honda R. J. Proske E. T. Yeh Regulation of reactive oxygen species-induced apoptosis and necrosis by caspase 3-like proteases Oncogene 1998 17 2753-2760.
149. K. Danno T. Horio M. Takigawa S. Imamura Role of oxygen intermediates in UV-induced epidermal cell injury J. Invest. Dermatol. 1984 83 166-168.
150. K. Hanada D. Sawamura K. Tamai I. Hashimoto S. Kobayashi Photoprotective effect of esterified glutathione against ultraviolet B-induced sunburn cell formation in the hairless mice J. Invest. Dermatol. 1997 108 727-730.
151. K. Werninghaus M. Meydani J. Bhawan R. Margolis J. B. Blumberg B. A. Gilchrest Evaluation of the photoprotective effect of oral vitamin E supplementation Arch. Dermatol. 1994 130 1257-1261.
152. D. L. Bissett R. Chatterjee D. P. Hannon Photoprotective effect of superoxide-scavenging antioxidants against ultraviolet radiation-induced chronic skin damage in the hairless mouse Photodermatol. Photoimmunol. Photomed. 1990 7 56-62.
153. D. Darr S. Combs S. Dunston T. Manning S. Pinnell Topical vitamin C protects porcine skin from ultraviolet radiation-induced damage Br. J. Dermatol. 1992 127 247-253.
154. D. Darr S. Dunston H. Faust S. Pinnell Effectiveness of antioxidants (vitamin C and E) with and without sunscreens as topical photoprotectants Acta Derm. Venereol. 1996 76 264-268.
155. L. Benassi D. Ottani F. Fantini A. Marconi C. Chiodino A. Giannetti C. Pincelli 1,25-dihydroxyvitamin D3, transforming growth factor beta1, calcium, and ultraviolet B radiation induce apoptosis in cultured human keratinocytes J. Invest. Dermatol. 1997 109 276-282.
156. D. A. Norris Differential control of cell death in the skin [editorial] Arch. Dermatol. 1995 131 945-948.
157. M. Cario-Andre C. Pain Y. Gall J. Ginestar O. Nikaido A. Taieb Studies on epidermis reconstructed with and without melanocytes: melanocytes prevent sunburn cell formation but not appearance of DNA damaged cells in fair-skinned caucasians J. Invest. Dermatol. 2000 115 193-199.
158. S. Zhai M. Yaar S. M. Doyle B. A. Gilchrest Nerve growth factor rescues pigment cells from ultraviolet-induced apoptosis by upregulating BCL-2 levels Exp. Cell Res. 1996 224 335-343.
159. K. Isoherranen I. Sauroja C. Jansen K. Punnonen UV irradiation induces downregulation of bcl-2 expression in vitro and in vivo Arch. Dermatol. Res. 1999 291 212-216.
160. V. A. Tron G. Li V. Ho M. J. Trotter Ultraviolet radiation-induced p53 responses in the epidermis are differentiation-dependent J. Cutaneous Med. Surg. 1999 3 280-283.
161. A. M. Montgomery R. A. Reisfeld D. A. Cheresh Integrin alpha v beta 3 rescues melanoma cells from apoptosis in three-dimensional dermal collagen Proc. Natl. Acad. Sci. U. S. A. 1994 91 8856-8860.
162. J. E. J. Meredith B. Fazeli M. A. Schwartz The extracellular matrix as a cell survival factor Mol. Biol. Cell 1993 4 953-961.
163. A. J. Zhu I. Haase F. M. Watt Signaling via beta1 integrins and mitogen-activated protein kinase determines human epidermal stem cell fate in vitro Proc. Natl. Acad. Sci. U. S. A. 1999 96 6728-6733.
164. R. Gniadecki M. Hansen H. C. Wulf Two pathways for induction of apoptosis by ultraviolet radiation in cultured human keratinocytes J. Invest. Dermatol. 1997 109 163-169.
165. A. Fourtanier Mexoryl SX protects against solar-simulated UVR-induced photocarcinogenesis in mice Photochem. Photobiol. 1996 64 688-693.
166. J. A. Harrison S. L. Walker S. R. Plastow M. D. Batt J. L. Hawk A. R. Young Sunscreens with low sun protection factor inhibit ultraviolet B and A photoaging in the skin of the hairless albino mouse Photodermatol. Photoimmunol. Photomed. 1991 8 12-20.
167. C. Nishigori D. B. Yarosh C. Donawho M. L. Kripke The immune system in ultraviolet carcinogenesis J. Invest. Dermatol. Symp. Proc. 1996 143-146.
168. M. L. Kripke P. A. Cox L. G. Alas D. B. Yarosh Pyrimidine dimers in DNA initiate systemic immunosuppression in UV-irradiated mice Proc. Natl. Acad. Sci. U. S. A. 1992 89 7516-7520.
169. P. Wolf D. B. Yarosh M. L. Kripke 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.
170. A. R. Young J. M. Sheehan C. A. Chadwick C. S. Potten Protection by ultraviolet A and B sunscreens against in situ dipyrimidine photolesions in human epidermis is comparable to protection against sunburn J. Invest. Dermatol. 2000 115 37-41.
171. G. L. Grove K. H. Kaidbey Sunscreens prevent sunburn cell formation in human skin J. Invest. Dermatol. 1980 75 363-364.
172. J. P. Cesarini A. Chardon O. Binet C. Hourseau J. F. Grollier High-protection sunscreen formulation prevents UVB-induced sunburn cell formation Photodermatology 1989 6 20-23.
173. M. Garmyn N. Sohrabvand R. Roelandts Modification of sunburn cell production in 8-MOP sensitized mouse epidermis: a method of assessing UVA sunscreen efficacy J. Invest. Dermatol. 1989 92 642-645.
174. K. H. Kaidbey K. H. Grove A. M. Kligman The influence of longwave ultraviolet radiation on sunburn cell production by UVB J. Invest. Dermatol. 1979 73 743-745.
175. C. A. Elmets A. Vargas C. Oresajo Photoprotective effects of sunscreens in cosmetics on sunburn and Langerhans cell photodamage Photodermatol. Photoimmunol. Photomed. 1992 9 113-120.
176. P. Wolf P. Cox D. B. Yarosh M. L. Kripke 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.
177. D. E. Godar Light and Death: Photons and Apoptosis J. Invest. Dermatol. 1999 4 17-23.
178. D. E. Godar UVA1 radiation triggers two different final apoptotic pathways J. Invest. Dermatol. 1999 112 3-12.
179. G. Kroemer N. Zamzami S. A. Susin Mitochondrial control of apoptosis Immunol. Today 1997 18 44-51.
180. C. Scaffidi S. Fulda A. Srinivasan C. Friesen F. Li K. J. Tomaselli K. M. Debatin P. H. Krammer M. E. Peter Two CD95 (APO-1/Fas) signaling pathways EMBO J. 1998 17 1675-1687.
181. M. Bennett K. Macdonald S. W. Chan J. P. Luzio R. Simari P. Weissberg Cell surface trafficking of Fas: a rapid mechanism of p53-mediated apoptosis [see comments] Science 1998 282 290-293.
182. S. A. Susin E. Daugas L. Ravagnan K. Samejima N. Zamzami M. Loeffler P. Costantini K. F. Ferri T. Irinopoulou M. C. Prevost G. Brothers T. W. Mak J. Penninger W. C. Earnshaw G. Kroemer Two distinct pathways leading to nuclear apoptosis J. Exp. Med. 2000 192 571-580.
183. M. Li V. O. Ona C. Guegan M. Chen V. Jackson-Lewis L. J. Andrews A. J. Olszewski P. E. Stieg J. P. Lee S. Przedborski R. M. Friedlander Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model [see comments] Science 2000 288 335-339.
184. Y. Tsujimoto J. Cossman E. Jaffe C. M. Croce Involvement of the bcl-2 gene in human follicular lymphoma Science 1985 228 1440-1443.
185. H. G. Zhang Y. Wang J. F. Xie X. Liang D. Liu P. Yang H. C. Hsu R. B. Ray J. D. Mountz Regulation of tumor necrosis factor alpha-mediated apoptosis of rheumatoid arthritis synovial fibroblasts by the protein kinase Akt Arthritis Rheum. 2001 44 1555-1567.
186. H. Walczak R. E. Miller K. Ariail B. Gliniak T. S. Griffith M. Kubin W. Chin J. Jones A. Woodward T. Le C. Smith P. Smolak R. G. Goodwin C. T. Rauch J. C. Schuh D. H. Lynch Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo [see comments] Nature Medicine 1999 5 157-163.
187. D. W. Nicholson From bench to clinic with apoptosis-based therapeutic agents Nature 2000 407 810-816.
188. A. Ouhtit A. Gorny H. K. Muller L. L. Hill L. Owen-Schaub H. N. Ananthaswamy Loss of Fas-ligand expression in mouse keratinocytes during UV carcinogenesis Am. J. Pathol. 2000 157 1975-1981.
189. A. S. Jonason S. Kunala G. J. Price R. J. Restifo H. M. Spinelli J. A. Persing D. J. Leffell R. E. Tarone D. E. Brash Frequent clones of p53-mutated keratinocytes in normal human skin [see comments] Proc. Natl. Acad. Sci. U. S. A. 1996 93 14025-14029.
190. R. J. Berg K. H. van Kranen H. G. Rebel A. de Vries W. A. van Vloten C. F. Van Kreijl J. C. van der Leun F. R. de Gruijl Early p53 alterations in mouse skin carcinogenesis by UVB radiation: immunohistochemical detection of mutant p53 protein in clusters of preneoplastic epidermal cells Proc. Natl. Acad. Sci. U. S. A. 1996 93 274-278.