Apoptosis and cytokine release induced by ionizing or ultraviolet B radiation in primary and immortalized human keratinocytes

Carcinogenesis

Volumn 21, Issue 6, 2000, Pages 1087-1095

  Petit Frère, Corinne ^a,e   Capulas, Emily ^a   Lyon, Debbie A ^b   Norbury, Christopher J ^c   Lowe, Jillian E ^a   Clingen, Peter H ^a,f   Riballo, Enriqueta ^a   Green, Michael H L ^a,d   Arlett, Colin F ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF BRIGHTON   (United Kingdom)

^e KAROLINSKA INSTITUTE   (Sweden)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; MITOXANTRONE;

APOPTOSIS; ARTICLE; CELL IMMORTALIZATION; CELL KILLING; CELL LINE; CYTOKINE RELEASE; FIBROBLAST; GAMMA RADIATION; HUMAN; HUMAN CELL; IONIZING RADIATION; KERATINOCYTE; MALE; NEWBORN; PRIORITY JOURNAL; ULTRAVIOLET B RADIATION;

EID: 0034084789     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/21.5.087     Document Type: Article

References (65)

1. Arlett, C.F. (1992) Human cellular radiosensitivity - the search for the holy grail or a poisoned chalice. Adv. Radiat biol., 16, 273-292.
2. Arlett, C.F. and Lehmann, A.R. (1996) Xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy: sun sensitivity, DNA repair defects and skin cancer. In Eeles,R., Ponder,B., Easton,D. and Horwich,E.A. (eds) Genetic Predisposition to Cancer. Chapman and Hall, London, UK, pp. 185-206.
3. Boukamp, P., Petrussevska, R.T., Breitkreutz, D., Hornung, J., Markham, A. and Fusenig, N.E. (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol., 106, 761-771.
4. Boukamp, P., Popp, S., Altmeyer, S., Hulsen, A., Fasching, C., Cremer, T. and Fusenig, N.E. (1997) Sustained nontumorigenic phenotype correlates with a largely stable chromosome content during long-term culture of the human keratinocyte line HaCaT. Genes Chromosom. Cancer, 19, 201-214.
5. UKCCCR (1999) UKCCCR Guidelines for the Use of Cell Lines in Cancer Research. UKCCCR, London, UK.
6. Orwell, G. (1948) 1984. Penguin, London, UK.
7. Duchaud, E., Ridet, A., Stoppa-Lyonnet, D., Janin, N., Moustacchi, E. and Rosselli, F. (1996) Deregulated apoptosis in ataxia telangiectasia: association with clinical stigmata and radiosensitivity. Cancer Res., 56, 1400-1404.
8. Foray, N., Priestley, A, Alsbeih, G., Badie, C., Capulas, E.P., Arlett, C.F. and Malaise, E.P. (1997) Hypersensitivity of ataxia-telangiectasia fibroblasts to ionizing radiation is associated with a repair deficiency of DNA doublestrand breaks. Int. J. Radiat. Biol., 72, 271-283.
9. Foray, N., Arlett, C.F. and Malaise, E.P. (1997) Radiation-induced DNA double-strand breaks and the radiosensitivity of human cells: a closer look. Biochimie, 79, 567-575.
10. Enns, L., Barley, R.D.C., Paterson, M.C. and Mirzayans, R. (1998) Radiosensitivity in ataxia telangiectasia fibroblasts is not associated with deregulated apoptosis. Radiat. Res., 150, 11-16.
11. Arlett, C.F., Green, M.H.L., Priestley, A., Harcourt, S.A. and Mayne, L.V. (1988) Comparative human cellular radiosensitivity: 1. The effect of SV40 immortalisation on the gamma-irradiation survival of skin derived fibroblasts from normal individuals and from ataxia-telangiectasia patients and heterozygotes. Int. J. Radiat. Biol., 54, 911-928.
12. Mayne, L.V., Priestley, A., James, M.R. and Burke, J.F. (1986) Efficient immortalization and morphological transformation of human fibroblasts by transfection with SV40 DNA linked to a dominant marker. Exp. Cell Res., 162, 530-538.
13. Yang, T.T., Namba, H., Hara, T., Takmura, N., Nagayama, Y., Fukata, S., Ishikawa, N., Kuma, K., Ito, K. and Yamashita, S. (1997) p53 induced by ionizing radiation mediates DNA end-jointing activity, but not apoptosis of thyroid cells. Oncogene, 14, 1511-1519.
14. IARC (1992) Solar and Ultraviolet Radiation. IARC, Lyon.
15. Longstreth, J., De Gruijl, F.R., Kripke, M.L., Abseck, S., Arnold, F., Slaper, H.I., Velders, G., Takizawa, Y. and van der Leun, J.C. (1998) Health risks. J. Photochem. Photobiol. B Biol., 46, 20-39.
16. Young, A.R. (1987) The sunburn cell. Photodermatalogy, 4, 127-134.
17. Brash, D.E., Ziegler, A., Jonason, A.S., Simon, J.A., Kunala, S. and Lefell, D.J. (1996) Sunlight and sunburn in human skin cancer: p53, apoptosis and tumor promotion. J. Invest. Dermatol, Symp. Proc., 1, 136-142.
18. Ziegler, A., Jonason, A.S., Leffell, D.J., Simon, J.A., Sharma, H.W., Kimmelman, J., Remington, L., Jacks, T. and Brash, D.E. (1994) Sunburn and p53 in the onset of skin cancer. Nature, 372, 773-776.
19. Casciola-Rosen, L.A., Anhalt, G. and Rosen, A. (1994) Autoantigens targeted in systemic lupus-erythematosus are clustered in 2 populations of surface-structures on apoptotic keratinocytes. J. Exp. Med., 179, 1317-1330.
20. Schwarz, A., Bhardwaj, R., Aragane, Y., Mahnke, K., Riemann, H., Metze, D., Luger, T.A. and Schwarz, T. (1995) Evidence for partial involvement of tumor-necrosis-factor-alpha in the formation of sunburn cells. J. Invest. Dermatol., 104, 922-927.
21. Benassi, L., Ottani, D., Fantini, F., Marconi, A., Chiodino, C., Giannetti, A. and Pincelli, C. (1997) 1.25-dihydroxyvitamin D-3, transforming growth factor beta 1, calcium and ultraviolet B radiation induce apoplosis in cultured human keratinocytes. J. Invest. Dermatol., 109, 276-282.
22. Gniadecki, R., Hansen, M. and Wulf, H.C. (1997) Two pathways for induction of apoptosis by ultraviolet radiation in cultured human keratinocytes. J. Invest. Dermatol., 109, 163-169.
23. Leverkus, M., Yaar, M. and Gilchrest, B.A. (1997) Fas/Fas ligand interaction contributes to UV-induced apoptosis in human keratinocytes. Exp. Cell Res., 232, 255-262.
24. Aragane, Y., Kulms, D., Metze, D., Wilkes, G., Poppelmann, B., Luger, T.A. and Schwarz, T. (1998) Ultraviolet light induces apoptosis via direct activation of CD95 (Fas/APO-1) independently of its ligand CD95L. J. Cell Biol., 140, 171-182.
25. Beetz, A., Messer, G., Oppel, T., Van Beuningen, D., Peter, R.U. and Kind, P. (1997) Induction of interleukin-6 by ionizing radiation in a human epithelial cell line: control by corticosteroids. Int. J. Radiat. Biol., 72, 33-43.
26. Brach, M.A., Gruss, H.J., Kaisho, T., Asano, Y., Hirano, T. and Herrmann, F. (1993) Ionizing-radiation induces expression of interleukin-6 by human fibroblasts involving activation of nuclear factor-kappa-B. J. Biol. Chem., 268, 8466-8472.
27. Petit-Frère, C., Clingen, P.H., Grewe, M., Krutmann, J., Roza, L., Arlett, C.F. and Green, M.H.L. (1998) Induction of interleukin-6 production by ultraviolet radiation in normal human epidermal keratinocytes and in a human keratinocyte cell line is mediated by DNA damage. J. Invest. Dermatol., 111, 354-359,
28. Iglesias, M., Yen, K., Gaiotti, D., Hildesheim, A., Stoler, M.H. and Woodworth, C.D. (1998) Human papillomavirus type 16 E7 protein sensitizes cervical keratinocytes to apoptosis and release of interleukin-1 alpha. Oncogene, 17, 1195-1205.
29. Magic, Z., Maticivanovic, S., Savic, J. and Poznanovic, G. (1995) Ionizing radiation-induced expression of the genes associated with the acute response to injury in the rat. Radiat. Res., 143, 187-193.
30. Urbanski, A., Schwarz, T., Neuner, P., Krutmann, J., Kirnbauer, R., Köck, A. and Luger, T.A. (1990) Ultraviolet light induces increased circulating interleukin-6 in humans. J. Invest. Dermatol., 94, 808-811.
31. Gauldie, J., Richards, C., Harnish, D., Lansdorp, P. and Baumann, H. (1987) Interferon B2/B-cell stimulatory factor type 2 shares identity with monocyte-derived hepatocyte-stimulating factor and regulates the major acute phase protein response in liver cells. Proc. Natl Acad. Sci. USA, 84, 7251-7255.
32. Nijsten, M.W.N., De Groot, E.R., Ten Duis, H.J., Klasen, H.J., Hack, C.E. and Aarden, L.A. (1987) Serum levels of interleukin-6 and acute phase responses. Lancet, ii, 921.
33. Nishigori, C., Yarosh, D.B., Ulrich, S.E., Vink, A.A., Bucana, C.D., Roza, L. and Kripke, M.L. (1996) Evidence that DNA damage triggers IL-10 cytokine production in UV-irradiated murine keratinocytes. Proc. Natl Acad. Sci. USA, 93, 10354-10359.
34. Santin, A., Hiserodt, J.C., Di Saia, P.J., Pecorelli, S. and Granger, G.A. (1996) Differential effects of high-dose gamma irradiation on the production of transforming growth factor-beta in fresh and established human ovarian cancer. Gynecol. Oncol., 61, 403-408.
35. ATCC (2000) ATCC Online Catalog, http://phage.atcc.org/
36. Ogura, H., Yoshinouchi, M., Kudo, T., Imura, M., Fujiwara, T. and Yabe, Y. (1993) Human papillomavirus type-18 DNA in so-called HEP-2-cells, KB-cells and Fl-cells - further evidence that these cells are HeLa-cell derivatives. Cell. Mol. Biol., 39, 463-4-67.
37. Gey, G.O., Coffman, W.D. and Kubicek, M.T. (1952) Tissue culture studies of the proliferative capacity of cervical carcinoma and normal epithelium. Cancer Res., 12, 264-265.
38. Arlett, C.F., Lowe, J.E., Harcourt, S.A., Waugh, A.P.W., Cole, J., Roza, L., Diffey, B.L., Mori, T., Nikaido,O. and Green,M.H.L. (1993) Hypersensitivity of human lymphocytes to UV-B and solar irradiation. Cancer Res., 53, 609-614.
39. Goodhead,D.T.,Thacker,J. and Cox,R. (1993) Effects of radiations of different qualities on cells: molecular mechanisms of damage and repair. Int. J. Radiat Biol., 63, 43-556.
40. Von Hoff,D.D., Coltman,C.A. and Forseth,B. (1981) Activity of mitoxantrone in a human-tumor cloning system. Cancer Res., 41, 1853-1855.
41. Stacey,G.N., Masters,J.R.W., Hay,R.J., Drexler,H.G., McCleod,R.A.F. and Freshney, R.I. (2000) Cell contamination leads to inaccurate data: we must take action now. Nature, 403, 356.
42. Kumar, M.G., Hurwitz, S.A., Cotton, J. and Spandau, D.F. (1999) Subphysiological concentrations of extracellular calcium sensitize normal human keratinocytes to UVB-induced apoptosis. Arch. Dermatol. Res., 291, 37-46.
43. Clingen, P.H., Arlett, C.F., Harcourt, S.A., Waugh, A.P.W., Lowe, J.E., Hermanova, N., Cole, J., Green, M.H.L., Roza, L., Mori, T. and Nikaido, O. (1995) Correlation of UVC and UVB cytotoxicity with the induction of specific photoproducts in T-lymphocytes and fibroblasts from normal human donors. Photochem. Photobiol., 61, 163-170.
44. Goodhead, D.T. (1994) Initial events in the cellular effects of ionizing-radiations - clustered damage in DNA. Int. J. Radiat. Biol., 65, 7-17.
45. Weller, E.M., Hain, J., Jung, T., Kinder, R., Kofferlein, M., Burkart, W. and Nusse, M. (1996) UV-B-induced cell cycle perturbations, micronucleus induction and modulation by caffeine in human keratinocytes. Int. J. Radiat. Biol., 69, 371-384.
46. Greenwood, S.K., Armstrong, M.J., Hill, R.B., Bradt, C.I., Johnson, T.E., Milliard, C.A. and Galloway, S.M. (1998) Fewer chromosome aberrations and earlier apoptosis induced by DNA synthesis inhibitors, a topoisomerase II inhibitor or alkylating agents in human cells with normal compared with mutant p53. Mutat. Res., 401, 39-53.
47. Xia, F., Wang, X., Wang, Y.H., Tsang, N.M., Yandell, D.W., Kelsey, K.T. and Liber, H.L. (1995) Altered p53 status correlates with differences in sensitivity to radiation-induced mutation and apoptosis in 2 closely-related human lymphoblast lines. Cancer Res., 55, 12-15.
48. Lehman, T.A., Modali, R., Boukamp, P., Stanek, J., Bennett, W.P., Welsh, J.A., Metcalf, R.A., Stampfer, M.R., Fusenig, N., Rogan, E.M. and Harris, C.C. (1993) p53 mutations in human immortalized epithelial-cell lines. Carcinogenesis, 14, 833-839.
49. Mogi, Y., Kato, J., Horimoto, M., Takimoto, R., Murakami, T., Hirayama, A., Kohgo, Y., Watanabe, N. and Niitsu, Y. (1994) Close correlation between the dephosphorylation of p53 and growth suppression by transforming growth-factor-beta-1 in nasopharyngeal carcinoma-cells transduced with adenovirus early region genes. Jpn. J. Cancer Res., 85, 459-463.
50. Danen-Van Oorschot, A.A.A.M., Fischer, D.F., Grimbergen, J.M., Klein, B., Zhuang, S.M., Falkenburg, J.H.F., Backendorf, C., Quax, P.H.A., van der Eb, A.J. and Noteborn, M.H.M. (1997) Apoptin induces apoptosis in human transformed and malignant cells but not in normal cells. Proc. Natl Acad. Sci. USA, 94, 5843-5847.
51. Kothny-Wilkes, G., Kulms, D., Poppelmann, B., Luger, T.A., Kubin, M. and Schwarz, T. (1998) Imerleukin-1 protects transformed keratinocytes from tumor necrosis factor-related apoptosis-inducing ligand. J. Biol. Chem., 273, 29247-29253.
52. Williams, K.J., Boyle, J.M., Birch, J.M., Norton, J.D. and Scott, D. (1997) Cell cycle arrest defect in Li-Fraumeni Syndrome: a mechanism of cancer predisposition? Oncogene, 14, 277-282.
53. Di Leonardo, A., Linke, S.P., Clarkin, K. and Wahl, G.M. (1994) DNA-damage triggers a prolonged P53-dependent G(1) arrest and long-term induction of Cipl in normal human fibroblasts. Genes Dev., 8, 2540-2551.
54. Linke, S.P., Clarkin, K.C. and Wahl, G.M. (1997) p53 mediates permanent arrest over multiple cell cycles in response to gamma-irradiation. Cancer Res., 57, 1171-1179.
55. Olive, P.L. and Durand, R.E. (1997) Apoplosis: an indicator of radiosensitivity in vitro? Int. J. Radiat. biol., 71, 695-707.
56. Levine, E.L., Renehan, A., Gossiel, R., Davidson, S.E., Roberts, S.A., Chadwick, C., Wilks, D.P., Potten, C.S., Hendry, J.H., Hunter, R.D. and West, C.M.L. (1995) Apoptosis, intrinsic radiosensitivity and prediction of radiotherapy response in cervical carcinoma. Radiother. Oncol., 37, 1-9.
57. Kock, A., Schwarz, T., Kirnbauer, R., Urbanski, A., Perry, P., Ansel, J.C and Luger, T.A. (1990) Human keratinocytes are a source for tumor necrosis factor alpha: evidence for synthesis and release upon stimulation with endotoxin or ultraviolet light. J. Exp. Med., 172, 1609-1614.
58. Devos, S., Brach, M., Budnik, A., Grewe, M., Herrmann, F. and Krutmann, J. (1994) Posttranscriptional regulation of interleukin-6 gene-expression in human keratinocytes by ultraviolet-B radiation. J. Invest. Dermatol., 103, 92-96.
59. Enk, C.D., Mahanty, S., Blauvelt, A. and Katz, S. (1996) UVB induces IL-12 transcription in human keratinocytes in vivo and in vitro. Photochem. Photobiol., 63, 854-859.
60. Hallahan, D.E., Spriggs, D.R., Beckett, M.A., Kufe, D.W. and Weichselbaum, R.R. (1989) Increased tumor necrosis factor-alpha messenger-RNA after cellular exposure to ionizing-radiation. Proc. Natl Acad. Sci. USA, 86, 10104-10107.
61. Weill, D., Gay, F., Tovey, M.G. and Chouaib, S. (1996) Induction of tumor necrosis factor alpha expression in human T lymphocytes following ionizing gamma irradiation. J. Interferon Cytokine Res., 16, 395-402.
62. Gaugler, M.H., Squiban, C., van der Meeren, A., Bertho, J.M., van Damme, M. and Mouthon, M.A. (1997) Late and persistent up-regulalion of intercellular adhesion molecule-1 (ICAM-1) expression by ionizing radiation in human endothelial cells in vitro. Int. J. Radiat. Biol., 72, 201-209.
63. Hachiya, M., Shimizu, S., Osawa, Y. and Akashi, M. (1997) Endogenous production of tumour necrosis factor is required for manganese superoxide dismutase expression by irradiation in the human monocytic cell line THP-1. Biochem. J., 328, 615-623.
64. Pons, J., Gras, G., Courberand, S., Benveniste, O. and Dormont, D. (1997) Consequences of gamma-irradiation on inflammatory cytokine regulation in human monocytes/macrophages. Int. J. Radiat. Biol., 71, 157-166.
65. Hendry, J.H. and West, C.M.L. (1997) Apoptosis and mitotic cell death: their relative contributions to normal-tissue and tumour radiation response. Int. J. Radiat. Biol., 71, 709-719.