Human papillomavirus E6 and E7 oncoproteins alter cell cycle progression but not radiosensitivity of carcinoma cells treated with low-dose-rate radiation

International Journal of Radiation Oncology Biology Physics

Volumn 37, Issue 1, 1997, Pages 145-154

  Deweese, Theodore L ^a,b   Walsh, Jonathan C ^a   Dillehay, Larry E ^a   Kessis, Theodore D ^c   Hedrick, Lora ^a   Cho, Kathleen R ^a   Nelson, William G ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS HOSPITAL   (United States)

^c NONE

Author keywords

Cell cycle; Cell cycle checkpoints; Human papillomaviruses (HPVs); Low dose rate radiation; p53

Indexed keywords

ONCOPROTEIN;

ARTICLE; CARCINOMA CELL; CELL CYCLE G1 PHASE; CELL DEATH; CELL KILLING; CELL PROLIFERATION; CELL SURVIVAL; DNA DAMAGE; HUMAN; HUMAN CELL; IONIZING RADIATION; LOW ENERGY RADIATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RADIATION EXPOSURE; RADIOSENSITIVITY; TARGET CELL; WART VIRUS;

COLONIC NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA DAMAGE; G1 PHASE; G2 PHASE; HUMANS; ONCOGENE PROTEINS, VIRAL; RADIATION DOSAGE; RADIATION TOLERANCE; REPRESSOR PROTEINS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0031040705     PISSN: 03603016     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0360-3016(96)00448-8     Document Type: Article

References (85)

1. Barbosa, M. S.; Edmonds, C.; Fisher, C.; Schiller, J. T.; Lowy, D. R.; Vousden, K. H. The region of HPV E7 oncoprotein homologous to adenovirus E1a and SV40 large T antigen contains separable domains for Rb binding and casein kinase II phosphorylation. EMBO J. 9:153-160; 1990.
2. Beamish, H.; Khanna, K. K.; Lavin, M. F. Ionizing radiation and cell cycle progression in ataxia telangiectasia. Radiat. Res. 138:S130-S133; 1994.
3. Bedford, J. S.; Mitchell, J. B.; Fox, M. H. Variations in responses of several mammalian cell lines to low dose-rate irradiation. In: Meyn, R. E.; Withers, R., eds. Radiation biology in cancer research. New York: Raven Press: 1980:241-262.
4. Blasko, J. C.; Grimm, P. D.; Ragde, H. Brachytherapy and organ preservation in the management of the prostate. Semin. Radiat. Oncol. 3:240-249; 1993.
5. Bosch, F. X.; Manos, M. M.; Munoz, N.; Sherman, M.; Jansen, A. M.; Peto, J.; Schiffman, M. H.; Moreno, V.; Kurman, R.; Shah, K. V.; IBSCC Study Group. Prevalence of human papillomavirus in cervical cancer: A worldwide perspective. J. Natl. Cancer Inst. 87:796-802; 1995.
6. Bracey, T. S.; Miller, J. C.; Preece, A.; Paraskeva, C. Gamma-radiation-induced apoptosis in human colorectal adenoma and carcinoma cell lines can occur in the absence of wild type p53. Oncogene 10:2391-2396; 1995.
7. Brachman, D. G.; Beckett, M.; Graves, D.; Haraf, D.; Vokes, E.; Weichselbaum, R. R. P53 mutation does not correlate with radiosensitivity in 24 head and neck cancer cell lines. Cancer Res. 53:3667-3669; 1993.
8. Braid, D. S. F.; Martin, M.; Le Rhoun, Y.; Duthu, A.; Lefaix, J. L.; May, E.; May, P. Concominant p53 gene mutation and increased radiosensitivity in rat lung embryo epithelial cells during neoplastic development. Cancer Res. 54:3361-3364; 1994.
9. Bristow, R. G.; Jang, A.; Peacock, J.; Chung, S.; Ben Chimol, S.; Hill, R. P. Mutant p53 increases radioresistance in rat embryo fibroblasts simulanteously transfected with HPV16-E7 and/or activated H-ras. Oncogene 9:1527-1536; 1994.
10. Burton, K. Determination of DNA concentration with diphenylamine. Methods Enzymol. 12B:163-166; 1968.
11. Butz, K.; Shahabeddin, L.; Geisen, C.; Spitkovsky, D.; Ullmann, A.; Hoppe-Seyler, F. Functional p53 protein in human papillomavirus-positive cancer cells. Oncogene 10:927-936; 1995.
12. Canman, C. E.; Gilmer, T. M.; Coutts, S. B.; Kastan, M. B. Growth factor modulation of p53-mediated growth arrest vs. apoptosis. Genes Dev. 9:600-611; 1995.
13. Cheong, N.; Wang, Y.; Iliakis, G. Radioresistance induced in rat embryo cells by transfection with the oncogenes H-ras plus v-myc is cell cycle dependent and maximal during S and G2. Int. J. Radiat. Biol. 63:623-629; 1993.
14. Clarke, A. R.; Purdie, C. A.; Harrison, D. J.; Morris, R. G.; Bird, C. C.; Hooper, M. L.; Wyllie, A. H. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature 362:849-852; 1993.
15. Coia, L.; Wen, M.; Lanciano, R.; Marcial, V. A.; Murtz, K.; Hanks, G. The patterns of care outcome study for cancer of the uterine cervix: Results of the second national practice survey. Cancer 66:2451-2456; 1990.
16. Crook, T.; Fisher, C.; Masterson, R. J.; Vousden, K. H. Modulation of transcriptional regulatory properties of p53 by HPV E6. Oncogene 9:1225-1230; 1994.
17. Crook, T.; Tidy, J. A.; Vousden, K. H. Degradation of p53 can be targeted by HPV E6 sequences distinct from those required for p53 binding and transactivation. Cell 67:547-556; 1991.
18. Demers, G. W.; Foster, S. A.; Halbert, C. L.; Galloway, D. A. Growth arrest by induction of p53 in DNA damaged keratinocytes is bypassed by human papillomavirus 16 E7. Proc. Nat'l. Acad. Sci. USA 91:4382-4386; 1994.
19. CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82:675-684; 1995.
20. Dulic, V.; Kaufmann, W. K.; Wilson, S. J.; Tlsty, T. D.; Lees, E.; Harper, J. W.; Elledge, S. J.; Reed, S. I. P53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76:1013-1023; 1994.
21. Dyson, N.; Howley, P. M.; Munger, K.; Harlow, E. The human papillomavirus-16 E7 oncoprotein is able to bind the retinoblastoma gene product. Science 243:934-937; 1989.
22. El-Deiry, W. S.; Harper, J. W.; O Connor, P. M.; Velculescu, V. E.; Canman, C. E.; Jackman, J.; Pietenpol, J. A.; Burrell, M.; Hill, D. E.; Wang, Y.; Wiman, K. G.; Mercer, W. E.; Kastan, M. B.; Kohn, K. W.; Elledge, S. J.; Kinzler, K. W.; Vogelstein, B. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 54:1169-1174; 1994.
23. El-Deiry, W. S.; Tokino, T.; Velculescu, V. E.; Levy, D. B.; Parsons, R.; Trent, J. M.; Lin, D.; Mercer, W. E.; Kinzler, K. W.; Vogelstein, B. WAF-1, a potential mediator of p53 tumor suppression. Cell 75:817-825; 1993.
24. Fan, S.; El-Deiry, W. S.; Bae, I.; Freeman, J.; Jondle, D.; Bhatia, K.; Fornace, A. J.; Magrath, I.; Kohn, K. W.; O'Connor, P. M. P53 gene mutations are associated with decreased sensitivity of human lymphoma cells to DNA damaging agents. Cancer Res. 54:5824-5830; 1994.
25. Fan, S.; Smith, M. L.; Rivet, D. J.; Duba, D.; Zhan, Q.; Kohn, K. W.; Fornace, A. J.; O Connor, P. M. Disruption of p53 function sensitizes breast cancer MCF-7 cells to cisplatin and pentoxifylline. Cancer Res. 55:1649-1654; 1995.
26. Foster, S. A.; Demers, G. W.; Etscheid, B. G.; Galloway, D. A. The ability of human papillomavirus E6 proteins to target p53 for degradation in vivo correlates with their ability to abrogate actinomycin D-induced growth arrest. J. Virol. 68:5698-5705; 1994.
27. Fowler, J. F. Radiobiological aspects of low dose rate in radioimmunotherapy. Int. J. Radiat. Oncol. Biol. Phys. 18:1261-1269; 1990.
28. Griffith, T. D.; Tolmach, L. J. Lethal response of HeLa cells to x-irradiation in the latter part of the generation cycle. Biophys. J. 16:303-318; 1976.
29. Haas-Kogan, D. A.; Kogan, S.C.; Levi, D.; Dazin, P.; T'Ang, A.; Fung, Y. -K.; Israel, M. A. Inhibition of apoptosis by the retinoblastoma gene product. EMBO J. 14:461-472; 1995.
30. Hartwell, L. H.; Kastan, M. B. Cell cycle control and cancer. Science 266:1821-1828; 1994.
31. Hickman, E. S.; Picksley, S. M.; Vousden, K. H. Cells expressing HPV 16 E7 continue cell cycle progression following DNA damage induced p53 activation. Oncogene 9:2177-2181; 1994.
32. Hockenberry, D.; Nunez, G.; Milliman, C.; Schreiber. P. D.; Korsmayer, S. J. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348:334-336; 1990.
33. Isacson, C.; Kessis, T. D.; Hedrick, L.; Cho, K. R. Both cell proliferation and apoptosis increase with lesion grade in cervical neoplasia but do not correlate with human papillomavirus type. Cancer Res. 56:669-674; 1996.
34. Jung, M.; Notario, V.; Dritschilo, A. A mutation in the p53 gene in radiation sensitive and resistant human squamous carcinoma cells. Cancer Res. 52:6390-6393; 1992.
35. Kal, H. B.; Barendsen, G. W.; Bakker-van Haue, R.; Roeke. H. Increased radiosensitivity of rat rhabdomyosarcoma cells induced by protracted irradiation. Radiat. Res. 63:521-530; 1975.
36. Kastan, M. B.; Onyekwere, O.; Sidransky, D.; Vogelstein, B.; Craig, R. W. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51:6304-6311; 1991.
37. Kastan, M. B.; Zhan, Q.; El-Deiry, W. S.; Carrier, F.; Jacks, T.; Walsh, B. S.; Plunkett, B. S.; Vogelstein, B.; Fornace, A. J. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell 71:587-597; 1992.
38. Keng, P. C.; Siemann, D. W.; Wheeler, K. T. Comparison of tumor age response to radiation for cells derived from tissue culture or solid tumors. Br. J. Cancer 50:519-526; 1984.
39. Kessis, T. D.; Slebos, R. J.; Nelson, W. G.; Kastan, M. B.; Plunkett, B. S.; Han, S. M.; Lorincz, A. T.; Hedrick, L.; Cho, K. R. Human papillomavirus 16 E6 expression disrupts the p53-mediated cellular response to DNA damage. Proc. Natl. Acad. Sci. USA 90:3988-3992; 1993.
40. Kitada, S.; Krajewski, S.; Miyatshita, T.; Krajewska, M.; Reed, J. C. Gamma-radiation induces upregulation of Bax protein and apoptosis in radiosensitive cells in vivo. Oncogene 12:187-192; 1996.
41. Kuerbitz, S. J.; Plunkett, B. S.; Walsh, W. V.; Kastan, M. B. Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc. Natl. Acad. Sci. USA 89:7491-7495; 1992.
42. Lee, J. M.; Bernstein, A. P53 mutations increase resistance to ionizing radiation. Proc. Natl. Acad. Sci. USA 90:5742-5746; 1993.
43. Leeper, D. B.; Schneiderman, M. H.; Dewey, W. C. Radiation-induced cycle delay in synchronized Chinese hamster cells: Comparison between DNA synthesis and division. Radiat. Res. 53:326-337; 1973.
44. Leith, J. T. Correspondence re: D. G. Brachman et al.: P53 mutation does not correlate with radiosensitivity in 24 head and neck cancer cell lines. Cancer Res. 54:5021; 1994.
45. Lotem, J.; Sachs, L. Hematopoietic cells from mice deficient in wild-type p53 are more resistant to induction of apoptosis by some agents. Blood 82:1092-1096; 1993.
46. Lowe, S. W.; Bodis, S.; McClatchey, A.; Remington. L.; Ruley, H. E.; Fisher, D. E.; Housman, D. E.; Jacks, T. P53 status and the efficacy of cancer therapy in vivo. Science 266:807-810; 1994.
47. Lowe, S. W.; Ruley, H. E.; Jacks, T.; Housman, D. E. p53-Dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74:957-967; 1993.
48. Lowe, S. W.; Scmitt, E. M.; Smith, S. W.; Osborne, B. A.; Jacks, T. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 362:847-849; 1993.
49. Lücke-Huhle, C. Alterations in oncogene expression and radiosensitivity in the most frequently used SV40-transformed human skin fibiroblast. Int. J. Radiat. Biol. 65:665-673; 1994.
50. MacLeod, K. F.; Sherry, N.; Hannon, G.; Beach, D.; Tokino, T.; Kinzler, K.; Vogelstein, B.; Jacks, T. p53-Dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev. 9:935-944; 1995.
51. Maity, A.; McKenna, W. G.; Muschel, R. J. The molecular basis for cell cycle delays following ionizing radiation: A review. Radiother. Oncol. 31:1-13; 1994.
52. Malaise, E. P.; Fertil, B.; Chavaudra, N.; Guichard, M. Distribution of radiation sensitivities for human tumor cells of specific histological types: Comparison of in vitro to in vivo data. Int. J. Radiat. Oncol. Biol. Phys. 12:617-624; 1986.
53. McIlwrath, A. J.; Vasey, P. A.; Ross, G. M.; Brown, R. Cell cycle arrests and radiosensitivity of human tumor cell lines: Dependence on wild-type p53 for radiosensitivity. Cancer Res. 54:3718-3722; 1994.
54. Mietz, J. A.; Unger, T.; Huibregtse, J. M.; Howley, P. M. The transcriptional transactivation function of wild-type p53 is inhibited by SV40 large T-antigen and by HPV-16 E6 oncoprotein. EMBO J. 11:5013-5020; 1992.
55. Mitchell, J. B.; Bedford, J. S.; Bailey, S. M. Dose-rate effects in mammalian cells in culture. III. Comparison of cell killing and cell proliferation during continuous irradiation for six different cell lines. Radiat, Res. 79:537-551; 1979.
56. Miyashita, T.; Krajewski, S.; Krajewska, M.; Wang, H. G.; Lin, H. K.; Hoffman, B.; Reed, J. C. Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9:1799-1805; 1994.
57. Miyashita, T.; Reed. J. C. Bcl-2 gene transfer increases relative resistance of S49. 1 and WEH17.2 lymphoid cells to cell death and DNA fragmentation induced by glucocorticoid and multiple chemotherapeutic drugs. Cancer Res. 52:5407-5411; 1992.
58. Miyashita, T.; Reed, J. C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80:293-297; 1995.
59. Munger, K.; Werness, B. A.; Dyson, N.; Phelps, W. C.; Howley, P. M. Complex formation of human papillomavirus E7 proteins with the retionoblastoma tumor suppressor gene product. EMBO J. 8:4099-4105; 1989.
60. Muschel, R. J.; Zhang, H. B.; McKenna, W. G. Differential effect of ionizing radiation on the expression of cyclin A and cyclin B in HeLa cells. Cancer Res. 53:1128-1135; 1993.
61. Nelson, W. G.; Kastan, M. B. DNA strand breaks: The DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol. Cell. Biol. 14:1815-1823; 1994.
62. O'Connor, P. M.; Jackman, J.; Jondle, D.; Bhatia, K.; Magrath, I.; Kohn, K. W. Role of the p53 tumor suppression gene in cell cycle arrest and radiosensitivity of Burkitt's lymphoma cell lines. Cancer Res. 53:4776-1780; 1993.
63. Oltvai, Z. N.; Milliman, C. L.; Korsmeyer, S. J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619; 1993.
64. CIP1 in muscle and other terminally differentiating cells. Science 267:1024-1027; 1995.
65. Peacock, J. W.; Chung, S.; Bristow, R. G.; Hill, R. P.; Benchimol, S. The p53-mediated G1 checkpoint is retained in tumorigenic rat embryo fibroblast clones transformed by the human papillomavirus type E7 gene and EJ-ras. Mol. Cell. Biol. 15:1446-1454; 1995.
66. Parshad, R.; Price, F. M.; Pirollo, K. F.; Chang, E. H.; Sanford, K. K. Cytogenetic response to G2-phase x-irradiation in relation to DNA repair and radiosensitivity in a cancer-prone family with Li-Fraumeni syndrome. Radiat. Res. 136:236-240; 1993.
67. Powell, S. N.; DeFrank, J. S.; Connell, P.; Eogan, M.; Preffer, F.; Dombkowski, D.; Tang, W.; Friend, S. Differential sensitivity of p53(-) and p53(+) cells to caffeine-induced radiosensitization and override of G2 delay. Cancer Res. 55:1643-1648; 1995.
68. Russell, K. J.; Wiens, L. W.; Demers, G. W.; Galloway, D. A.; Pion, S. E.; Groudine, M. Abrogation of the G2 checkpoint results in differential radiosensitization of G1 checkpoint-deficient and G1 checkpoint-competent cells. Cancer Res. 55:1639-1642; 1995.
69. Sheffner, M.; Werness, B. A.; Huibregtse, J. M.; Levine, A. J.; Howley, P. M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136; 1990.
70. Shero, J. H.; Bordwell, B.; Rothfield, N. R.; Earnshaw, W. C. High titer of autoantibodies to topoisomerase I (Scl-70) in sera from scleroderma patients. Science 231:737-740; 1986.
71. Sinclair, W. K. Cyclic X-ray responses in mammalian cells in vitro. Radiat. Res. 33:620-643; 1968.
72. Sinclair, W. K.; Morton, R. A. X-Ray sensitivity during the cell generation cycle of cultured Chinese hamster cells. Radiat. Res. 29:450-479; 1966.
73. Slebos, R. J.; Lee, M. H.; Plunkett, B. S.; Kessis, T. D.; Williams, B. O.; Jacks, T.; Hedrick, L.; Kastan, M. B.; Cho, K. R. p53-Dependent G1 arrest involves pRB-related proteins and is disrupted by the human papillomavirus 16 E7 oncoprotein. Proc. Natl. Acad. Sci. USA 91:5320-5324; 1994.
74. Slichenmyer, W. J.; Nelson, W. G.; Slebos, R. J.; Kastan, M. B. Loss of a p53-associated G1 checkpoint does not decrease cell survival following DNA damage. Cancer Res. 53:4164-4168; 1993.
75. Strasser, A.; Harris, A. W.; Jacks, T.; Cory, S. DNA damage can induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhibitable by Bcl-2, Cell 79:329-339; 1994.
76. Su, L.-N.; Little, J. B. Transformation and radiosensitivity of human diploid skin fibroblasts transfected with SV40 T-antigen mutant defective in RB and p53 binding domains. Int. J. Radiat. Biol. 62:461-468; 1992.
77. Tolmach, L. J.; Jones, R. W.; Busse, P. M. The action of caffeine on X-irradiated HeLa cells. I. Delayed inhibition of DNA synthesis. Radiat. Res. 71:653-665; 1977.
78. Tsang, N.-M.; Little, J. B. Effect of restoration of retinoblastoma gene function on the radiosensitivity of cells of human tumor cell lines. Radiat. Res. 140:172-179; 1994.
79. Tsang, N. M.; Nagasawa, H.; Li, C.; Little, J. B. Abrogation of p53 function by transfection of HPV16 E6 gene enhances the resistance of human diploid fibroblasts to ionizing radiation. Oncogene 10:2403-2408; 1995.
80. Vindelov, L. L. Flow microfluorometric analysis of nuclear DNA in cells from solid tumors and cell suspensions. Virchows Arch. Cell. Pathol. 24:227-242; 1977.
81. Wang, Y.; Okan, I.; Szekely, L.; Klein, G.; Wiman, K. G. bcl-2 inhibits wild-type p53-triggered apoptosis but not G1 cell cycle arrest and transactivation of WAF1 and bax. Cell. Growth Differ. 6:1071-1075; 1995.
82. Werness, B. A.; Levine, A. J.; Howley, P. M. Association of human papillomavirus types 16 and 18 E6 protein with p53. Science 248:76-79; 1990.
83. Xu, C.; Meikrantz, W.; Schlegel, R.; Sager, R. The human papilloma virus 16 E6 gene sensitizes human mammary epithelial cells to apoptosis induced by DNA damage. Proc. Natl. Acad. Sci. USA 92:7829-7833; 1995.
84. Zhan, Q.; Fan, S.; Bae, I.; Guilouf, C.; Liebermann, D. A.; O Connor, P. M.; Fornace, A. J. Induction of bax by genotoxic stress in human cells correlates with normal p53 status and apoptosis. Oncogene 9:3743-3751; 1994.
85. zur Hausen, H. Papillomaviruses as carcinomaviruses. In: Klein, G., ed. Advances in viral oncology, Vol. 8. New York: Raven Press; 1989:1-26.