Hypersensitivity of human testicular tumors to etoposide-induced apoptosis is associated with functional p53 and a high Bax:Bcl-2 ratio

Cancer Research

Volumn 56, Issue 8, 1996, Pages 1834-1841

  Chresta, Christine M ^a   Masters, John R W ^b   Hickman, John A ^a  

^a School of Biological Sciences   (United Kingdom)

^b INSTITUTE OF UROLOGY AND NEPHROLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ETOPOSIDE; PROTEIN P53;

APOPTOSIS; ARTICLE; BLADDER CANCER; CANCER CHEMOTHERAPY; CANCER SUSCEPTIBILITY; CHEMOSENSITIVITY; DNA DAMAGE; DNA STRAND BREAKAGE; DRUG SENSITIVITY; GENOTOXICITY; HUMAN; HUMAN CELL; HYPERSENSITIVITY; METASTASIS; PRIORITY JOURNAL; TESTIS TUMOR; TRANSACTIVATION; TRANSCRIPTION REGULATION;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; CELL SURVIVAL; DNA DAMAGE; DNA, NEOPLASM; DOSE-RESPONSE RELATIONSHIP, DRUG; ETOPOSIDE; FLOW CYTOMETRY; HUMANS; MALE; NOCODAZOLE; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; TESTICULAR NEOPLASMS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53; URINARY BLADDER NEOPLASMS;

EID: 0029929672     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (70)

1. Frei, E., III. Curative cancer chemotherapy. Cancer Res , 45: 6532-6537, 1985
2. Masters, J. R., Osborne, E. J., Walker, M C., and Parris, C. N. Hypersensitivity of human testis-tumour cell lines to chemotherapeutic drugs. Int. J Cancer, 53: 340-346, 1993.
3. Parris, C. N., Arlett C. F., Lehmann, A. R., Green, M. H., and Masters, J R, Differential sensitivities to γ radiation of human bladder and testicular tumour cell lines. Int J Radiat Biol & Relat Stud. Phys Chem. & Med , 53: 599-608, 1988.
4. Fry, A. M., Chresta, C. M., Davies, S M , Walker, M C , Harriys, A L., Hartley, J. A., Masters, J. R , and Hickson, I. D. Relationship between topoisomerase II level and chemosensitivity in human tumor cell lines. Cancer Res., 51: 6592-6595, 1991
5. Bedford, P., Fichtinger-Schepman, A M J., Shellard, S. A , Walker, M. C , Masters, J. R W., and Hill, B. T. Differential repair of platinum-DNA adducts in human bladder and testicular tumor continuous cell lines Cancer Res., 48 3019-3024, 1988.
6. O'Connor, P M., Wassermann, K., Sarang, M., Magrath, I , Bohr, V. A., and Kohn, K. W Relationship between DNA cross-links, cell cycle, and apoptosis in Burkitt's lymphoma cell lines differing in sensitivity to nitrogen mustard. Cancer Res., 51: 6550-6557, 1991.
7. Lowe, S. W., Ruley, H. E., Jacks, T., and Housman, D E p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell, 74: 957-967, 1993.
8. Lowe, S. W., Schmitt, E. M , Smith, S W , Osborne, B. A., and Jacks. T p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature (Lond ), 362: 847-849, 1993
9. Dive, C., and Hickman, J. A. Drug-target interactions, only the first step in the commitment to a programmed cell death? Br. J Cancer, 64: 192-196, 1991.
10. Fisher, T. C , Milner, A E., Gregory, C. D., Jackman, A. L , Aherne, G. W., Hartley, J A., Dive, C , and Hickman, J A. Bcl-2 modulation of apoptosis induced by anticancer drugs: resistance to thymidylate stress is independent of classical resistance pathways. Cancer Res., 53: 3321-3326, 1993.
11. Clarke, A. R , Purdie, C A , Harrison, D. J , Morris, R G , Bird, C C , Hooper, M L., and Wyllie, A. H. Thymocyte apoptosis induced by p53-dependent and independent pathways Nature (Lond.), 362: 849-852, 1993
12. Merritt, A. J , Potten, C S., Kemp, C. J., Hickman, J. A., Balmain, A , Lane, D P., and Hall, P A The role of p53 in spontaneous and radiation-induced apoptosis in the gastrointestinal tract of normal and p53-deficient mice. Cancer Res , 54, 614-617, 1994.
13. Maltzman, W., and Czyzyk, L. UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells Mol Cell Biol , 4 1689-1694, 1984.
14. Fritsche, M , Haessler, C., and Brandner, G. Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents [published erratum appears in Oncogene, 8: 2605, 1993]. Oncogene, 8, 307-318, 1993.
15. 1 arrest and apoptosis. Cancer Res., 54: 1169-1174, 1994
16. Barak, Y , Juven, T., Haffner, R., and Oren, M. mdm2 expression is induced by wild type p53 activity. EMBO J., 12: 461-468, 1993.
17. Perry, M. E., Piette, J , Zawadzki, J A., Harvey, D., and Levine, A. J. The mdm-2 gene is induced in response to UV light in a p53-dependent manner. Proc. Natl Acad. Sci USA, 90: 11623-11627, 1993.
18. Zhan, Q., Bae, I., Kastan, M. B., and Fornace, A. J The p53-dependent γ-ray response of GADD45. Cancer Res., 54, 2755-2760, 1994.
19. Kastan, M. B , Onyekwere, O., Sidransky, D , Vogelstein, B., and Craig, R. W. Participation of p53 protein in the cellular response to DNA damage. Cancer Res , 51: 6304-6311, 1991
20. Kuerbitz, S. J., Plunkett, B. S., Walsh, W. V., and Kastan, M. B. Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc Natl. Acad. Sci. USA, 89: 7491-7495, 1992.
21. Canman, C. E., Gilmer, T. M., Coutts, S. B., and Kastan, M. B. Growth factor modulation of p53-mediated growth arrest versus apoptosis. Genes & Dev., 9: 600-611, 1993.
22. Yin, X. M., Oltval, Z N., and Korsmeyer, S. J. BH1 and 8BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature (Lond.), 369: 321-323, 1994.
23. Korsmeyer, S. J. Shutter, J R., Veis, D J., Merry, D. E., and Oltvai, Z N. Bcl-2/Bax: a rheostat that regulates an anti-oxidant pathway and cell death. Semin Cancer Biol , 4: 327-332, 1993
24. Olivai, Z N , Milliman, C. L., and Korsmeyer, S J Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell, 74: 609-619, 1993.
25. Farrow, S. N., White, J. H. M., Martinou, I., Raven, T , Pun, K-T., Grinham, C. J., Martinou, J-C , and Brown, R. Cloning of a Bcl-2 homologue by interaction with adenovirus E1B 19K Nature (Lond.), 374, 731-733, 1995.
26. Yang, E., Zha, J , Jockei, J., Boise, L. H., Thompson, C B., and Korsmeyer, S. J. Bad, a heterodimeric partner for Bcl-XL and Bcl-2 displaces Bax and promotes death. Cell, 80: 285-291, 1995.
27. Boise, L H , Gonzalez, G M., Postema, C. E., Ding, L., Lindsten, T., Turka, L. A., Mao, X , Nunez, G., and Thompson, C. B. bcl-x, a Bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell, 74: 597-608, 1993
28. Reed, J. C. Bcl-2 and the regulation of programmed cell death. J. Cell Biol., 124: 1-6, 1994.
29. Walton, M. I., Whysong, D., O'Connor, P. M., Hockenbery, D., Korsmeyer, S. J., and Kohn, K W Constitutive expression of human Bcl-2 modulates nitrogen mustard and camptothecin induced apoptosis. Cancer Res , 53: 1853-1861, 1993
30. Takayama, S., Sato, T , Krajewski, S., Kochel, K., Irie, S., Millan, J. A. and Reed, J. C. Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell, 80, 279-284, 1995.
31. Peckham, M. J., Horwich, A., Blackmore, C., and Hendry, W. F. Etoposide and cisplatin with or without bleomycin as first-line chemotherapy for patients with small-volume metastases of testicular nonseminoma. Cancer Treat. Rep., 69: 483-488, 1985.
32. Fitzharris, B. M., Kaye, S. B., Saverymuttu, S., Newlands, E. S., Barrett, A., Peckham, M. J , and McElwain, T J. VP16-213 as a single agent in advanced testicular tumors. Eur J. Cancer. 16, 1193-1197, 1980.
33. Kamesaki, S , Kamesaki, H , Jorgensen, T. S., Tanizawa, A , Pommier, Y., and Cossman, J. Bcl-2 protein inhibits etoposide-induced apoptosis through its effects on events subsequent to topoisomerase II-induced DNA strand breaks and their repair. Cancer Res., 53. 4251-4256, 1993.
34. Kondo, S , Yin, D., Takeuchi, J , Morimura, T , Oda, Y , and Kikuchi, H. Bcl-2 gene enables rescue from in vitro myelosuppression (bone marrow cell death) induced by chemotherapy. Br J Cancer, 70. 421-426, 1994.
35. Peng, H. Q., Hogg, D , Malkin, D., Bailey, D., Gallie, B L., Bulbul, M , Jewett, M., Buchanan, J., and Goss, P. E. Mutations of the p53 gene do not occur in testis cancer. Cancer Res , 53 3574-3578, 1993.
36. Heimdal, K , Lothe, R A., Lystad, S , Holm, R., Fossa, S. D., and Borresen, A. L. No germline TP53 mutations detected in familial and bilateral testicular cancer. Genes Chromosomes & Cancer. 6: 92-97, 1993.
37. Sidransky, D , Von, E A., Tsai, Y C., Jones, P., Summerhayes, I., Marshall, F., Paul, M., Green, P., Hamilton, S R , Frost, P., and Vogelstein, B. Identification of p53 gene mutations in bladder cancers and urine samples Science (Washington DC), 252: 706-709, 1991
38. Fujimoto, K , Yamada, Y , Okajima, E , Kakizoe, T , Sasaki, H., Sugimura, T., and Terada, M. Frequent association of p53 gene mutation in invasive bladder cancer. Cancer Res., 52 1393-1398, 1992.
39. Hockenbery, D. M , Zutter, M., Hickey, W., Nahm, M , and Korsmeyer, S. J. BCL2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc Natl. Acad. Sci USA, 88. 6961-6965, 1991
40. Krajewski, S., Bodrug, S , Gascoyne, R , Berean, K., Krajewska, M , and Reed, J C Immunohistochemical analysis of Mcl-1 and Bcl-2 proteins in normal and neoplastic lymph nodes. Am. J. Pathol., 145. 515-525, 1994
41. Bertrand, R., Sarang, M . Jenkin, J , Kerrigan, D., and Pommier, Y. Differential induction of secondary DNA fragmentation by topoisomerase II inhibitors in human tumor cell lines with amplified c-myc expression. Cancer Res., 51: 6280-6285, 1991.
42. Beere, H M , Chresta, C M., Alejo-Herberg, A., Skladanowski, A., Dive, C., Kragh-Larsen, A., and Hickman, J. A. Investigation of the mechanism of higher order chromatin fragmentation observed in drug-induced apoptosis Mol. Pharmacol , 47: 986-996, 1995
43. Kohn, K W., Erickson, L C , Ewig, R , and Friedman, C. A Fractionation of DNA from mammalian cells by alkaline elution Biochemistry, 15: 4629-1637, 1976
44. Kawasaki, T., Tomita, Y , Watanabe, R., Tanikawa, T., Kumanishi, T., and Sato, S. mRNA and protein expression of p53 mutations in human bladder cancer cell lines. Cancer Lett., 82, 113-121, 1994.
45. Fan, S , El-Deiry, W., Bae, I., Freeman, J., Jondle, D., Bhatia, K., Fornace, A. J., Magrath, I., Kohn, K. W., and 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.
46. Miyashita, T., Harigai, M , Hanada, M., and Reed, J. C. Identification of a p53-dependent negative response element in the Bcl-2 gene. Cancer Res., 54: 3131-3135, 1994.
47. Miyashita, T , Krajewski, S., Krajewska, M , Wang, H. G., Lin, H. K , Liebermann, D. A., Hoffman, B., and Reed, J. C. Tumor suppressor p53 is a regulator of Bcl-2 and box gene expression in vitro and in vivo. Oncogene, 9: 1799-1805, 1994.
48. Walker, M. C., Parris, C. N., and Masters, J. R Differential sensitivities of human testicular and bladder tumor cell lines to chemotherapeutic drugs. J. Natl. Cancer Inst., 79: 213-216, 1987
49. Sark, M. W. J., Timmer-Bosscha, H., Meijer, C , Uges, D. R. A., Sluiter, W J., Peters, W. H. M , Mulder, N. H , and deVries, E. G. E. Cellular basis for differential sensitivity to cis-platin in human germ cell rumour and colon carcinoma cell lines. Br. J. Cancer, 71: 684-690, 1995.
50. Fleischhacker, M , Strohmeyer, T , Imai, Y., Slamon, D J , and Koeffler, H. P. Mutations of the p53 gene are not detectable in human testicular tumors. Mod. Pathol., 7: 435-439, 1994.
51. Bartek, J., Bartkova, J., Vojtesek, B., Staskova, Z., Lukas, J , Rejthar, A., Kovarik, J., Midgley, C. A., Gannon, J V, and Lane, D. P. Aberrant expression of the p53 oncoprotein is a common feature of a wide spectrum of human malignancies. Oncogene, 6: 1699-1703, 1991.
52. Bartkova, J., Bartek, J., Lukas, J., Vojtesek, B., Staskova, Z., Rejthar, A., Kovarik, J., Midgley, C. A., and Lane, D. P. p53 protein alterations in human testicular cancer including pre-invasive intratubular germ-cell neoplasia. Int. J. Cancer, 49: 196-202, 1991.
53. Reich, N. C., Oren, M., and Levine, A. J. Two distinct mechanisms regulate the levels of a cellular tumor antigen, p53. Mol. Cell. Biol., 3. 2143-2150, 1983.
54. Rogel, A., Popliker, M., Webb, C G , and Oren, M. p53 cellular tumor antigen. analysis of mRNA levels in normal adult tissues, embryos, and tumors. Mol. Cell. Biol., 5: 2851-2855, 1985
55. Tesch, H., Furbass, R., Casper, J , Lyons, J., Bartram, C. R., Schmoll, H. J., and Bronson, D. L. Cellular oncogenes in human teratocarcinoma cell lines. Int. J Androl., 13: 377-388, 1990.
56. Zhang, H., Hannon, G. J., and Beach, D p21-containing cyclin kinases exist in both active and inactive states. Genes & Dev., 8: 1750-1758, 1994.
57. Michieli, P., Chedid, M., Lin, D., Pierce, J H., Mercer, W. E., and Givol, D. Induction of WAF1/CIP1 by a p53-independent pathway. Cancer Res., 54: 3391-3395, 1994.
58. Fanning, P., Bulovas, K., Saini, K. S., Libertino, J. A , Joyce, A D., and Summerhayes, I. C. Elevated expression of pp60c-src in low-grade human bladder carcinoma. Cancer Res., 52. 1457-1462, 1992.
59. Burchill, S. A , Neal, D E., and Lunec, J. Frequency of H-ras mutations in human bladder cancer detected by direct sequencing. Br. J. Urol., 73: 516-521, 1994.
60. Levesque, P., Ramchurren, N., Saini, K., Joyce, A , Libertino, J., and Summerhayes, I C. Screening of human bladder tumors and urine sediments for the presence of H-ras mutations. Int. J. Cancer, 55: 785-790, 1993.
61. Wagner, A J., Kokontis, J. M., and Hay, N. Myc-mediated apoptosis requires wild-type p53 in a manner independent of cell cycle arrest and the ability of p53 to induce p21waf1/cip1. Genes & Dev., 8: 2817-2830, 1994.
62. 1 arrest. Proc. Natl Acad. Sci. USA, 91: 10079-10083, 1994.
63. Wu, X., and Levine, A. J. p53 and E2F-I cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA, 91: 3602-3606, 1994.
64. Misaki, H., Shuin, T., Yao, M , Kubota, Y., and Hosaka, M. Expression of myc family oncogenes in primary human testicular cancer. Nippon Hinyokika Gakkai Zasshi, 80: 1509-1513, 1989.
65. Watson, J V., Stewart, J., Evan, G. I., Ritson, A., and Sikora, K. The clinical significance of flow cytometric c-myc oncoprotein quantitation in testicular cancer. Br. J Cancer, 53: 331-337, 1986.
66. Caelles, C., Helmberg, A., and Karin, M. p53-dependent apoptosis in the absence of transcriptional activation of p53 target genes. Nature (Lond.), 370, 220-223, 1994.
67. Shen, Y., and Shenk, T. Relief of p53-mediated transcriptional repression by the adenovirus E1B 19 kDa protein or the cellular Bcl-2 protein. Proc. Natl. Acad Sci. USA, 91: 8940-8944, 1994.
68. Sabbatini, P., Chiou, S. K., Rao, L , and White, E. Modulation of p53-mediated transcriptional repression and apoptosis by the adenovirus E1B 19K protein Mol. Cell Biol , 15 1060-1070, 1995.
69. Selvakumaran, M, Lin, H. K., Miyashita, T., Wang, H. G., Krajewski, S., Reed, J. C., Hoffman, B., and Liebermann, D. Immediate early up-regulation of bax expression by p53 but not TGF β1: a paradigm for distinct apoptotic pathways. Oncogene, 9: 1791-1798, 1994.
70. Zhan, Q., Fan, S., Bae, I , Guillouf, C., Liebermann, D. A., O'Connor, P. M., and Fornace, A J. Induction of bax by genotoxic stress in human cells correlates with normal p53 status and apoptosis. Oncogene, 9: 3743-3751, 1994.