Cisplatin inhibits paclitaxel-induced apoptosis in cisplatin-resistant ovarian cancer cell lines: Possible explanation for failure of combination therapy

Cancer Research

Volumn 59, Issue 10, 1999, Pages 2425-2432

  Judson, Patricia L ^a   Watson, Joanna M ^b   Gehrig, Paola A ^a   Fowler Jr , Wesley C ^a   Haskill, J Stephen ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; PACLITAXEL;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG INHIBITION; DRUG SENSITIVITY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; MICROTUBULE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN DEGRADATION; TREATMENT FAILURE;

ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL CYCLE; CISPLATIN; DNA FRAGMENTATION; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; MICRONUCLEUS TESTS; MICROTUBULES; NEOPLASM PROTEINS; OVARIAN NEOPLASMS; PACLITAXEL; PROTO-ONCOGENE PROTEINS C-BCL-2; TREATMENT FAILURE; TUMOR CELLS, CULTURED; TUMOR STEM CELLS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0033562991     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

1. Rowinsky, E. K., and Donehower, R. C. Paclitaxel (paclitaxel). N. Engl. J. Med., 332: 1004-1014, 1995.
2. Thigpen, J. T., Blessing, J. A., Ball, H., Hummel, S. J., and Barrett, R. J. Phase II trial of paclitaxel in patients with progressive ovarian carcinoma after platinum-based chemotherapy: a Gynecologic Oncology Group study. J. Clin. Oncol., 12: 1748-1753, 1994.
3. McGuire, W. P., Hoskins, W. J., Brady, M. F., Kucera, P. R., Partridge, E. E., Look, K. Y., Clarke-Pearson, D. L., and Donaldson, M. Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. N. Engl. J. Med., 334: 1-6, 1996.
4. Mayerhoffer, K., Kucera, E., Zeisler, H., Speiser, P., Reinthaller, A., and Sevelda, P. Taxol as second-line treatment in patients with advanced ovarian cancer after platinum-based first-line chemotherapy. Gynecol. Oncol., 64: 109-113, 1997.
5. Fennelly, D., Aghajanian, C., Shapiro, F., O'Flaherty, C., McKenzie, M., O'Connor, C., Tong, W., Norton, L., and Spriggs, D. Phase I and pharmacologic study of paclitaxel administered weekly in patients with relapsed ovarian cancer. J. Clin. Oncol., 15: 187-192, 1997.
6. Kaufmann, W. K., and Paules, R. S. DNA damage and cell cycle checkpoints. FASEB J., 10: 238-247, 1996.
7. Brown, R., Clugson, C., Burns, P., Edlin, A., Vasey, P., Vojtesek, B., and Kaye, S. B. Increased accumulation of p53 protein in cisplatin-resistant ovarian cell lines. Int. J. Cancer, 55: 678-684, 1993.
8. Perego, P., Giarola, M., Righelti, S. C., Supino, R., Caserini, C., Delia, D., Pierotti, M. A., Miyashita, T., Reed, J. C., and Zunino, F. Association between cisplatin resistance and mutation of p53 gene and reduced bax expression in ovarian carcinoma cell systems. Cancer Res., 56: 556-562, 1996.
9. Hawkins, D. S., Demers, G. W., and Galloway, D. A. Inactivation of p53 enhances sensitivity to multiple chemotherapeutic agents. Cancer Res., 56: 892-898, 1996.
10. Jekunen, A. P., Christen, R. D., Shalinsky, D. R., and Howell, S. B. Synergistic interaction between cisplatin and Taxol in human ovarian carcinoma cells in vitro. Br. J. Cancer, 69: 299-306, 1994.
11. Horowitz, S. B. Mechanism of Taxol action. Trends Pharmacol. Sci., 13: 134-136, 1992.
12. Woods, C. M., Zhu, J., McQueney, P. A., Bollag, D., and Lazarides E. Taxol-induced mitotic block triggers rapid onset of a p53-independent apoptotic pathway. Mol. Med., 1: 506-526, 1995.
13. Haldar, S., Chintapalli, J., and Croce, C. M. Taxol induces bcl-2 phosphorylation and death of prostate cancer cells. Cancer Res., 56: 1253-1255, 1996.
14. Jordan, M. A., Wendell, K., Gardiner, S., Derry W. B., Copp. H., and Wilson, L. Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death. Cancer Res., 56: 816-825, 1996.
15. Debernardis, D., Sire, E. G., De Feudis, P., Vikhanskaya, F., Valenti, M., Russo, P., Parodi, S., D'Incali, M., and Broggini, M. p53 status does not affect sensitivity of human ovarian cancer cell lines to paclitaxel. Cancer Res., 57: 870-874, 1997.
16. 2/M arrest and apoptosis. Nat. Med., 2: 72-79. 1996.
17. Kavallaris, M., Kuo, D. Y-S., Burkhart, C. A., Regl, D. L., Morris, M. D., Haber, M., and Horowitz, S. B. Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific β-tubulin isotypes. J. Clin. Investig., 100: 1282-1293, 1997.
18. Ranganathan, S., Benetatos, C. A., Colarusso, P. J., Dexter, D. W., and Hudes, G. R. Altered β-tubulin isotype expression in paclitaxel-resistant human prostate carcinoma cells. Br. J. Cancer, 77: 562-566, 1998.
19. Giannakakou, P., Sackett, D. L., Kang, Y. K., Zhan, Z., Buters, J. T., Fojo, T., and Puruchynsky, M. S. Paclitaxel-resistant human ovarian cancer cells have mutant β-tubulins that exhibit impaired paclitaxel-driven polymerization. J. Biol. Chem., 272: 17118-17125, 1997.
20. Dumontet, C., Duran, G. E., Steger, K. A., Beketic-Oreskovic, L., and Sikic, B. I. Resistance mechanisms in human sarcoma mutants derived from single-step exposure to paclitaxel (Taxol). Cancer Res., 56: 1091-1097, 1996.
21. Wang, T. H., Wang, H. S., Jchijo, H., Giannalalou, P., Foster, J. S., Fojo, T., and Wimalesena, J. Microtubule-interfering agents activate c-Jun N-terminal kinase/stress activated protein kinase through both Ras and apoptosis signal-regulating kinase pathways. J. Biol. Chem., 273: 4928-4938, 1998.
22. 2-terminal kinase/activator protein 1 pathway and inhibition of extracellular signal-regulated kinase are early effects in paclitaxel-mediated apoptosis in human B lymphoblasts. Cancer Res., 58: 241-247, 1998.
23. Lee, L-F., Haskill, J. S., Mukaida, N., Matsushima, K., and Ting, J. P-Y. Identification of tumor-specific paclitaxel (Taxol)-responsive regulatory elements in the interleukin-8 promoter. Mol. Cell. Biol., 17: 5097-5105, 1997.
24. Das, K. C., and White, C. W. Activation of NF-κB by antineoplastic agents. Role of protein kinase C. J. Biol. Chem., 272: 14914-14920, 1997.
25. Gately, D. P., and Howell, S. B. Paclitaxel activation of GADDI53 promoter through a cellular injury response element containing an essential Sp1 binding site. J. Biol. Chem., 271: 20588-20593, 1996.
26. Perera, P. Y., Quereshi, N., and Vogel, S. N. Paclitaxel (Taxol)-induced nuclear factor κB translocation in murine macrophages. Infect. Immun., 64: 878-884, 1996.
27. Tishler, R. B., Lamppu, D. M., Park, S., and Price, B. D. Microtubule-active drugs Taxol, vinblastine, and nocodazole increase the levels of transcriptionally active p53. Cancer Res., 55: 6021-6025, 1995.
28. Gately, D. P., Sharma, A., Christen, R. D., and Howell, S. B. Cisplatin and Taxol activate different signal pathways regulating cellular injury-induced expression of GADDI53. Br. J. Cancer, 73: 18-23, 1996.
29. Lee, L-F., Schuerer-Maly, C-C., Lofquist, A. K., van-Haaften-Day, C., Ting, J. P-Y., White, C. M., Martin, B. K., and Haskill, J. S. Taxol-dependent transcriptional activation of IL-8 expression in a subset of human ovarian cancer. Cancer Res., 56: 1303-1309, 1996.
30. Watson, J. M., Kingston, D. G. I., Chordia, M. D., Chaudhary, A. G., Rinehart, C. A., and Haskill, J. S. Identification of the structural region of Taxol that may be responsible for cytokine gene induction and cytotoxicity in human ovarian cancer cells. Cancer Chemother. Pharmacol., 41: 391-397, 1998.
31. Ding, A. H., Porteu, F., Sanchez, E., and Nathan, C. F. Shared actions of endotoxin and Taxol on TNF receptors and TNF release. Science (Washington DC), 248: 370-372, 1990.
32. Bogdan, C., and Ding, A. Taxol, a microtubule-stabilizing antineoplastic agent, induces expression of tumor necrosis factor α and interleukin-1 in macrophages. J. Leukocyte Biol., 52: 119-121, 1992.
33. Moos, P. J., and Fitzpatrick, F. A. Taxane-mediated gene induction is independent of microtubule stabilization: induction of transcription regulators and enzymes that modulate inflammation and apoptosis. Proc. Natl. Acad. Sci. USA, 95: 3896-3901, 1998.
34. Kirikae, T., Kirikae, F., Oghiso, Y., and Nakano, M. Microtubule-disrupting agents inhibit nitric oxide production in murine peritoneal macrophages stimulated with lipopolysaccharide or paclitaxel (Taxol). Infect. Immun., 64: 3379-3384, 1996.
35. White, C. M., Martin, B. K., Lee, L-F., Haskill, J. S., and Ting, J. P-Y. Effects of paclitaxel on cytokine synthesis by unprimed human monocytes, T lymphocytes and breast cancer cells. Cancer Immunol. Immunother., 46: 104-112, 1998.
36. Kumar, C. C., Kim, J. H., Bushel, P., Armstrong, L., and Catino, J. J. Activation of smooth muscle α-actin promoter in ras-transformed cells by treatments with antimitotic agents: correlation with stimulation of SRF:SRE mediated gene transcription. J. Biochem., 118: 1285-1292, 1995.
37. Milross, C. G., Peters, L. J., Hunter, N. K., Mason, K. A., and Milas, L. Sequence-dependent antitumor activity of paclitaxel (Taxol) and cisplatin in vivo. Int. J. Cancer, 62: 599-604, 1995.
38. Vanhoefer, U., Harstick, A., Wilke, H., Schleucher, N., Walles, H., Schröder, J., and Seeber, S. Schedule-dependent antagonism of paclitaxel and cisplatin in human gastric and ovarian carcinoma cell lines in vitro. Eur. J. Cancer, 31A: 92-97, 1995.
39. Mossmann, T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods, 83: 55-58, 1983.
40. Cistulli, C. A., and Kaufmann, W. K. p53-dependent signaling sustains DNA replication and enhances clonogenic survival in 254 nm ultraviolet-irradiated human fibroblasts. Cancer Res., 58: 1993-2002, 1998.
41. Ling, Y. H., Tomos, C., and Perez-Soler, R. Phosphorylation of Bcl-2 is a marker of M phase events and not a determinant of apoptosis. J. Biol. Chem., 273: 18984-18991, 1998.
42. Siddik, Z. H., Mims, B., Lozano, G., and Thai, G. Independent pathways of p53 induction by cisplatin and X-rays in a cisplatin-resistant ovarian tumor cell line. Cancer Res., 58: 698-703, 1998.
43. Motzer, R. J., Chou, T. C., Schwatz, L., Bosl, G. J., Bajorin, D. F., and Hutter, H. Paclitaxel in germ cell cancers. Semin. Oncol., 22 (Suppl. 6): 12-15, 1995.
44. Woo, H. L., Swanerton, K. D., and Hoskins, P. J. Taxol is active in platinum-resistant endometrial adenocarcinoma. Am. J. Clin. Oncol., 19: 290-291, 1996.
45. Fossella, F. V., Lee, J. S., Shin, D. M., Calayag, M., Huber, M., Perez-Soler, R., Murphy, W. K., Lippman, S., Benner, S., Glisson, B., Chasen, M., Hong, W. K., and Raber, M. Phase II study of docetaxel for advanced or metastatic platinum-refractory non-small cell lung cancer. J. Clin. Oncol., 13: 645-651, 1995.
46. Rowinsky, E. K. Paclitaxel pharmacology and other tumor types. Semin. Oncol., 24: S19-1-S19-12, 1997.
47. Johnson, K. R., Wang, L. M., Miller, M. C., Willingham, M. C., and Fan, W. M. 5-Fluorouracil interferes with paclitaxel cytotoxicity against human solid cancer cells. Clin. Cancer Res., 3: 1729-1745, 1997.
48. Johnson, S. W., Laub, P. B., Beesley, J. S., Ozols, R. F., and Hamilton, T. C. Increased platinum-DNA damage tolerance is associated with cisplatin resistance and cross-resistance to various chemotherapeutic agents in unrelated human ovarian cancer cell lines. Cancer Res., 57: 850-856, 1997.
49. Eichholtz-Wirth, H., Stoetzer, O., and Marx, K. Reduced expression of the ICE-related protease CPP32 is associated with radiation-induced cisplatin resistance in HeLa cells. Br. J. Cancer, 76: 1322-1327, 1997.
50. Kern, M. A., Helmbach, H., Artuc, M., Karmann, D., Jurgovsky, K., and Schadendorf, D. Human melanoma cell lines selected in vitro displaying various levels of drug resistance against cisplatin, fotemustine, vindesine, or etoposide: modulation of proto-oncogene expression. Anticancer Res., 17: 4359-4370, 1997.
51. Mello, J. A., Lippard, S. J., and Essigmann, J. M. DNA adducts of cis-diamminedichloroplatinum (II) and its trans-isomer inhibit RNA polymerase II differentially in vivo. Biochemistry, 34: 14788-14791, 1995.
52. Samuel, S. K., Spencer, V. A., Banjo, L., Sun, J. M., Holth, L. T., Oesterreich, S., and Davie, J. R. In situ cross-linking by cisplatin of nuclear matrix-bound transcription factors to nuclear DNA of human breast cancer cells. Cancer Res., 58: 3004-3008, 1998.
53. Jordan, P., and Carmofonseca, M. Cisplatin blocks synthesis of ribosomal RNA in vivo. Nucleic Acids Res., 26: 2831-2836, 1998.
54. Levasseur, L. M., Greco, W. R., Rustum, Y. M., and Slocum, H. K. Combined action of paclitaxel and cisplatin against wildtype and resistant human ovarian carcinoma cells. Cancer Chemother. Pharmacol., 40: 495-505, 1997.
55. Kano, Y., Akutsu, M., Tsunoda, S., Mori, K., Suzuki, K., and Adachi, K. I. In vitro schedule-dependent interaction between paclitaxel and SN-38 (the active metabolite of irinotecan) in human carcinoma cell lines. Cancer Chemother. Pharmacol., 42: 91-98, 1998.