Interferon-γ-Induced Sensitization of Colon Carcinomas to ZD9331 Targets Caspases, Downstream of Fas, Independent of Mitochondrial Signaling and the Inhibitor of Apoptosis Survivin

Clinical Cancer Research

Volumn 9, Issue 17, 2003, Pages 6504-6515

  Geller, James ^a   Petak, Istvan ^a   Szucs, Kinga Szekely ^a   Nagy, Katalin ^a   Tillman, David M ^a   Houghton, Janet A ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CASPASE 3; CASPASE 4; CASPASE 7; CASPASE 8; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FAS LIGAND; FLUOROURACIL; FOLINIC ACID; GAMMA INTERFERON; GENE PRODUCT; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NOK1 PROTEIN; NOK2 PROTEIN; PLEVITREXED; PROTEIN BCL 2; PROTEIN P53; RETROVIRUS VECTOR; SURVIVIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL SURVIVAL; COLON CARCINOMA; CONTROLLED STUDY; DNA DAMAGE; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; DRUG POTENTIATION; DRUG SENSITIZATION; DRUG TARGETING; ENZYME ACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; TUMOR CELL LINE;

ANTIGENS, CD95; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-X PROTEIN; CASPASE 3; CASPASE 7; CASPASE 8; CASPASES; CASPASES, INITIATOR; CELL LINE; CELL LINE, TUMOR; COLONIC NEOPLASMS; CYSTEINE ENDOPEPTIDASES; DNA, COMPLEMENTARY; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; ENZYME INHIBITORS; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOBLOTTING; INTERFERON TYPE II; KINETICS; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MULTIENZYME COMPLEXES; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-BCL-2; QUINAZOLINES; RETROVIRIDAE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 0346431866     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (69)

1. Houghton, J. A. Developing novel and highly effective new therapeutic strategies for treatment of colorectal cancer: where do we go from here? Curr. Opin. Investig. Drugs, 2: 674-676, 2001.
2. Cutsem, E. V., Dicato, M., and Wils, J. Recent advances in the management of colorectal cancer. Eur. J. Cancer, 37: 2302-2309, 2001.
3. Papamichael, D. The use of thymidylate synthase inhibitors in the treatment of advanced colorectal cancer: current status. Oncologist, 4: 478-487, 1999.
4. Advanced Colorectal Cancer Meta-analysis Project. Modulation of fluorouracil by leucovorin in patients with advanced colorectal cancer: evidence in terms of response rate. J. Clin. Oncol., 10: 896-903, 1992.
5. Ferguson, P. J., Collins, O. Dean, M. M., DeMoor, J., Sha-Li, C., Vincent, M. D., and Koropatnick, J. Antisense down-regulation of thymidylate synthase to suppress growth and enhance cytotoxicity of 5-FudR, 5-FU and Tomudex in HeLa cells. Br. J. Pharm., 127: 1777-1786, 1999.
6. Ladner, R., and Caradonna, S. Lowering dUTPase levels through antisense induces sensitivity to fluorodeoxyuridine in HT29 cells. Proc. Am. Assoc. Cancer Res., 28: 4126a, 1999.
7. Webley, S. D., Hardcastle, A. Ladner, R. D., Jackman, A. L., and Aherne, G. W. Deoxyuridine triphosphatase (dUTPase). expression and sensitivity to the thymidylate synthase (TS) inhibitor ZD9331. Br. J. Cancer, 83: 792-799, 2000.
8. Tillman, D. M., Petak, I., and Houghton, J. A. A Fas-dependent component in 5-fluorouracil/leucovorin-induced cytotoxicity in colon carcinoma cells. Clin. Cancer Res., 5: 425-430, 1999.
9. Schwartzberg, L. S., Petak, I., Stewart, C., Turner, P. K., Ashley, J., Tillman, D. M., Doublas, L., Tan, M., Billups, C., Mihalik, R., Weir, A., Tauer, K., Shope, S., and Houghton, J. A. Modulation of the Fas signaling pathway by IFN-γ in therapy of colon cancer: Phase I trial and correlative studies of IFN-γ, 5-fluorouracil, and leucovorin. Clin. Cancer Res., 8: 2488-2498, 2002.
10. Ikeda, H., Old, L. J., and Schreiber, R. D. The roles of IFNγ in protection against tumor development and cancer immunoediting. Cytokine Growth Factor Rev., 13: 95-109, 2002.
11. Varela, N., Munoz-Pinedo, C., Ruiz-Ruiz, C., Robledo, G., Pedroso, M., and Lopez-Rivas, A. Interferon-γ sensitizes human myeloid leukemia cells to death receptor-mediated apoptosis by a pleiotropic mechanism. J. Biol. Chem., 276: 17779-17787, 2001.
12. Boehm, U. Kamp, T., Groot, M., and Howard, J. C. Cellular responses to interferon-γ, Annu. Rev. Immunol., 15: 749-795, 1997.
13. Marsham, P. R., Wardelworth, J. M., Boyle, F. T., Hennequin, L. F., Kimbell, R., Brown, M., and Jackman, A. L. Design and synthesis of potent non-polyglutamatable quinazoline antifolate thymidylate synthase inhibitors. J. Med. Chem., 42: 3809-3820, 1999.
14. Jackman, A. L., Kimbell, R., Aherne, G. W., Brunton, L., Jansen, G., Stephens, T. C., Smith, M. N., Wardleworth, J. M., and Boyle, F. T. Cellular pharmacology and in vivo activity of a new anticancer agent, ZD9331: A water-soluble, nonpolyglutamatable, qunazoline-based inhibitor of thymidylate synthase. Clin. Cancer Res., 3: 911-921, 1997.
15. Jackman, A. L., Kimbell, R., Brown, M., Brunton, L., Harrap, K. R., Wardleworth, J. M., and Boyle, F. T. The Antitumor Activity of ZD9331. A Non-Polyglutamatable Quinazoline Thymidylate Synthase Inhibitor, Purine and Pyrimidine Metabolism in Man VIII, pp. 185-188. Sahota, A., and Taylor, M. (eds.), New York: Plenum Press: 1995.
16. Cunningham, D., Zalcberg, J., Maroun, J., James, R., Clarke, S., Maughan, T. S., Vincent, M., Schulz, J., Gonzalez Baron, M., and Facchini, T. Efficacy, tolerability and management of raltitrexed (Tomudex) monotherapy in patients with advanced colorectal cancer: a review of phase II/III trials. Eur. J. Cancer, 38: 478-86, 2002.
17. Jackman, A. L., Kelland, L. R., Kimbell, R., Brown, M., Gibson, W., Aherne, G. W., Hardcastle, A., and Boyle, F. T. Mechanisms of acquired resistance to the quinazoline thymidylate synthase inhibitor ZD1694 (tomudex) in one mouse and three human cell lines. Br. J. Cancer 71: 914-24, 1995.
18. Patterson, A. V., Talbot, D. C., Stratford, I. J., and Harris, A. L. Thymidine phosphorylase moderates thymidine-dependent rescue after exposure to the thymidylate synthase inhibitor ZD1694 (tomudex) in vitro. Cancer Res., 58: 2737-2740, 1998.
19. Cheradame, S., Chazal, M., Fischel, J. L., Formento, P., Renee, N., and Milano, G. Variable intrinsic sensitivity of human tumor cell lines to raltitrexed (Tomudex) and folylpolyglutamate synthetase activity. Anticancer Drugs, 10: 505-510, 1999.
20. Jackman, A. L., Melin, C. M., Kimbell, R., Brunton, L., Aherne, G. W., Theti, D. S., and Walton, M. A rationale for the clinical development of the thymidylate synthase inhibitor ZD9331 in ovarian and other solid tumors. Biochim. Biophys. Acta, 1587: 215-223, 2002.
21. Houghton, J. A., Adkins, D. A., Rahman, A., and Houghton, P. G. Interaction between 5-flurouracil, [6RS] leucovorin, and recombinant human interferon-α2a in cultured colon adenocarcinoma cells. Cancer Commun., 3: 223-231, 1991.
22. Houghton, J. A., Tillman, D. M., and Harwood, F. G. Ratio of 2′-deoxyadenosine-5′-triphosphate/thymidine-5′-triphosphate influences the commitment of human colon carcinoma cells to thymineless death. Clin. Cancer Res., 1: 723-730, 1995.
23. Teitz, T., Wei, T., Valentine, M. B., Vanin, E. F., Grenet, J., Valentine, V. A., Behm, F. G., Look, A. T., Lahti, J. M., and Kidd, V. J. Caspase 8 is deleted or silenced preferentially in childhood neuroblastomas with amplification of MYCN. Nat. Med., 6: 529-535, 2000.
24. Persons, D. A., Allay, J. A., Allay, E. R., Ashmun, R. A., Orlic, D., Jane, S. M., Cunningham, J. M., and Nienhuis, A. W. Enforced expression of the GATA-2 transcription factor blocks normal hematopoiesis. Blood, 93: 488-499, 1999.
25. Petak, I., Tillman, D. M., Harwood, F. G., Mihalik, R., and Houghton, J. A. Fas-dependent and independent mechanisms of cell death following DNA damage in human colon carcinoma cells. Cancer Res., 60: 2643-2650, 2000.
26. Petak, I., Tillman, D. M., and Houghton, J. A. P53 dependence of Fas induction and acute apoptosis in response to 5-fluorouracil-leucovorin in human colon carcinoma cell lines. Clin. Cancer Res., 1, 6: 4432-4441, 2000.
27. Takemura, Y., and Jackman, A. L. Folate-based thymidylate synthase inhibitors in cancer chemotherapy. Anticancer Drugs, 8: 3-16, 1997.
28. Danenberg, P. V., Malli, H., and Swenson, S. Thymidylate synthase inhibitors. Semin. Oncol., 26: 621-631, 1999.
29. Cassidy, J. Thymidylate synthase inhibitors in colorectal cancer. Semin. Int. Oncol. 27(Suppl. 10): 83-87, 2000.
30. Van Triest, B., Pinedo, H. M., van Hensbergen, Y., Smid, K., Telleman, F., Schoenmakers, P. S., van der Wilt, C. L. van Laar, J. A. M., Noordhuis, P., Jansen, G., and Peters, G. J. Thymidylate synthase level as the main predictive parameter for sensitivity to 5-fluorouracil, but not for folate-based thymidylate synthase inhibitors, in 13 nonselected colon cancer cell lines. Clin. Cancer Res., 5: 643-654, 1999.
31. Welsh, S. J., Titley, J., Brunton, L., Valenti, M., Monaghan, P., Jackman, A. L., and Aherne, G. W. Comparison of thymidylate synthase (TS) protein up-regulation after exposure to TS inhibitors in normal and tumor cell lines and tissues. Clin. Cancer Res., 6: 2538-2546, 2000.
32. Lanza, G., Maestri, I., Dubini, A., Gafa, R., Santini, A., Ferretti, S., and Cavazzini, L. p53 expression in colorectal cancer: relation to tumor type, DNA ploidy pattern and short-term survival. Am. J. Clin. Pathol., 105: 604-12, 1996.
33. Poulaki, V., Mitsiades, C. S., and Mitsiades, N. The role of Fas and FasL as mediators of anticancer chemotherapy. Drug Resist. Updates, 4: 233-242, 2001.
34. Timmer, T., de Vries, E. G. E., and de Jong, S. Fas receptor-mediated apoptosis: a clinical application? J. Pathol., 196: 125-134, 2002.
35. Algeciras-Schimnich, A., Shen, L., Barnhart, B. C., Murmann, A. E., Burkhardt, J. K., and Peter, M. E. Molecular ordering of the initial signaling events of CD95. Mol. Cell. Biol., 22: 207-220, 2002.
36. Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K. J., Debatin, K. m., Krammer, P. H., and Peter, M. E. Two CD95 (APO-I/Fas) signaling pathways. EMBO J., 17: 1675-1687, 1998.
37. Tillman, D. M., Izeradjene, K., Szekely Szucs, K., Douglas, L., and Houghton, J. A. Rottlerin sensitizes colon carcinoma cells to TRAIL-induced apoptosis via uncoupling of the mitochondria independent of PKC. Cancer Res., in press, 2003.
38. Tillman, D. M., Harwood, F. G., Gibson, A. A., and Houghton, J. A. Expression of genes that regulate Fas signaling and Fas-mediated apoptosis in colon carcinoma cells. Cell Death Diff., 5: 450-457, 1998.
39. Houghton, J. A., Harwood, F. G., and Tillman, D. M. Thymineless death in colon carcinoma cells is mediated via Fas signaling. Proc. Natl. Acad. Sci. USA, 94: 8144-8149, 1997.
40. Houghton, J. A., Harwood, F. G., Gibson, A. A., and Tillman, D. M. The Fas signaling pathway is functional in colon carcinoma cells and induces apoptosis. Clin. Cancer Res., 3: 2205-2209, 1997.
41. Eichhorst, S. T., Muller, M., Li-Weber, M., Schulze-Bergkamen, H., Angel, P., and Krammer, P. H. A novel AP-1 element in the CD95 ligand promoter is required for induction of apoptosis in hepatocellular carcinoma cells upon treatment with anticancer drugs. Mol. Cell. Biol., 20: 7826-7837, 2000.
42. Eichhorst, S. T., Muerkoster, S., Weigand, M. A., and Krammer, P. H. The chemotherapeutic drug 5-fluorouracil induces apoptosis in mouse thymocytes in vivo via activation of the CD95(APO-1/Fas) system. Cancer Res., 61: 243-248, 2001.
43. Shao, R. G., Cao, C. X., Nieves-Neira, W., Dimanche-Boitrel, M. T., Solary, E., and Pommier, Y. Activation of the Fas pathway independently of Fas ligand during apoptosis induced by camptothecin in p53 mutant human colon carcinoma cells. Oncogene, 20: 1852-1859, 2001.
44. Micheau, O., Solary, E., Hammann, A., and Dimanche-Boitrel, M. T. Fas ligand-independent, FADD-mediated activation of the Fas death pathway by anticancer drugs. J. Biol. Chem., 274: 7987-7992, 1999.
45. Wesselborg, S., Engels, i. H., Rossmann, E., Los, M., and Schulze-Osthoff, K. Anticancer drugs induce caspase-8/FLICE activation and apoptosis in the absence of CD95 receptor/ligand interaction. Blood, 93: 3053-3063, 1999.
46. Holler, N., Zaru, R., Micheau, O., Thome, M., Attinger, A., Valitutti, S., Bodmer, J. L., Schneider, P., Seed, B., and Tschopp, J. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol., 1: 489-495, 2000.
47. Ossina, N. K., Cannas, A., Powers, V. C., Fitzpatrick, P. A., Knight, J. D., Gilbert, J. R., Shekhtman, E. M., Tomei, L. D., Umansky, S. R., and Kiefer, M. C. Interferon-γ modulates a p53-independent apoptotic pathway and apoptosis-related gene expression. J. Biol. Chem., 272: 16351-16357, 1997.
48. O'Connell, J., Bennett, M. W., Nally, k., O'Sullivan, G. C., Collins, J. K., and Shanahan, F. Interferon-γ ensitizes colonic epithelial cell lines to physiological and therapeutic inducers of colonocyte apoptosis. J. Cell Physiol., 185: 331-338, 2000.
49. Ruiz-Ruiz, C., Munnoz-Pinedo, C., and Lopez-Rivas, A. Interferon-γ treatment elevates caspase-8 expression and sensitizes human breast tumor cells to a death receptor-induced mitochondria-operated apoptotic program. Cancer Res., 60: 5673-5680, 2000.
50. Fulda, S., and Debatin, K. M. IFN-γ sensitizes for apoptosis by upregulating caspase-8 expression through the Statl pathway. Oncogene, 21: 2295-2308, 2002.
51. Adachi, Y., Taketani, S., Oyaizu, H., Ikebukuro, K., Tokunaga, R., and Ikehara, S. Apoptosis of colorectal adenocarcinoma induced by 5-FU and/or IFN-γ through caspase 3 and caspase 8. Int. J. Oncol., 15: 1191-1196, 1999.
52. Peart, M. J., Tainton, K. M., Ruefli, A. A., Dear, A. E., Sedelies, K. A., O'Reilly, L. A., Waterhouser, N. J., Trapani, J. A., and Johnstone, R. W. Novel mechanisms of apoptosis induced by histone deacetylase inhibitors. Cancer Res., 63: 4460-4471, 2003.
53. Green, D. R., and Beere, H. M. Killers or clean-up crew: how central are the central mechanisms of apoptosis. In: J. A. Hickman, and C. Dive (eds.), Apoptosis and Cancer Therapy, pp. 157-174, Totowa, NY: Humana Press Inc., 1999.
54. McCarthy, N. J., Whyte, M. K. B., Gilbert, C. S., and Evan, G. I. Inhibition of ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J. Cell Biol., 136: 215-227, 1997.
55. Engels, I. H., Stepczynska, A., Stroh, C., Lauber, K., Berg, C., Schwenzer, R., Wajant, H., Janicke, R. U., Porter, A. G., Belka, C., Gregor, M., Schulze-Osthoff, K., and Wesselborg, S. Caspase-8/FLICE functions as an executioner caspase in anticancer drug-induced apoptosis. Oncogene, 19: 4563-4573, 2000.
56. Wu, X. X., Kakehi, Y., Mizutani, Y., Lu, J., Terachi, T., and Ogawa, O. Activation of caspase-3 in renal cell carcinoma cells by anthracyclines or 5-fluorouracil. Int. J. Oncol., 19: 19-24, 2001.
57. Lee, D. H., and Goldberg, A. L. Proteasome inhibitors: valuable new tools for cell biologists. Cell Biol., 8: 397-403, 1998.
58. Weissman, A. M. Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell. Biol., 2: 169-178, 2001.
59. Yang, Y., Fang, S., Jensen, J. P., Weissman, A. M., and Ashwell, J. D. Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science (Wash. DC), 288: 874-877, 2000.
60. Watanabe, K., Kubota, M., Hamahata, K., Lin, Y., and Usami, I. Prevention of etoposide-induced apoptosis by proteasome inhibitors in a human leukemic cell line but not in fresh acute leukemia blasts. Biochem. Pharmacol., 60: 823-830, 2000.
61. Adams, J. Proteasome inhibition in cancer: development of PS-341. Semin. Oncol., 28: 613-619, 2001.
62. Kim, Y., Suh, N., Sporn, M., and Reed, J. C. An inducible pathway for degradation of FLIP protein sensitizes tumor cells to TRAIL-induced apoptosis. J. Biol. Chem., 277: 22320-22329, 2002.
63. Dimmeler, S., Breitschopf, K., Haendeler, J., and Zeiher, A. M. Dephosphorylation targets Bcl-2 ubiquitin-dependent degradation: A link between the apoptosome and the proteasome pathway. J. Exp. Med., 89: 1815-1822, 1999.
64. Zhao, J., Tenev, T., Martins, L. M., Downward, J., and Lemoine, N. R. The ubiquitin-proteasome pathway regulates survivin degradation in a cell cycle-dependent manner. J. Cell Sci., 113: 4363-4371, 2000.
65. Palombella, V. J., Rando, O. J., Goldberg, A. L., and Maniatis, T. The Ubiquitin-proteasome pathway is required for processing the NF-B1 precursor protein and the activation of NF-kB. Cell, 78: 773-785, 1994.
66. Kawasaki, H., Toyoda, M., Shinohara, H., Okuda, J., Watanabe, I., Yamamoto, T., Tanaka, K., Tenjo, T., and Tanigawa, N. Expression of survivin correlates with apoptosis, proliferation, and angiogenesis during human colorectal tumorigenesis. Cancer (Phila.), 91: 2026-2032, 2001.
67. Sarela, A. I., Scott, N., Ramsdale, J., Markham, A. F., and Guillou, P. J. Immunohistochemical detection of the anti-apoptosis protein, survivin, predicts survival after curative resection of stage II colorectal carcinomas. Ann. Surg. Oncol., 8: 305-310, 2001.
68. Sandler, A., Scott, D., Azuhata, T., Takamizawa, S., and O'Dorisio, S. The survivin:Fas ratio is predictive of recurrent disease in neuroblastoma. J. Ped. Surg., 37: 507-511, 2002.
69. Takamizawa, S., Scott, D., Wen, J., Grundy, P., Bishop, W., Kimura, K., and Sandler, A. The survivin:Fas ratio in pediatric renal tumors. J. Ped. Surg., 36: 37-42, 2001.