Apoptosis induction in prostate cancer cells and xenografts by combined treatment with Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand and CPT-11

Cancer Research

Volumn 63, Issue 15, 2003, Pages 4713-4723

  Ray, Subrata ^a   Almasan, Alex ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APO2 LIGAND; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; CASPASE 8; IRINOTECAN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL OMEGA; PROTEIN BCL X; PROTEIN BCL XL; PROTEIN BCL XS; PROTEIN BID; RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CONTROL; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CAMPTOTHECIN; CASPASE 3; CASPASE 7; CASPASES; DRUG SYNERGISM; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, NUDE; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RECEPTORS, TUMOR NECROSIS FACTOR; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR CELLS, CULTURED; TUMOR NECROSIS FACTOR-ALPHA; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 0041633807     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Greenlee, R. T., Murray, T., Bolden, S., and Wingo, P. A. Cancer statistics, 2000. CA Cancer J. Clin., 50: 7-33, 2000.
2. Thalmann, G. N., Anezinis. P. E., Chang, S. M., Zhau, H. E., Kim, E. E., Hopwood, V. L., Pathak, S., von Eschenbach, A. C., and Chung, L. W. Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer. Cancer Res., 54: 2577-2581, 1994.
3. Thalmann, G. N., Sikes, R. A., Wu, T. T., Degeorges, A., Chang, S. M., Ozen, M., Pathak, S., and Chung, L. W. LNCaP progression model of human prostate cancer: androgen-independence and osseous metastasis. Prostate, 44: 91-103, 2000.
4. Pitti, R. M., Marsters, S. A., Ruppert, S., Donahue, C. J., Moore, A., and Ashkenazi, A. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem., 271: 12687-12690, 1996.
5. Wiley, S. R., Schooley, K., Smolak, P. J., Din, W. S., Huang, C. P., Nicholl, J. K., Sutherland, G. R., Smith, T. D., Rauch, C., Smith, C. A., et al. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity, 3: 673-682, 1995.
6. Hymowitz, S. G., Christinger, H. W., Fuh, G., Ultsch, M., O'Connell, M., Kelley, R. F., Ashkenazi, A., and de Vos, A. M. Triggering cell death: the crystal structure of Apo2L/TRAIL in a complex with death receptor 5. Mol. Cell, 4: 563-571, 1999.
7. Mongkolsapaya, J., Grimes, J. M., Chen, N., Xu, X. N., Stuart, D. I., Jones, E. Y., and Screaton, G. R. Structure of the TRAIL-DR5 complex reveals mechanisms conferring specificity in apoptotic initiation. Nat. Struct. Biol., 6: 1048-1053, 1999.
8. Hymowitz, S. G., O'Connell, M. P., Ultsch, M. H., Hurst, A., Totpal, K., Ashkenazi, A., de Vos, A. M., and Kelley, R. F. A unique zinc-binding site revealed by a high-resolution X-ray structure of homotrimeric Apo2L/TRAIL. Biochemistry, 39: 633-640, 2000.
9. Bodmer, J. L., Meier, P., Tschopp, J., and Schneider, P. Cysteine 230 is essential for the structure and activity of the cytotoxic ligand TRAIL. J. Biol. Chem., 275: 20632-20637, 2000.
10. Jo, M., Kim, T. H., Seol, D. W., Esplen, J. E., Dorko, K. Billiar, T. R., and Strom, S. C. Apoptosis induced in normal human hepatocytes by tumor necrosis factor-related apoptosis-inducing ligand. Nat. Med., 6: 564-567, 2000.
11. Lawrence, D., Shahrokh, Z., Marsters, S., Achilles, K., Shih, D., Mounho, B., Hillan, K., Totpal, K., DeForge, L., Schow, P., Hooley, J., Sherwood, S., Pai, R., Leung, S., Khan, L., Gliniak, B., Bussiere, J., Smith, C. A., Strom, S. S., Kelley, S., Fox, J. A., Thomas, D., and Ashkenazi, A. Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat. Med., 7: 383-385, 2001.
12. Qin, J., Chaturvedi, V., Bonish, B., and Nickoloff, B. J. Avoiding premature apoptosis of normal epidermal cells. Nat. Med., 7: 385-386, 2001.
13. Walczak, H., Miller, R. E., Ariail, K., Gliniak, B., Griffith, T. S., Kubin, M., Chin, W., Jones, J., Woodward, A., Le, T., Smith, C., Smolak, P., Goodwin, R. G., Rauch, C. T., Schuh, J. C., and Lynch, D. H. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med., 5: 157-163, 1999.
14. Griffith, T. S., Chin, W. A., Jackson, G. C., Lynch, D. H., and Kubin, M. Z. Intracellular regulation of TRAIL-induced apoptosis in human melanoma cells. J. Immunol., 161: 2833-2840, 1998.
15. Mariani, S. M., Matiba, B., Armandola, E. A., and Krammer, P. H. Interleukin 1 β-converting enzyme related proteases/caspases are involved in TRAIL-induced apoptosis of myeloma and leukemia cells. J. Cell Biol., 137: 221-229, 1997.
16. Ashkenazi, A. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat. Rev. Cancer, 2: 420-430, 2002.
17. Ashkenazi, A., Pai, R. C., Fong, S., Leung, S., Lawrence, D. A., Marsters, S. A., Blackie, C., Chang, L., McMurtrey, A. E., Hebert, A., DeForge, L., Koumenis, I. L., Lewis, D., Harris, L., Bussiere, J., Koeppen, H., Shahrokh, Z., and Schwall, R. H. Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Investig., 104: 155-162, 1999.
18. Kelley, S. K., Harris, L. A., Xie, D., Deforge, L., Totpal, K., Bussiere, J., and Fox, J. A. Preclinical studies to predict the disposition of Apo2L/tumor necrosis factor-related apoptosis-inducing ligand in humans: characterization of in vivo efficacy, pharmacokinetics, and safety. J. Pharmacol. Exp. Ther., 299: 31-38, 2001.
19. Mitsiades, C. S., Treon, S. P., Mitsiades, N., Shima, Y., Richardson, P., Schlossman, R., Hideshima, T., and Anderson, K. C. TRAIL/Apo2L ligand selectively induces apoptosis and overcomes drug resistance in multiple myeloma: therapeutic applications. Blood, 98: 795-804, 2001.
20. Roth, W., Isenmann, S., Naumann, U., Kugler, S., Bahr, M., Dichgans, J., Ashkenazi, A., and Weller, M. Locoregional Apo2L/TRAIL eradicates intracranial human malignant glioma xenografts in athymic mice in the absence of neurotoxicity. Biochem. Biophys. Res. Commun., 265, 479-483, 1999.
21. Pollack, I. F., Erff, M., and Ashkenazi, A. Direct stimulation of apoptotic signaling by soluble Apo2L/tumor necrosis factor-related apoptosis-inducing ligand leads to selective killing of glioma cells. Clin. Cancer Res., 7: 1362-1369, 2001.
22. Gliniak, B., and Le, T. Tumor necrosis factor-related apoptosis-inducing ligand's antitumor activity in vivo is enhanced by the chemotherapeutic agent CPT-11. Cancer Res., 59: 6153-6158, 1999.
23. Gong, B., and Almasan, A. Apo2 ligand/TNF-related apoptosis-inducing ligand and death receptor 5 mediate the apoptotic signaling induced by ionizing radiation in leukemic cells. Cancer Res., 60: 5754-5760, 2000.
24. Chinnaiyan, A. M., Prasad, U., Shankar, S., Hamstra, D. A., Shanaiah, M., Chenevert, T. L., Ross, B. D., and Rehemtulla, A. Combined effect of tumor necrosis factor-related apoptosis-inducing ligand and ionizing radiation in breast cancer therapy. Proc. Natl. Acad. Sci. USA, 97: 1754-1759, 2000.
25. Houghton, P. J., Cheshire, P. J., Hallman, J. C., Bissery, M. C., Mathieu-Boue, A., and Houghton, J. A. Therapeutic efficacy of the topoisomerase I inhibitor 7-ethyl-10-(4-[1-piperidino]-1-piperidino)-carbonyloxy-camptothecin against human tumor xenografts: lack of cross-resistance in vivo in tumors with acquired resistance to the topoisomerase I inhibitor 9-dimethylaminomethyl-10-hydroxycamptothecin. Cancer Res., 53: 2823-2829, 1993.
26. Keane, M. M., Ettenberg, S. A., Nau, M. M., Russell, E. K., and Lipkowitz, S. Chemotherapy augments TRAIL-induced apoptosis in breast cell lines. Cancer Res., 59: 734-741, 1999.
27. Xiang, H., Fox, J. A., Totpal, K., Aikawa, M., Dupree, K., Sinicropi, D., Lowe, J., and Escandon, E. Enhanced tumor killing by Apo2L/TRAIL and CPT-11 co-treatment is associated with p21 cleavage and differential regulation of Apo2L/TRAIL ligand and its receptors. Oncogene, 21: 3611-3619, 2002.
28. LeBlank, H., and Ashkenazi, A. Apo2L/TRAIL and its death and decoy receptors. Cell Death Differ., 10: 66-75, 2003.
29. Sheridan, J. P., Marsters, S. A., Pitti, R. M., Gurney, A., Skubatch, M., Baldwin, D., Ramakrishnan, L., Gray, C. L., Baker, K., Wood, W. I., Goddard, A. D., Godowski, P., and Ashkenazi, A. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science (Wash. DC), 277: 818-821, 1997.
30. Kischkel, F. C., Lawrence, D. A., Chuntharapai, A., Schow, P., Kim, K. J., and Ashkenazi, A. Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5. Immunity, 12: 611-620, 2000.
31. Kischkel, F. C., Lawrence, D. A., Tinel, A., LeBlanc, H., Virmani, A., Schow, P., Gazdar, A., Blenis, J., Arnott, D., and Ashkenazi, A. Death receptor recruitment of endogenous caspase-10 and apoptosis initiation in the absence of caspase-8. J. Biol. Chem., 276: 46639-46646, 2001.
32. Green, D. R., and Evan, G. I. A matter of life and death. Cancer Cell, 1: 19-30, 2002.
33. Lazebnik, Y. A., Kaufmann, S. H., Desnoyers, S., Poirier, G. G., and Earnshaw, W. C. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature (Lond.), 371: 346-347, 1994.
34. Wang, X. The expanding role of mitochondria in apoptosis. Genes Dev., 15: 2922-2933, 2001.
35. Cory, S., and Adams, J. M. The bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer, 2: 647-656, 2002.
36. Oltvai, 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.
37. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell, 94: 481-490, 1998.
38. Zou, H., Li, Y., Liu, X., and Wang, X. An APAF-1 cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem., 274: 11549-11556, 1999.
39. Srinivasula, S. M., Ahmad, M., Fernandes-Alnemri, T., and Alnemri, E. S. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol. Cell, 1: 949-957, 1998.
40. 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-1/Fas) signaling pathways. EMBO J., 17: 1675-1687, 1998.
41. MacFarlane, M., Ahmad, M., Srinivasula, S. M., Fernandes-Alnemri, T., Cohen, G. M., and Alnemri, E. S. Identification and molecular cloning of two novel receptors for the cytotoxic ligand TRAIL. J. Biol. Chem., 272: 25417-25420, 1997.
42. Chen, Q., Gong, B., Mahmoud-Ahmed, A. S., Zhou, A., Hsi, E. D., Hussein, M., and Almasan, A. Apo2L/TRAIL and Bcl-2-related proteins regulate type I interferon-induced apoptosis in multiple myeloma. Blood, 98: 2183-2192, 2001.
43. Chen, Q., Gong, B., and Almasan, A. Distinct stages of cytochrome c release from mitochondria: evidence for a feedback amplification loop linking caspase activation to mitochondrial dysfunction in genotoxic stress induced apoptosis. Cell Death Differ., 7: 227-233, 2000.
44. Nagane, M., Pan, G., Weddle, J. J., Dixit, V. M., Cavenee, W. K., and Huang, H. J. Increased death receptor 5 expression by chemotherapeutic agents in human gliomas causes synergistic cytotoxicity with tumor necrosis factor-related apoptosis-inducing ligand in vitro and in vivo. Cancer Res., 60: 847-853, 2000.
45. Gong, B., Chen, Q., Endlich, B., Mazumder, S., and Almasan, A. Ionizing radiation-induced, Bax-mediated cell death is dependent on activation of cysteine and serine proteases. Cell Growth Differ., 10: 491-502, 1999.
46. Marcelli, M., Cunningham, G. R., Walkup, M., He, Z., Sturgis, L., Kagan, C., Mannucci, R., Nicoletti, I., Teng, B., and Denner, L. Signaling pathway activated during apoptosis of the prostate cancer cell line LNCaP: overexpression of caspase-7 as a new gene therapy strategy for prostate cancer. Cancer Res., 59: 382-390, 1999.
47. Hsu, Y. T., and Youle, R. J. Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J. Biol. Chem., 273: 10777-10783, 1998.
48. Eilon, G. F., Gu, J., Slater, L. M., Hara, K., and Jacobs, J. W. Tumor apoptosis induced by epoxide-containing piperazines, a new class of anti-cancer agents. Cancer Chemother. Pharmacol., 45: 183-191, 2000.
49. Jeremias, I., Herr, I., Boehler, T., and Debatin, K. M. TRAIL/Apo-2-ligand-induced apoptosis in human T cells. Eur. J. Immunol., 28: 143-152, 1998.
50. Krajewska, M., Zapata, J. M., Meinhold-Heerlein, I., Hedayat, H., Monks, A., Bettendorf, H., Shabaik, A., Bubendorf, L., Kallioniemi, O. P., Kim, H., Reifenberger, G., Reed, J. C., and Krajewski, S. Expression of Bcl-2 family member Bid in normal and malignant tissues. Neoplasia, 4: 129-140, 2002.
51. Wei, M. C., Zong, W. X., Cheng, E. H., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B., and Korsmeyer, S. J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science (Wash. DC), 292: 727-730, 2001.
52. Lindsten, T., Ross, A. J., King, A., Zong, W. X., Rathmell, J. C., Shiels, H. A., Ulrich, E., Waymire, K. G., Mahar, P., Frauwirth, K., Chen, Y., Wei, M., Eng, V. M., Adelman, D. M. Simon, M. C., Ma, A., Golden, J. A., Evan, G., Korsmeyer, S. J., MacGregor, G. R., and Thompson, C. B. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol. Cell, 6: 1389-1399, 2000.
53. LeBlanc, H., Lawrence, D., Varfolomeev, E., Totpal, K., Morlan, J., Schow, P., Fong, S., Schwall, R., Sinicropi, D., and Ashkenazi, A. Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat. Med., 8: 274-281, 2002.
54. Deng, Y., Lin, Y., and Wu, X. TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes Dev., 16: 33-45, 2002.
55. Finnegan, N. M., Curtin, J. F., Prevost, G., Morgan, B., and Cotter, T. G. Induction of apoptosis in prostate carcinoma cells by BH3 peptides which inhibit Bak/Bcl-2 interactions. Br. J. Cancer, 85: 115-121, 2001.
56. Lebedeva, I., Rando, R., Ojwang, J., Cossum, P., and Stein, C. A. Bcl-xL in prostate cancer cells: effects of overexpression and down-regulation on chemosensitivity. Cancer Res., 60: 6052-6060, 2000.
57. Liu, Q. Y., and Stein, C. A. Taxol and estramustine-induced modulation of human prostate cancer cell apoptosis via alteration in bcl-xL and bak expression. Clin. Cancer Res., 3: 2039-2046, 1997.
58. Wolter, K. G., Hsu, Y. T., Smith, C. L., Nechushtan, A., Xi, X. G., and Youle, R. J. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol., 139: 1281-1292, 1997.
59. Griffiths, G. J., Dubrez, L., Morgan, C. P., Jones, N. A., Whitehouse, J., Corfe, B. M., Dive, C., and Hickman, J. A. Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis. J. Cell Biol., 144: 903-914, 1999.
60. Desagher, S., Osen-Sand, A., Nichols, A., Eskes, R., Montessuit, S., Lauper, S., Maundrell, K., Antonsson, B., and Martinou, J. C. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol., 144: 891-901, 1999.
61. Murphy, K. M., Streips, U. N., and Lock, R. B. Bcl-2 inhibits a Fas-induced conformational change in the Bax N terminus and Bax mitochondrial translocation. J. Biol. Chem., 275: 17225-17228, 2000.
62. Gilmore, A. P., Metcalfe, A. D., Romer, L. H., and Streuli, C. H. Integrin-mediated survival signals regulate the apoptotic function of Bax through its conformation and subcellular localization. J. Cell Biol., 149: 431-446, 2000.
63. Eskes, R., Desagher, S., Antonsson, B., and Martinou, J. C. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol. Cell Biol., 20: 929-935, 2000.
64. Gibson, S. B., Oyer, R., Spalding, A. C., Anderson, S. M., and Johnson, G. L. Increased expression of death receptors 4 and 5 synergizes the apoptosis response to combined treatment with etoposide and TRAIL. Mol. Cell Biol., 20: 205-212, 2000.
65. Rokhlin, O. W., Gudkov, A. V., Kwek, S., Glover, R. A., Gewies, A. S., and Cohen, M. B. p53 is involved in tumor necrosis factor-α-induced apoptosis in the human prostatic carcinoma cell line LNCaP. Oncogene, 19: 1959-1968, 2000.