Heterogeneous apoptotic responses of prostate cancer cell lines identify an association between sensitivity to staurosporine-induced apoptosis, expression of Bcl-2 family members, and caspase activation

Prostate

Volumn 42, Issue 4, 2000, Pages 260-273

  Marcelli, Marco ^a   Marani, Michela ^a   Li, Xiaoying ^a   Sturgis, Lydia ^b   Haidacher, S Joe ^b   Trial, JoAnn ^a   Mannucci, Roberta ^c   Nicoletti, Ildo ^c   Denner, Larry ^b  

^a MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b TEXAS BIOTECHNOLOGY CORPORATION   (United States)

^c UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Apoptosis; Caspases; Prostate cancer; Staurosporine

Indexed keywords

CASPASE 3; CASPASE 7; CYTOCHROME C OXIDASE; DNA FRAGMENT; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; PROTEIN BCL X; STAUROSPORINE;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER HORMONE THERAPY; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DEGRADATION; PROTEIN EXPRESSION;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BIOLOGICAL TRANSPORT; CASPASE 3; CASPASE 7; CASPASES; CATALYSIS; CELL SURVIVAL; CYTOCHROME C GROUP; CYTOSOL; DNA FRAGMENTATION; DNA TOPOISOMERASES, TYPE II; ENZYME ACTIVATION; ENZYME INHIBITORS; HUMANS; IN SITU NICK-END LABELING; INTRACELLULAR MEMBRANES; MALE; MITOCHONDRIA; NECROSIS; POLY(ADP-RIBOSE) POLYMERASES; PROSTATIC NEOPLASMS; PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; STAUROSPORINE; TUMOR CELLS, CULTURED;

EID: 0033981234     PISSN: 02704137     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0045(20000301)42:4<260::AID-PROS3>3.0.CO;2-0     Document Type: Article

References (77)

1. Huggins C, Hodges CV. The effect of castration, of estrogens and androgen injection on serum phosphatase in metastatic carcinoma of the prostate. Cancer Res 1941;1:293-297.
2. Crawford ED, Eisenberger MA, McLeod DG, Spaulding JT, Benson R, Dorr FA, Blumenstein BA, Davis MA, Goodman PJ. A controlled trial of leuprolide with and without flutamide in prostatic carcinoma. N Engl J Med 1989;321:419-424.
3. Ghosh J, Myers CE. Inhibition of arachidonate 5-lipoxygenase triggers massive apoptosis in human prostate cancer cells. Proc Natl Acad Sci USA 1998;95:13182-13187.
4. Van der Kwast T, Tetu B. Androgen receptors in untreated and treated prostatic intraepithelial neoplasia. Eur Urol 1996;30:265-268.
5. Sadi MV, Walsh PC, Barrack ER. Immunohistochemical study of androgen receptors in metastatic prostate cancer. Cancer 1991; 67:3057-3064.
6. Tilley WD, Lim-Tio SS, Horsfall DJ, Aspinall JO, Marshall VR, Skinner JM. Detection of discrete androgen receptor epitopes in prostate cancer by immunostaining: measurement by color video image analysis. Cancer Res 1994;54:4096-4102.
7. Hobisch A, Culig Z, Radmayr C, Bartsch G, Klocker H, Hittmair A. Androgen receptor status of lymph node metastases from prostate cancer. Prostate 1996;28:129-135.
8. Hobisch A, Culig Z, Radmayr C, Bartsch G, Klocker H, Hittmair A. Distant metastases from prostatic carcinoma express androgen receptor protein. Cancer Res 1995;55:3068-3072.
9. Van der Kwast TH, Schalken J, Ruizeveld de Winter JA, Van Vroonhoven CCJ, Mulder E, Boersma W, Trapman J. Androgen receptors in endocrine-therapy resistant human prostate cancer. Int J Cancer 1991;48:189-193.
10. Isaacs J, Lundmo P, Berges R, Martikainen P, Kyprianou N, English H. Androgen regulation of programmed cell death of normal and malignant prostatic cells. J Androl 1992;13:457-464.
11. Colombel M, Symmans F, Gil S, O'Toole K, Chopin D, Benson M, Olsson C, Korsmeyer S, Buttyan R. Detection of the apoptosis suppressing oncoprotein bcl-2 in hormone refractory human prostate cancers. Am J Pathol 1993;143:390-400.
12. McDonnel TJ, Troncoso P, Brisbay SM, Logothesis C, Chang LWK, Hsieh J-T, Tu S-M, Campbell ML. Expression of the protooncogene bcl-2 in the prostate and its association with emergence of androgen-independent prostate cancer. Cancer Res 1992;52:6940-6944.
13. Ashkenazi A, Dixit V. Death receptors: signaling and modulation. Science 1998;281:1305-1308.
14. Green D, Reed J. Mitochondria and apoptosis. Science 1998;281: 1309-1312.
15. Green D. Apoptotic pathways: the roads to ruin. Cell 1998;94: 695-698.
16. Thornberry N, Lazebnick Y. Caspases: enemies within. Science 1998;281:1312-1316.
17. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972;26:239-257.
18. Wyllie AH, Kerr JF, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol 1980;68:251-306.
19. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM, Green DR. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpres-sion of Bcl-2 and Abl. J Exp Med 1995;182:1545-1556.
20. Alnemri E, Livingston D, Nicholson D, Salvesen G, Thornberry N, Wong W, Yuan J. Human ICE/CED3 protease nomenclature. Cell 1996;87:171.
21. Liu X, Kim C, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996;86:147-157.
22. Susin S, Lorenzo H, Zamzani N, Marzo I, Snow B, Brothers G, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett D, Aebersold R, Siderovski D, Penninger J, Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999;397:441-446.
23. Gross A, Jockel J, Wei MC, Korsmeyer SJ. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J 1998;17:3878-3885.
24. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998;94:481-490.
25. Li H, Zhu H, Xu C-J, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998;94:491-501.
26. Gross A, Yin XM, Wang K, Wei MC, Jockel J, Milliman C, Erdjument-Bromage H, Tempst P, Korsmeyer SJ. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem 1999;274:1156-1163.
27. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997;91:479-489.
28. Marcelli M, Cunnigham G, Haidacher S, Padayatty S, Sturgis L, Kagan C, Denner L. Caspase-7 is activated during lovastatin-induced apoptosis of the prostate cancer cell line LNCaP. Cancer Res 1998;58:76-83.
29. Marcelli M, Cunningham G, Walkup M, He Z, Sturgis L, Kagan C, Mannucci R, Nicoletti I, Teng B, Denner L. Signaling pathway activated during apoptosis of the prostate cancer cell line LN-CaP: overexpression of caspase-7 as a new gene therapy strategy for the treatment of prostate cancer. Cancer Res 1999;59: 398-406.
30. MacFarlane M, Cain K, Sun XM, Alnemri ES, Cohen GM. Processing/activation of at least four interleukin-1beta converting enzyme-like proteases occurs during the execution phase of apoptosis in human monocytic tumor cells. J Cell Biol 1997;137: 469-479.
31. Chandler J, Cohen G, MacFarlane M. Different subcellular distribution of caspase-3 and caspase-7 following Fas-induced apoptosis in mouse liver. J Biol Chem 1998;273:10815-10818.
32. Horoszewicz JS, Leong SS, Chu TM, Wajsman ZL, Friedman M, Papsidero L, Kirn U, Chai LS, Kakati S, Arya SK, Sandberg AA. The LNCaP cell line - a new model for studies on human prostatic carcinoma. Prog Clin Biol Res 1980;37:115-132.
33. Kaighn ME, Narayan KS, Ohnuki Y, Lechner JF, Jones LW. Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol 1979;17:16-23.
34. Stone KR, Mickey DD, Wunderli H, Mickey GH, Paulson DF. Isolation of a human prostate carcinoma cell line (DU 145). Int J Cancer 1978;21:274-281.
35. Iizumi T, Yazaki T, Kanoh S, Kondo I, Koiso K. Establishment of a new prostatic carcinoma cell line (TSU-Pr1). J Urol 1987;137: 1304-1306.
36. Gavrielli Y, Sherman Y, Ben-Sasson S. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992;119:493-501.
37. Bossy-Wetzel E, Newmeyer DD, Green DR. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J 1998;17:37-49.
38. Thornberry NA, Rano TA, Peterson EP, Rasper DM, Timkey T, Garcia-Calvo M, Houtzager VM, Nordstrom PA, Roy S, Vaillancourt JP, Chapman KT, Nicholson DW. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J Biol Chem 1997;272:17907-17911.
39. Pandey S, Walker PR, Sikoska M. Separate pools endonuclease activity are responsible for internucleosomal and high molecular mass DNA fragmentation during apoptosis. Biochem Cell Biol 1994;72:625-629.
40. Marchetti P, Castedo M, Susin SA, Zamzami N, Hirsch T, Macho A, Haeffner A, Hirsch F, Geuskens M, Kroemer G. Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 1996;184:1155-1160.
41. Kluck R, Bossy-Wetzel E, Green D, Newmeyer D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997;275:1132-1136.
42. L. J Biol Chem 1999;274:2225-2233.
43. Yang J, Liu X, Bhalla K, Kim C, Ibrado A, Cai J, Peng T-I, Jones D, Wang X. Prevention of apoptosis by BCL-2: release of cytochrome c from mitochondria blocked. Science 1997;275:1129-1132.
44. Zhivotovsky B, Orrenius S, Brustugun O, Doskeland S. Injected cytochrome c induces apoptosis. Nature 1998;391:449-450.
45. Kaufmann S, Desnoyers S, Ottaviano Y, Davidson N, Poirier G. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res 1993;53:3976-3985.
46. Liu X, Zou H, Slaughter C, Wang X. DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 1997;89:175-184.
47. Casiano CA, Ochs RL, Tan EM. Distinct cleavage products of nuclear proteins in apoptosis and necrosis revealed by autoantibody probes. Cell Death Differ 1998;5:183-190.
48. Shah GM, Shah RG, Poirier GG. Different cleavage pattern for poly(ADP-ribose) polymerase during necrosis and apoptosis in HL-60 cells. Biochem Biophys Res Commun 1996;229:838-844.
49. L as an inhibitor of cytosolic cytochrome C accumulation in DNA damage-induced apoptosis. Proc Natl Acad Sci USA 1997;94:6939-6942.
50. L interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc Natl Acad Sci USA 1998;95:4386-4391.
51. L, and apaf-1 form a ternary complex. J Biol Chem 1998;273:5841-5845.
52. Raffo A, Perlman H, Chen M-W, Day M, Streitman J, Buttyan R. Overexpression of bcl-2 protects cancer cells from apoptosis in vitro and confers resistance to androgen depletion in vivo. Cancer Res 1995;55:4438-4445.
53. Rokhlin OW, Hostager BS, Bishop GA, Sidorenko SP, Glover RA, Gudkov AV, Cohen MB. Dominant nature of the resistance to Fas- and tumor necrosis factor-alpha-mediated apoptosis in human prostatic carcinoma cell lines. Cancer Res 1997;57:3941-3943.
54. Tang DG, Li L, Chopra DP, Porter AT. Extended survivability of prostate cancer cells in the absence of trophic factors: increased proliferation, evasion of apoptosis, and the role of apoptosis proteins. Cancer Res 1998;58:3466-3479.
55. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ. Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 1997;139:1281-1292.
56. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HL, Prevost MC, Xie Z, Matsuyama S, Reed JC, Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 1998;281:2027-2031.
57. Xiang J, Chao D, Korsmeyer S. Bax-induced cell death may not require interleukin 1beta-converting enzyme-like proteases. Proc Natl Acad Sci USA 1996;93:14559-14563.
58. Rosse T, Olivier R, Monney L, Rager M, Conus S, Fellay I, Jansen B, Borner C. Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature 1998;391:496-499.
59. Pastorino JG, Chen ST, Tafani M, Snyder JW, Farber JL. The overexpression of Bax produces cell death upon induction of the mitochondrial permeability transition. J Biol Chem 1998;273: 7770-7775.
60. Tamm I, Wang Y, Sausville E, Scudiero D, Vigna N, Oltersdorf T, Reed J. IAP-family protein survivin inhibits caspase activity and apoptosis induced by fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res 1998;58:5315-5320.
61. Rokhlin OW, Bishop GA, Hostager BS, Waldschmidt TJ, Sidorenko SP, Pavloff N, Kiefer MC, Umansky SR, Glover RA, Cohen MB. Fas-mediated apoptosis in human prostatic carcinoma cell lines. Cancer Res 1997;57:1758-1768.
62. Palayoor ST, Bump EA, Teicher BA, Coleman CN. Apoptosis and clonogenic cell death in PC3 human prostate cancer cells after treatment with gamma radiation and suramin. Radiat Res 1997;148:105-114.
63. Palayoor ST, Bump EA, Calderwood SK, Bartol S, Coleman CN. Combined antitumor effect of radiation and ibuprofen in human prostate carcinoma cells. Clin Cancer Res 1998;4:763-771.
64. Ahmad N, Feyes D, Nieminen A-L, Agarwal R, Muktar H. Green tea constituent epigallocatechin-3-gallate and induction of apoptosis and cell cycle arrest in human carcinoma cells. J Natl Cancer Inst 1997;89:1881-1886.
65. Planchon S, Wuerzberger S, Frydman B, Witiak D, Hutson P, Church D, Wilding C, Boothman D. Beta-lapachone-mediated apoptosis in human promyelocytic leukemia (HL- 60) and human prostate cancer cells: a p53-independent response. Cancer Res 1995;55:3706-3711.
66. Eiseman J, Rogers JL J, Guo Y, Kauffman Y, Sentz D, Klinger M, Callery P, Kyprianou N. Tumor-targeted apoptosis by a novel spermine analogue, 1,12-diaziridinyl-4,9-diazadodecane, results in therapeutic efficacy and enhanced radiosensitivity of human prostate cancer. Cancer Res 1998;58:4864-4870.
67. Furuya Y, Lundmo P, Short AD, Gill DL, Isaacs JT. The role of calcium, pH, and cell proliferation in the programmed (apoptotic) death of androgen-independent prostatic cancer cells induced by thapsigargin. Cancer Res 1994;54:6167-6175.
68. Kyprianou N, King ED, Bradbury D, Rhee JG. bcl-2 overexpression delays radiation-induced apoptosis without affecting the clonogenic survival of human prostate cancer cells. Int J Cancer 1997;70:341-348.
69. Kyprianou N, Bains AK, Jacobs SC. Induction of apoptosis in androgen-independent human prostate cancer cells undergoing thymineless death. Prostate 1994;25:66-75.
70. Carroll AG, Voeller HJ, Sugars L, Gelmann EP. p53 oncogene mutations in three human prostate cancer cell lines. Prostate 1993;23:123-134.
71. Isaacs WB, Carter BS, Ewing CM. Wild-type p53 suppresses growth of human prostate cancer cells containing mutant p53 alleles. Cancer Res 1991;51:4716-4720.
72. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, Puc J, Miliaresis C, Rodgers L, McCombie R, Bigner SH, Giovanella BC, Ittmann M, Tycko B, Hibshoosh H, Wigler MH, Parsons R. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 1997;275: 1943-1947.
73. Dong J, Lamb P, Rinker-Schaeffer C, Vukanovic J, Ichikawa T, Isaacs J, Barrett J. KAI1, a metastasis suppressor gene for prostate cancer on human chromosome 11p11.2. Science 1995;268: 884-886.
74. Bookstein R, Rio P, Madreperla SA, Hong F, Allred C, Grizzle WE, Lee WH. Promoter deletion and loss of retinoblastoma gene expression in human prostate carcinoma. Proc Natl Acad Sci USA 1990;87:7762-7766.
75. Zhao X, Gschwend JE, Powell CT, Foster RG, Day KC, Day ML. Retinoblastoma protein-dependent growth signal conflict and caspase activity are required for protein kinase C-signaled apoptosis of prostate epithelial cells. J Biol Chem 1997;272:22751-22757.
76. Bowen C, Spiegel S, Gelmann EP. Radiation-induced apoptosis mediated by retinoblastoma protein. Cancer Res 1998;58:3275-3281.
77. Zhang H, Hoang T, Saeed B, Ng SC. Induction of apoptosis in prostatic tumor cell line DU145 by staurosporine, a potent inhibitor of protein kinases. Prostate 1996;29:69-76.