The Proteasome Inhibitor Bortezomib Stabilizes a Novel Active Form of p53 in Human LNCaP-Pro5 Prostate Cancer Cells

Cancer Research

Volumn 63, Issue 21, 2003, Pages 7338-7344

  Williams, Simon A ^a   McConkey, David J ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; PROTEASOME; PROTEASOME INHIBITOR; PROTEIN INHIBITOR; PROTEIN MDM2; PROTEIN P53; SERINE; UNCLASSIFIED DRUG;

ADVANCED CANCER; ARTICLE; CANCER CELL; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CELL DEATH; DNA BINDING; DRUG EFFECT; DRUG MECHANISM; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REPORTER GENE;

APOPTOSIS; BORONIC ACIDS; CELL LINE, TUMOR; DNA, NEOPLASM; ETOPOSIDE; HUMANS; MALE; NUCLEAR PROTEINS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PEPTIDE HYDROLASES; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MDM2; PYRAZINES; SUBCELLULAR FRACTIONS; TRANS-ACTIVATION (GENETICS); TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0242610835     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (78)

1. Centers for Disease Control and Prevention. Recent trends in mortality rates for four major cancers, by sex and race/ethnicity-United States, 1990-1998. J. Am. Med. Assoc., 287: 1391-1392, 2002.
2. Feldman, B. J., and Feldman, D. The development of androgen-independent prostate cancer. Nat. Rev. Cancer, 1: 34-45, 2001.
3. Adams, J., Palombella, V. J., Sausville, E. A., Johnson, J., Destree, A., Lazarus, D. D., Maas, J., Pien, C. S., Prakash, S., and Elliott, P. J. Proteasome inhibitors: a novel class of potent and effective antitumor agents. Cancer Res., 59: 2615-2622, 1999.
4. Adams. J. Proteasome inhibition in cancer: development of PS-341. Semin. Oncol., 28: 613-619, 2001.
5. Adams, J., Palombella, V. J., and Elliott, P. J. Proteasome inhibition: a new strategy in cancer treatment. Investig. New Drugs, 18: 109-121, 2000.
6. Lakin, N. D., and Jackson, S. P. Regulation of p53 in response to DNA damage. Oncogene, 18: 7644-7655, 1999.
7. 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.
8. Tao, W., and Levine, A. J. Nucleocytoplasmic shuttling of oncoprotein Hdm2 is required for Hdm2-mediated degradation of p53. Proc. Natl. Acad. Sci. USA. 96: 3077-3080, 1999.
9. Honda, R., Tanaka, H., and Yasuda, H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett., 420: 25-27, 1997.
10. Fields, S., and Jang, S. K. Presence of a potent transcription activating sequence in the p53 protein. Science (Wash. DC), 249: 1046-1049, 1990.
11. Raycroft, L., Wu, H. Y., and Lozano, G. Transcriptional activation by wild-type but not transforming mutants of the p53 anti-oncogene. Science (Wash. DC), 249: 1049-1051, 1990.
12. 2/M transition by p53. Oncogene, 20: 1803-1815, 2001.
13. Appella, E., and Anderson, C. W. Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem., 268: 2764-2772, 2001.
14. Dong, J. T., Isaacs, W. B., and Isaacs, J. T. Molecular advances in prostate cancer. Curr. Opin. Oncol., 9: 101-107, 1997.
15. MacLaren, A. P., Chapman, R. S., Wyllie, A. H., and Watson, C. J. p53-dependent apoptosis induced by proteasome inhibition in mammary epithelial cells. Cell Death Differ., 8: 210-218, 2001.
16. Naujokat, C., Sezer, O., Zinke, H., Leclere, A., Hauptmann, S., and Possinger, K. Proteasome inhibitors induced caspase-dependent apoptosis and accumulation of p21WAF1/Cip1 in human immature leukemic cells. Eur. J. Haematol., 65: 221-236, 2000.
17. Chen, F., Chang, D., Goh, M., Klibanov, S. A., and Ljungman, M. Role of p53 in cell cycle regulation and apoptosis following exposure to proteasome inhibitors. Cell Growth Differ., 11: 239-246, 2000.
18. Lopes, U. G., Erhardt, P., Yao, R., and Cooper, G. M. p53-dependent induction of apoptosis by proteasome inhibitors. J. Biol. Chem., 272: 12893-12896, 1997.
19. Shinohara, K., Tomioka, M., Nakano, H., Tone, S., Ito, H., and Kawashima, S. Apoptosis induction resulting from proteasome inhibition. Biochem. J., 317: 385-388, 1996.
20. Dietrich, C., Bartsch, T., Schanz, F., Oesch, F., and Wieser, R. J. p53-dependent cell cycle arrest induced by N-acetyl-L-leucinyl-L-leucinyl-L-norleucinal in platelet-derived growth factor-stimulated human fibroblasts. Proc. Natl. Acad. Sci. USA, 93: 10815-10819, 1996.
21. Blagosklonny, M. V., Wu, G. S., Omura, S., and el Deiry, W. S. Proteasome-dependent regulation of p21WAF1/CIP1 expression. Biochem. Biophys. Res. Commun., 227: 564-569, 1996.
22. An, W. G., Hwang, S. G., Trepel, J. B., and Blagosklonny, M. V. Protease inhibitor-induced apoptosis: accumulation of wt p53, p21WAF1/CIP1, and induction of apoptosis are independent markers of proteasome inhibition. Leukemia (Baltimore). 14: 1276-1283, 2000.
23. Stempien-Otero, A., Karsan, A., Cornejo, C. J., Xiang, H., Eunson, T., Morrison, R. S., Kay, M., Winn, R., and Harlan, J. Mechanisms of hypoxia-induced endothelial cell death. Role of p53 in apoptosis. J. Biol. Chem., 274: 8039-8045, 1999.
24. Pettaway, C. A., Pathak, S., Greene, G., Ramirez, E., Wilson, M. R., Killion, J. J., and Fidler, I. J. Selection of highly metastatic variants of different human prostatic carcinomas using orthotopic implantation in nude mice. Clin. Cancer Res., 2: 1627-1636, 1996.
25. McConkey, D. J., Greene, G., and Pettaway, C. A. Apoptosis resistance increases with metastatic potential in cells of the human LNCaP prostate carcinoma line. Cancer Res., 56: 5594-5599, 1996.
26. Maki, C. G., Huibregtse, J. M., and Howley, P. M. In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res., 56: 2649-2654, 1996.
27. Mihara, M., Erster, S., Zaika, A., Petrenko, O., Chittenden, T., Pancoska, P., and Moll, U. M. p53 has a direct apoptogenic role at the mitochondria. Mol. Cell, 11: 577-590, 2003.
28. Chang, N. S. A potential role of p53 and WOX1 in mitochondrial apoptosis. Int. J. Mol. Med., 9: 19-24, 2002.
29. Dumont, P., Leu, J. I., Della Pietra, A. C., George, D. L., and Murphy, M. The codon 72 polymorphic variants of p53 have markedly different apoptotic potential. Nat. Genet., 33: 357-365, 2003.
30. Moll, U. M., and Zaika, A. Nuclear and mitochondrial apoptotic pathways of p53. FEBS Lett., 493: 65-69, 2001.
31. Regula, K. M., and Kirshenbaum, L. A. p53 activates the mitochondrial death pathway and apoptosis of ventricular myocytes independent of de novo gene transcription. J. Mol. Cell Cardiol., 33: 1435-1445, 2001.
32. Schuler, M., and Green, D. R. Mechanisms of p53-dependent apoptosis. Biochem. Soc. Trans., 29: 684-688, 2001.
33. el Deiry, W. S., Kem, S. E., Pietenpol, J. A., Kinzler, K. W., and Vogelstein, B. Definition of a consensus binding site for p53. Nat. Genet., 1: 45-49, 1992.
34. Funk, W. D., Pak. D. T., Karas, R. H., Wright, W. E., and Shay, J. W. A transcriptionally active DNA-binding site for human p53 protein complexes. Mol. Cell. Biol., 12: 2866-2871, 1992.
35. Scheffner, M., Werness, B. A., Huibregtse, J. M., Levine, A. J., and Howley, P. M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell, 63: 1129-1136, 1990.
36. Owen-Schaub, L. B., Zhang, W., Cusack, J. C., Angelo, L. S., Santee, S. M., Fujiwara, T., Roth, J. A., Deisseroth, A. B., Zhang, W. W., Kruzel, E., and Radinsky, R. Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol. Cell. Biol., 15: 3032-3040, 1995.
37. Kastan, M. B., Zhan, Q., el Deiry, W. S., Carrier, F., Jacks, T., Walsh, W. V., Plunkett, B. S., Vogelstein, B., and Fornace, A. J., Jr. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell, 71: 587-597, 1992.
38. Wu, G. S., Burns, T. F., McDonald, E. R., III, Jiang, W., Meng, R., Krantz, I. D., Kao, G., Gan, D. D., Zhou, J. Y., Muschel, R., Hamilton, S. R., Spinner, N. B., Markowitz, S., Wu, G., and el Deiry, W. S. KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat. Genet., 17: 141-143, 1997.
39. el Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. B., Parsons, R., Trent, J. M., Lin, D., Mercer, W. E., Kinzler, K. W., and Vogelstein, B. WAFI, a potential mediator of p53 tumor suppression. Cell, 75: 817-825, 1993.
40. Miyashita, T., and Reed, J. C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell, 80: 293-299, 1995.
41. Barak, Y., Juven, T., Haffner, R., and Oren, M. mdm2 expression is induced by wild type p53 activity. EMBO J., 12: 461-468, 1993.
42. Sunwoo, J. B., Chen, Z., Dong, G., Yeh, N., Crowl, B. C., Sausville, E., Adams, J., Elliott, P., and Van Waes, C. Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor-κB, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma. Clin. Cancer Res., 7: 1419-1428, 2001.
43. Deroo, B. J., and Archer, T. K. Proteasome inhibitors reduce luciferase and β-galactosidase activity in tissue culture cells. J. Biol. Chem., 277: 20120-20123, 2002.
44. Moul, J. W. Angiogenesis, p53, bcl-2 and Ki-67 in the progression of prostate cancer after radical prostatectomy. Eur. Urol., 35: 399-407, 1999.
45. MacGrogan, D., and Bookstein, R. Tumour suppressor genes in prostate cancer. Semin. Cancer Biol., 8: 11-19, 1997.
46. Kamradt, J. M., and Pienta, K. J. Etoposide in prostate cancer. Exp. Opin. Pharmacother., 1: 271-275, 2000.
47. Oh, W. K. Chemotherapy for patients with advanced prostate carcinoma: a new option for therapy. Cancer (Phila.), 88: 3015-3021, 2000.
48. Adams, J. Proteasome inhibition: a novel approach to cancer therapy. Trends Mol. Med., 8: S49-S54, 2002.
49. Cusack, J. C., Jr., Liu, R., Houston, M., Abendroth, K., Elliott, P. J., Adams, J., and Baldwin, A. S., Jr. Enhanced chemosensitivity to CPT-11 with proteasome inhibitor PS-341: implications for systemic nuclear factor-κB inhibition. Cancer Res., 61: 3535-3540, 2001.
50. Imajoh-Ohmi, S., Kawaguchi, T., Sugiyama, S., Tanaka, K., Omura, S., and Kikuchi, H. Lactacystin, a specific inhibitor of the proteasome, induces apoptosis in human monoblast U937 cells. Biochem. Biophys. Res. Commun., 217: 1070-1077, 1995.
51. Kudo, Y., Takata, T., Ogawa, I., Kaneda, T., Sato, S., Takekoshi, T., Zhao, M., Miyauchi, M., and Nikai, H. p27Kip1 accumulation by inhibition of proteasome function induces apoptosis in oral squamous cell carcinoma cells. Clin. Cancer Res., 6: 916-923, 2000.
52. Sun, J., Nam, S., Lee, C. S., Li, B., Coppola, D., Hamilton, A. D., Dou, Q. P., and Sebti, S. M. CEP1612, a dipeptidyl proteasome inhibitor, induces p21WAF1 and p27KIP1 expression and apoptosis and inhibits the growth of the human lung adenocarcinoma A-549 in nude mice. Cancer Res., 61: 1280-1284, 2001.
53. Adams, J. Potential for proteasome inhibition in the treatment of cancer. Drug Discov. Today, 8: 307-315, 2003.
54. Berenson, J. R., Ma, H. M., and Vescio, R. The role of nuclear factor-κB in the biology and treatment of multiple myeloma. Semin. Oncol., 28: 626-633, 2001.
55. Epinat, J. C., and Gilmore, T. D. Diverse agents act at multiple levels to inhibit the Rel/NF-κB signal transduction pathway. Oncogene, 18: 6896-6909, 1999.
56. Deroo, B. J., Rentsch, C., Sampath, S., Young, J., DeFranco, D. B., and Archer, T. K. Proteasomal inhibition enhances glucocorticoid receptor transactivation and alters its subnuclear trafficking. Mol. Cell. Biol., 22: 4113-4123, 2002.
57. Lonard, D. M., Nawaz, Z., Smith, C. L., and O'Malley, B. W. The 26S proteasome is required for estrogen receptor-α and coactivator turnover and for efficient estrogen receptor-α transactivation. Mol. Cell. 5: 939-948, 2000.
58. Lin, H. K., Altuwaijri, S., Lin, W. J., Kan, P. Y., Collins, L. L., and Chang, C. Proteasome activity is required for androgen receptor transcriptional activity via regulation of androgen receptor nuclear translocation and interaction with coregulators in prostate cancer cells. J. Biol. Chem., 277: 36570-36576, 2002.
59. Hideshima, T., Mitsiades, C., Akiyama, M., Hayashi, T., Chauhan, D., Richardson, P., Schlossman, R., Podar, K., Munshi, N. C., Mitsiades, N., and Anderson, K. C. Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood. 101: 1530-1534, 2003.
60. Orlowski, R. Z., Small, G. W., and Shi, Y. Y. Evidence that inhibition of p44/42 mitogen-activated protein kinase signaling is a factor in proteasome inhibitor-mediated apoptosis. J. Biol. Chem. 277: 27864-27871, 2002.
61. Zimmermann, J., Lamerant, N., Grossenbacher, R., and Furst, P. Proteasome- and p38-dependent regulation of ERK3 expression. J. Biol. Chem., 276: 10759-10766, 2001.
62. Meriin, A. B., Gabai, V. L., Yaglom, J., Shifrin, V. I., and Sherman, M. Y. Proteasome inhibitors activate stress kinases and induce Hsp72. Diverse effects on apoptosis. J. Biol. Chem., 273: 6373-6379, 1998.
63. Kurland, J. F., and Meyn, R. E. Protease inhibitors restore radiation-induced apoptosis to Bcl-2-expressing lymphoma cells. Int. J. Cancer, 96: 327-333, 2001.
64. Gao, C., Nakajima, T., Taya, Y., and Tsuchida, N. Activation of p53 in MDM2-overexpressing cells through phosphorylation. Biochem. Biophys. Res. Commun., 264: 860-864, 1999.
65. Wagenknecht, B., Hermisson, M., Eitel, K., and Weller, M. Proteasome inhibitors induce p53/p21-independent apoptosis in human glioma cells. Cell Physiol. Biochem., 9: 117-125, 1999.
66. Kitagawa, H., Tani, E., Ikemoto, H., Ozaki, I., Nakano, A., and Omura, S. Proteasome inhibitors induce mitochondria-independent apoptosis in human glioma cells. FEBS Lett., 443: 181-186, 1999.
67. An, B., Goldfarb, R. H., Siman, R., and Dou, Q. P. Novel dipeptidyl proteasome inhibitors overcome Bcl-2 protective function and selectively accumulate the cyclin-dependent kinase inhibitor p27 and induce apoptosis in transformed, but not normal, human fibroblasts. Cell Death Differ., 5: 1062-1075, 1998.
68. Herrmann, J. L., Briones, F., Jr., Brisbay, S., Logothetis, C. J., and McDonnell, T. J. Prostate carcinoma cell death resulting from inhibition of proteasome activity is independent of functional Bcl-2 and p53. Oncogene. 17: 2889-2899, 1998.
69. Caspari, T. How to activate p53. Curr. Biol., 10: R315-R317, 2000.
70. Enoch, T., and Norbury, C. Cellular responses to DNA damage: cell-cycle check-points, apoptosis and the roles of p53 and ATM. Trends Biochem. Sci., 20: 426-430, 1995.
71. Liang, S. H., and Clarke, M. F. Regulation of p53 localization. Eur. J. Biochem., 268: 2779-2783, 2001.
72. Michael, D., and Oren, M. The p53-Mdm2 module and the ubiquitin system. Semin. Cancer Biol., 13: 49-58, 2003.
73. Fuchs, B., O'Connor, D., Fallis, L., Scheidtmann, K. H., and Lu, X. p53 phosphorylation mutants retain transcription activity. Oncogene, 10: 789-793, 1995.
74. Blattner, C., Tobiasch, E., Litfen, M., Rahmsdoff, H. J., and Herrlich, P. DNA damage induced p53 stabilization: no indication for an involvement of p53 phosphorylation. Oncogene, 18: 1723-1732, 1999.
75. Zauberman, A., Barak, Y., Ragimov, N., Levy, N., and Oren, M. Sequence-specific DNA-binding by p53: identification of target sites and lack of binding to p53Mdm2 complexes. EMBO J., 12: 2799-2808, 1993.
76. Bykov, V. J., Issaeva, N., Selivanova, G., and Wiman, K. G. Mutant p53-dependent growth suppression distinguishes PRIMA-1 from known anticancer drugs: a statistical analysis of information in the National Cancer Institute database. Carcinogenesis (Lond.), 23: 2011-2018, 2002.
77. Bykov, V. J., Issaeva, N., Shilov, A., Hultcrantz, M., Pugacheva, E., Chumakov, P., Bergman, J., Wiman, K. G., and Selivanova, G. Restoration of the tumor suppressor function to mutant p53 by a low-molecular-weight compound. Nat. Med., 8: 282-288, 2002.
78. Rippin, T. M., Bykov, V. J., Freund, S. M., Selivanova, G., Wiman, K. G., and Fersht, A. R. Characterization of the p53-rescue drug CP-31398 in vitro and in living cells. Oncogene, 21: 2119-2129, 2002.