Akt inactivation is a key event in indole-3-carbinol-induced apoptosis in PC-3 cells

Clinical Cancer Research

Volumn 8, Issue 4, 2002, Pages 1228-1236

  Chinni, Sreenivasa R ^a   Sarkar, Fazlul H ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 INDOLEMETHANOL; GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAD; PROTEIN BCL XL; PROTEIN KINASE B;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BRASSICA; CANCER CELL; CELL GROWTH; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG ACTIVITY; ENZYME ACTIVATION; ENZYME INACTIVATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; LATENT PERIOD; MITOSIS INHIBITION; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

APOPTOSIS; BCL-ASSOCIATED DEATH PROTEIN; BCL-X PROTEIN; BLOTTING, WESTERN; CARRIER PROTEINS; CELL SURVIVAL; DOWN-REGULATION; ENZYME ACTIVATION; HUMANS; INDOLES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TIME FACTORS; TUMOR CELLS, CULTURED;

EID: 0036554871     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

1. de Vos, R. H., and Blijleven, W. G. The effect of processing conditions on glucosinolates in cruciferous vegetables. Z. Lebensm. Unters. Forsch., 187: 525-529, 1988.
2. Verhoeven, D. T., Verhagen, H., Goldbohm, R. A., van den Brandt, P. A., and van Poppel, G. A review of mechanisms underlying anticarcinogenicity by brassica vegetables. Chem. Biol. Interact., 103: 79-129, 1997.
3. Michnovicz, J. J., and Bradlow, H. L. Induction of estradiol metabolism by dietary indole-3-carbinol in humans. J. Natl. Cancer Inst. (Bethesda), 82: 947-949, 1990.
4. Michnovicz, J. J., and Bradlow, H. L. Altered estrogen metabolism and excretion in humans following consumption of indole-3-carbinol. Nutr. Cancer, 16: 59-66, 1991.
5. Kall, M. A., Vang, O., and Clausen, J. Effects of dietary broccoli on human in vivo drug metabolizing enzymes: evaluation of caffeine, oestrone and chlorzoxazone metabolism. Carcinogenesis (Lond.), 17: 793-799, 1996.
6. Liu, H., Wormke, M., Safe, S. H., and Bjeldanes, L. F. Indolo[3,2-b]carbazole: a dietary-derived factor that exhibits both antiestrogenic and estrogenic activity. J. Natl. Cancer Inst. (Bethesda), 86: 1758-1765, 1994.
7. Rahman, K. M., Aranha, O., Glazyrin, A., Chinni, S. R., and Sarkar, F. H. Translocation of Bax to mitochondria induces apoptotic cell death in indole-3-carbinol (I3C) treated breast cancer cells. Oncogene, 19: 5764-5771, 2000.
8. Cover, C. M., Hsieh, S. J., Tran, S. H., Hallden, G., Kim, G. S., Bjeldanes, L. F., and Firestone, G. L. Indole-3-carbinol inhibits the expression of cyclin-dependent kinase-6 and induces a G1 cell cycle arrest of human breast cancer cells independent of estrogen receptor signaling. J. Biol. Chem., 273: 3838-3847, 1998.
9. Chinni, S. R., Li, Y., Upadhyay, S., Koppolu, P. K., and Sarkar, F. H. Indole-3-carbinol (I3C) induced cell growth inhibition, G1 cell cycle arrest and apoptosis in prostate cancer cells. Oncogene, 20: 2927-2936, 2001.
10. ACS Cancer facts and figures, American Cancer Society Inc., Atlanta, GA. 2001.
11. Sakr, W. A., Grignon, D. J., Haas, G. P., Schomer, K. L., Heilbrun, L. K., Cassin, B. J., Powell, J., Montie, J. A., Pontes, J. E., and Crissman, J. D. Epidemiology of high grade prostatic intraepithelial neoplasia. Pathol. Res. Pract., 191: 838-841, 1995.
12. Block, G., Patterson, B., and Subar, A. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr. Cancer, 18: 1-29, 1992.
13. Boone, C. W., Kelloff, G. J., and Malone, W. E. Identification of candidate cancer chemopreventive agents and their evaluation in animal models and human clinical trials: a review. Cancer Res., 50: 2-9, 1990.
14. Culig, Z., Hobisch, A., Cronauer, M. V., Radmayr, C., Hittmair, A., Zhang, J., Thurnher, M., Bartsch, G., and Klocker, H. Regulation of prostatic growth and function by peptide growth factors. Prostate, 28: 392-405, 1996.
15. Osherov, N., Gazit, A., Gilon, C., and Levitzki, A. Selective inhibition of the epidermal growth factor and HER2/neu receptors by tyrphostins. J. Biol. Chem., 268: 11134-11142, 1993.
16. Fong, C. J., Sherwood, E. R., Mendelsohn, J., Lee, C., and Kozlowski, J. M. Epidermal growth factor receptor monoclonal anti-body inhibits constitutive receptor phosphorylation, reduces autonomous growth, and sensitizes androgen-independent prostatic carcinoma cells to tumor necrosis factor a. Cancer Res., 52: 5887-5892, 1992.
17. Beerli, R. R., Graus-Porta, D., Woods-Cook, K., Chen, X., Yarden, Y., and Hynes, N. E. Neu differentiation factor activation of ErbB-3 and ErbB-4 is cell specific and displays a differential requirement for ErbB-2. Mol. Cell. Biol, 15: 6496-6505, 1995.
18. Huang, G. C., Ouyang, X., and Epstein, R. J. Proxy activation of protein ErbB2 by heterologous ligands implies a heterotetrameric mode of receptor tyrosine kinase interaction. Biochem. J., 331: 113-119, 1998.
19. Tzahar, E., Waterman, H., Chen, X., Levkowitz, G., Karunagaran, D., Lavi, S., Ratzkin, B. J., and Yarden, Y. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol., 16: 5276-5287, 1996.
20. Brodbeck, D., Cron, P., and Hemmings, B. A. A human protein kinase Bγ with regulatory phosphorylation sites in the activation loop and in the C-terminal hydrophobic domain. J. Biol. Chem., 274: 9133-9136, 1999.
21. Masure, S., Haefner, B., Wesselink, J. J., Hoefnagel, E., Mortier, E., Verhasselt, P., Tuytelaars, A., Gordon, R., and Richardson, A. Molecular cloning, expression and characterization of the human serine/threonine kinase Akt-3. Eur. J. Biochem., 265: 353-360, 1999.
22. Nakatani, K., Sakaue, H., Thompson, D. A., Weigel, R. J., and Roth, R. A. Identification of a human Akt3 (protein kinase B γ) which contains the regulatory serine phosphorylation site. Biochem. Biophys. Res. Commun., 257: 906-910, 1999.
23. Alessi, D. R., James, S. R., Downes, C. P., Holmes, A. B., Gaffney, P. R., Reese, C. B., and Cohen, P. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Ba. Curr. Biol., 7: 261-269, 1997.
24. Vanhaesebroeck, B., and Alessi, D. R. The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J., 346: 561-576, 2000.
25. Myers, M. P., Stolarov, J. P., Eng, C., Li, J., Wang, S. I., Wigler, M. H., Parsons, R., and Tonks, N. K. P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc. Natl. Acad. Sci. USA, 94: 9052-9057, 1997.
26. Maehama, T., and Dixon, J. E. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem., 273: 13375-13378, 1998.
27. Damen, J. E., Liu, L., Rosten, P., Humphries, R. K., Jefferson, A. B., Majerus, P. W., and Krystal, G. The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. Proc. Natl. Acad. Sci. USA, 93: 1689-1693, 1996.
28. Kavanaugh, W. M., Pot, D. A., Chin, S. M., Deuter-Reinhard, M., Jefferson, A. B., Norris, F. A., Masiarz, F. R., Cousens, L. S., Majerus, P. W., and Williams, L. T. Multiple forms of an inositol polyphosphate 5-phosphatase form signaling complexes with Shc and Grb2. Curr. Biol., 6: 438-445, 1996.
29. Lioubin, M. N., Algate, P. A., Tsai, S., Carlberg, K., Aebersold, A., and Rohrschneider, L. R. p150Ship, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev., 10: 1084-1095, 1996.
30. Downward, J. How BAD phosphorylation is good for survival. Nat. Cell Biol., 1: E33-E35, 1999.
31. Cardone, M. H., Roy, N., Stennicke, H. R., Salvesen, G. S., Franke, T. F., Stanbridge, E., Frisch, S., and Reed, J. C. Regulation of cell death protease caspase-9 by phosphorylation. Science (Wash. DC), 282: 1318-1321, 1998.
32. Philpott, N. J., Turner, A. J., Scopes, J., Westby, M., Marsh, J. C., Gordon-Smith, E. C., Dalgleish, A. G., and Gibson, F. M. The use of 7-amino actinomycin D in identifying apoptosis: simplicity of use and broad spectrum of application compared with other techniques. Blood, 87: 2244-2251, 1996.
33. Bonnesen, C., Eggleston, I. M., and Hayes, J. D. Dietary indoles and isothiocyanates that are generated from cruciferous vegetables can both stimulate apoptosis and confer protection against DNA damage in human colon cell lines. Cancer Res., 61: 6120-6130, 2001.
34. Meng, Q., Yuan, F., Goldberg, I. D., Rosen, E. M., Auborn, K., and Fan, S. Indole-3-carbinol is a negative regulator of estrogen receptor-α signaling in human tumor cells. J. Nutr., 130: 2927-2931, 2000.
35. Meng, Q., Qi, M., Chen, D. Z., Yuan, R., Goldberg, I. D., Rosen, E. M., Auborn, K., and Fan, S. Suppression of breast cancer invasion and migration by indole-3-carbinol: associated with up-regulation of BRCA1 and E-cadherin/catenin complexes. J. Mol. Med., 78: 155-165, 2000.
36. McMenamin, M. E., Soung, P., Perera, S., Kaplan, I., Loda, M., and Sellers, W. R. Loss of PTEN expression in paraffin-embedded primary prostate cancer correlates with high Gleason score and advanced stage. Cancer Res., 59: 4291-4296, 1999.
37. Li, J., Yen, C., Liaw, D., Podsypanina, K., Bose, S., Wang, S. I., Puc, J., Miliaresis, C., Rodgers, L., McCombie, R., Bigner, S. H., Giovanella, B. C., Ittmann, M., Tycko, B., Hibshoosh, H., Wigler, M. H., and Parsons, R. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science (Wash. DC), 275: 1943-1947, 1997.
38. Morris, G. L., and Dodd, J. G. Epidermal growth factor receptor mRNA levels in human prostatic tumors and cell lines. J. Urol., 143: 1272-1274, 1990.
39. Scher, H. I., Sarkis, A., Reuter, V., Cohen, D., Netto, G., Petrylak, D., Lianes, P., Fuks, Z., Mendelsohn, J., and Cordon-Cardo, C. Changing pattern of expression of the epidermal growth factor receptor and transforming growth factor α in the progression of prostatic neoplasms. Clin. Cancer Res., 1: 545-550, 1995.
40. Ng, S. S. W., Tsao, M. S., Chow, S., and Hedley, D. W. Inhibition of phosphatidylinositide 3-kinase enhances gemcitabine-induced apoptosis in human pancreatic cancer cells. Cancer Res., 60: 5451-5455, 2000.
41. Nakashio, A., Fujita, N., Rokudai, S., Sato, S., and Tsuruo, T. Prevention of phosphatidylinositol 3′-kinase-Akt survival signaling pathway during topotecan-induced apoptosis. Cancer Res., 60: 5303-5309, 2000.
42. Zundel, W., and Giaccia, A. Inhibition of the anti-apoptotic PI(3)K/Akt/Bad pathway by stress. Genes Dev., 12: 1941-1946, 1998.
43. Wang, X., McCullough, K. D., Franke, T. F., and Holbrook, N. J. Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J. Biol. Chem., 275: 14624-14631, 2000.
44. Levitzki, A., and Gazit, A. Tyrosine kinase inhibition: an approach to drug development. Science (Wash. DC), 267: 1782-1788, 1995.
45. Tilley, W. D., Wilson, C. M., Marcelli, M., and McPhaul, M. J. Androgen receptor gene expression in human prostate carcinoma cell lines. Cancer Res., 50: 5382-5386, 1990.
46. Peng, D., Fan, Z., Lu, Y., DeBlasio, T., Scher, H., and Mendelsohn, J. Anti-epidermal growth factor receptor monoclonal antibody 225 upregulates p27KIP1 and induces G1 arrest in prostatic cancer cell line DU145. Cancer Res., 56: 3666-3669, 1996.
47. Sizemore, N., Choo, C. K., Eckert, R. L., and Rorke, E. A. Transcriptional regulation of the EGF receptor promoter by HPV16 and retinoic acid in human ectocervical epithelial cells. Exp. Cell Res., 244: 349-356, 1998.
48. Zheng, Z. S., Polakowska, R., Johnson, A., and Goldsmith, L. A. Transcriptional control of epidermal growth factor receptor by retinoic acid. Cell Growth Differ., 3: 225-232, 1992.
49. Liu, X. W., Katagiri, Y., Jiang, H., Gong, L. J., Guo, L. Y., Shibutani, M., Johnson, A. C., and Guroff, G. Cloning and characterization of the promoter region of the rat epidermal growth factor receptor gene and its transcriptional regulation by nerve growth factor in PC12 cells. J. Biol. Chem., 275: 7280-7288, 2000.
50. Csordas, G., Santra, M., Reed, C. C., Eichstetter, I., McQuillan, D. J., Gross, D., Nugent, M. A., Hajnoczky, G., and Iozzo, R. V. Sustained down-regulation of the epidermal growth factor receptor by decorin. A mechanism for controlling tumor growth in vivo. J. Biol. Chem., 275: 32879-32887, 2000.
51. Bae, S. S., Choi, J. H., Oh, Y. S., Perry, D. K., Ryu, S. H., and Suh, P. G. Proteolytic cleavage of epidermal growth factor receptor by caspases. FEBS Lett., 491: 16-20, 2001.
52. Levkowitz, G., Waterman, H., Zamir, E., Kam, Z., Oved, S., Langdon, W. Y., Beguinot, L., Geiger, B., and Yarden, Y. c-Cb1/Sli-l regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev., 12: 3663-3674, 1998.
53. Bao, J., Alroy, I., Waterman, H., Schejter, E. D., Brodie, C., Gruenberg, J., and Yarden, Y. Threonine phosphorylation diverts internalized epidermal growth factor receptors from a degradative pathway to the recycling endosome. J. Biol. Chem., 275: 26178-26186, 2000.
54. Jost, M., Huggett, T. M., Kari, C., Boise, L. H., and Rodeck, U. Epidermal growth factor receptor-dependent control of keratinocyte survival and Bcl-xL expression through a MEK-dependent pathway. J. Biol. Chem., 276: 6320-6326, 2001.
55. Fukumi, S., Horiguchi-Yamada, J., Nakada, S., Nagai, M., Ohno, T., and Yamada, H. Differential responses of Bcl-2 family genes to etoposide in chronic myeloid leukemia K562 cells. Mol. Cell. Biochem., 206: 43-50, 2000.