Inactivation of Akt and NF-κB play important roles during indole-3-carbinol-induced apoptosis in breast cancer cells

Nutrition and Cancer

Volumn 48, Issue 1, 2004, Pages 84-94

  Rahman, K M Wahidur ^a   Li, Yiwei ^a   Sarkar, Fazlul H ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

3 INDOLEMETHANOL; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE B;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER MORTALITY; CANCER PREVENTION; CELL STRAIN MCF 10A; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; EPITHELIUM CELL; GENE CONSTRUCT; GENE FUNCTION; GENE INACTIVATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOLECULAR MECHANICS; PHENOTYPE; PRECANCER; PROTEIN DNA BINDING; REPORTER GENE; WESTERN BLOTTING;

MINK CELL FOCUS-FORMING VIRUS;

EID: 3042642131     PISSN: 01635581     EISSN: None     Source Type: Journal    
DOI: 10.1207/s15327914nc4801_12     Document Type: Article

References (59)

1. Flagg EW, Coates RJ, Calle EE, Potischman N, and Thun MJ: Validation of the American Cancer Society Cancer Prevention Study II Nutrition Survey Cohort Food Frequency Questionnaire. Epidemiology 11, 462-468, 2000.
2. American Institution for Cancer Research: Food, Nutrition and the Prevention of Cancer: A Global Perspective, Washington, DC: American Institution for Cancer Research, 1997, pp 436-446.
3. Freudenheim JL, Marshall JR, Vena JE, Laughlin R, Brasure JR, et al.: Premenopausal breast cancer risk and intake of vegetables, fruits, and related nutrients. JNCI 88, 340-348, 1996.
4. Shertzer HG: Indole-3-carbinol protects against covalent binding of benzo[a]pyrene and N-nitrosodimethylamine metabolites to mouse liver macromolecules. Chem Biol Interact 48, 81-90, 1984.
5. Loub WD, Wattenberg LW, and Davis DW: Aryl hydrocarbon hydroxylase induction in rat tissues by naturally occurring indoles of cruciferous plants. JNCI 54, 985-988, 1975.
6. Wattenberg LW and Loub WD: Inhibition of polycyclic aromatic hydrocarbon-induced neoplasia by naturally occurring indoles. Cancer Res 38, 1410-1413, 1978.
7. Bradfield CA and Bjeldanes LF: Modification of carcinogen metabolism by indolylic autolysis products of Brassica oleraceae. Adv Exp Med Biol 289, 153-163, 1991.
8. Bailey G, Selivonchick D, and Hendricks J: Initiation, promotion, and inhibition of carcinogenesis in rainbow trout. Environ Health Perspect 71, 147-153, 1987.
9. Grubbs CJ, Steele VE, Casebolt T, Juliana MM, Eto I, et al.: Chemoprevention of chemically-induced mammary carcinogenesis by indole-3-carbinol. Anticancer Res 15, 709-716, 1995.
10. Tiwari RK, Guo L, Bradlow HL, Telang NT, and Osborne MP: Selective responsiveness of human breast cancer cells to indole-3-carbinol, a chemopreventive agent. JNCI 86, 126-131, 1994.
11. Staub RE, Feng C, Onisko B, Bailey GS, Firestone GL, et al.: Fate of indole-3-carbinol in cultured human breast tumor cells. Chem Res Toxicol 15, 101-109, 2002.
12. Chinni SR and Sarkar FH: Akt inactivation is a key event in indole-3-carbinol-induced apoptosis in PC-3 cells. Clin Cancer Res 8, 1228-1236, 2002.
13. Dashwood RH: Indole-3-carbinol: anticarcinogen or tumor promoter in brassica vegetables? Chem Biol Interact 110, 1-5, 1998.
14. Rahman KM, Aranha O, Glazyrin A, Chinni SR, and Sarkar FH: Translocation of Bax to mitochondria induces apoptotic cell death in indole-3-carbinol (I3C) treated breast cancer cells. Oncogene 19, 5764-5771, 2000.
15. Rahman KM, Aranha O, and Sarkar FH: Indole-3 carbinol (I3C) induces apoptosis in tumorigenic but not in non-tumorigenic breast epithelial cells. Nutr Cancer 45, 101-102, 2003.
16. Kojima T, Tanaka T, and Mori H: Chemoprevention of spontaneous endometrial cancer in female donryu rats by dietary indole-3-carbinol. Cancer Res 54, 1446-1449, 1994.
17. Howells LM, Gallacher-Horley B, Houghton CE, Manson MM, and Hudson EA: Indole-3-carbinol inhibits protein kinaseB/Akt and induces apoptosis in the human breast tumor cell line MDA MB468 but not in the nontumorigenic HBL100 line. Mol Cancer Ther 1, 1161-1172, 2002.
18. Chen ZJ, Parent L, and Maniatis T: Site-specific phosphorylation of IκBα by a novel ubiquitination-dependent protein kinase activity. Cell 84, 853-862, 1996.
19. Nakshatri H, Bhat-Nakshatri P, Martin DA, Goulet RJ Jr, and Sledge GW Jr: Constitutive activation of NF-κB during progression of breast cancer to hormone-independent growth. Mol Cell Biol 17, 3629-3639, 1997.
20. Chen L, Fischle W, Verdin E, and Greene WC: Duration of nuclear NF-κB action regulated by reversible acetylation. Science 293, 1653-1657, 2001.
21. Beg AA and Baltimore D: An essential role for NF-κB in preventing TNF-alpha-induced cell death. Science 274, 782-784, 1996.
22. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, and Baldwin AS Jr: NF-κB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281, 1680-1683, 1998.
23. Beg AA, Sha WC, Bronson RT, Ghosh S, and Baltimore D: Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κB. Nature 376, 167-170, 1995.
24. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, et al.: The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81, 727-736, 1995.
25. Okano J, Gaslightwala I, Birnbaum MJ, Rustgi AK, and Nakagawa H: Akt/protein kinase B isoforms are differentially regulated by epidermal growth factor stimulation. J Biol Chem 275, 30934-30942, 2000.
26. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, et al.: Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 15, 6541-6551, 1996.
27. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, et al.: Regulation of cell death protease caspase-9 by phosphorylation. Science 282, 1318-1321, 1998.
28. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, et al.: Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868, 1999.
29. Romashkova JA and Makarov SS: NF-κB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401, 86-90, 1999.
30. Ozes ON, Mayo LD, Gustin JA, Pfeffer SR, Pfeffer LM, et al.: NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401, 82-85, 1999.
31. Li Y and Sarkar FH: Inhibition of nuclear factor κB activation in PC3 cells by genistein is mediated via Akt signaling pathway. Clin Cancer Res 8, 2369-2377, 2002.
32. Soule HD, Maloney TM, Wolman SR, Peterson WD Jr, Brenz R, et al.: Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res 50, 6075-6086, 1990.
33. Tait L, Soule HD, and Russo J: Ultrastructural and immunocytochemical characterization of an immortalized human breast epithelial cell line, MCF-10. Cancer Res 50, 6087-6094, 1990.
34. Miller FR: Xenograft models of premalignant breast disease. J Mammary Gland Biol Neoplasia 5, 379-391, 2000.
35. Rosen CA, Woodson GE, Thompson JW, Hengesteg AP, and Bradlow HL: Preliminary results of the use of indole-3-carbinol for recurrent respiratory papillomatosis. Otolaryngol Head Neck Surg 118, 810-815, 1998.
36. Wong GY, Bradlow L, Sepkovic D, Mehl S, Mailman J, et al.: Dose-ranging study of indole-3-carbinol for breast cancer prevention. J Cell Biochem 28-29(Suppl), 111-116, 1997.
37. Anderton MJ, Jukes R, Lamb JH, Manson MM, Gescher A, et al.: Liquid chromatographic assay for the simultaneous determination of indole-3-carbinol and its acid condensation products in plasma. J Chromatogr B Anal Technol Biomed Life Sci 787, 281-291, 2003.
38. Ramaswamy S, Nakamura N, Vazquez F, Batt DB, Perera S, et al.: Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc Natl Acad Sci USA 96, 2110-2115, 1999.
39. Davis JN, Kucuk O, and Sarkar FH: Genistein inhibits NF-κB activation in prostate cancer cells. Nutr Cancer 35, 167-174, 1999.
40. Vlahos CJ, Matter WF, Hui KY, and Brown RF: A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4- morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 269, 5241-5248, 1994.
41. Cardone M and Mostov K: Wortmannin inhibits transcytosis of dimeric IgA by the polymeric immunoglobulin receptor. FEBS Lett 376, 74-76, 1995.
42. Mori N, Fujii M, Cheng G, Ikeda S, Yamasaki Y, et al.: Human T-cell leukemia virus type I tax protein induces the expression of anti-apoptotic gene Bcl-xL in human T-cells through nuclear factor-κB and c-AMP responsive element binding protein pathways. Virus Genes 22, 279-287, 2001.
43. Sevilla L, Zaldumbide A, Pognonec P, and Boulukos KE: Transcriptional regulation of the bcl-x gene encoding the anti-apoptotic Bcl-xL protein by Ets, Rel/NFκB, STAT and AP1 transcription factor families. Histol Histopathol 16, 595-601, 2001.
44. Elmore E, Luc TT, Steele VE, and Redpath JL: Comparative tissue-specific toxicities of 20 cancer preventive agents using cultured cells from 8 different normal human epithelia. In Vitro Mol Toxicol 14, 191-207, 2001.
45. Katdare M, Osborne MP, and Telang NT: Inhibition of aberrant proliferation and induction of apoptosis in pre-neoplastic human mammary epithelial cells by natural phytochemicals. Oncol Rep 5, 311-315, 1998.
46. Bellacosa A, Testa JR, Staal SP, and Tsichlis PN: A retroviral oncogene, akt, encoding a serine-threonine kinase containing an SH2-like region. Science 254, 274-277, 1991.
47. Nakatani K, Sakaue H, Thompson DA, Weigel RJ, and Roth RA: Identification of a human Akt3 (protein kinase B gamma) which contains the regulatory serine phosphorylation site. Biochem Biophys Res Commun 257, 906-910, 1999.
48. Altomare DA, Guo K, Cheng JQ, Sonoda G, Walsh K, et al.: Cloning, chromosomal localization and expression analysis of the mouse Akt2 oncogene. Oncogene 11, 1055-1060, 1995.
49. Datta SR, Brunet A, and Greenberg ME: Cellular survival: a play in three Akts. Genes Dev 13, 2905-2927, 1999.
50. Cross DA, Watt PW, Shaw M, van der Kaay J, Downes CP, et al.: Insulin activates protein kinase B, inhibits glycogen synthase kinase-3 and activates glycogen synthase by rapamycin-insensitive pathways in skeletal muscle and adipose tissue. FEBS Lett 406, 211-215, 1997.
51. Pap M and Cooper GM: Role of glycogen synthase kinase-3 in the phosphatidylinositol-3kinase/Akt cell survival pathway. J Biol Chem 273, 19929-19932, 1998.
52. Miller JR and Moon RT: Signal transduction through β-catenin and specification of cell fate during embryogenesis. Genes Dev 10, 2527-2539, 1996.
53. Scheid MP and Duronio V: Dissociation of cytokine-induced phosphorylation of Bad and activation of PKB/akt: involvement of MEK upstream of Bad phosphorylation. Proc Natl Acad Sci USA 95, 7439-7444, 1998.
54. Boise LH, Gonzalez-Garcia M, Postema CE, Ding L, Lindsten T, et al.: bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74, 597-608, 1993.
55. Shimizu S, Eguchi Y, Kosaka H, Kamiike W, Matsuda H, et al.: Prevention of hypoxia-induced cell death by Bcl-2 and Bcl-xL. Nature 374, 811-813, 1995.
56. Gottschalk AR, Boise LH, Thompson CB, and Quintans J: Identification of immunosuppressant-induced apoptosis in a murine B-cell line and its prevention by bcl-x but not bcl-2. Proc Natl Acad Sci USA 91, 7350-7354, 1994.
57. Kane LP, Shapiro VS, Stokoe D, and Weiss A: Induction of NF-κB by the Akt/PKB kinase. Curr Biol 9, 601-604, 1999.
58. Factor V, Oliver AL, Panta GR, Thorgeirsson SS, Sonenshein GE, et al.: Roles of Akt/PKB and IKK complex in constitutive induction of NF-κB in hepatocellular carcinomas of transforming growth factor α/c-myc transgenic mice. Hepatology 34, 32-41, 2001.
59. Nakayama H, Ikebe T, Beppu M, and Shirasuna K: High expression levels of nuclear factor κB, IκB kinase α and Akt kinase in squamous cell carcinoma of the oral cavity. Cancer 92, 3037-3044, 2001.