In vivo pharmacodynamics of indole-3-carbinol in the inhibition of prostate cancer in transgenic adenocarcinoma of mouse prostate (TRAMP) mice: Involvement of Nrf2 and cell cycle/apoptosis signaling pathways

Molecular Carcinogenesis

Volumn 51, Issue 10, 2012, Pages 761-770

  Wu, Tien Yuan ^a   Saw, Constance Lay Lay ^a   Khor, Tin Oo ^a   Pung, Douglas ^a   Boyanapalli, Sarandeep S S ^a   Kong, Ah Ng Tong ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Indole 3 carbinol; Nrf2; Phase II detoxifying antioxidant enzymes; Prostate cancer; TRAMP mice

Indexed keywords

3 INDOLEMETHANOL; PROTEIN; PROTEIN NQO 1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; CELL CYCLE; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG MECHANISM; FEMALE; GENE EXPRESSION; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PHARMACODYNAMICS; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TRAMP MOUSE; TREATMENT DURATION; WESTERN BLOTTING;

ADENOCARCINOMA; ANIMALS; ANTICARCINOGENIC AGENTS; APOPTOSIS; CELL CYCLE; DIETARY SUPPLEMENTS; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INDOLES; MALE; MICE; MICE, TRANSGENIC; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROSTATIC NEOPLASMS; RESPONSE ELEMENTS;

MUS;

EID: 84866180818     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20841     Document Type: Article

References (40)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010; 60: 277-300.
2. Safe S, Papineni S, Chintharlapalli S. Cancer chemotherapy with indole-3-carbinol, bis(3'-indolyl)methane and synthetic analogs. Cancer Lett 2008; 269: 326-338.
3. Abate-Shen C, Shen MM. Molecular genetics of prostate cancer. Genes Dev 2000; 14: 2410-2434.
4. Carter BS, Carter HB, Isaacs JT. Epidemiologic evidence regarding predisposing factors to prostate cancer. Prostate 1990; 16: 187-197.
5. Sarkar FH, Li Y. Indole-3-carbinol and prostate cancer. J Nutr 2004; 134: 3493S-3498S.
6. Bradlow HL, Michnovicz J, Telang NT, Osborne MP. Effects of dietary indole-3-carbinol on estradiol metabolism and spontaneous mammary tumors in mice. Carcinogenesis 1991; 12: 1571-1574.
7. Grubbs CJ, Steele VE, Casebolt T, et al. Chemoprevention of chemically-induced mammary carcinogenesis by indole-3-carbinol. Anticancer Res 1995; 15: 709-716.
8. Jin L, Qi M, Chen DZ, et al. Indole-3-carbinol prevents cervical cancer in human papilloma virus type 16 (HPV16) transgenic mice. Cancer Res 1999; 59: 3991-3997.
9. Kojima T, Tanaka T, Mori H. Chemoprevention of spontaneous endometrial cancer in female Donryu rats by dietary indole-3-carbinol. Cancer Res 1994; 54: 1446-1449.
10. Oganesian A, Hendricks JD, Williams DE. Long term dietary indole-3-carbinol inhibits diethylnitrosamine-initiated hepatocarcinogenesis in the infant mouse model. Cancer Lett 1997; 118: 87-94.
11. Yu Z, Mahadevan B, Lohr CV, et al. Indole-3-carbinol in the maternal diet provides chemoprotection for the fetus against transplacental carcinogenesis by the polycyclic aromatic hydrocarbon dibenzo[a, l]pyrene. Carcinogenesis 2006; 27: 2116-2123.
12. Weng JR, Tsai CH, Kulp SK, Chen CS. Indole-3-carbinol as a chemopreventive and anti-cancer agent. Cancer Lett 2008; 262: 153-163.
13. Higdon JV, Delage B, Williams DE, Dashwood RH. Cruciferous vegetables and human cancer risk: Epidemiologic evidence and mechanistic basis. Pharmacol Res 2007; 55: 224-236.
14. Kim YS, Milner JA. Targets for indole-3-carbinol in cancer prevention. J Nutr Biochem 2005; 16: 65-73.
15. Tsai JT, Liu HC, Chen YH. Suppression of inflammatory mediators by cruciferous vegetable-derived indole-3-carbinol and phenylethyl isothiocyanate in lipopolysaccharide-activated macrophages. Mediators Inflamm 2010; 29: 36-42.
16. Minich DM, Bland JS. A review of the clinical efficacy and safety of cruciferous vegetable phytochemicals. Nutr Rev 2007; 65: 259-267.
17. Fan S, Meng Q, Saha T, Sarkar FH, Rosen EM. Low concentrations of diindolylmethane, a metabolite of indole-3-carbinol, protect against oxidative stress in a BRCA1-dependent manner. Cancer Res 2009; 69: 6083-6091.
18. Pathak SK, Sharma RA, Steward WP, Mellon JK, Griffiths TR, Gescher AJ. Oxidative stress and cyclooxygenase activity in prostate carcinogenesis: Targets for chemopreventive strategies. Eur J Cancer 2005; 41: 61-70.
19. Barve A, Khor TO, Nair S, et al. Gamma-tocopherol-enriched mixed tocopherol diet inhibits prostate carcinogenesis in TRAMP mice. Int J Cancer 2009; 124: 1693-1699.
20. Frohlich DA, McCabe MT, Arnold RS, Day ML. The role of Nrf2 in increased reactive oxygen species and DNA damage in prostate tumorigenesis. Oncogene 2008; 27: 4353-4362.
21. Hu R, Saw CL, Yu R, Kong AN. Regulation of NF-E2-related factor 2 signaling for cancer chemoprevention: Antioxidant coupled with antiinflammatory. Antioxid Redox Signal 2010; 13: 1679-1698.
22. Yu R, Mandlekar S, Lei W, Fahl WE, Tan TH, Kong AN. p38 mitogen-activated protein kinase negatively regulates the induction of phase II drug-metabolizing enzymes that detoxify carcinogens. J Biol Chem 2000; 275: 2322-2327.
23. Chen C, Yu R, Owuor ED, Kong AN. Activation of antioxidant-response element (ARE), mitogen-activated protein kinases (MAPKs) and caspases by major green tea polyphenol components during cell survival and death. Arch Pharm Res 2000; 23: 605-612.
24. Prawan A, Keum YS, Khor TO, et al. Structural influence of isothiocyanates on the antioxidant response element (ARE)-mediated heme oxygenase-1 (HO-1) expression. Pharm Res 2008; 25: 836-844.
25. Jeong WS, Keum YS, Chen C, et al. Differential expression and stability of endogenous nuclear factor E2-related factor 2 (Nrf2) by natural chemopreventive compounds in HepG2 human hepatoma cells. J Biochem Mol Biol 2005; 38: 167-176.
26. Wu TY, Khor TO, Saw CL, et al. Anti-inflammatory/anti-oxidative stress activities and differential regulation of Nrf2-mediated genes by non-polar fractions of tea Chrysanthemum zawadskii and Licorice glycyrrhiza uralensis AAPS J 2011; 13: 1-13.
27. Foster BA, Gingrich JR, Kwon ED, Madias C, Greenberg NM. Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res 1997; 57: 3325-3330.
28. Nair S, Hebbar V, Shen G, et al. Synergistic effects of a combination of dietary factors sulforaphane and (-) epigallocatechin-3-gallate in HT-29 AP-1 human colon carcinoma cells. Pharm Res 2008; 25: 387-399.
29. Barve A, Khor TO, Nair S, et al. Pharmacogenomic profile of soy isoflavone concentrate in the prostate of Nrf2 deficient and wild-type mice. J Pharm Sci 2008; 97: 4528-4545.
30. Souli E, Machluf M, Morgenstern A, Sabo E, Yannai S. Indole-3-carbinol (I3C) exhibits inhibitory and preventive effects on prostate tumors in mice. Food Chem Toxicol 2008; 46: 863-870.
31. Kassie F, Matise I, Negia M, Upadhyaya P, Hecht SS. Dose-dependent inhibition of tobacco smoke carcinogen-induced lung tumorigenesis in A/J mice by indole-3-carbinol. Cancer Prev Res (PhilaPa) 2008; 1: 568-576.
32. Barve A, Khor TO, Hao X, et al. Murine prostate cancer inhibition by dietary phytochemicals-Curcumin and phenyethylisothiocyanate. Pharm Res 2008; 25: 2181-2189.
33. Khor TO, Yu S, Barve A, et al. Dietary feeding of dibenzoylmethane inhibits prostate cancer in transgenic adenocarcinoma of the mouse prostate model. Cancer Res 2009; 69: 7096-7102.
34. Park JH, Walls JE, Galvez JJ, et al. Prostatic intraepithelial neoplasia in genetically engineered mice. Am J Pathol 2002; 161: 727-735.
35. Saw CL, Huang Y, Kong AN. Synergistic anti-inflammatory effects of low doses of curcumin in combination with polyunsaturated fatty acids: Docosahexaenoic acid or eicosapentaenoic acid. Biochem Pharmacol 79: 421-430.
36. Saw CL, Olivo M, Chin WW, Soo KC, Heng PW. Transport of hypericin across chick chorioallantoic membrane and photodynamic therapy vasculature assessment. Biol Pharm Bull 2005; 28: 1054-1060.
37. Nachshon-Kedmi M, Yannai S, Haj A, Fares FA. Indole-3-carbinol and 3, 3′-diindolylmethane induce apoptosis in human prostate cancer cells. Food Chem Toxicol 2003; 41: 745-752.
38. Hsu JC, Dev A, Wing A, Brew CT, Bjeldanes LF, Firestone GL. Indole-3-carbinol mediated cell cycle arrest of LNCaP human prostate cancer cells requires the induced production of activated p53 tumor suppressor protein. Biochem Pharmacol 2006; 72: 1714-1723.
39. Cho HJ, Park SY, Kim EJ, Kim JK, Park JH. 3, 3′-Diindolylmethane inhibits prostate cancer development in the transgenic adenocarcinoma mouse prostate model. Mol Carcinog 2011; 50: 100-112.
40. Nair S, Li W, Kong AN. Natural dietary anti-cancer chemopreventive compounds: Redox-mediated differential signaling mechanisms in cytoprotection of normal cells versus cytotoxicity in tumor cells. Acta Pharmacol Sin 2007; 28: 459-472.