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Review

Putative mechanisms of action for indole-3-carbinol in the prevention of colorectal cancer

, MB BCh BAO PhD MRCS & , MB BS MD FRACS FRCS
Pages 729-738 | Published online: 15 May 2008

Bibliography

  • Brockmoller J, Cascorbi I, Henning S, et al. Molecular genetics of cancer susceptibility. Pharmacol 2000;61(3):212-27
  • Doll R, Peto R. The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst 1981;66(6):1191-308
  • Willett WC. Diet, nutrition, and avoidable cancer. Environ Health Perspect 1995;103(Suppl 8):165-70
  • Correa Lima MP, Gomes-Da-Silva MH. Colorectal cancer: lifestyle and dietary factors. Nutr Hosp 2005;20(4):235-41
  • Steinmetz KA, Potter JD. Vegetables, fruit, and cancer prevention: a review. J Am Diet Assoc 1996;96(10):1027-39
  • Steinmetz KA, Potter JD. Vegetables, fruit, and cancer. I. Epidemiology. Cancer Causes Control 1991;2(5):325-57
  • Michaud D, Spiegelman D, Clinton S, et al. Fruit and vegetable intake and incidence of bladder cancer in a male prospective cohort. J Natl Cancer Inst 1999;91:605-13
  • National Health And Medical Research Council. Guidelines for the prevention, early detection and management of Colorectal Cancer. edition. Australian Government Publishing Service, Canberra, 1999. p. 196. Available from: http://www.nhmrc.gov.au/publications/synopses/withdrawn/cp62.pdf [Last accessed 9 April 2008]
  • Cohen J, Kristal A, Stanford J. Fruit and vegetable intakes and prostate cancer risk. J Natl Cancer Inst 2000;92:61-8
  • Potter J. Colorectal cancer: molecules and populations. J Natl Cancer Inst 1999;91:916-32
  • Schulman CC, Ekane S, Zlotta AR. Nutrition and prostate cancer: evidence or suspicion? Urology 2001;58(3):318-34
  • Giovannucci E. Tomatoes, tomato-based products, lycopene, and cancer: review of the epidemiologic literature. J Natl Cancer Inst 1999;91(4):317-31
  • Giovannucci E, Rimm EB, Liu Y, et al. A prospective study of tomato products, lycopene, and prostate cancer risk. J Natl Cancer Inst 2002;94(5):391-8
  • Terry P, Giovannucci E, Michels KB, et al. Fruit, vegetables, dietary fiber, and risk of colorectal cancer. J Natl Cancer Inst 2001;93(7):525-33
  • Block G, Patterson B, Subar A. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr Cancer 1992;18(1):1-29
  • Larsson SC, Hakansson N, Naslund I, et al. Fruit and vegetable consumption in relation to pancreatic cancer risk: a prospective study. Cancer Epidemiol Biomarkers Prev 2006;15(2):301-5
  • Ambrosone CB, McCann SE, Freudenheim JL, et al. Breast cancer risk in premenopausal women is inversely associated with consumption of broccoli, a source of isothiocyanates, but is not modified by GST genotype. J Nutr 2004;134:1134
  • Verhoeven DT, Goldbohm RA, Van Poppel G, et al. Epidemiological studies on brassica vegetables and cancer risk. Cancer Epidemiol Biomarkers Prev 1996;5(9):733-48
  • Hsing AW, Chokkalingam AP, Gao Y-T, et al. Allium Vegetables and risk of prostate cancer: a population-based study. J Natl Cancer Inst 2002;94(21):1648-51
  • Le Marchand L, Murphy SP, Hankin JH, et al. Intake of flavonoids and lung cancer. J Natl Cancer Inst 2000;92(2):154-60
  • Michels KB, Edward G, Joshipura KJ, et al. Prospective study of fruit and vegetable consumption and incidence of colon and rectal cancers. J Natl Cancer Inst 2000;92(21):1740-52
  • Viner JL, Umar A, Hawk ET. Chemoprevention of colorectal cancer: problems, progress, and prospects. Gastroenterol Clin North Am 2002;31(4):971-99
  • Manson MM. Cancer prevention – the potential for diet to modulate molecular signalling. Trends Mol Med 2003;9(1):11-8
  • Clapper ML, Szarka CE. Glutathione S-transferases – biomarkers of cancer risk and chemopreventive response. Chem Biol Inter 1998;111-112:377-88
  • Gescher AJ, Sharma RA, Steward WP. Cancer chemoprevention by dietary constituents: a tale of failure and promise. Lancet Oncol 2001;2(6):371-9
  • Hayes JD, McMahon M. Molecular basis for the contribution of the antioxidant responsive element to cancer chemoprevention. Cancer Lett 2001;174(2):103-13
  • Kirlin WG, Cai J, Delong MJ, et al. Dietary compounds that induce cancer preventive phase 2 enzymes activate apoptosis at comparable doses in HT29 colon carcinoma cells. J Nutr 1999;129(10):1827-35
  • Prochaska HJ, Santamaria AB, Talalay P. Rapid detection of inducers of enzymes that protect against carcinogens. Proc Natl Acad Sci USA 1992;89(6):2394-8
  • Mabberley DJ, editor. The plant-book: a portable dictionary of the vascular plants utilizing Kubitzki's The families and genera of vascular plants (1990-), Cronquist's An integrated system of classification of flowering plants (1981), and current botanical literature, arranged largely on the principles of editions 1 – 6 (1896/97 – 1931) of Willis's A dictionary of the flowering plants and ferns. Cambridge University Press: Cambridge, United Kingdom; New York; 1997. p. xvi, 858
  • Fenwick GR, Heaney RK, Mullin WJ. Glucosinolates and their breakdown products in food and food plants. Crit Rev Food Sci Nutr 1983;18(2):123-201
  • Steinkellner H, Rabot S, Freywald C, et al. Effects of cruciferous vegetables and their constituents on drug metabolizing enzymes involved in the bioactivation of DNA-reactive dietary carcinogens. Mutat Res 2001;480-481:285-97
  • Lin HJ, Probst-Hensch NM, Louie AD, et al. Glutathione transferase null genotype, broccoli, and lower prevalence of colorectal adenomas. Cancer Epidemiol Biomarkers Prev 1998;7(8):647-52
  • Joseph MA, Moysich KB, Freudenheim JL, et al. Cruciferous vegetables, genetic polymorphisms in glutathione S-transferases M1 and T1, and prostate cancer risk. Nutr Cancer 2004;50(2):206-13
  • Slattery ML, Kampman E, Samowitz W, et al. Interplay between dietary inducers of GST and the GSTM-1 genotype in colon cancer. Int J Cancer 2000;87(5):728-33
  • Wang LI, Giovannucci EL, Hunter D, et al. Dietary intake of cruciferous vegetables, glutathione S-transferase (GST) polymorphisms and lung cancer risk in a Caucasian population. Cancer Causes Control 2004;15(10):977-85
  • Kohlmeier L, Simonsen N, Mottus K. Dietary modifiers of carcinogenesis. Environ Health Perspect 1995;103(Suppl 8):177-84
  • Mithen RF, Dekker M, Verkerk R, et al. The nutritional significance, biosynthesis and bioavailability of glucosinolates in human foods. J Science Food Agric 2000;80(7):967-84
  • Musk SR, Johnson IT. Allyl isothiocyanate is selectively toxic to transformed cells of the human colorectal tumour line HT29. Carcinogenesis 1993;14(10):2079-83
  • Smith TK, Lund EK, Clarke RG, et al. Effects of Brussels sprout juice on the cell cycle and adhesion of human colorectal carcinoma cells (HT29) in vitro. J Agric Food Chem 2005;53(10):3895-901
  • Lynn A, Collins A, Fuller Z, et al. Cruciferous vegetables and colo-rectal cancer. Proc Nutr Soc 2006;65(1):135-44
  • Bones AM, Rossiter JT. The myrosinase-glucosinolate system, its organisation and biochemistry. Physiol Plant 1996;97(1):194-208
  • Fahey JW, Zhang Y, Talalay P. Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc Natl Acad Sci 1997;94(19):10367-72
  • Halkier BA, Gershenzon J. Biology and biochemistry of glucosinolates. Ann Rev Plant Biol 2006;57:303-33
  • Talalay P, Fahey JW. Phytochemicals from cruciferous plants protect against cancer by modulating carcinogen metabolism. J Nutr 2001;131(11 Suppl):S3027-33
  • McDanell R, McLean AEM, Hanley AB, et al. The effect of feeding brassica vegetables and intact glucosinolates on mixed-function-oxidase activity in the livers and intestines of rats. Food Chem Toxicol 1989;27(5):289-94
  • Kris-Etherton PM, Hecker KD, Bonanome A, et al. Bioactive compounds in foods: their role in the prevention of cardiovascular disease and cancer. Am J Med 2002;113(Suppl 9B):S71-88
  • Shapiro TA, Fahey JW, Wade KL, et al. Human metabolism and excretion of cancer chemoprotective glucosinolates and isothiocyanates of cruciferous vegetables. Cancer Epidemiol Biomarkers Prev 1998;7(12):1091-100
  • Conaway CC, Getahun SM, Liebes LL, et al. Disposition of glucosinolates and sulforaphane in humans after ingestion of steamed and fresh broccoli. Nutr Cancer 2000;38(2):168-78
  • Shapiro TA, Fahey JW, Wade KL, et al. Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: metabolism and excretion in humans. Cancer Epidemiol Biomarkers Prev 2001;10(5):501-8
  • Vermeulen M, Vandenberg R, Freidig AP, et al. Association between consumption of cruciferous vegetables and condiments and excretion in urine of isothiocyanate mercapturic Acids. J Agric Food Chem 2006;54(15):5350-8
  • Gasper AV, Al-Janobi A, Smith JA, et al. Glutathione S-transferase M1 polymorphism and metabolism of sulforaphane from standard and high-glucosinolate broccoli. Am J Clin Nutr 2005;82(6):1283-91
  • Hayes JD, Flanagan JU, Jowsey IR. Glutathione transferases. Ann Rev Pharmacol Toxicol 2005;45:51-88
  • Fahey JW, Zalcmann AT, Talalay P. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 2001;56(1):5-51
  • Rogan EG. The natural chemopreventive compound indole-3-carbinol: state of the science. In Vivo 2006;20(2):221-8
  • Ge X, Yannai S, Rennert G, et al. 3,3′-Diindolylmethane induces apoptosis in human cancer cells. Biochem Biophys Res Commun 1996;228(1):153-8
  • Bell MC, Crowley-Nowick P, Bradlow HL, et al. Placebo-controlled trial of indole-3-carbinol in the treatment of CIN. Gynecol Oncol 2000;78(2):123-9
  • Reed GA, Peterson KS, Smith HJ, et al. A Phase I study of indole-3-carbinol in women: tolerability and effects. Cancer Epidemiol Biomarkers Prev 2005;14(8):1953-60
  • Rosen CA, Bryson PC. Indole-3-carbinol for recurrent respiratory papillomatosis: long-term results. J Voice 2004;18(2):248-53
  • Anderton MJ, Manson MM, Verschoyle RD, et al. Pharmacokinetics and tissue disposition of indole-3-carbinol and its acid condensation products after oral administration to mice. Clin Cancer Res 2004;10(15):5233-41
  • Aggarwal BB, Ichikawa H. Molecular targets and anticancer potential of Indole-3-carbinol and its derivatives. Cell Cycle 2005;4(9):1201-15
  • Mori H, Niwa K, Zheng Q, et al. Cell proliferation in cancer prevention; effects of preventive agents on estrogen-related endometrial carcinogenesis model and on an in vitro model in human colorectal cells. Mutat Res 2001;480-481:201-7
  • Chinni SR, Li Y, Upadhyay S, et al. Indole-3-carbinol (I3C) induced cell growth inhibition, G1 cell cycle arrest and apoptosis in prostate cancer cells. Oncogene 2001;20(23):2927-36
  • Chen YR, Wang W, Kong AN, Tan TH. Molecular mechanisms of c-Jun N-terminal kinase-mediated apoptosis induced by anticarcinogenic isothiocyanates. J Biol Chem 1998;273(3):1769-75
  • Gamet-Payrastre L, Li P, Lumeau S, et al. Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Res 2000;60(5):1426-33
  • Huang C, Ma WY, Li J, et al. Essential role of p53 in phenethyl isothiocyanate-induced apoptosis. Cancer Res 1998;58(18):4102-6
  • Chiao JW, Chung FL, Kancherla R, et al. Sulforaphane and its metabolite mediate growth arrest and apoptosis in human prostate cancer cells. Int J Oncol 2002;20(3):631-6
  • Takada Y, Andreeff M, Aggarwal BB. Indole-3-carbinol suppresses NF-kB and IkBa kinase activation, causing inhibition of expression of NF-kB-regulated antiapoptotic and metastatic gene products and enhancement of apoptosis in myeloid and leukaemia cells. Blood 2005;106(2):641-9
  • Keck AS, Finley JW. Cruciferous vegetables: cancer protective mechanisms of glucosinolate hydrolysis products and selenium. Integr Cancer Ther 2004;3(1):5-12
  • Herraiz T, Galisteo J. Endogenous and dietary indoles: a class of antioxidants and radical scavengers in the ABTS assay. Free Radic Res 2004;38(3):323-31
  • Plumb GW, Lambert N, Chambers SJ. Are whole extracts and purified glucosinolates from cruciferous vegetables antioxidants? Free Radic Res 1996;25:75-86
  • Lampe JW. Health effects of vegetables and fruit: assessing mechanisms of action in human experimental studies. Am J Clin Nutr 1999;70(3 Suppl):S475-90
  • Itoh K, Chiba T, Takahashi S, et al. An Nrf2/small Maf heterodimer mediates the induction of Phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 1997;236(2):313-22
  • Lampe JW, Peterson S. Brassica, biotransformation and cancer risk: genetic polymorphisms alter the preventive effects of cruciferous vegetables. J Nutr 2002;132(10):2991-4
  • Talalay P, Fahey JW, Holtzclaw WD, et al. Chemoprotection against cancer by phase 2 enzyme induction. Toxicol Lett 1995;82-83:173-9
  • Smith G, Stanley LA, Sim E, et al. Metabolic polymorphisms and cancer susceptibility. Cancer Surv 1995;25:27-65
  • Beecher C. Cancer preventive properties of varieties of Brassica oleracea: a review. Am J Clin Nutr 1994;59(Suppl):S1166-70
  • Bonnesen C, Eggleston IM, Hayes JD. 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 2001;61(16):6120-30
  • Lampe JW, Chen C, Li S, et al. Modulation of human glutathione S-transferases by botanically defined vegetable diets. Cancer Epidemiol Biomarkers Prev 2000;9(8):787-93
  • Pence BC, Buddingh F, Yang SP. Multiple dietary factors in the enhancement of dimethylhydrazine carcinogenesis: main effect of indole-3-carbinol. J Natl Cancer Inst 1986;77(1):269-76
  • Wong GY, Bradlow L, Sepkovic D, et al. Dose-ranging study of indole-3-carbinol for breast cancer prevention. J Cell Biochem Suppl 1997;28-29:111-6
  • Van Iersel ML, Verhagen H, Van Bladeren PJ. The role of biotransformation in dietary (anti)carcinogenesis. Mutat Res 1999;443(1-2):259-70
  • Cover CM, Hsieh SJ, Tran SH, et al. 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 signalling. J Biol Chem 1998;273(7):3838-47
  • Mcguire KP, Ngoubilly N, Neavyn M, Lanza-Jacoby S. 3,3′-diindolylmethane and paclitaxel act synergistically to promote apoptosis in HER2/Neu human breast cancer cells. J Surg Res 2006;132(2):208-13
  • Bradlow HL, Michnovicz JJ, Halper M, et al. Long-term responses of women to indole-3-carbinol or a high fiber diet. Cancer Epidemiol Biomarkers Prev 1994;3(7):591-5
  • Kall MA, Vang O, Clausen J. Effects of dietary broccoli on human in vivo drug metabolizing enzymes: evaluation of caffeine, oestrone and chlorzoxazone metabolism. Carcinogenesis 1996;17(4):793-9
  • Dashwood RH. Indole-3-carbinol: anticarcinogen or tumor promoter in brassica vegetables? Chem Biol Inter 1998;110(1-2):1-5
  • Bailey GS, Hendricks JD, Shelton DW, et al. Enhancement of carcinogenesis by the natural anticarcinogen indole-3-carbinol. J Natl Cancer Inst 1987;78(5):931-4
  • Kim DJ, Han BS, Ahn B, et al. Enhancement by indole-3-carbinol of liver and thyroid gland neoplastic development in a rat medium-term multiorgan carcinogenesis model. Carcinogenesis 1997;18(2):377-81
  • Fahey JW, Talalay P. Antioxidant functions of sulforaphane: a potent inducer of Phase II detoxication enzymes. Food Chem Toxicol 1999;37(9-10):973-9
  • Villafania A, Anwar K, Amar S, et al. Glutathione-S-transferase as a selective inhibitor of oncogenic ras-p21-induced mitogenic signalling through blockade of activation of jun by jun-N-terminal kinase. Ann Clin Lab Sci 2000;30(1):57-64
  • Yeh CC, Hsieh LL, Tang R, et al. Vegetable/fruit, smoking, glutathione S-transferase polymorphisms and risk for colorectal cancer in Taiwan. World J Gastroenterol 2005;11(10):1473-80
  • Clapper ML, Szarka CE, Pfeiffer GR, et al. Preclinical and clinical evaluation of broccoli supplements as inducers of glutathione S-transferase activity. Clin Cancer Res 1997;3(1):25-30
  • Grubben MJ, Van Den Braak CC, Nagengast FM, Peters WH. Low colonic glutathione detoxification capacity in patients at risk for colon cancer. Eur J Clin Invest 2006;36(3):188-92
  • Mulder TP, Roelofs HM, Peters WH, et al. Glutathione S-transferases in liver metastases of colorectal cancer. A comparison with normal liver and primary carcinomas. Carcinogenesis 1994;15(10):2149-53
  • Pietsch EC, Hurley AL, Scott EE, et al. Oxathiolene oxides: a novel family of compounds that induce ferritin, glutathione S-transferase, and other proteins of the Phase II response. Biochem Pharmacol 2003;65(8):1261-9
  • Engel LS, Taioli E, Pfeiffer R, et al. Pooled analysis and meta-analysis of glutathione S-transferase M1 and bladder cancer: a HuGE review. Am J Epidemiol 2002;156(2):95-109
  • Eaton DL, Bammler TK. Concise review of the glutathione S-transferases and their significance to toxicology. Toxicol Sci 1999;49(2):156-64
  • Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974;249(22):7130-9
  • Brooks JD, Paton VG, Vidanes G. Potent induction of phase 2 enzymes in human prostate cells by sulforaphane. Cancer Epidemiol Biomarkers Prev 2001;10(9):949-54
  • Spigelman AD, Nugent KP, Penna C, et al. Glutathione S-transferase Mu phenotype in patients with familial adenomatous polyposis and in unaffected controls. Cancer Detect Prev 1994;18(4):253-8
  • Spitz MR, Duphorne CM, Detry MA, et al. Dietary intake of isothiocyanates: evidence of a joint effect with glutathione S-transferase polymorphisms in lung cancer risk. Cancer Epidemiol Biomarkers Prev 2000;9(10):1017-20
  • Szarka CE, Pfeiffer GR, Hum ST, et al. Glutathione S-transferase activity and glutathione S-transferase μ expression in subjects with risk for colorectal cancer. Cancer Res 1995;55(13):2789-93
  • Zhong S, Wyllie AH, Barnes D, et al. Relationship between the GSTM1 genetic polymorphism and susceptibility to bladder, breast and colon cancer. Carcinogenesis 1993;14(9):1821-4
  • Ansher SS, Dolan P, Bueding E. Biochemical effects of dithiolthiones. Food Chem Toxicol 1986;24(5):405-15
  • Bradfield CA, Bjeldanes LF. Effect of dietary indole-3-carbinol on intestinal and hepatic monooxygenase, glutathione S-transferase and epoxide hydrolase activities in the rat. Food Chem Toxicol 1984;22(12):977-82
  • Gill CI, Haldar S, Porter S, et al. The effect of cruciferous and leguminous sprouts on genotoxicity, in vitro and in vivo. Cancer Epidemiol Biomarkers Prev 2004;13(7):1199-205
  • Nijhoff WA, Grubben MJ, Nagengast FM, et al. Effects of consumption of Brussels sprouts on intestinal and lymphocytic glutathione S-transferases in humans. Carcinogenesis 1995;16(9):2125-8
  • Salbe AD, Bjeldanes LF. The effects of dietary Brussels sprouts and Schizandra chinensis on the xenobiotic-metabolizing enzymes of the rat small intestine. Food Chem Toxicol 1985;23(1):57-65
  • Vella F, Ferry G, Delagrange P, Boutin JA. NRH:quinone reductase 2: an enzyme of surprises and mysteries. Biochem Pharmacol 2005;71(1-2):1-12
  • Frydoonfar HR, McGrath DR, Spigelman AD. The effect of indole-3-carbinol and sulforaphane on a prostate cancer cell line. ANZ J Surg 2003;73(3):154-6
  • Frydoonfar HR, McGrath DR, Spigelman AD. Inhibition of proliferation of a colon cancer cell line by indole-3-carbinol. Colorect Dis 2002;4(3):205-7
  • Chang X, Tou JC, Hong C, et al. 3,3′-Diindolylmethane inhibits angiogenesis and the growth of transplantable human breast carcinoma in athymic mice. Carcinogenesis 2005;26(4):771-8
  • Brew CT, Aronchik I, Hsu JC, et al. Indole-3-carbinol activates the ATM signaling pathway independent of DNA damage to stabilize p53 and induce G1 arrest of human mammary epithelial cells. Int J Cancer 2006;118(4):857-68
  • Chiao JW, Chung F, Krzeminski J, et al. Modulation of growth of human prostate cancer cells by the N-acetylcysteine conjugate of phenethyl isothiocyanate. Int J Oncol 2000;16(6):1215-9
  • Qi M, Anderson AE, Chen D, et al. Indole-3-carbinol prevents PTEN loss in cervical cancer in vivo. Mol Med 2005;11(1-12):59-63
  • Wu HT, Lin SH, Chen YH. Inhibition of cell proliferation and in vitro markers of angiogenesis by indole-3-carbinol, a major indole metabolite present in cruciferous vegetables. J Agric Food Chem 2005;53(13):5164-9
  • Sundar SN, Kerekatte V, Equinozio CN, et al. Indole-3-carbinol selectively uncouples expression and activity of estrogen receptor subtypes in human breast cancer cells. Mol Endocrinol 2006;20(12):3070-82
  • Zhang Y. Role of glutathione in the accumulation of anticarcinogenic isothiocyanates and their glutathione conjugates by murine hepatoma cells. Carcinogenesis 2000;21(6):1175-82
  • Zhang Y. Molecular mechanism of rapid cellular accumulation of anticarcinogenic isothiocyanates. Carcinogenesis 2001;22(3):425-31
  • Zhang Y, Callaway EC. High cellular accumulation of sulforaphane, a dietary anticarcinogen, is followed by rapid transporter-mediated export as a glutathione conjugate. Biochem J 2002;364(1):301-7

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