Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-27T17:57:32.029Z Has data issue: false hasContentIssue false
  • English
  • Français

Dietary supplementation of resveratrol suppresses colonic tumour incidence in 1,2-dimethylhydrazine-treated rats by modulating biotransforming enzymes and aberrant crypt foci development

Published online by Cambridge University Press:  08 March 2007

Murugan Sengottuvelan  and
Namasivayam Nalini
Murugan Sengottuvelan
Affiliation:
Department of Biochemistry and Biotechnology, Annamalai University, Annamalainagar – 608 002, Tamilnadu, India
Namasivayam Nalini*
Affiliation:
Department of Biochemistry and Biotechnology, Annamalai University, Annamalainagar – 608 002, Tamilnadu, India
*
*Corresponding author: Dr N. Nalini, fax +91 4144 238343, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Diet-induced changes in the activities of bacterial enzymes are known to play a role in colon cancer development. Resveratrol has been implicated as a protective agent in carcinogenesis. In the present study, the effect of resveratrol on the activities of faecal and colonic biotransforming enzymes such as β-glucuronidase, β-glucosidase, β-galactosidase, mucinase, nitroreductase and faecal sulfatase activity was assessed. The total number of aberrant crypt foci and their distribution in the proximal, medial and distal colon were observed in 1,2-dimethylhydrazine (DMH)-induced rats (group 3) and other treatment groups (groups 4–6). DMH (0.02g/kg body weight) was given subcutaneously once a week for 15 consecutive weeks, and the experiment was terminated at 30 weeks. DMH-treated rats showed elevated levels of cancer-associated bacterial enzyme activities, whereas on resveratrol supplementation in three different regimens, rats showed lowered activities. Resveratrol supplementation throughout the experimental period (group 6) exerted a more pronounced effect (P<0·01) by modulating the development of aberrant crypt foci and the activities of bacterial enzymes than did the other treatment regimens (groups 4 and 5). Thus, the present results demonstrate the inhibitory effect of resveratrol on DMH-induced colon carcinogenesis in rats.

Keywords

Bacterial enzymesResveratrolAberrant crypt fociColon carcinogenesis
Type
Research Article
Information
British Journal of Nutrition , Volume 96 , Issue 1 , January 2006 , pp. 145 - 153
Copyright
Copyright © The Nutrition Society 2006

References

Bird, RPObservation and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: preliminary findings. Cancer Lett (1987) 37, 147–151.CrossRefGoogle ScholarPubMed
Bird, RPRole of aberrant crypt foci in understanding the pathogenesis of colon cancer. Cancer Lett (1995) 93, 55–71.CrossRefGoogle ScholarPubMed
Bird, RP & Good, CKThe significance of aberrant crypt foci in understanding the pathogenesis of colon cancer. Toxicol Lett (2000) 112–113, 395–402.CrossRefGoogle ScholarPubMed
Bratton, AC & Marshall, EKA new coupling component for sulfanilamide determination. J Biol Chem (1939) 128, 537–550.CrossRefGoogle Scholar
Burkitt, DPEpidemiology of cancer of the colon and rectum. Dis Colon Rectum (1993) 36, 1071–1082.CrossRefGoogle ScholarPubMed
Chan, MMAntimicrobial effect of resveratrol on dermatophytes and bacterial pathogens of the skin. Biochem Pharmacol (2002) 63, 99–104.CrossRefGoogle ScholarPubMed
Ector, BJ, Magee, JB, Hegwood, CP & Coign, MResveratrol concentration in muscadine berries, juice, pomace, purees, seeds and wines. Am J Enol Vitic (1996) 47, 57–62.CrossRefGoogle Scholar
Eriyamremu, GE & Adamson, IAlterations in rat colonic faeces exposed to an acute level of deoxycholate and fed on a Nigerian-like diet. Nutr Res (1995) 15, 869–880.CrossRefGoogle Scholar
George, SE, Nelson, GM, Swank, AE, Brooks, LR, Bailey, K, George, M & DeAngelo, AThe disinfection by-products dichloro-, dibromo-, and bromochloroacetic acid impact intestinal microflora and metabolism in Fischer 344 rats upon exposure in drinking water. Toxicol Sci (2000) 56, 282–289.CrossRefGoogle ScholarPubMed
George, SE, Wolf, DC, Brooks, LR, Bailey, KC, Hooth, MJ & Rlelson, GMChanges in caecal microbial metabolism of rats induced by individual and a mixture of drinking water disinfection by-products. Cancer Lett (2004) 204, 15–21.CrossRefGoogle Scholar
Goldin, BRChemical induction of colon tumours in animals: an overview. Prog Clin Biol Res (1998) 279, 319–333.Google Scholar
Goldin, BR & Gorbach, SLAlterations of the intestinal micro-flora by diet, oral antibiotics, and Lactobacillus: decreased production of free amines from aromatic nitro compounds, azo dyes, and glucuronides. J Natl Cancer Inst (1984) 73, 689–695.Google Scholar
Gorbach, SL & Goldin, BRThe intestinal microflora and the colon cancer connection. Rev Infect Dis (1990) 12, S252–S261.CrossRefGoogle ScholarPubMed
Gusman, J, Malonne, H & Atassi, GA reappraisal of the potential chemopreventive and chemotherapeutic properties of resveratrol. Carcinogenesis (2001) 22, 1111–1117.CrossRefGoogle ScholarPubMed
Haase, P, Cowen, DM, Knowles, JC & Cooper, EHEvaluation of dimethylhydrazine induced tumours in mice as a model system for colorectal cancer. Br J Cancer (1973) 28, 530–543.CrossRefGoogle Scholar
Hill, MJ, Drasar, BS, Hawksworth, G, Aries, V, Crowther, JS & Williams, REBacteria and aetiology of cancer of large bowel. Lancet (1971) 16, 95–100.CrossRefGoogle Scholar
Jang, M, Cai, L, Udeani, GO, et al. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science (1997) 275, 218–220.CrossRefGoogle ScholarPubMed
Jeandet, P, Douillet-Breuil, AC, Bessis, R, Debord, S, Sbaghi, M & Adrian, MPhytoalexins from the Vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. J Agric Food Chem (2002) 50, 2731–2741.CrossRefGoogle ScholarPubMed
Johansson, G, Holmen, A, Persson, L, Hogstedt, B, Wassen, C, Ottova, L & Gustafsson, JADietary influence on some proposed risk factors for colon cancer: faecal and urinary mutagenic activity and the activity of some intestinal bacterial enzymes. Cancer Detect Prev (1997) 21, 258–266.Google ScholarPubMed
Kawamori, T, Tanaka, T, Hara, A, Yamahara, J, Mori, H, Modifying effects of naturally occurring products on the development of colonic aberrant crypt foci induced by azoxymethane in F344 rats. Cancer Res (1995) 55 1277–1282.Google ScholarPubMed
Kimura, Y, Ohminami, H, Okuda, H, Baba, K, Kozawa, M, Arichi, S, Effects of stilbene components of roots of Polygonum ssp. on liver injury in peroxidized oil-fed rats. Planta Med (1983) 49 51–54.CrossRefGoogle ScholarPubMed
Kinouchi, T, Kataoka, K, Miyanishi, K, Akimoto, S, Ohnishi, y, Biological activities of the intestinal microflora in mice treated with antibiotics or untreated and the effects of the microflora on absorption and metabolic activation of orally administered glutathione conjugates of K-region epoxides of 1-nitropyrene. Carcinogenesis (1993) 14 869–874.CrossRefGoogle ScholarPubMed
Laqueur, GL, Spatz, M, Toxicology of cycasin.. Cancer Res (1968) 28 2262–2267.Google ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL, Randall, RJ, Protein measurement with the Folin phenol reagent. J Biol Chem (1951) 193 265–275.CrossRefGoogle ScholarPubMed
Manju, V, Nalini, NChemopreventive efficacy of ginger, a naturally occurring anticarcinogen during the initiation, postinitiation stages of 1,2 dimethylhydrazine-induced colon cancer. Clin Chim Acta (2005) 358 60–67.CrossRefGoogle Scholar
Miller, NJ, Rice-Evans, CA, Antioxidant activity of resveratrol in red wine. Clin Chem (1995) 41 1789.CrossRefGoogle ScholarPubMed
Morse, MA, Stoner, GD, Cancer chemoprevention: principles and prospects. Carcinogenesis (1993) 14 1737–1746.CrossRefGoogle ScholarPubMed
Nalini, N, Manju, V, Menon, VP, 2004) Effect of coconut cake on the bacterial enzyme activity in 1,2-dimethylhydrazine induced colon cancer. Clin Chim Acta (2004) 342 203–210.CrossRefGoogle ScholarPubMed
Nalini, N, Sabitha, K, Viswanathan, P, Menon, VP, Influence of spices on the bacterial (enzyme) activity in experimental colon cancer. J Ethnopharmacol (1998) 62 15–24.CrossRefGoogle Scholar
Nieuw Amerongen, AV, Bolscher, JG, Bloemena, E, Veerman, EC, Sulfomucins in the human body. Biol Chem (1998) 379 1–18.Google ScholarPubMed
Nonomura, S, Kanagawa, H & Makimoto, a, Chemical constituents of polygonaceous plants. I. Studies on the components of kojo-kon (Polygonum cuspidatum SIEB. ET ZUCC.). Yakugaku Zasshi (1963) 83 988–990.CrossRefGoogle Scholar
Reddy, BS, Engle, A, Simi, B, Goldman, M, Effect of dietary fiber on colonic bacterial enzymes and bile acids in relation to colon cancer. Gastroenterology (1992) 102 1475–1482.CrossRefGoogle ScholarPubMed
Reddy, BS, Hedges, AR, Laakso, K&Wynder, EL, Metabolic epidemiology of large bowel cancer. Cancer (1978) 42, 2832–2838.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Rembacken, BJ, Snelling, AM, Hawkey, PM, Chalmers, DM&Axon, AT, Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomized trial. Lancet (1999) 354, 635–639.CrossRefGoogle Scholar
Rhodes, JM, Gallimore, R, Elias, E& Kennedy, JF, Faecal sulphatase in health and in inflammatory bowel disease. Gut (1985) 26, 466–469.CrossRefGoogle ScholarPubMed
Riddell, RH, Dysplasia and cancer in ulcerative colitis: a soluble problem?. Scand J Gastroenterol (1984) 104, 137–149.Google ScholarPubMed
Rowland, IR, Mallett, AK& Wise, A, A comparison of the activity of five microbial enzymes in caecal content from rats, mice, and hamsters, and response to dietary pectin. Toxicol Appl Pharmacol (1983) 69, 143–148.CrossRefGoogle ScholarPubMed
Rowland, IR, Rumney, CJ, Coutts, JT & Lievense, L, Effect of Bifidobacterium longum and carcinogen-induced aberrant crypt foci in rats. Carcinogenesis (1998) 19, 281–285.CrossRefGoogle ScholarPubMed
Schneider, Y, Duranton, B, Gosse, F,Schleiffer, R,Seiler, N & Raul, FResveratrol inhibits intestinal tumourigenesis and modulates host-defense-related gene expression in an animal modelof human familial adenomatous polyposis. Nutr Cancer (2001) 39 102–107.CrossRefGoogle Scholar
Seregni, E, Botti, C, Massaron, S, Lombardo, C, Capobianco, A, Bogni, A & Bombardieri, EStructure, function and gene expression of epithelial mucins. Tumori (1997) 83 625–632.CrossRefGoogle ScholarPubMed
Shiau, SY & Chang, GWEffects of dietary fiber on faecal mucinase and b-glucuronidase activity in rats. J Nutr (1983) 113 138–144.CrossRefGoogle Scholar
Shiau, SY & Ong, YOEffects of cellulose, agar and their mixture on colonic mucin degradation in rats. J Nutr Sci Vitaminol (1992) 38 49–55.CrossRefGoogle ScholarPubMed
Shimotoyodome, A, Meguro, S, Hase, T, Tokimitsu, I & Sakata, TDecreased colonic mucus in rats with loperamide-induced constipation. Comp Biochem Physiol A Mol Integr Physiol (2000) 126 203–212.CrossRefGoogle ScholarPubMed
Simon, GL & Gorbach, SLIntestinal flora in health and disease. Gastroenterology (1984) 86 174–193.CrossRefGoogle ScholarPubMed
Sporn, MB & Suh, NChemoprevention of cancer. Carcinogenesis (2000) 21 525–530.CrossRefGoogle ScholarPubMed
Tajima, K, Hirose, K, Nakagawa, N,Kuroishi, T & Tominaga, SUrban-rural difference in the trend of colo-rectal cancer mortality with special reference to the subsites of colon cancer in Japan. Jpn J Cancer Res (1985) 76 717–728.Google Scholar
Tessitore, L, Davit, A, Sarotto, I & Caderni, GResveratrol depresses the growth of colorectal aberrant crypt foci by affecting bax and p21 CIP expression. Carcinogenesis (2000) 21 1619–1622.CrossRefGoogle ScholarPubMed
Thurnherr, N, Deschner, EE, Stonehill, EH & Lipkin, MInduction of adenocarcinomas of the colon in mice by weekly injections of 1,2-dimethylhydrazine. Cancer Res (1973) 33 940–945.Google Scholar
Wattenberg, LWChemoprevention of cancer. Cancer Res (1985) 45 1–8.Google ScholarPubMed
Young, GP & Le Leu, RKPreventing cancer: dietary lifestyle or clinical intervention?. Asia Pac J Clin Nutr (2002) 11 618–631.CrossRefGoogle ScholarPubMed