Predictive Markers and Cancer Prevention

You have full text access to this OnlineOpen article

Intake of beer inhibits azoxymethane-induced colonic carcinogenesis in male Fischer 344 rats

  1. Hajime Nozawa1,†,*,
  2. Aruto Yoshida1,
  3. Osamu Tajima2,
  4. Mikio Katayama2,
  5. Hiromi Sonobe2,
  6. Keiji Wakabayashi3,
  7. Keiji Kondo1

Article first published online: 21 OCT 2003

DOI: 10.1002/ijc.11541

Issue

International Journal of Cancer

International Journal of Cancer

Volume 108, Issue 3, pages 404–411, 20 January 2004

Additional Information

How to Cite

Nozawa, H., Yoshida, A., Tajima, O., Katayama, M., Sonobe, H., Wakabayashi, K. and Kondo, K. (2004), Intake of beer inhibits azoxymethane-induced colonic carcinogenesis in male Fischer 344 rats. Int. J. Cancer, 108: 404–411. doi: 10.1002/ijc.11541

Author Information

  1. 1

    Central Laboratories for Key Technology, Kirin Brewery Co., Ltd., Yokohama, Japan

  2. 2

    Research Center for Product Safety and Assessment, Kirin Brewery Co., Ltd., Gunma, Japan

  3. 3

    Cancer Prevention Division, National Cancer Center Research Institute, Tokyo, Japan

  1. †

    Fax: +81-45-788-4042

*Central Laboratories for Key Technology, Kirin Brewery Co., Ltd., 1-13-5 Fukuura, Kanazawa-ku, Yokohama 236-0004, Japan

Publication History

  1. Issue published online: 21 NOV 2003
  2. Article first published online: 21 OCT 2003
  3. Manuscript Accepted: 22 AUG 2003
  4. Manuscript Revised: 13 AUG 2003
  5. Manuscript Received: 14 MAR 2003

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (137K)

REFERENCES

  • 1
    Rimm EB, Giovannucci EL, Willett WC, Colditz GA, Ascherio A, Rosner B, Stampfer MJ. Prospective study of alcohol consumption and risk of coronary disease in men. Lancet 1991; 338: 464–8.
  • 2
    Tsugane S, Fahey MT, Sasaki S, Baba S. Alcohol consumption and all-cause and cancer mortality among middle-aged Japanese men: seven-year follow-up of the JPHC study Cohort I. Japan Public Health Center. Am J Epidemiol 1999; 150: 1201–7.
  • 3
    Riboli E, Cornee J, Macquart-Moulin G, Kaaks R, Casagrande C, Guyader M. Cancer and polyps of the colorectum and lifetime consumption of beer and other alcoholic beverages. Am J Epidemiol 1991; 134: 157–66.
  • 4
    Sharpe CR, Siemiatycki J, Rachet B. Effects of alcohol consumption on the risk of colorectal cancer among men by anatomical subsite (Canada). Cancer Causes Control 2002; 13: 483–91.
  • 5
    Sharpe CR, Siemiatycki J. Case-control study of alcohol consumption and prostate cancer risk in Montreal, Canada. Cancer Causes Control 2001; 12: 589–98.
  • 6
    La Vecchia C, Negri E, Franceschi S, D'Avanzo B. Moderate beer consumption and the risk of colorectal cancer. Nutr Cancer 1993; 19: 303–6.
  • 7
    Jain MG, Hislop GT, Howe GR, Burch JD, Ghadirian P. Alcohol and other beverage use and prostate cancer risk among Canadian men. Int J Cancer 1998; 78: 707–11.
    Direct Link:
  • 8
    Sesso HD, Paffenbarger RS, Jr., Lee IM. Alcohol consumption and risk of prostate cancer: The Harvard Alumni Health Study. Int J Epidemiol 2001; 30: 749–55.
  • 9
    Block G, Patterson B, Subar A. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr Cancer 1992; 18: 1–29.
  • 10
    Chen W, Sohn OS, Fiala ES, Weisburger JH. Effect of tea on the formation of DNA adducts by azoxymethane. Xenobiotica 1998; 28: 213–7.
  • 11
    Suaeyun R, Kinouchi T, Arimochi H, Vinitketkumnuen U, Ohnishi Y. Inhibitory effects of lemon grass (Cymbopogon citratus Stapf) on formation of azoxymethane-induced DNA adducts and aberrant crypt foci in the rat colon. Carcinogenesis 1997; 18: 949–55.
  • 12
    Weisburger JH, Rivenson A, Reinhardt J, Aliaga C, Braley J, Pittman B, Zang E. Effect of black tea on azoxymethane-induced colon cancer. Carcinogenesis 1998; 19: 229–32.
  • 13
    Tanaka T, Kohno H, Tsukio Y, Honjo S, Tanino M, Miyake M, Wada K. Citrus limonoids obacunone and limonin inhibit azoxymethane- induced colon carcinogenesis in rats. Biofactors 2000; 13: 213–8.
    Direct Link:
  • 14
    Kohno H, Tanaka T, Kawabata K, Hirose Y, Sugie S, Tsuda H, Mori H. Silymarin, a naturally occurring polyphenolic antioxidant flavonoid, inhibits azoxymethane-induced colon carcinogenesis in male F344 rats. Int J Cancer 2002; 101: 461–8.
    Direct Link:
  • 15
    Middleton E, Jr., Kandaswami C. Effects of flavonoids on immune and inflammatory cell functions. Biochem Pharmacol 1992; 43: 1167–79.
  • 16
    Ho CT, Chen Q, Shi H, Zhang KQ, Rosen RT. Antioxidative effect of polyphenol extract prepared from various Chinese teas. Prev Med 1992; 21: 520–5.
  • 17
    Shiraki M, Hara Y, Osawa T, Kumon H, Nakayama T, Kawakishi S. Antioxidative and antimutagenic effects of theaflavins from black tea. Mutat Res 1994; 323: 29–34.
  • 18
    Arimoto-Kobayashi S, Sugiyama C, Harada N, Takeuchi M, Takemura M, Hayatsu H. Inhibitory effects of beer and other alcoholic beverages on mutagenesis and DNA adduct formation induced by several carcinogens. J Agric Food Chem 1999; 47: 221–30.
  • 19
    Paper DH. Natural products as angiogenesis inhibitors. Planta Med 1998; 64(8): 686–95.
  • 20
    Singh NP, McCoy MT, Tice RR, Schneider EL. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 1988; 175: 184–91.
  • 21
    Sasaki YF, Tsuda S, Izumiyama F, Nishidate E. Detection of chemically induced DNA lesions in multiple mouse organs (liver, lung, spleen, kidney, and bone marrow) using the alkaline single cell gel electrophoresis (Comet) assay. Mutat Res 1997; 388: 33–44.
  • 22
    Kassie F, Rabot S, Uhl M, Huber W, Qin HM, Helma C, Schulte-Hermann R, Knasmuller S. Chemoprotective effects of garden cress (Lepidium sativum) and its constituents towards 2-amino-3-methyl-imidazo[4,5-f]quinoline (IQ)-induced genotoxic effects and colonic preneoplastic lesions. Carcinogenesis 2002; 23: 1155–61.
  • 23
    Guglielmi F, Luceri C, Giovannelli L, Dolara P, Lodovici M. Effect of 4-coumaric and 3,4-dihydroxybenzoic acid on oxidative DNA damage in rat colonic mucosa. Br J Nutr 2003; 89: 581–7.
  • 24
    Lazze MC, Pizzala R, Savio M, Stivala LA, Prosperi E, Bianchi L. Anthocyanins protect against DNA damage induced by tert-butyl-hydroperoxide in rat smooth muscle and hepatoma cells. Mutat Res 2003; 535: 103–15.
  • 25
    Bird RP. Observation and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: preliminary findings. Cancer Lett 1987; 37: 147–51.
  • 26
    Pretlow TP, Cheyer C, OTapos;Riordan MA. Aberrant crypt foci and colon tumors in F344 rats have similar increases in proliferative activity. Int J Cancer 1994; 56: 599–602.
    Direct Link:
  • 27
    Roncucci L, Stamp D, Medline A, Cullen JB, Bruce WR. Identification and quantification of aberrant crypt foci and microadenomas in the human colon. Hum Pathol 1991; 22: 287–94.
  • 28
    Olivo S, Wargovich MJ. Inhibition of aberrant crypt foci by chemopreventive agents. In Vivo 1998; 12: 159–66.
  • 29
    Wargovich MJ, Jimenez A, McKee K, Steele VE, Velasco M, Woods J, Price R, Gray K, Kelloff GJ. Efficacy of potential chemopreventive agents on rat colon aberrant crypt formation and progression. Carcinogenesis 2000; 21: 1149–55.
  • 30
    Nelson RL, Samelson SL. Neither dietary ethanol nor beer augments experimental colon carcinogenesis in rats. Dis Colon Rectum 1985; 28: 460–2.
  • 31
    Hamilton SR, Hyland J, McAvinchey D, Chaudhry Y, Hartka L, Kim HT, Cichon P, Floyd J, Turjman N, Kessie G, Nair PP, Dick J. Effects of chronic dietary beer and ethanol consumption on experimental colonic carcinogenesis by azoxymethane in rats. Cancer Res 1987; 47: 1551–9.
  • 32
    Madigan D MI, Smyth MR. Rapid determination of 4-vinyl guaiacol and ferulic acid in beers and worts by high-performance liquid chromatography. J Am Soc Brew Chem 1994; 52: 152–5.
  • 33
    Lapcik O HM, Hampl R, Wahala K, Adlercreutz H. Identification of isoflavonoids in beer. Steroids 1998; 63: 14–20.
  • 34
    Madigan D MI, Smyth MR. Determination of proanthocyanidins and catechins in beer and barley by high-performance liquid chromatography with dual-electrode electrochemical detection. Analyst 1994; 119: 863–8.
  • 35
    Whittle N EH, Bartley J. Identification of the polyphenols in barley and beer by HPLC/MS and HPLC/Electrochemical Detection. J. Inst. Brew. 1999; 105: 89–99.
  • 36
    Ghiselli A, Natella F, Guidi A, Montanari L, Fantozzi P, Scaccini C. Beer increases plasma antioxidant capacity in humans 2000; 11: 76–80.
  • 37
    Miranda CL, Yang YH, Henderson MC, Stevens JF, Santana-Rios G, Deinzer ML, Buhler DR. Prenylflavonoids from hops inhibit the metabolic activation of the carcinogenic heterocyclic amine 2-amino-3-methylimidazo[4, 5-f]quinoline, mediated by cDNA-expressed human CYP1A2. Drug Metab Dispos 2000; 28: 1297–302.
  • 38
    Henderson MC, Miranda CL, Stevens JF, Deinzer ML, Buhler DR. In vitro inhibition of human P450 enzymes by prenylated flavonoids from hops, Humulus lupulus. Xenobiotica 2000; 30: 235–51.
  • 39
    Miranda CL, Stevens JF, Helmrich A, Henderson MC, Rodriguez RJ, Yang YH, Deinzer ML, Barnes DW, Buhler DR. Antiproliferative and cytotoxic effects of prenylated flavonoids from hops (Humulus lupulus) in human cancer cell lines. Food Chem Toxicol 1999; 37: 271–85.
  • 40
    Yasukawa K, Takeuchi M, Takido M. Humulon, a bitter in the hop, inhibits tumor promotion by 12-O-tetradecanoylphorbol-13-acetate in two-stage carcinogenesis in mouse skin. Oncology 1995; 52: 156–8.
  • 41
    Shimamura M, Hazato T, Ashino H, Yamamoto Y, Iwasaki E, Tobe H, Yamamoto K, Yamamoto S. Inhibition of angiogenesis by humulone, a bitter acid from beer hop. Biochem Biophys Res Commun 2001; 289: 220–4.
  • 42
    Yamamoto K, Wang J, Yamamoto S, Tobe H. Suppression of cyclooxygenase-2 gene transcription by humulon of beer hop extract studied with reference to glucocorticoid. FEBS Lett 2000; 465: 103–6.
  • 43
    Zhao F, Nozawa H, Daikonnya A, Kondo K, Kitanaka S. Inhibitors of Nitric Oxide Production from Hops (Humulus lupulus L.). Biol Pharm Bull 2003; 26: 61–5.
  • 44
    Pool-Zobel BL, Bertram B, Knoll M, Lambertz R, Neudecker C, Schillinger U, Schmezer P, Holzapfel WH. Antigenotoxic properties of lactic acid bacteria in vivo in the gastrointestinal tract of rats. Nutr Cancer 1993; 20: 271–81.
  • 45
    Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 2000; 35: 206–21.
    Direct Link:
  • 46
    Ward JM. Morphogenesis of chemically induced neoplasms of the colon and small intestine in rats. Lab Invest 1974; 30: 505–13.
  • 47
    Hong MY, Lupton JR, Morris JS, Wang N, Carroll RJ, Davidson LA, Elder RH, Chapkin RS. Dietary fish oil reduces O6-methylguanine DNA adduct levels in rat colon in part by increasing apoptosis during tumor initiation. Cancer Epidemiol Biomarkers Prev 2000; 9: 819–26.
  • 48
    Mori H, Kawabata K, Yoshimi N, Tanaka T, Murakami T, Okada T, Murai H. Chemopreventive effects of ferulic acid on oral and rice germ on large bowel carcinogenesis. Anticancer Res 1999; 19: 3775–8.
  • 49
    Kawabata K, Yamamoto T, Hara A, Shimizu M, Yamada Y, Matsunaga K, Tanaka T, Mori H. Modifying effects of ferulic acid on azoxymethane-induced colon carcinogenesis in F344 rats. Cancer Lett 2000; 157: 15–21.
  • 50
    Han BS, Park CB, Takasuka N, Naito A, Sekine K, Nomura E, Taniguchi H, Tsuno T, Tsuda H. A ferulic acid derivative, ethyl 3-(4′-geranyloxy-3-methoxyphenyl)-2-propenoate, as a new candidate chemopreventive agent for colon carcinogenesis in the rat. Jpn J Cancer Res 2001; 92: 404–9.
  • 51
    Woffenden HM, Ames JM, Chandra S, Anese M, Nicoli MC. Effect of kilning on the antioxidant and pro-oxidant activities of pale malts. J Agric Food Chem 2002; 50: 4925–33.
  • 52
    Pereira MA. Prevention of colon cancer and modulation of aberrant crypt foci, cell proliferation, and apoptosis by retinoids and NSAIDs. Adv Exp Med Biol 1999; 470: 55–63.
  • 53
    Li H, Kramer PM, Lubet RA, Steele VE, Kelloff GJ, Pereira MA. Termination of piroxicam treatment and the occurrence of azoxymethane-induced colon cancer in rats. Cancer Lett 1999; 147: 187–93.
  • 54
    Yoshimi N, Shimizu M, Matsunaga K, Yamada Y, Fujii K, Hara A, Mori H. Chemopreventive effect of N-(2-cyclohexyloxy-4-nitrophenyl)methane sulfonamide (NS-398), a selective cyclooxygenase-2 inhibitor, in rat colon carcinogenesis induced by azoxymethane. Jpn J Cancer Res 1999; 90: 406–12.
  • 55
    Shpitz B, Bomstein Y, Kariv N, Shalev M, Buklan G, Bernheim J. Chemopreventive effect of aspirin on growth of aberrant crypt foci in rats. Int J Colorectal Dis 1998; 13: 169–72.
  • 56
    Sohn OS, Ishizaki H, Yang CS, Fiala ES. Metabolism of azoxymethane, methylazoxymethanol and N-nitrosodimethylamine by cytochrome P450IIE1. Carcinogenesis 1991; 12: 127–31.
  • 57
    Sohn OS, Fiala ES, Requeijo SP, Weisburger JH, Gonzalez FJ. Differential effects of CYP2E1 status on the metabolic activation of the colon carcinogens azoxymethane and methylazoxymethanol. Cancer Res 2001; 61: 8435–40.
  • 58
    Lieber CS. Biochemical and molecular basis of alcohol-induced injury to liver and other tissues. N Engl J Med 1988; 319: 1639–50.
  • 59
    Seitz HK, Czygan P, Waldherr R, Veith S, Raedsch R, Kassmodel H, Kommerell B. Enhancement of 1,2-dimethylhydrazine-induced rectal carcinogenesis following chronic ethanol consumption in the rat. Gastroenterology 1984; 86: 886–91.
  • 60
    Adolph E. Quantitative relations in the physiological constitutions of mammals. Science 1949; 109: 579–85.
View Full Article (HTML) Get PDF (137K)