Inhibitory effect of yogurt on aberrant crypt foci formation in the rat colon and colorectal tumorigenesis in RasH2 mice

Experimental Animals

Volumn 59, Issue 4, 2010, Pages 487-494

  Narushima, Seiko ^a   Sakata, Tadashi ^b   Hioki, Kyoji ^c   Itoh, Toshio ^c   Nomura, Tatsuji ^c   Itoh, Kikuji ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b MEIJI DAIRIES CORPORATION   (Japan)

^c CENTRAL INSTITUTE FOR EXPERIMENTAL ANIMALS   (Japan)

Author keywords

Aberrant crypt foci; Colon tumor; PHIP; Rash2 mouse; Yogurt

Indexed keywords

RAS PROTEIN; YOGHURT; 2-AMINO-1-METHYL-6-PHENYLIMIDAZO(4,5-B)PYRIDINE; ANTINEOPLASTIC AGENT; CARCINOGEN; IMIDAZOLE DERIVATIVE; RRAS PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; COLON CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; DIET SUPPLEMENTATION; FEMALE; FUNCTIONAL FOOD; INTESTINE CRYPT; LACTOBACILLUS DELBRUECKII; MALE; MILK; MOUSE; NONHUMAN; RAT; STREPTOCOCCUS THERMOPHILUS; TRANSGENIC MOUSE; TUMOR VOLUME; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CHEMICALLY INDUCED; COLON; COLORECTAL NEOPLASMS; DISEASE MODEL; DRUG EFFECTS; FISCHER 344 RAT; GENETICS; HUMAN; INTESTINE MUCOSA; ONCOGENE RAS; PATHOLOGY; PRECANCEROUS CONDITIONS; RECTUM; TOXICITY;

LACTOBACILLUS DELBRUECKII SUBSP. BULGARICUS; MUS; MUS MUSCULUS; RATTUS; STREPTOCOCCUS THERMOPHILUS;

ANIMALS; ANTICARCINOGENIC AGENTS; CARCINOGENS; COLON; COLORECTAL NEOPLASMS; DISEASE MODELS, ANIMAL; FEMALE; GENES, RAS; HUMANS; IMIDAZOLES; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; PRECANCEROUS CONDITIONS; RAS PROTEINS; RATS; RATS, INBRED F344; RECTUM; YOGURT;

EID: 77957243184     PISSN: 13411357     EISSN: None     Source Type: Journal    
DOI: 10.1538/expanim.59.487     Document Type: Article

References (44)

1. Adolfsson, O., Meydani, S.N., and Russell, R.M. 2004. Yogurt and gut function. Am. J. Clin. Nutr. 80: 245-256.
2. Bird, R.P. 1987. Observation and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: preliminary findings. Cancer Lett. 37: 147-151.
3. Bird, R.P. 1995. Role of aberrant crypt foci in understanding the pathogenesis of colon cancer. Cancer Lett. 93: 55-71.
4. Bodana, A.R. and Rao, D.R. 1990. Antimutagenic activity of milk fermented by Streptococcus thermophilus and Lactobacillus bulgaricus. J. Dairy Sci. 73: 3379-3384.
5. Bolognani, F., Rumney, C.J., Pool-Zobel, B.L., and Rowland, I.R. 2001. Effect of lactobacilli, bifidobacteria and inulin on the formation of aberrant crypt foci in rats. Eur. J. Nutr. 40: 293-300.
6. Buonarati, M.H., Turteltaub, K.W., Shen, N.H., and Felton, J.S. 1990. Role of sulfation and acetylation in the activation of 2-hydroxyamino-1-methyl-6-phenylimidazo[4,5-b] pyridine to intermediates which bind DNA. Mutat Res. 245: 185-190.
7. de Moreno, de Leblanc, A. and Perdigon, G. 2004. Yogurt feeding inhibits promotion and progression of experimental colorectal cancer. Med. Sci. Monit. 10: BR96-104.
8. del Campo, R., Bravo, D., Canton, R., Ruiz-Garbajosa, P., Garcia-Albiach, R., Montesi-Libois, A., Yuste, F.J., Abraira, V., and Baquero, F. 2005. Scarce evidence of yogurt lactic acid bacteria in human feces after daily yogurt consumption by healthy volunteers. Appl. Environ. Microbiol. 71: 547-549.
9. Elli, M., Callegari, M.L., Ferrari, S., Bessi, E., Cattivelli, D., Soldi, S., Morelli, L., Goupil Feuillerat, N., and Antoine, J.M. 2006. Survival of yogurt bacteria in the human gut. Appl. Environ. Microbiol. 72: 5113-5117.
10. Friesen, M.D., Garren, L., Bereziat, J.C., Kadlubar, F., and Lin, D. 1993. Gas chromatography-mass spectrometry analysis of 2-amino-1-methyl-6-phenylimidazo[4,5-b] pyridine in urine and feces. Environ. Health Perspect. 99: 179-181.
11. Goldin, B.R. and Gorbach, S.L. 1980. Effect of Lactobacillus acidophilus dietary supplements on 1,2-dimethylhydrazine dihydrochloride-induced intestinal cancer in rats. J. Natl. Cancer. Inst. 64: 263-265.
12. Hosono, A., Kashina, T., and Kada, T. 1986. Antimutagenic properties of lactic acid-cultured milk on chemical and fecal mutagens. J. Dairy Sci. 69: 2237-2242.
13. Ito, N., Hasegawa, R., Sano, M., Tamano, S., Esumi, H., Takayama, S., and Sugimura, T. 1991. A new colon and mammary carcinogen in cooked food, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Carcinogenesis 12: 1503-1506.
14. Kaderlik, K.R., Minchin, R.F., Mulder, G.J., Ilett, K.F., Daugaard-Jenson, M., Teitel, C.H., and Kadlubar, F.F. 1994. Metabolic activation pathway for the formation of DNA adducts of the carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in rat extrahepatic tissues. Carcinogenesis 15: 1703-1709.
15. Kato, I., Kobayashi, S., Yokokura, T., and Mutai, M. 1981. Antitumor activity of Lactobacillus casei in mice. Gann 72: 517-523.
16. Kohwi, Y., Imai, K., Tamura, Z., and Hashimoto, Y. 1978. Antitumor effect of Bifidobacterium infantis in mice. Gann 69: 613-618.
17. Layton, D.W., Bogen, K.T., Knize, M.G., Hatch, F.T., Johnson, V.M., and Felton, J.S. 1995. Cancer risk of heterocyclic amines in cooked foods: an analysis and implications for research. Carcinogenesis 16: 39-52.
18. Lin, M.Y. and Yen, C.L. 1999. Reactive oxygen species and lipid peroxidation product-scavenging ability of yogurt organisms. J. Dairy Sci. 82: 1629-1634.
19. MacDonald, J., French, J.E., Gerson, R.J., Goodman, J., Inoue, T., Jacobs, A., Kasper, P., Keller, D., Lavin, A., Long, G., McCullough, B., Sistare, F.D., Storer, R., and van der Laan, J.W. 2004. The utility of genetically modified mouse assays for identifying human carcinogens: a basic understanding and path forward. The Alternatives to Carcinogenicity Testing Committee ILSI HESI. Toxicol. Sci. 77: 188-194.
20. Machida, K., Urano, K., Yoshimura, M., Tsutsumi, H., Nomura, T., and Usui, T. 2008. Carcinogenic comparative study on rasH2 mice produced by two breeding facilities. J. Toxicol. Sci. 33: 493-501.
21. Mater, D.D., Bretigny, L., Firmesse, O., Flores, M.J., Mogenet, A., Bresson, J.L., and Corthier, G. 2005. Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus survive gastrointestinal transit of healthy volunteers consuming yogurt. FEMS Microbiol. Lett. 250: 185-187.
22. Metchnikoff, E. 2004. The Prolongation of Life: Optimistic Studies (Mitchell, P.B. trans.), Springer, New York.
23. Meydani, S.N. and Ha, W.K. 2000. Immunologic effects of yogurt. Am. J. Clin. Nutr. 71: 861-872.
24. Miyamoto, S., Yasui, Y., Kim, M., Sugie, S., Murakami, A., Ishigamori-Suzuki, R., and Tanaka, T. 2008. A novel rasH2 mouse carcinogenesis model that is highly susceptible to 4-NQO-induced tongue and esophageal carcinogenesis is useful for preclinical chemoprevention studies. Carcinogenesis 29: 418-426.
25. Nagafuchi, S., Takahashi, T., Yajima, T., Kuwata, T., Hirayama, K., and Itoh, K. 1999. Strain dependency of the immunopotentiating activity of Lactobacillus delbrueckii subsp. bulgaricus. Biosci. Biotechnol. Biochem. 63: 474-479.
26. Narushima, S., Itoh, K., Mitsuoka, T., Nakayama, H., Itoh, T., Hioki, K., and Nomura, T. 1998. Effect of mouse intestinal bacteria on incidence of colorectal tumors induced by 1,2-dimethylhydrazine injection in gnotobiotic transgenic mice harboring human prototype c-Ha-ras genes. Exp. Anim. 47: 111-117.
27. Nozawa, H., Tazumi, K., Sato, K., Yoshida, A., Takata, J., Arimoto-Kobayashi, S., and Kondo, K. 2004. Inhibitory effects of beer on heterocyclic amine-induced mutagenesis and PhIP-induced aberrant crypt foci in rat colon. Mutat. Res. 559: 177-187.
28. Oberley, T.D. 2002. Oxidative damage and cancer. Am. J. Pathol. 160: 403-408.
29. Ochiai, M., Ushigome, M., Fujiwara, K., Ubagai, T., Kawamori, T., Sugimura, T., Nagao, M., and Nakagama, H. 2003. Characterization of dysplastic aberrant crypt foci in the rat colon induced by 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine. Am. J. Pathol. 163: 1607-1614.
30. Ohno, K., Narushima, S., Takeuchi, S., Itoh, K., Mitsuoka, T., Nakayama, H., Itoh, T., Hioki, K., and Nomura, T. 2000. Inhibitory effect of apple pectin and culture condensate of Bifidobacterium longum on colorectal tumors induced by 1,2-dimethylhydrazine in transgenic mice harboring human prototype c-Ha-ras genes. Exp. Anim. 49: 305-307.
31. Pedrosa, M.C., Golner, B.B., Goldin, B.R., Barakat, S., Dallal, G.E., and Russell, R.M. 1995. Survival of yogurt-containing organisms and Lactobacillus gasseri (ADH) and their effect on bacterial enzyme activity in the gastrointestinal tract of healthy and hypochlorhydric elderly subjects. Am. J. Clin. Nutr. 61: 353-359.
32. Rafter, J.J. 1995. The role of lactic acid bacteria in colon cancer prevention. Scand. J. Gastroenterol. 30: 497-502.
33. Reeves, P.G., Nielsen, F.H., and Fahey, G.C. Jr. 1993. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123: 1939-1951.
34. Saitoh, A., Kimura, M., Takahashi, R., Yokoyama, M., Nomura, T., Izawa, M., Sekiya, T., Nishimura, S., and Katsuki, M. 1990. Most tumors in transgenic mice with human c-Ha-ras gene contained somatically activated transgenes. Oncogene 5: 1195-1200.
35. Schut, H.A. and Herzog, C.R. 1992. Formation of DNA adducts of2-amino-1-methyl-6-phenylimidazo[4,5-b] pyridine (PhIP) in male Fischer-344 rats. Cancer Lett. 67: 117-124.
36. Shackelford, L.A., Rao, D.R., Chawan, C.B., and Pulusani, S.R. 1983. Effect of feeding fermented milk on the incidence of chemically induced colon tumors in rats. Nutr. Cancer 5: 159-164.
37. Singh, J., Rivenson, A., Tomita, M., Shimamura, S., Ishibashi, N., and Reddy, B.S. 1997. Bifidobacterium longum, a lactic acid-producing intestinal bacterium inhibits colon cancer and modulates the intermediate biomarkers of colon carcinogenesis. Carcinogenesis 18: 833-841.
38. Takahashi, S., Ogawa, K., Ohshima, H., Esumi, H., Ito, N., and Sugimura, T. 1991. Induction of aberrant crypt foci in the large intestine of F344 rats by oral administration of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine. Jpn. J. Cancer Res. 82: 135-137.
39. Tavan, E., Cayuela, C., Antoine, J.M., Trugnan, G., Chaugier, C., and Cassand, P. 2002. Effects of dairy products on heterocyclic aromatic amine-induced rat colon carcinogenesis. Carcinogenesis 23: 477-483.
40. Terahara, M., Nishide, S., and Kaneko, T. 2000. Preventive effect of Lactobacillus delbrueckii subsp. Bulgaricus on the oxidation of LDL. Biosci. Biotechnol. Biochem.64: 1868-1873.
41. Weisburger, J.H., Braley, J., Reinhardt, J., Aliaga, C., Rivenson, A., Hard, G.C., Zhang, X.M., Takahashi, M., Esumi, H., and Sugimura, T. 1994. The role of fat and calcium in the production of foci of aberrant crypts in the colon of rats fed 2-amino-1-methyl-6-phenylimidazo[4,5- b]-pyridine. Environ. Health Perspect. 102: 53-55.
42. Wollowski, I., Ji, S.T., Bakalinsky, A.T., Neudecker, C., and Pool-Zobel, B.L. 1999. Bacteria used for the production of yogurt inactivate carcinogens and prevent DNA damage in the colon of rats. J. Nutr. 129: 77-82.
43. Yamamoto, S., Mitsumori, K., Kodama, Y., Matsunuma, N., Manabe, S., Okamiya, H., Suzuki, H., Fukuda, T., Sakamaki, Y., Sunaga, M., Nomura, G., Hioki, K., Wakana, S., Nomura, T., and Hayashi, Y. 1996. Rapid induction of more malignant tumors by various genotoxic carcinogens in transgenic mice harboring a human prototype c-Ha-ras gene than in control non-transgenic mice. Carcinogenesis 17: 2455-2461.
44. Zsivkovits, M., Fekadu, K., Sontag, G., Nabinger, U., Huber, W.W., Kundi, M., Chakraborty, A., Foissy, H., and Knasmuller, S. 2003. Prevention of heterocyclic amine- induced DNA damage in colon and liver of rats by different lactobacillus strains. Carcinogenesis 24: 1913-1918.