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Plasma enterolactone or intestinal Bifidobacterium levels do not explain adenoma formation in multiple intestinal neoplasia (Min) mice fed with two different types of rye-bran fractions

Published online by Cambridge University Press:  07 June 2007

S. Oikarinen ,
S. Heinonen ,
S. Karppinen ,
J. Mättö ,
H. Adlercreutz ,
K. Poutanen  and
M. Mutanen
S. Oikarinen*
Affiliation:
Department of Applied Chemistry and Microbiology, Division of Nutrition, PO Box 27, FIN-00014 University of Helsinki, Finland
S. Heinonen
Affiliation:
Institute for Preventive Medicine, Nutrition and Cancer, Folkhälsan Research Centre and Division of Clinical Chemistry, FIN-00014 University of Helsinki, Finland
S. Karppinen
Affiliation:
VTT Biotechnology, PO Box 1500, FIN-02044 VTT, Finland
J. Mättö
Affiliation:
VTT Biotechnology, PO Box 1500, FIN-02044 VTT, Finland
H. Adlercreutz
Affiliation:
Institute for Preventive Medicine, Nutrition and Cancer, Folkhälsan Research Centre and Division of Clinical Chemistry, FIN-00014 University of Helsinki, Finland
K. Poutanen
Affiliation:
VTT Biotechnology, PO Box 1500, FIN-02044 VTT, Finland
M. Mutanen
Affiliation:
Department of Applied Chemistry and Microbiology, Division of Nutrition, PO Box 27, FIN-00014 University of Helsinki, Finland
*
*Corresponding author: Dr Seija Oikarinen, fax +358 9 191 58269, email Seija.Oikarinen@Helsinki.fi
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Abstract

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The study was designed to evaluate whether two types of rye-bran fractions result in distinct bifidogenic effect or enterolactone production in multiple intestinal neoplasia (Min) mice and whether these parameters are associated with intestinal tumorigenesis in this animal model. The experimental diets were a non-fibre diet (control), a rye-bran diet, and diets containing either the soluble extract or the insoluble fraction prepared from rye bran. The main result on adenoma formation in these experiments was the observation that the soluble extract increased number (P=0·012) and size (P=0·008) of adenomas in the distal small intestine when compared with the non-fibre group. All rye-supplemented diets supported similarly the in vivo growth of Bifidobacterium (108–109 colony forming units/g) in Min mice, whereas the non-fibre diet lowered intestinal Bifidobacterium below the level of detection. The results show that water solubility does not affect the bifidogenicity of rye bran. Mean plasma enterolactone concentration was highest in the rye-bran group (30·0 nmol/l; P=0·002), which along with the soluble-extract group (16·2 nmol/l; P=0·024) differed significantly from the non-fibre diet group (7·5nmol/l). Thus, the mice fed with the rye bran were the best enterolactone producers. In conclusion, rye bran and rye fractions influence adenoma formation in Min mice to a varying degree but plasma enterolactone levels or the production of bifidogenic bacteria do not mediate the effect.

Keywords

Min miceRye branBifidobacteriumLignansEnterolactone
Type
Research Article
Information
British Journal of Nutrition , Volume 90 , Issue 1 , July 2003 , pp. 119 - 125
Copyright
Copyright © The Nutrition Society 2003

References

Adlercreutz, H (2002) Phyto-oestrogens and cancer. The Lancet Oncol 3, 32–41.CrossRefGoogle ScholarPubMed
Adlercreutz, H, Wang, GJ & Lapcík, O, et al. (1998) Time-resolved fluoroimmunoassay for plasma enterolactone. Anal Biochem 265, 208–215.CrossRefGoogle ScholarPubMed
Arimochi, H, Kinouchi, T, Kataoka, K, Kuwahara, T & Ohnishi, Y (1997) Effect of intestinal bacteria on formation of azoxymethane-induced aberrant crypt foci in the rat colon. Biochem and Biophys Res Commun 238, 753–757.CrossRefGoogle ScholarPubMed
Asp, N-G, Johansson, C-G, Hallmer, H & Siljerström, M (1983) Rapid enzymatic assay of insoluble and soluble dietary fibre. J Agric Food Chem 31, 476–482.CrossRefGoogle Scholar
Beerens, H (1990) An elective and selective isolation medium for Bifidobacterium spp. Lett Appl Microbiol 11, 155–157.CrossRefGoogle Scholar
Bingham, SA, Atkinson, C, Liggins, J, Bluck, L & Coward, A (1998) Phyto-oestrogens: where are we now?. Br J Nutr 79, 393–406.CrossRefGoogle ScholarPubMed
Challa, A, Rao, DR, Chawan, CB & Chackelford, L (1997) Bifidobacterium longum and lactulose suppress azoxymathane-induced colonic aberrant crypt foci in rats. Carcinogenesis 18, 517–521.CrossRefGoogle ScholarPubMed
Crittenden, R, Karppinen, S, Ojanen, S, et al. (2002) In vitro fermentation of cereal dietary fibre carbohydrates by probiotic and intestinal bacteria. J Sci Food Agric 82, 781–789.CrossRefGoogle Scholar
Davies, MJ, Bowey, A, Adlercreutz, HA, Rowland, IR & Rumsby, PC (1999) Effects of soy or rye supplementation of high-fat diets on colon tumour development in azoxymethane-treated rats. Carcinogenesis 20, 927–931.CrossRefGoogle ScholarPubMed
Dietrich, WF, Lander, ES & Smith, JS, et al. (1993) Genetic identification of Mom-1, a major modifier locus affecting Min-induced intestinal neoplasia in the mouse. Cell 75, 631–639.CrossRefGoogle Scholar
Douglas, SA (1981) A rapid method for the determination of pentosans in wheat flour. Food Chem 7, 139–145.CrossRefGoogle Scholar
Ferguson, LR, Chavan, RR & Harris, PJ (2001) Changing concepts of dietary fiber: implications for carcinogenesis. Nutr Cancer 39, 155–169.CrossRefGoogle ScholarPubMed
Good, CK, Lasko, CM, Adam, J & Bird, RP (1998) Diverse effect of fish oil on the growth of aberrant crypt foci and tumor multiplicity in F344 rats. Nutr Cancer 31, 204–211.CrossRefGoogle ScholarPubMed
Hardman, WE, Cameron, IL, Heitman, DW & Contreras, E (1991) Demonstration of the need for end point validation of putative biomarker - failure of aberrant crypt foci to predict colon cancer incidence. Cancer Res 5, 6388–6392.Google Scholar
Heinonen, S, Nurmi, T & Liukkonen, K, et al. (2001) In vitro metabolism of plant lignans: New precursors of mammalian lignans enterolactone and enterodiol. J Agric Food Chem 49, 3178–3186.CrossRefGoogle ScholarPubMed
Jacobs, LR & Lupton, JR (1986) Relationship between colonic luminal pH, cell proliferation and colon carcinogenesis in 1,2-dimethylhydrazine treated rats fed high fibre diets. Cancer Res 46, 1727–1734.Google Scholar
Jenab, M & Thompson, LU (1996) The influence of flaxseed and lignans on colon carcinogenesis and β-glucuronidase activity. Carcinogenesis 17, 1343–1348.CrossRefGoogle ScholarPubMed
Karppinen, S, Kiiliäinen, K, Liukkonen, K, Forssell, P & Poutanen, K (2001) Extraction and in vitro fermentation of rye bran fractions. J Cereal Sci 34, 269–278.CrossRefGoogle Scholar
Karppinen, S, Myllymäki, O, Forssell, P & Poutanen, K (2003) Fructan content of rye and rye products. Cereal Chem 80, 168–171.CrossRefGoogle Scholar
Kitts, DD, Yan, YV, Wijewickreme, AN & Thompson, LU (1999) Antioxidant activity of the flaxseed lignan secoisolaricirecinol diglycoside and its mammalian lignan metabolites enterodiol and enterolactone. Mol Cell Biochem 202, 91–100.CrossRefGoogle Scholar
McIntyre, A, Gibson, PR & Young, GP (1993) Butyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut 34, 386–391.CrossRefGoogle ScholarPubMed
Mazur, W (1998) Phytoestrogen content in foods. Baillieres Clin Endocrinol Metab 12, 729–742.CrossRefGoogle ScholarPubMed
Mazur, W, Fotsis, T, Wähälä, K, Ojala, S, Salakka, A & Adlercreutz, H (1996) Isotope dilution gas chromatographic-mass spectrometric method for the determination of isoflavonoids, coumesterol and lignans in food samples. Anal Biochem 223, 169–180.CrossRefGoogle Scholar
Moser, AR, Pitot, HC & Dove, WF (1990) A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 247, 322–324.CrossRefGoogle ScholarPubMed
Mutanen, M, Pajari, A-M & Oikarinen, SI (2000) Beef induces and rye bran prevents formation of intestinal polyps in APCMin mice: relation to β-catenin and PKC-isoforms. Carcinogenesis 21, 1167–1173.CrossRefGoogle Scholar
Oikarinen, SI, Pajari, A-M & Mutanen, M (2000) Chemopreventive activity of crude hydroxymatairesinol (HMR) extract in ApcMin mice. Cancer Lett 161, 253–258.CrossRefGoogle Scholar
Onoue, M, Kado, S, Sakaitani, Y, Uchida, K & Morotomi, M (1997) Specific species of intestinal bacteria influence the induction of aberrant crypt foci by 1,2-dimethylhydrazine in rats. Cancer Lett 113, 179–186.CrossRefGoogle ScholarPubMed
Pierre, F, Perrin, P, Bassonga, E, Bornet, F, Meflah, K & Menanteau, J (1999) T cell status influences colon tumor occurrence in Min mice fed short chain fructo-oligosaccharides as a diet supplement. Carcinogenesis 20, 1953–1956.CrossRefGoogle Scholar
Pierre, F, Perrin, P, Hamp, M, Bornet, F, Meflah, K & Menanteau, J (1997) Short-chain fructo-oligosaccharides reduce the occurrence of colon tumours and develop gut-associated lymphoid tissue in Min mice. Cancer Res 57, 225–228.Google ScholarPubMed
Reddy, BS, Hamid, R & Rao, C (1997) Effect of dietary oligofructose and inulin on colonic preneoplastic aberrant crypt foci inhibition. Carcinogenesis 18, 1371–1374.CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FH & Fahey, GC Jr (1993) AIN-93 purified diets for laboratory rodents: Final report of the American Institute of Nutrition Ad Hoc Committee on the reformulation of the AIN-76A rodent diet. J Nutr 123, 1939–1951.CrossRefGoogle Scholar
Rowland, IR, Rumney, C, Coutts, JT & Lievense, LC (1998) Effect of Bifidobacterium longum and inulin on gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats. Carcinogenesis 19, 281–285.CrossRefGoogle ScholarPubMed
Saarinen, NM, Huovinen, R & Wärri, A, et al. (2001) Uptake and metabolism of hydoxymatairesinol in relation to its anticarcinogenicity in DMBA-induced rat mammary carcinoma model. Nutr Cancer 41, 82–90.CrossRefGoogle ScholarPubMed
Saarinen, NM, Wärri, A & Mäkelä, SI (2000) Hydroxymatairesinol, a novel enterolactone precursor with antitumor properties from coniferous tree (Picea abies). Nutr Cancer 36, 207–216.CrossRefGoogle ScholarPubMed
Singh, J, Rivenson, A & Tomita, M, et al. (1997) Bifidobacterium longum, a lactic acid-producing intestinal bacterium inhibits colon cancer and modulates the intermediate biomarkers of colon carcinogenesis. Carcinogenesis 18, 833–841.CrossRefGoogle ScholarPubMed
Stumpf, K, Uehara, M, Nurmi, T & Adlercreutz, H (2000) Changes in the time-resolved fluoroimmunoassay for plasma enterolactone. Anal Biochem 284, 153–157.CrossRefGoogle ScholarPubMed
Tannock, GW (1995) In Human Microflora. London: Chapman & Hall.Google Scholar
Thompson, LU, Seidl, MM, Richard, SE, Orcheson, LJ & Fong, HH (1996) Antitumorigenic effect of a mammalian lignan precursor from flaxseed. Nutr Cancer 26, 159–165.CrossRefGoogle ScholarPubMed
Yamada, Y, Hata, K & Hirose, Y, et al. (2002) Microadenomatous lesions involving loss of Apc heterozygosity in the colon of adult ApcMin/+ mice. Cancer Res 62, 6367–6370.Google Scholar
Zoran, DL, Turner, ND, Taddeo, SS, Chapkin, RS & Lupton, JR (1997) Wheat bran diet reduces tumor incidence in a rat model of colon cancer independent of effects on distal luminal butyrate concentrations. J Nutr 127, 2217–2225.CrossRefGoogle Scholar