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Proliferative effect of whey from cows’ milk varying in phyto-oestrogens in human breast and prostate cancer cells

Published online by Cambridge University Press:  27 January 2012

Tina S. Nielsen*
Affiliation:
Department of Animal Science, Faculty of Science and Technology, Aarhus University, Blichers Allé 20, P.O. Box 50, DK-8830 Tjele, Denmark
Annika Höjer
Affiliation:
Swedish University of Agricultural Sciences, Department of Agricultural Research for Northern Sweden, SE-901 83 Umeå, Sweden
Anne-Maj Gustavsson
Affiliation:
Swedish University of Agricultural Sciences, Department of Agricultural Research for Northern Sweden, SE-901 83 Umeå, Sweden
Jens Hansen-Møller
Affiliation:
Department of Animal Science, Faculty of Science and Technology, Aarhus University, Blichers Allé 20, P.O. Box 50, DK-8830 Tjele, Denmark
Stig Purup
Affiliation:
Department of Animal Science, Faculty of Science and Technology, Aarhus University, Blichers Allé 20, P.O. Box 50, DK-8830 Tjele, Denmark
*
*For correspondence; e-mail: [email protected]

Abstract

Intake of dietary phyto-oestrogens has received a great deal of attention owing to their potential influence on hormone-sensitive cancers such as breast and prostate cancer. Cows’ milk contains phyto-oestrogens and the content varies according to the composition of the feed and the type and amount of legumes used. In this study we evaluated the proliferative effect of milk (whey) with different phyto-oestrogen content in human breast (MCF-7) and prostate cancer cells (PC-3). Milk was obtained from cows fed either a birdsfoot trefoil-timothy silage based ration (B1) or two different red clover silage based diets (R1 and R2) resulting in total phyto-oestrogen contents of 403, 1659 and 1434 ng/ml for the B1, R1 and R2 diets, respectively. Whey was produced from the milk and added to cell culture medium in concentrations up to 10% for MCF-7 cells and 5% for PC-3 cells. Cell proliferation was measured fluorometrically after 7 d for MCF-7 cells and 5 d for PC-3 cells. There was no significant difference in the proliferative effect of whey from the different dietary treatments at any of the whey concentrations tested. An anti-proliferative effect (P<0·01) of 5 and 10% whey was seen when tested in the presence of 10 pm oestradiol in the medium. This effect was independent of dietary treatment of cows. Whey induced a significant (P<0·01) proliferative response in PC-3 cells independent of dietary treatment. Purified equol in concentrations similar to equol concentrations in milk decreased PC-3 cell proliferation, and therefore the stimulatory effect of whey in PC-3 cells is believed to be mediated by other bioactives than equol. In conclusion, our results suggest that using whey in these proliferation assays, it was not possible to discriminate between milk with high or low levels of phyto-oestrogens.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2012

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References

Andersen, C, Nielsen, TS, Purup, S, Kristensen, T, Eriksen, J, Søegaard, K, Sørensen, J & Fretté, XC 2009 Phyto-oestrogens in herbage and milk from cows grazing white clover, red clover, lucerne or chicory-rich pastures. Animal 3 11891195Google Scholar
Andersen, C, Weisbjerg, MR, Hansen-Møller, J & Sejrsen, K 2008 Effect of forage on the content of phyto-oestrogens in bovine milk. Animal 1 16Google Scholar
Antignac, JP, Cariou, R, Bizec, BL & Andre, F 2004 New data regarding phyto-oestrogens content in bovine milk. Food Chemistry 87 275281CrossRefGoogle Scholar
Antignac, JP, Cariou, R, Le Bizec, B, Cravedi, JP & Andre, F 2003 Identification of phyto-oestrogens in bovine milk using liquid chromatography/electrospray tandem mass spectrometry. Rapid Communications in Mass Spectrometry 17 12561264CrossRefGoogle ScholarPubMed
Booth, NL, Overk, CR, Yao, P, Totura, S, Deng, YF, Hedayat, AS, Bolton, JL, Pauli, GF & Farnsworth, NR 2006 Seasonal variation of red clover (Trifolium pratense L., Fabaceae) isoflavones and estrogenic activity. Journal of Agricultural and Food Chemistry 54 12771282CrossRefGoogle ScholarPubMed
Committee on Toxicity 2003 Phyto-Oestrogens and Health, pp. 1444. London: The Foods Standard AgencyGoogle Scholar
Dabre, PD & Daly, RJ 1989 Effects of oestrogen on human breast cancer cells in culture. Proceedings of the Royal Society of Edingburgh 95B 119132Google Scholar
Dip, R, Lenz, S, Antignac, JP, Le Bizec, B, Gmuender, H & Naegeli, H 2008 Global gene expression profiles induced by phyto-oestrogens in human breast cancer cells. Endocrine-Related Cancer 15 161173CrossRefGoogle ScholarPubMed
Grunfeld, HT & Bonefeld-Jorgensen, EC 2004 Effect of in vitro estrogenic pesticides on human oestrogen receptor [alpha] and [beta] mRNA levels. Toxicology Letters 151 467480CrossRefGoogle ScholarPubMed
Gutendorf, B & Westendorf, J 2001 Comparison of an array of in vitro assays for the assessment of the estrogenic potential of natural and synthetic estrogens, phyto-oestrogens and xenoestrogens. Toxicology 166 7989Google Scholar
Hedlund, TE, Johannes, WU & Miller, GJ 2003 Soy isoflavonoid equol modulates the growth of benign and malignant prostatic epithelial cells in vitro. Prostate 54 6878CrossRefGoogle ScholarPubMed
Hoikkala, A, Mustonen, E, Saastamoinen, I, Jokela, T, Taponen, J, Saloniemi, H & Wahala, K 2007 High levels of equol in organic skimmed Finnish cow milk. Molecular Nutrition and Food Research 51 782786Google Scholar
Kanagaraj, P, Vijayababu, MR, Ilangovan, R, Senthilkumar, K, Venkataraman, P, Aruldhas, MM & Arunakaran, J 2007 Effect of 17beta-oestradiol on apoptosis, IGF system components and gelatinases A and B in prostate cancer cells (PC-3). Clinica Chimica Acta 377 7078Google Scholar
Kano, M, Takayanagi, T, Harada, K, Sawada, S & Ishikawa, F 2006 Bioavailability of isoflavones after ingestion of soy beverages in healthy adults. Journal of Nutrition 136 22912296Google Scholar
Kelsey, JL, Gammon, MD & John, EM 1993 Reproductive factors and breast cancer. Epidemiologic Reviews 15 3647CrossRefGoogle ScholarPubMed
King, RA, Mano, MM & Head, RJ 1998 Assessment of isoflavonoid concentrations in Australian bovine milk samples. Journal of Dairy Research 65 479489Google Scholar
Kuhnle, GGC, Dell’ Aquila, C, Aspinall, SM, Runswick, SA, Mulligan, AA & Bingham, SA 2008 Phyto-oestrogen content of foods of animal origin: Dairy products, eggs, meat, fish, and seafood. Journal of Agricultural and Food Chemistry 56 1009910104CrossRefGoogle ScholarPubMed
Lau, KM, LaSpina, M, Long, J & Ho, SM 2000 Expression of estrogen receptor (ER)-alpha and ER-beta in normal and malignant prostatic epithelial cells: regulation by methylation and involvement in growth regulation. Cancer Research 60 31753182Google Scholar
Matsumura, A, Ghosh, A, Pope, GS & Darbre, PD 2005 Comparative study of oestrogenic properties of eight phyto-oestrogens in MCF7 human breast cancer cells. Journal of Steroid Biochemistry and Molecular Biology 94 431443CrossRefGoogle ScholarPubMed
Mitchell, JH, Duthie, SJ & Collins, AR 2000 Effects of phyto-oestrogens on growth and DNA integrity in human prostate tumor cell lines: PC-3 and LNCaP. Nutrition and Cancer 38 223228Google Scholar
Mustonen, EA, Tuori, M, Saastamoinen, I, Taponen, J, Wahala, K, Saloniemi, H & Vanhatalo, A 2009 Equol in milk of dairy cows is derived from forage legumes such as red clover. British Journal of Nutrition 102 15521556CrossRefGoogle ScholarPubMed
Nielsen, TS, Norgaard, JV, Purup, S, Frette, XC & Bonefeld-Jorgensen, EC 2009 Estrogenic activity of bovine milk high or low in equol using immature mouse uterotrophic responses and an estrogen receptor transactivation assay. Cancer Epidemiology 33 6168CrossRefGoogle ScholarPubMed
Nielsen, TS, Purup, S, Warri, A, Godschalk, RW & Hilakivi-Clarke, L 2011 Effects of maternal exposure to cow's milk high or low in isoflavones on carcinogen-induced mammary tumorigenesis among rat offspring. Cancer Prevention Research (Philadelphia) 4 694701Google Scholar
Prins, GS & Korach, KS 2008 The role of estrogens and estrogen receptors in normal prostate growth and disease. Steroids 73 233244CrossRefGoogle Scholar
Rasmussen, TH, Nielsen, F, Andersen, HR, Nielsen, JB, Weihe, P & Grandjean, P 2003 Assessment of xenoestrogenic exposure by a biomarker approach: application of the E-Screen bioassay to determine estrogenic response of serum extracts. Environmental Health 2 12Google Scholar
Rowland, I, Faughnan, M, Hoey, L, Wahala, K, Williamson, G & Cassidy, A 2003 Bioavailability of phyto-oestrogens. British Journal of Nutrition 89 S45S58CrossRefGoogle ScholarPubMed
Sivesind, E & Seguin, P 2005 Effects of the environment, cultivar, maturity, and preservation method on red clover isoflavone concentration. Journal of Agricultural and Food Chemistry 53 63976402CrossRefGoogle ScholarPubMed
Steinshamn, H, Purup, S, Thuen, E & Hansen-Moller, J 2008 Effects of clover-grass silages and concentrate supplementation on the content of phyto-oestrogens in dairy cow milk. Journal of Dairy Science 91 27152725Google Scholar
Tsao, R, Papadopoulos, Y, Yang, R, Young, JC & McRae, K 2006 Isoflavone profiles of red clovers and their distribution in different parts harvested at different growing stages. Journal of Agricultural and Food Chemistry 54 57975805CrossRefGoogle ScholarPubMed
Wu, Q, Wang, M & Simon, JE 2003 Determination of isoflavones in red clover and related species by high-performance liquid chromatography combined with ultraviolet and mass spectrometric detection. Journal of Chromatography A 1016 195209Google Scholar