Dose-dependent effects of isoflavone exposure during early lifetime on the rat mammary gland: Studies on estrogen sensitivity, isoflavone metabolism, and DNA methylation

Molecular Nutrition and Food Research

Volumn 59, Issue 2, 2015, Pages 270-283

  Blei, Tina ^a   Soukup, Sebastian T ^b   Schmalbach, Katja ^c   Pudenz, Maria ^d   Möller, Frank Josef ^e   Egert, Björn ^b   Wörtz, Nadine ^c   Kurrat, Anne ^a   Müller, Dennis ^a   Vollmer, Günter ^e   Gerhäuser, Clarissa ^d   Lehmann, Leane ^c   Kulling, Sabine E ^b   Diel, Patrick ^a  

^a GERMAN SPORT UNIVERSITY COLOGNE   (Germany)

^b FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Epigenetics; Isoflavones; Mammary gland; Phase II metabolism; Proliferation

Indexed keywords

RATTUS; RATTUS NORVEGICUS;

ESTROGEN; ESTROGEN RECEPTOR; ISOFLAVONE DERIVATIVE; LEPTIN;

ANIMAL; BLOOD; BODY WEIGHT; CELL PROLIFERATION; CHEMISTRY; DNA METHYLATION; DOSE RESPONSE; DRUG EFFECTS; FEMALE; GENETICS; HUMAN; MCF 7 CELL LINE; METABOLISM; RAT; SOYBEAN; UDDER; UTERUS; WISTAR RAT;

ANIMALS; BODY WEIGHT; CELL PROLIFERATION; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTROGENS; FEMALE; HUMANS; ISOFLAVONES; LEPTIN; MAMMARY GLANDS, ANIMAL; MCF-7 CELLS; RATS; RATS, WISTAR; RECEPTORS, ESTROGEN; SOYBEANS; UTERUS;

EID: 84922713872     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201400480     Document Type: Article

References (59)

1. Wu, A. H., Yu, M. C., Tseng, C. C., Pike, M. C., Epidemiology of soy exposures and breast cancer risk. Br. J. Cancer 2008, 98, 9-14.
2. Dong, J.-Y., Qin, L.-Q., Soy isoflavones consumption and risk of breast cancer incidence or recurrence: a meta-analysis of prospective studies. Breast Cancer Res. Treat. 2011, 125, 315-323.
3. Nagata, C., Mizoue, T., Tanaka, K., Tsuji, I. et al., Soy intake and breast cancer risk: an evaluation based on a systematic review of epidemiologic evidence among the Japanese population. Jpn. J. Clin. Oncol. 2014, 44, 282-295.
4. Lee, S.-A., Shu, X.-O., Li, H., Yang, G. et al., Adolescent and adult soy food intake and breast cancer risk: results from the Shanghai Women's Health Study. Am. J. Clin. Nutr. 2009, 89, 1920-1926.
5. Wada, K., Nakamura, K., Tamai, Y., Tsuji, M. et al., Soy isoflavone intake and breast cancer risk in Japan: from the Takayama study: isoflavone and breast cancer risk in Japan. Int. J. Cancer 2013, 133, 952-960.
6. Shu, X. O., Zheng, Y., Cai, H., Gu, K. et al., Soy food intake and breast cancer survival. JAMA 2009, 302, 2437-2443.
7. Whitsett, T. G., Jr., Lamartiniere, C. A., Genistein and resveratrol: mammary cancer chemoprevention and mechanisms of action in the rat. Expert Rev. Anticancer Ther. 2006, 6, 1699-1706.
8. Travis, R. C., Allen, N. E., Appleby, P. N., Spencer, E. A. et al., A prospective study of vegetarianism and isoflavone intake in relation to breast cancer risk in British women. Int. J. Cancer 2008, 122, 705-710.
9. Magee, P. J., Rowland, I., Soy products in the management of breast cancer. Curr. Opin. Clin. Nutr. Metab. Care 2012, 15, 586-591.
10. Nagata, C., Factors to consider in the association between soy isoflavone intake and breast cancer risk. J. Epidemiol. 2010, 20, 83-89.
11. Arai, Y., Uehara, M., Sato, Y., Kimira, M. et al., Comparison of isoflavones among dietary intake, plasma concentration and urinary excretion for accurate estimation of phytoestrogen intake. J. Epidemiol. 2000, 10, 127-135.
12. Lampe, J. W., Isoflavonoid and lignan phytoestrogens as dietary biomarkers. J. Nutr. 2003, 133(Suppl 3), 956S-964S.
13. Hulka, B. S., Moorman, P. G., Breast cancer: hormones and other risk factors. Maturitas 2001, 38, 103-113.
14. Lu, L. J., Anderson, K. E., Grady, J. J., Nagamani, M., Effects of soya consumption for one month on steroid hormones in premenopausal women: implications for breast cancer risk reduction. Cancer Epidemiol. Biomarkers Prev. 1996, 5, 63-70.
15. Toniolo, P. G., Levitz, M., Zeleniuch-Jacquotte, A., Banerjee, S. et al., A prospective study of endogenous estrogens and breast cancer in postmenopausal women. J. Natl. Cancer Inst. 1995, 87, 190-197.
16. National Toxicology Program, Toxicology and carcinogenesis studies of genistein (Cas No. 446-72-0) in Sprague-Dawley rats (feed study). Natl. Toxicol. Program Tech. Rep. Ser. 2008, 545, 1-240.
17. Möller, F. J., Diel, P., Zierau, O., Hertrampf, T. et al., Long-term dietary isoflavone exposure enhances estrogen sensitivity of rat uterine responsiveness mediated through estrogen receptor alpha. Toxicol. Lett. 2010, 196, 142-153.
18. Molzberger, A. F., Soukup, S. T., Kulling, S. E., Diel, P., Proliferative and estrogenic sensitivity of the mammary gland are modulated by isoflavones during distinct periods of adolescence. Arch. Toxicol. 2013, 87, 1129-1140.
19. Soukup, S. T., Al-Maharik, N., Botting, N., Kulling, S. E., Quantification of soy isoflavones and their conjugative metabolites in plasma and urine: an automated and validated UHPLC-MS/MS method for use in large-scale studies. Anal. Bioanal. Chem. 2014, 406, 6007-6020.
20. Soto, A. M., Sonnenschein, C., Chung, K. L., Fernandez, M. F. et al., The E-SCREEN assay as a tool to identify estrogens: an update on estrogenic environmental pollutants. Environ. Health Perspect. 1995, 103, 113-122.
21. Lehmann, L., Jiang, L., Wagner, J., Soy isoflavones decrease the catechol-O-methyltransferase-mediated inactivation of 4-hydroxyestradiol in cultured MCF-7 cells. Carcinogenesis 2008, 29, 363-370.
22. Lewis, E. M., Barnett, J. F. Jr., Freshwater, L., Hoberman, A. M. et al., Sexual maturation data for Crl Sprague-Dawley rats: criteria and confounding factors. Drug Chem. Toxicol. 2002, 25, 437-458.
23. Molzberger, A. F., Vollmer, G., Hertrampf, T., Möller, F. J. et al., In utero and postnatal exposure to isoflavones results in a reduced responsivity of the mammary gland towards estradiol. Mol. Nutr. Food Res. 2012, 56, 399-409
24. Ronis, M. J. J., Shankar, K., Gomez-Acevedo, H., Hennings, L. et al., Mammary gland morphology and gene expression differ in female rats treated with 17β-estradiol or fed soy protein isolate. Endocrinology 2012, 153, 6021-6032.
25. Pudenz, M., Roth, K., Gerhauser, C., Impact of soy isoflavones on the epigenome in cancer prevention. Nutrients 2014, 6, 4218-4272.
26. Faryna, M., Konermann, C., Aulmann, S., Bermejo, J. L. et al., Genome-wide methylation screen in low-grade breast cancer identifies novel epigenetically altered genes as potential biomarkers for tumor diagnosis. FASEB J. 2012, 26, 4937-4950.
27. Prasain, J. K., Barnes, S., Metabolism and bioavailability of flavonoids in chemoprevention: current analytical strategies and future prospectus. Mol. Pharm. 2007, 4, 846-864.
28. Stone, A., Valdes-Mora, F., Gee, J. M. W., Farrow, L. et al., Tamoxifen-induced epigenetic silencing of oestrogen-regulated genes in anti-hormone resistant breast cancer. PLoS One 2012, 7, e40466.
29. Unsicker, K., Spittau, B., Krieglstein, K., The multiple facets of the TGF-β family cytokine growth/differentiation factor-15/macrophage inhibitory cytokine-1. Cytokine Growth Factor Rev. 2013, 24, 373-384.
30. Ruttkay-Nedecky, B., Nejdl, L., Gumulec, J., Zitka, O. et al., The role of metallothionein in oxidative stress. Int. J. Mol. Sci. 2013, 14, 6044-6066.
31. Morito, K., Hirose, T., Kinjo, J., Hirakawa, T. et al., Interaction of phytoestrogens with estrogen receptors alpha and beta. Biol. Pharm. Bull. 2001, 24, 351-356.
32. Messina, M., Nagata, C., Wu, A. H., Estimated Asian adult soy protein and isoflavone intakes. Nutr. Cancer 2006, 55, 1-12.
33. Yamamoto, S., Sobue, T., Sasaki, S., Kobayashi, M. et al., Validity and reproducibility of a self-administered food-frequency questionnaire to assess isoflavone intake in a Japanese population in comparison with dietary records and blood and urine isoflavones. J. Nutr. 2001, 131, 2741-2747.
34. van der Velpen, V., Hollman, P. C., van Nielen, M., Schouten, E. G. et al., Large inter-individual variation in isoflavone plasma concentration limits use of isoflavone intake data for risk assessment. Eur. J. Clin. Nutr. 2014, 68, 1141-1147.
35. Rucker, R., Storms, D., Interspecies comparisons of micronutrient requirements: metabolic vs. absolute body size. J. Nutr. 2002, 132, 2999-3000.
36. Schneider, K., Oltmanns, J., Hassauer, M., Allometric principles for interspecies extrapolation in toxicological risk assessment-empirical investigations. Regul. Toxicol. Pharmacol. 2004, 39, 334-347.
37. Hosoda, K., Furuta, T., Ishii, K., Metabolism and disposition of isoflavone conjugated metabolites in humans after ingestion of kinako. Drug Metab. Dispos. 2011, 39, 1762-1767.
38. Lephart, E., Noble rats display decreased weight gain and visceral adiposity via lifelong exposure to an isoflavone rich diet. J. Nutr. Health Food Sci. 2014, 2, 1-6.
39. Weigt, C., Hertrampf, T., Zoth, N., Fritzemeier, K. H. et al., Impact of estradiol, ER subtype specific agonists and genistein on energy homeostasis in a rat model of nutrition induced obesity. Mol. Cell. Endocrinol. 2012, 351, 227-238.
40. Velders, M., Schleipen, B., Fritzemeier, K. H., Zierau, O. et al., Selective estrogen receptor-β activation stimulates skeletal muscle growth and regeneration. FASEB J. 2012, 26, 1909-1920.
41. Strakovsky, R. S., Lezmi, S., Flaws, J. A., Schantz, S. L. et al., Genistein exposure during the early postnatal period favors the development of obesity in female, but not male rats. Toxicol. Sci. 2014, 138, 161-174.
42. Su, Y., Shankar, K., Simmen, R. C., Early soy exposure via maternal diet regulates rat mammary epithelial differentiation by paracrine signaling from stromal adipocytes. J. Nutr. 2009, 139, 945-951.
43. Warri, A., Saarinen, N. M., Makela, S., Hilakivi-Clarke, L., The role of early life genistein exposures in modifying breast cancer risk. Br. J. Cancer 2008, 98, 1485-1493.
44. El Sheikh Saad, H., Meduri, G., Phrakonkham, P., Berges, R. et al., Abnormal peripubertal development of the rat mammary gland following exposure in utero and during lactation to a mixture of genistein and the food contaminant vinclozolin. Reprod. Toxicol. 2011, 32, 15-25.
45. Vandenberg, L. N., Colborn, T., Hayes, T. B., Heindel, J. J. et al., Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr. Rev. 2012, 33, 378-455.
46. Delclos, K. B., Weis, C. C., Bucci, T. J., Olson, G. et al., Overlapping but distinct effects of genistein and ethinyl estradiol (EE(2)) in female Sprague-Dawley rats in multigenerational reproductive and chronic toxicity studies. Reprod. Toxicol. 2009, 27, 117-132.
47. Guerrero-Bosagna, C. M., Sabat, P., Valdovinos, F. S., Valladares, L. E. et al., Epigenetic and phenotypic changes result from a continuous pre and post natal dietary exposure to phytoestrogens in an experimental population of mice. BMC Physiol. 2008, 8, 17.
48. Mardon, J., Mathey, J., Kati-Coulibaly, S., Puel, C. et al., Influence of lifelong soy isoflavones consumption on bone mass in the rat. Exp. Biol. Med. 2008, 233, 229-237.
49. Golub, M. S., Collman, G. W., Foster, P. M. D., Kimmel, C. A. et al., Public health implications of altered puberty timing. Pediatrics 2008, 121(Suppl 3), S218-S230.
50. Adgent, M., Daniels, J., Rogan, W., Adair, L. et al., Early-life soy exposure and age at menarche. Paediatr. Perinat. Epidemiol. 2012, 26, 163-175.
51. Dewi, F. N., Wood, C. E., Lees, C. J., Willson, C. J. et al., Dietary soy effects on mammary gland development during the pubertal transition in nonhuman primates. Cancer Prev. Res. 2013, 6, 832-842.
52. Limer, J. L., Speirs, V., Phyto-oestrogens and breast cancer chemoprevention. Breast Cancer Res. 2004, 6, 119-132.
53. Messina, M., Hilakivi-Clarke, L., Early intake appears to be the key to the proposed protective effects of soy intake against breast cancer. Nutr. Cancer 2009, 61, 792-798.
54. Brown, N. M., Belles, C. A., Lindley, S. L., Zimmer-Nechemias, L. et al., Mammary gland differentiation by early life exposure to enantiomers of the soy isoflavone metabolite equol. Food Chem. Toxicol. 2010, 48, 3042-3050.
55. Li, Y., Liu, L., Andrews, L. G., Tollefsbol, T. O., Genistein depletes telomerase activity through cross-talk between genetic and epigenetic mechanisms. Int. J. Cancer 2009, 125, 286-296.
56. Molinié, B., Georgel, P., Genetic and epigenetic regulations of prostate cancer by genistein. Drug News Perspect. 2009, 22, 247-254.
57. Krupenko, S. A., Oleinik, N. V., 10-Formyltetrahydrofolate dehydrogenase, one of the major folate enzymes, is down-regulated in tumor tissues and possesses suppressor effects on cancer cells. Cell Growth Differ. 2002, 13, 227-236.
58. Campbell, S. M., Rosen, J. M., Hennighausen, L. G., Strech-Jurk, U. et al., Comparison of the whey acidic protein genes of the rat and mouse. Nucleic Acids Res. 1984, 12, 8685-8697.
59. Huang, J., Plass, C., Gerhauser, C., Cancer chemoprevention by targeting the epigenome. Curr. Drug Targets 2011, 12, 1925-1956.