Long-term dietary isoflavone exposure enhances estrogen sensitivity of rat uterine responsiveness mediated through estrogen receptor α

Toxicology Letters

Volumn 196, Issue 3, 2010, Pages 142-153

  Möller, Frank Josef ^a   Diel, Patrick ^b   Zierau, Oliver ^a   Hertrampf, Torsten ^b   Maaß, Juliane ^a   Vollmer, Günter ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b GERMAN SPORT UNIVERSITY COLOGNE   (Germany)

Author keywords

Genistein; Isoflavones; Long term exposure; Transgenerational study; Uterus

Indexed keywords

AQUAPORIN; DAIDZEIN; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; GENISTEIN; ISOFLAVONE DERIVATIVE; MESSENGER RNA; PHYTOESTROGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIETARY INTAKE; ENDOCRINE TUMOR; ENDOMETRIUM; FEMALE; GENE EXPRESSION; HISTOGENESIS; HOMEOSTASIS; HORMONE RESPONSE; HORMONE SENSITIVITY; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; UTERUS; UTERUS WEIGHT;

ANIMALS; AQUAPORIN 1; AQUAPORIN 3; BODY WEIGHT; CELL PROLIFERATION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENISTEIN; ISOFLAVONES; ORGAN SIZE; PROLIFERATING CELL NUCLEAR ANTIGEN; RATS; RATS, WISTAR; RECEPTORS, PROGESTERONE; RNA, MESSENGER; UTERUS;

RATTUS;

EID: 77953287695     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2010.03.1117     Document Type: Article

References (51)

1. Akiyama T., Ishida J., Nakagawa S., Ogawara H., Watanabe S., Itoh N., Shibuya M., Fukami Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 1987, 262:5592-5595.
2. Barkhem T., Carlsson B., Nilsson Y., Enmark E., Gustafsson J., Nilsson S. Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol. Pharmacol. 1998, 54:105-112.
3. Beral V., Banks E., Reeves G. Evidence from randomised trials on the long-term effects of hormone replacement therapy. Lancet 2002, 360:942-944.
4. Beral V. Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 2003, 362:419-427.
5. Beral V., Bull D., Reeves G. Endometrial cancer and hormone-replacement therapy in the Million Women Study. Lancet 2005, 365:1543-1551.
6. Bouker K.B., Hilakivi-Clarke L. Genistein: does it prevent or promote breast cancer?. Environ. Health Perspect. 2000, 108:701-708.
7. Chen W.F., Gao Q.G., Wong M.S. Mechanism involved in genistein activation of insulin-like growth factor 1 receptor expression in human breast cancer cells. Br. J. Nutr. 2007, 98:1120-1125.
8. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
9. Conneely O.M., Lydon J.P., De Mayo F., O'Malley B.W. Reproductive functions of the progesterone receptor. J. Soc. Gynecol. Investig. 2000, 7:S25-32.
10. Cooney C.A., Dave A.A., Wolff G.L. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J. Nutr. 2002, 132:2393S-2400S.
11. Cos P., De Bruyne T., Apers S., Vanden Berghe D., Pieters L., Vlietinck A.J. Phytoestrogens: recent developments. Planta Med. 2003, 69:589-599.
12. Cullinan-Bove K., Koos R.D. Vascular endothelial growth factor/vascular permeability factor expression in the rat uterus: rapid stimulation by estrogen correlates with estrogen-induced increases in uterine capillary permeability and growth. Endocrinology 1993, 133:829-837.
13. Diel P., Smolnikar K., Schulz T., Laudenbach-Leschowski U., Michna H., Vollmer G. Phytoestrogens and carcinogenesis-differential effects of genistein in experimental models of normal and malignant rat endometrium. Hum. Reprod. 2001, 16:997-1006.
14. Diel P., Schmidt S., Vollmer G. In vivo test systems for the quantitative and qualitative analysis of the biological activity of phytoestrogens. J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. 2002, 777:191-202.
15. Diel P., Thomae R.B., Caldarelli A., Zierau O., Kolba S., Schmidt S., Schwab P., Metz P., Vollmer G. Regulation of gene expression by 8-prenylnaringenin in uterus and liver of Wistar rats. Planta Med. 2004, 70:39-44.
16. Diel P., Hertrampf T., Seibel J., Laudenbach-Leschowsky U., Kolba S., Vollmer G. Combinatorial effects of the phytoestrogen genistein and of estradiol in uterus and liver of female Wistar rats. J. Steroid Biochem. Mol. Biol. 2006, 102:60-70.
17. Dolinoy D.C., Weidman J.R., Waterland R.A., Jirtle R.L. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ. Health Perspect. 2006, 114:567-572.
18. Fritzemeier K.H., Hillisch A., Elger W., Kaufmann U., Kollenkirchen U., Kosemund D., Lindenthal B., Muller G., Muhn P., Nubbemeyer R., Peters O., Siebel P., Hegele-Hartung C. Biological effects of ERalpha- and ERbeta-selective estrogens. Ernst Schering Res Found Workshop 2004, 127-150.
19. Gruber C.J., Tschugguel W., Schneeberger C., Huber J.C. Production and actions of estrogens. N. Engl. J. Med. 2002, 346:340-352.
20. Hakkak R., Korourian S., Shelnutt S.R., Lensing S., Ronis M.J., Badger T.M. Diets containing whey proteins or soy protein isolate protect against 7,12-dimethylbenz(a)anthracene-induced mammary tumors in female rats. Cancer Epidemiol. Biomarkers Prev. 2000, 9:113-117.
21. Hertrampf T., Degen G.H., Kaid A.A., Laudenbach-Leschowsky U., Seibel J., Di Virgilio A.L., Diel P. Supporting information to " Combined effects of physical activity, dietary isoflavones and 17beta-estradiol on movement drive, body weight and bone mineral density in ovariectomized female rats" Planta Med. 2006.
22. Hillisch A., Peters O., Kosemund D., Muller G., Walter A., Schneider B., Reddersen G., Elger W., Fritzemeier K.H. Dissecting physiological roles of estrogen receptor alpha and beta with potent selective ligands from structure-based design. Mol. Endocrinol. 2004, 18:1599-1609.
23. Ishibashi K., Morinaga T., Kuwahara M., Sasaki S., Imai M. Cloning and identification of a new member of water channel (AQP10) as an aquaglyceroporin. Biochim. Biophys. Acta 2002, 1576:335-340.
24. Jablonski E.M., McConnell N.A., Hughes F.M., Huet-Hudson Y.M. Estrogen regulation of aquaporins in the mouse uterus: potential roles in uterine water movement. Biol. Reprod. 2003, 69:1481-1487.
25. Jefferson W.N., Padilla-Banks E., Newbold R.R. Disruption of the developing female reproductive system by phytoestrogens: genistein as an example. Mol. Nutr. Food Res. 2007, 51:832-844.
26. Jirtle R.L., Skinner M.K. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 2007, 8:253-262.
27. King A., Young G. Characteristics and occurrence of phenolic phytochemicals. J. Am. Diet Assoc. 1999, 99:213-218.
28. Kuiper G.G., Carlsson B., Grandien K., Enmark E., Haggblad J., Nilsson S., Gustafsson J.A. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997, 138:863-870.
29. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., van der Burg B., Gustafsson J.A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998, 139:4252-4263.
30. Lee S.A., Shu X.O., Li H., Yang G., Cai H., Wen W., Ji B.T., Gao J., Gao Y.T., Zheng W. 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.
31. Meinild A.K., Klaerke D.A., Zeuthen T. Bidirectional water fluxes and specificity for small hydrophilic molecules in aquaporins 0-5. J. Biol. Chem. 1998, 273:32446-32451.
32. Möller F.J., Zierau O., Hertrampf T., Bliedtner A., Diel P., Vollmer G. Long-term effects of dietary isoflavones on uterine gene expression profiles. J. Steroid Biochem. Mol. Biol. 2009, 113:296-303.
33. Newbold R.R., Banks E.P., Bullock B., Jefferson W.N. Uterine adenocarcinoma in mice treated neonatally with genistein. Cancer Res. 2001, 61:4325-4328.
34. Nguyen T.T., Tran E., Nguyen T.H., Do P.T., Huynh T.H., Huynh H. The role of activated MEK-ERK pathway in quercetin-induced growth inhibition and apoptosis in A549 lung cancer cells. Carcinogenesis 2004, 25:647-659.
35. Olson S.H., Bandera E.V., Orlow I. Variants in estrogen biosynthesis genes, sex steroid hormone levels, and endometrial cancer: a HuGE review. Am. J. Epidemiol. 2007, 165:235-245.
36. Parkin D.M., Bray F., Ferlay J., Pisani P. Global cancer statistics, 2002. CA Cancer J. Clin. 2005, 55:74-108.
37. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
38. Ren M.Q., Kuhn G., Wegner J., Chen J. Isoflavones, substances with multi-biological and clinical properties. Eur. J. Nutr. 2001, 40:135-146.
39. Rice S., Whitehead S.A. Phytoestrogens oestrogen synthesis and breast cancer. J. Steroid Biochem. Mol. Biol. 2008, 108:186-195.
40. Setchell K.D. Phytoestrogens: the biochemistry, physiology, and implications for human health of soy isoflavones. Am. J. Clin. Nutr. 1998, 68:1333S-1346S.
41. Setchell K.D., Cassidy A. Dietary isoflavones: biological effects and relevance to human health. J. Nutr. 1999, 129:758S-767S.
42. Shu X.O., Zheng Y., Cai H., Gu K., Chen Z., Zheng W., Lu W. Soy food intake and breast cancer survival. JAMA 2009, 302:2437-2443.
43. Thigpen J.E., Locklear J., Haseman J.K., Saunders H., Grant M.F., Forsythe D.B. Effects of the dietary phytoestrogens daidzein and genistein on the incidence of vulvar carcinomas in 129/J mice. Cancer Detect. Prev. 2001, 25:527-532.
44. Travis R.C., Allen N.E., Appleby P.N., Spencer E.A., Roddam A.W., Key T.J. A prospective study of vegetarianism and isoflavone intake in relation to breast cancer risk in British women. Int. J. Cancer 2008, 122:705-710.
45. Unfer V., Casini M.L., Costabile L., Mignosa M., Gerli S., Di Renzo G.C. Endometrial effects of long-term treatment with phytoestrogens: a randomized, double-blind, placebo-controlled study. Fertil. Steril. 2004, 82:145-148. [quiz 265].
46. Weihua Z., Saji S., Makinen S., Cheng G., Jensen E.V., Warner M., Gustafsson J.A. Estrogen receptor (ER) beta, a modulator of ERalpha in the uterus. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:5936-5941.
47. Westley B.R., May F.E. Role of insulin-like growth factors in steroid modulated proliferation. J. Steroid Biochem. Mol. Biol. 1994, 51:1-9.
48. Wilson T., March H., Ban W.J., Hou Y., Adler S., Meyers C.Y., Winters T.A., Maher M.A. Antioxidant effects of phyto-and synthetic-estrogens on cupric ion-induced oxidation of human low-density lipoproteins in vitro. Life Sci. 2002, 70:2287-2297.
49. Wu A.H., Pike M.C. Dietary soy protein and hormonal status in females. Am. J. Clin. Nutr. 1995, 62:151-153.
50. Wu A.H., Ziegler R.G., Nomura A.M., West D.W., Kolonel L.N., Horn-Ross P.L., Hoover R.N., Pike M.C. Soy intake and risk of breast cancer in Asians and Asian Americans. Am. J. Clin. Nutr. 1998, 68:1437S-1443S.
51. Xu W.H., Zheng W., Xiang Y.B., Ruan Z.X., Cheng J.R., Dai Q., Gao Y.T., Shu X.O. Soya food intake and risk of endometrial cancer among Chinese women in Shanghai: population based case-control study. BMJ 2004, 328:1285.