Genistein alone and in combination with the mammalian lignans enterolactone and enterodiol induce estrogenic effects on bone and uterus in a postmenopausal breast cancer mouse model

Bone

Volumn 39, Issue 1, 2006, Pages 117-124

  Power, Krista A ^a   Ward, Wendy E ^a   Chen, Jian Min ^a   Saarinen, Niina M ^a   Thompson, Lilian U ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Bone; Breast cancer; Genistein; Mammalian lignans; Uterus

Indexed keywords

ENTEROLACTONE; GENISTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE; BONE DENSITY; BREAST CARCINOMA; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG EFFECT; FEMALE; FEMUR; LUMBAR VERTEBRA; MOUSE; NONHUMAN; OVARIECTOMY; TREATMENT OUTCOME; UTERUS;

4-BUTYROLACTONE; ANIMALS; ANTINEOPLASTIC AGENTS; BONE AND BONES; BONE DENSITY; DRUG COMBINATIONS; ESTROGENS; FEMALE; GENISTEIN; HUMANS; LIGNANS; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, INBRED BALB C; MICE, NUDE; ORGAN SIZE; OVARIECTOMY; PHYTOESTROGENS; POSTMENOPAUSE; UTERUS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 33744825972     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2005.12.015     Document Type: Article

References (55)

1. Adlercreutz H. Phyto-oestrogens and cancer. Lancet Oncol. 3 (2002) 364-373
2. Thompson L.U. Flaxseed, lignans, and cancer. In: Thompson L.U., and Cunanne S. (Eds). Flaxseed in Human Nutrition. 2nd ed. (2003), AOCS Press, Illinois 194-222
3. Turner N.J., Thomson B.M., and Shaw I.C. Bioactive isoflavones in functional foods: the importance of gut microflora on bioavailability. Nutr. Rev. 61 (2003) 204-213
4. Jacobs E., Kulling S.E., and Metzler M. Novel metabolites of the mammalian lignans enterolactone and enterodiol in human urine. J. Steroid Biochem. Mol. Biol. 68 (1999) 211-218
5. Adlercreutz H. Phytoestrogens and breast cancer. J. Steroid Biochem. Mol. Biol. 83 (2002) 113-118
6. Lamartiniere C. Protection against breast cancer with genistein: a component of soy. Am. J. Clin. Nutr. 71 (2000) 1705S-1707S
7. Duncan A.M., Phipps W.R., and Kurzer M.S. Phyto-oestrogens. Best Pract. Res., Clin. Endocrinol. Metab. 17 (2003) 253-271
8. Shao Z., Wu J., Shen Z., and Barsky S. Genistein exerts multiple suppressive effects on human breast carcinoma cells. Cancer Res. 58 (1998) 4851-4857
9. Constantinou A., Krygier A., and Mehta R. Genistein induces maturation of cultured human breast cancer cells and prevents tumor growth in nude mice. Am. J. Clin. Nutr. 68 (1998) 1426S-1430S
10. Allred C., Allred K., Ju Y., Virant S., and Helferich W. Soy diets containing varying amounts of genistein stimulate growth of estrogen-dependent (MCF-7) tumors in a dose-dependent manner. Cancer Res. 61 (2001) 5045-5050
11. Ju Y., Allred C., Allred K., Karko K., Doerge D., and Helferich W. Physiological concentrations of dietary genistein dose-dependently stimulate growth of estrogen-dependent human breast cancer (MCF-7) tumors implanted in athymic nude mice. J. Nutr. 131 (2001) 2957-2962
12. Power K.A., Saarinen N., Chen J., and Thompson L.U. Mammalian lignans enterolactone and enterodiol, alone and in combination with the isoflavone genistein, do not promote the growth of mcf-7 xenografts in ovariectomized athymic nude mice. Int. J. Cancer 118 (2006) 1316-1320
13. Petrakis N.L., Barnes S., King E.B., Lowenstein J., Wiencke J., Lee M.M., et al. Stimulatory influence of soy protein isolate on breast secretion in pre- and postmenopausal women. Cancer. Epidemiol. Biomark. Prev. 5 (1996) 785-794
14. Syed F., and Khosla S. Mechanisms of sex steroid effects on bone. Biochem. Biophys. Res. Commun. 328 (2005) 688-696
15. Harkness L.S., Fiedler K., Sehgal A.R., Oravec D., and Lerner E. Decreased bone resorption with soy isoflavone supplementation in postmenopausal women. J. Women's Health (Larchmt.) 13 (2004) 1000-1007
16. Horiuchi T., Onouchi T., Takahashi M., Ito H., and Orimo H. Effect of soy protein on bone metabolism in postmenopausal Japanese women. Osteoporos. Int. 11 (2000) 721-724
17. Alekel D.L., Germain A.S., Peterson C.T., Hanson K.B., Stewart J.W., and Toda T. Isoflavone-rich soy protein isolate attenuates bone loss in the lumbar spine of perimenopausal women. Am. J. Clin. Nutr. 72 (2000) 844-852
18. Chiechi L.M., Secreto G., D'Amore M., Fanelli M., Venturelli E., Cantatore F., et al. Efficacy of a soy rich diet in preventing postmenopausal osteoporosis: the Menfis randomized trial. Maturitas 42 (2002) 295-300
19. Morabito N., Crisafulli A., Vergara C., Gaudio A., Lasco A., Frisina N., et al. Effects of genistein and hormone-replacement therapy on bone loss in early postmenopausal women: a randomized double-blind placebo-controlled study. J. Bone Miner. Res. 17 (2002) 1904-1912
20. Wu J., Wang X., Chiba H., Higuchi M., Nakatani T., Ezaki O., et al. Combined intervention of soy isoflavone and moderate exercise prevents body fat elevation and bone loss in ovariectomized mice. Metabolism 53 (2004) 942-948
21. Arjmandi B.H., Birnbaum R., Goyal N.V., et al. Bone-sparing effect of soy protein in ovarian hormone-deficient rats is related to its isoflavone content. Am. J. Clin. Nutr. 68 (1998) 1364S-1368S (suppl)
22. Li B., and Yu S. Genistein prevents bone resorption diseases by inhibiting bone resorption and stimulating bone formation. Biol. Pharm. Bull. 26 (2003) 780-786
23. Arjmandi B.H. The role of phytoestrogens in the prevention and treatment of osteoporosis in ovarian hormone deficiency. J. Am. Coll. Nutr. 20 (2001) 398S-402S
24. Dodin S., Lemay A., Jacques H., Legare F., Forest J.C., and Masse B. The effects of flaxseed dietary supplement on lipid profile, bone mineral density, and symptoms in menopausal women: a randomized, double-blind, wheat germ placebo-controlled clinical trial. J. Clin. Endocrinol. Metab. 90 (2005) 1390-1397
25. Brooks J.D., Ward W.E., Lewis J.E., Hilditch J., Nickell L., Wong E., et al. Supplementation with flaxseed alters estrogen metabolism in postmenopausal women to a greater extent than does supplementation with an equal amount of soy. Am. J. Clin. Nutr. 79 (2004) 318-325
26. Lucas E.A., Wild R.D., Hammond L.J., Khalil D.A., Juma S., Daggy B.P., et al. Flaxseed improves lipid profile without altering biomarkers of bone metabolism in postmenopausal women. J. Clin. Endocrinol. Metab. 87 (2002) 1527-1532
27. Canadian Council on Animal Care. In: Ernest D., Olfert D.V.M., Brenda M., and Cross D.V.M. (Eds). Guide to the Care and Use of Experimental Animals. 2nd ed. vol. 1 (1993)
28. Reeves P.G., Nielsen F.H., and Fahey G.C. 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 (1993) 1939-1951
29. Fonseca D., and Ward W.E. Daidzein together with high calcium preserve bone mass and biomechanical strength at multiple sites in ovariectomized mice. Bone 35 (2004) 489-497
30. Messina M.J., and Loprinzi C.L. Soy for breast cancer survivors: a critical review of the literature. J. Nutr. 131 (2001) 3095S-3108S
31. Erlandsson M.C., Islander U., Moverare S., Ohlsson C., and Carlsten H. Estrogenic agonism and antagonism of the soy isoflavone genistein in uterus, bone and lymphopoiesis in mice. APMIS 113 (2005) 317-323
32. Ishimi Y., Arai Y., Wang X., et al. Difference in effective dosage of genistein on bone and uterus in ovariectomized mice. Biochem. Biophys. Res. Commun. 274 (2000) 697-701
33. Fanti P., Monier-Faugere M.C., Geng Z., et al. The phytoestrogen genistein reduces bone loss in short-term ovariectomized rats. Osteoporos. Int. 8 (1998) 274-281
34. Ishimi Y., Miyaura C., Ohmura M., et al. Selective effects of genistein, a soybean isoflavone, on B-lymphopoiesis and bone loss caused by estrogen deficiency. Endocrinology 140 (1999) 1893-1900
35. Onoe Y., Miyaura C., Ohta H., Nozawa S., and Suda T. Expression of estrogen receptor β in rat bone. Endocrinology 138 (1997) 4509-4512
36. Kuiper G., Lemmen J., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139 (1998) 4252-4263
37. Lindberg M.K., Alatalo S.L., Halleen J.M., Mohan S., Gustafsson J.A., and Ohlsson C. Estrogen receptor specificity in the regulation of the skeleton in female mice. J. Endocrinol. 171 (2001) 229-236
38. Lindberg M.K., Weihua Z., Andersson N., Moverare S., Gao H., Vidal O., et al. Estrogen receptor specificity for the effects of estrogen in ovariectomized mice. J. Endocrinol. 174 (2002) 167-178
39. Dang Z.C., and Lowik C. Dose-dependent effects of phytoestrogens on bone. Trends Endocrinol. Metab. 16 (2005) 207-213
40. Yamaguchi M., and Sugimoto E. Stimulatory effect of genistein and daidzein on protein synthesis in osteoblastic MC3T3-E1 cells: activation of aminoacyl-t-RNA synthetase. Mol. Cell. Biochem. 214 (2000) 97-102
41. Sugimoto E., and Yamaguchi M. Anabolic effect of genistein in osteoblastic MC3T3-E1 cells. Int. J. Mol. Med. 5 (2000) 515-520
42. Blair H.C., Jordan S.E., Peterson T.G., and Barnes S. Variable effects of tyrosine kinase inhibitors on avian osteoclastic activity and reduction of bone loss in ovariectomized rats. J. Cell. Biochem. 61 (1996) 629-637
43. Gao Y.H., and Yamaguchi M. Suppressive effect of genistein on rat bone osteoclasts: involvement of protein kinase inhibition and protein tyrosine phosphatase activation. Int. J. Mol. Med. 5 (2000) 261-267
44. Allred C.D., Allred K.F., Ju Y.H., Clausen L.M., Doerge D.R., Schantz S.L., et al. Dietary genistein results in larger MNU-induced, estrogen-dependent mammary tumors following ovariectomy of Sprague-Dawley rats. Carcinogenesis 25 (2004) 211-218
45. Kohlerova E., and Skarda J. Mouse bioassay to assess oestrogenic and anti-oestrogenic compounds: hydroxytamoxifen, diethylstilbestrol and genistein. J. Vet. Med. A. Physiol. Pathol. Clin. Med. 51 (2004) 209-217
46. Unfer V., Casini M.L., Costabile L., Mignosa M., Gerli S., and Di Renzo G.C. Endometrial effects of long-term treatment with phytoestrogens: a randomized, double-blind, placebo-controlled study. Fertil. Steril. 82 (2004) 145-148
47. Saarinen N., Huovinen R., Warri A., Makela S.I., Valentin-Blasini L., Sjoholm R., et al. Enterolactone inhibits the growth of 7,12-dimethylbenz(a)anthracene-induced mammary carcinomas in the rat. Mol. Cancer Ther. 1 (2002) 869-876
48. Ward W.E., Yuan Y.V., Cheung A.M., and Thompson L.U. Exposure to purified lignan from flaxseed (Linum usitatissimum) alters bone development in female rats. Br. J. Nutr. 86 (2001) 499-505
49. Mueller S.O., Simon S., Chae K., Metzler M., and Korach K.S. Phytoestrogens and their human metabolites show distinct agonistic and antagonistic properties on estrogen receptor alpha (ERalpha) and ERbeta in human cells. Toxicol. Sci. 80 (2004) 14-25
50. Magee P.J., and Rowland I.R. Phyto-oestrogens, their mechanism of action: current evidence for a role in breast and prostate cancer. Br. J. Nutr. 91 (2004) 513-531
51. Taylor A.H., and Al-Azzawi F. Immunolocalisation of oestrogen receptor beta in human tissues. J. Mol. Endocrinol. 24 (2000) 145-155
52. Chen J., Tan K.P., Ward W.E., and Thompson L.U. Exposure to flaxseed or its purified lignan during suckling inhibits chemically induced rat mammary tumorigenesis. Exp. Biol. Med. 228 (2003) 951-958
53. Chen J., Wang L., and Thompson L.U. Flaxseed and its components reduce metastasis after surgical excision of solid human breast tumor in nude mice. Cancer Lett. (2005 (May 20)) [electronic publication ahead of print]
54. Thompson L.U., Li T., Chen J., and Goss P. Dietary flaxseed alters tumor biological markers in postmenopausal breast cancer. Clin. Cancer Res. 11 (2005) 3828-3835
55. Sarkar F, Li Y. Chapter 14: Isoflavones, soybean phytoestrogens, and cancer. In: Atif AB, Bradford PG, editors. Nutrition and Cancer Prevention. CRC: Taylor and Francis Group; Boca Raton, FL, USA. 2006:295-312.