Phytoestrogens and bone health at different reproductive stages

References

• Marjoribanks J, Farquhar C, Roberts H, Lethaby A. Long term hormone therapy for perimenopausal and postmenopausal women. Cochrane Database Syst Rev 2012;7:CD004143
   PubMed Web of Science ®Google Scholar
• Castelo-Branco C, Palacios S, Calaf J, et al. Available medical choices for the management of menopause. Maturitas 2005;52: S61–70
   PubMed Web of Science ®Google Scholar
• Messina M. A brief historical overview of the past two decades of soy and isoflavone research. J Nutr 2010;140:1350–4S
   PubMed Web of Science ®Google Scholar
• Shukla SK, Gupta S, Ojha SK, Sharma SB. Cardiovascular friendly natural products: a promising approach in the management of CVD. Nat Prod Res 2010;24:873–98
   PubMed Web of Science ®Google Scholar
• Castelo-Branco C, Cancelo Hidalgo MJ. Isoflavones: effects on bone health. Climacteric 2011;14:204–11
   PubMed Web of Science ®Google Scholar
• Lee SJ, Ahn JK, Khanh TD, et al. Comparison of isoflavone concentrations in soybean (Glycine max (L.) Merrill) sprouts grown under two different light conditions. J Agric Food Chem 2007;55:9415–21
   PubMed Web of Science ®Google Scholar
• Villaseca P. Non-estrogen conventional and phytochemical treatments for vasomotor symptoms: what needs to be known for practice. Climacteric 2012;15:115–24
   PubMed Web of Science ®Google Scholar
• Muthyala RS, Ju YH, Sheng S, et al. Equol, a natural estrogenic metabolite from soy isoflavones: convenient preparation and resolution of R- and S-equols and their differing binding and biological activity through estrogen receptors alpha and beta. Bioorg Med Chem 2004;12:1559–67
   PubMed Web of Science ®Google Scholar
• Wu J, Oka J, Ezaki J, et al. Possible role of equol status in the effects of isoflavone on bone and fat mass in postmenopausal Japanese women: a double-blind, randomized, controlled trial. Menopause 2007;14:866–74
   PubMed Web of Science ®Google Scholar
• Niculescu MD, Pop EA, Fischer LM, Zeisel SH. Dietary isoflavones differentially induce gene expression changes in lymphocytes from postmenopausal women who form equol as compared with those who do not. J Nutr Biochem 2007;18:380–90
   PubMed Web of Science ®Google Scholar
• Couse JF, Lindzey J, Grandien K, et al. Tissue distribution and quantitative analysis of estrogen receptor-alpha (ERalpha) and estrogen receptor-beta (ERbeta) messenger ribonucleic acid in the wild-type and ERalpha-knockout mouse. Endocrinology 1997;138:4613–21
   PubMed Web of Science ®Google Scholar
• Windahl SH, Norgård M, Kuiper GG, et al. Cellular distribution of estrogen receptor beta in neonatal rat bone. Bone 2000;26:117–21
   PubMed Web of Science ®Google Scholar
• Chen FP, Hsu T, Hu CH, et al. Expression of estrogen receptors alpha and beta in human osteoblasts: identification of exon-2 deletion variant of estrogen receptor beta in postmenopausal women. Chang Gung Med J 2004;27:107–15
   PubMedGoogle Scholar
• Galea GL, Meakin LB, Sugiyama T, et al. Estrogen receptor α mediates proliferation of osteoblastic cells stimulated by estrogen and mechanical strain, but their acute down regulation of the Wnt antagonist Sost is mediated by Estrogen Receptor β. J Biol Chem. 2013;288:9035--48
   Google Scholar
• Chang EC, Charn TH, Park SH, et al. Estrogen receptors α and β as determinants of gene expression: influence of ligand, dose, and chromatin binding. Mol Endocrinol 2008;22:1032–43
   PubMed Web of Science ®Google Scholar
• Kuiper GG, Carlsson B, Grandien K, et al. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997;138:863–70
   PubMed Web of Science ®Google Scholar
• Kuiper GG, Lemmen JG, Carlsson B, et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998;139:4252–63
   PubMed Web of Science ®Google Scholar
• Morito K, Aomori T, Hirose T, et al. Interaction of phytoestrogens with estrogen receptors alpha and beta (II). Biol Pharm Bull 2002;25:48–52
   PubMed Web of Science ®Google Scholar
• Matsumura A, Ghosh A, Pope GS, Darbre PD. Comparative study of oestrogenic properties of eight phytoestrogens in MCF7 human breast cancer cells. J Steroid Biochem Mol Biol 2005;94:431–43
   PubMed Web of Science ®Google Scholar
• Marino M, Galluzzo P, Ascenz P. Estrogen signaling multiple pathways to impact gene transcription. Curr Genomics 2006;7:497–508
   PubMed Web of Science ®Google Scholar
• Leitman DC, Paruthiyil S, Yuan C, et al. Tissue-specific regulation of genes by estrogen receptors. Semin Reprod Med 2012;30:14–22
   PubMed Web of Science ®Google Scholar
• Gao H, Dahlman-Wright K. The gene regulatory networks controlled by estrogens. Mol Cell Endocrinol 2011;334:83–90
   Google Scholar
• Routledge EJ, White R, Parker MG, et al. Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ER beta. J Biol Chem 2000;275:35986–93
   PubMed Web of Science ®Google Scholar
• Crusodé de Souza M, Sasso-Cerri E, Cerri PS. Immunohistochemical detection of estrogen receptor beta in alveolar bone cells of estradiol-treated female rats: possible direct action of estrogen on osteoclast life span. J Anat 2009;215:673–81
   PubMed Web of Science ®Google Scholar
• Okazaki R, Inoue D, Shibata M, et al. Estrogen promotes early osteoblast differentiation and inhibits adipocyte differentiation in mouse bone marrow stromal cell lines that express estrogen receptor (ER) alpha or beta. Endocrinology 2002;143:2349–56
   PubMed Web of Science ®Google Scholar
• Somjen D, Katzburg S, Sharon O, et al. Sex specific response of cultured human bone cells to ERalpha and ERbeta specific agonists by modulation of cell proliferation and creatine kinase specific activity. J Steroid Biochem Mol Biol 2011;125:226–230,36
   PubMed Web of Science ®Google Scholar
• Bradford PG, Gerace KV, Roland RL, Chrzan BG. Estrogen regulation of apoptosis in osteoblasts. Physiol Behav 2010;99:181–5
   PubMed Web of Science ®Google Scholar
• Wright HL, McCarthy HS, Middleton J, Marshall MJ. RANK, RANKL and osteoprotegerin in bone biology and disease. Curr Rev Musculoskelet Med 2009;2:56–64
   PubMedGoogle Scholar
• Kong YY, Boyle WJ, Penninger JM. Osteoprotegerin ligand: a regulator of immune responses and bone physiology. Immunol Today 2000;21:495–502
   PubMedGoogle Scholar
• Robinson LJ, Yaroslavskiy BB, Griswold RD, et al. Estrogen inhibits RANKL-stimulated osteoclastic differentiation of human monocytes through estrogen and RANKL-regulated interaction of estrogen receptor-α with BCAR1 and Traf6. Exp Cell Res 2009;315:1287–301
   PubMed Web of Science ®Google Scholar
• Arjmandi BH, Birnbaum R, Goyal NV, et al. Bone-sparing effect of soy protein in ovarian hormone-deficient rats is related to its isoflavone content. Am J Clin Nutr 1998;68:1364S–68S
   PubMed Web of Science ®Google Scholar
• Marini H, Minutoli L, Polito F, et al. OPG and sRANKL serum concentrations in osteopenic, postmenopausal women after 2-year genistein administration. J Bone Miner Res 2008;23:715–20
   PubMed Web of Science ®Google Scholar
• Blair HC, Jordan SE, Peterson TG, Barnes S. Variable effects of tyrosine kinase inhibitors on avian osteoclastic activity and reduction of bone loss in ovariectomized rats. J Cell Biochem. 1996;61:629–37
   PubMed Web of Science ®Google Scholar
• Sugimoto E, Yamaguchi M. Stimulatory effect of daidzein in osteoblastic MC3T3-E1 cells. Biochem Pharmacol 2000;59;5:471–5
   Web of Science ®Google Scholar
• Arjmandi BH, Alekel L, Hollis BW, et al. Dietary soybean protein prevents bone loss in an ovariectomized rat model of osteoporosis. J Nutr 1996;126:161–7
   PubMed Web of Science ®Google Scholar
• Breslau NA, Brinkley L, Hill KD, Pak CY. Relationship of animal protein-rich diet to kidney stone formation and calcium metabolism. J Clin Endocrinol Metab 1988;66:140–6
   PubMed Web of Science ®Google Scholar
• Omi N, Aoi S, Murata K, Ezawa I. Evaluation of the effect of soybean milk and soybean milk peptides on bone metabolism in the rat model with ovariectomized osteoporosis. J Nutr Sci Vitaminol 1994;40:201–11
   PubMed Web of Science ®Google Scholar
• 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 1999;140:1893–900
   PubMed Web of Science ®Google Scholar
• Blair HC, Jordan SE, Peterson TG, Barnes S. Variable effects of tyrosine kinase inhibitors on avian osteoclastic activity and reduction of bone loss in ovariectomized rats. J Cell Biochem 1996;61:629–37
   PubMed Web of Science ®Google Scholar
• Arjmandi BH, Getlinger MJ, Goyal NV, et al. Role of soy protein with normal or reduced isoflavone content in reversing bone loss induced by ovarian hormone deficiency in rats. Am J Clin Nutr 1998; 68:1358S–63S
   PubMed Web of Science ®Google Scholar
• Picherit C, Bennetau-Pelissero C, Chanteranne B, et al. Soybean isoflavones dose-dependently reduce bone turnover but do not reverse established osteopenia in adult ovariectomized rats. J Nutr 2001;131:723–8
   PubMed Web of Science ®Google Scholar
• Fanti P, Monier-Faugere MC, Geng Z, et al. The phytoestrogen genistein reduces bone loss in short-term ovariectomized rats. Osteoporosis Int 1998;8:274–81
   PubMed Web of Science ®Google Scholar
• Dai R, Ma Y, Sheng Z, et al. Effects of genistein on vertebral trabecular bone microstructure, bone mineral density, microcracks, osteocyte density, and bone strength in ovariectomized rats. J Bone Miner Metab 2008;26:342–9
   PubMed Web of Science ®Google Scholar
• Lees CJ, Kaplan JR, Chen H, et al. Bone mass and soy isoflavones in socially housed, premenopausal macaques. Am J Clin Nutr 2007;86:245–50
   PubMed Web of Science ®Google Scholar
• Register TC, Jayo MJ, Anthony MS. Soy phytoestrogens do not prevent bone loss in postmenopausal monkeys. J Clin Endocrinol Metab 2003;88:4362–70
   PubMed Web of Science ®Google Scholar
• Lees CJ, Ginn TA. Soy protein isolate diet does not prevent increased cortical bone turnover in ovariectomized macaques. Calcif Tissue Int 1998;62:557–8
   PubMed Web of Science ®Google Scholar
• Rachon D, Seidlová-Wuttke D, Vortherms T, Wuttke W. Effects of dietary equol administration on ovariectomy induced bone loss in Sprague-Dawley rats. Maturitas 2007;58:308–15
   PubMed Web of Science ®Google Scholar
• Rachon D, Vortherms T, Seidlová-Wuttke D, et al. Uterotropic effects of dietary equol administration in ovariectomized Sprague-Dawley rats. Climacteric 2007;10:416–26
   PubMed Web of Science ®Google Scholar
• Wood CE, Appt SE, Clarkson TB, et al. Effects of high-dose soy isoflavones and equol on reproductive tissues in female cynomolgus monkeys. Biol Reprod 2006;75:477–86
   PubMed Web of Science ®Google Scholar
• Tousen Y, Ezaki J, Fujii Y, et al. Natural S-equol decreases bone resorption in postmenopausal, non-equol-producing Japanese women: a pilot randomized, placebo-controlled trial. Menopause 2011;18:563–74
   PubMed Web of Science ®Google Scholar
• Uesugi S, Watanabe S, Ishiwata N, et al. Effects of isoflavone supplements on bone metabolic markers and climacteric symptoms in Japanese women. Biofactors 2004;22:221–8
   PubMed Web of Science ®Google Scholar
• Ishimi Y. Dietary equol and bone metabolism in postmenopausal Japanese women and osteoporotic mice. J Nutr 2010;140:1373S–6S
   Web of Science ®Google Scholar
• Wu J, Oka J, Higuchi M, et al. Cooperative effects of isoflavones and exercise on bone and lipid metabolism in postmenopausal Japanese women: a randomized placebo-controlled trial. Metabolism 2006;55:423–33
   PubMed Web of Science ®Google Scholar
• Frankenfeld CL, McTiernan A, Thomas WK, et al. Postmenopausal bone mineral density in relation to soy isoflavone-metabolizing phenotypes. Maturitas 2006;53:315–24
   PubMed Web of Science ®Google Scholar
• Brink E, Coxam V, Robins S, et al. Long-term consumption of isoflavone-enriched foods does not affect bone mineral density, bone metabolism, or hormonal status in early postmenopausal women: a randomized, double-blind, placebo controlled study. Am J Clin Nutr 2008;87:761–70
   PubMed Web of Science ®Google Scholar
• Ho SC, Chan SG, Yi Q, et al. Soy intake and the maintenance of peak bone mass in Hong Kong Chinese women. J Bone Miner Res 2001;16:1363–9
   PubMed Web of Science ®Google Scholar
• Song Y, Paik HY, Joung H. Soybean and soy isoflavone intake indicate a positive change in bone mineral density for 2 years in young Korean women. Nutr Res 2008;28:25–30
   PubMed Web of Science ®Google Scholar
• Anderson JJ, Chen X, Boass A, et al. Soy isoflavones: no effects on bone mineral content and bone mineral density in healthy, menstruating young adult women after one year. J Am Coll Nutr. 2002;21:388–93
   PubMed Web of Science ®Google Scholar
• Di Leo C, Tarolo GL, Bestetti A, et al. Osteoporosis and phytoestrogens: an assessment of bone mineral density via quantitative peripheral computed tomography in milk-egg-vegetarian women in the premenopause. Radiol Med 2000;99:250–7
   PubMedGoogle Scholar
• Mei J, Yeung SSC, Kung AWC. High dietary phytoestrogen intake is associated with higher bone mineral density in postmenopausal but not premenopausal women. J Clin Endocrinol Metab 2001;86:5217–21
   PubMed Web of Science ®Google Scholar
• Ho SC, Chan SG, Yip YB, et al. Change in bone mineral density and its determinants in pre- and perimenopausal Chinese women: the Hong Kong Perimenopausal Women Osteoporosis Study. Osteoporos Int 2008;19:1785–96
   PubMed Web of Science ®Google Scholar
• Alekel DL, Germain AS, Peterson CT, et al. Isoflavone-rich soy protein isolate attenuates bone loss in the lumbar spine of perimenopausal women. Am J Clin Nutr 2000;72:844–52
   PubMed Web of Science ®Google Scholar
• Hsu CS, Shen WW, Hsueh YM, Yeh SL. Soy isoflavone supplementation in postmenopausal women. Effects on plasma lipids, antioxidant enzyme activities and bone density. J Reprod Med 2001;46:221–6
   Google Scholar
• Scheiber M, Liu J, Subbiah M, et al. Dietary soy supplementation reduces LDL oxidation and bone turnover in healthy post-menopausal women. Menopause 2001;8:384–92
   PubMed Web of Science ®Google Scholar
• Kreijkamp-Kaspers S, Kok L, Grobbee DE, et al. Effect of soy protein containing isoflavones on cognitive function, bone mineral density, and plasma lipids in postmenopausal women: a randomized controlled trial. J Am Med Assoc 2004;292:65–74
   PubMed Web of Science ®Google Scholar
• Potter SM, Baum JA, Teng H, et al. Soy protein and isoflavones: their effects on blood lipids and bone density in postmenopausal women. Am J Clin Nutr 1998;68:1375S–79S
   PubMed Web of Science ®Google Scholar
• Levis S, Strickman-Stein N, Ganjei-Azar P, et al. Soy isoflavones in the prevention of menopausal bone loss and menopausal symptoms: a randomized, double-blind trial. Arch Intern Med 2011;171:1363–9
   PubMed Web of Science ®Google Scholar
• Lydeking-Olsen E, Beck-Jensen JE, Setchell KD, Holm-Jensen T. Soymilk or progesterone for prevention of bone loss–a 2 year randomized, placebo-controlled trial. Eur J Nutr 2004;43:246–57
   PubMed Web of Science ®Google Scholar
• Marini H, Minutoli L, Polito F, et al. Effects of the phytoestrogen genistein on bone metabolism in osteopenic postmenopausal women: a randomized trial. Ann Intern Med 2007;146:839–47
   PubMed Web of Science ®Google Scholar
• Wong WW, Lewis RD, Steinberg FM, et al. Soy isoflavone supplementation and bone mineral density in menopausal women: a 2-y multicenter clinical trial. Am J Clin Nutr 2009;90:1433–9
   PubMed Web of Science ®Google Scholar
• Alekel DL, Van Loan MD, Koehler KJ, et al. The soy isoflavones for reducing bone loss (SIRBL) study: a 3-y randomized controlled trial in postmenopausal women. Am J Clin Nutr 2010;91:218–30
   PubMed Web of Science ®Google Scholar
• Arjmandi BH, Lucas EA, Khalil DA, et al. One year soy protein supplementation has positive effects on bone formation markers but not bone density in postmenopausal women. Nutr J 2005;4:8
   PubMed Web of Science ®Google Scholar
• Harkness LS, Fiedler K, Sehgal AR, et al. Decreased bone resorption with soy isoflavone supplementation in postmenopausal women. J Womens Health 2004;13:1000–7
   PubMed Web of Science ®Google Scholar
• Kenny AM, Mangano KM, Abourizk RH, et al. Soy proteins and isoflavones affect bone mineral density in older women: a randomized controlled trial. Am J Clin Nutr 2009;90:234–42
   PubMed Web of Science ®Google Scholar
• Chen YM, Ho SC, Lam SS, et al. Soy isoflavones have a favorable effect on bone loss in Chinese postmenopausal women with lower bone mass: a double-blind, randomized, controlled trial. J Clin Endocrinol Metab 2003;88:4740–7
   PubMed Web of Science ®Google Scholar
• Tai TY, Tsai KS, Tu ST, et al. The effect of soy isoflavone on bone mineral density in postmenopausal Taiwanese women with bone loss: a 2-year randomized double-blind placebo-controlled study. Osteoporos Int 2012;23:1571–80
   PubMed Web of Science ®Google Scholar
• Zhang X, Shu XO, Li H, et al. Prospective cohort study of soy food consumption and risk of bone fracture among postmenopausal women. Arch Intern Med 2005;165:1890–5
   PubMed Web of Science ®Google Scholar
• Ma DF, Qin LQ, Wang PY, Katoh R. Soy isoflavone intake inhibits bone resorption and stimulates bone formation in menopausal women: meta-analysis of randomized controlled trials. Eur J Clin Nutr 2008;62:155–61
   PubMed Web of Science ®Google Scholar
• Ma DF, Qin LQ, Wang PY, Katoh R. Soy isoflavone intake increases bone mineral density in the spine of menopausal women: meta-analysis of randomized controlled trials. Clin Nutr 2008;27:57–64
   PubMed Web of Science ®Google Scholar
• Liu J, Ho SC, Su YX, et al. Effect of long-term intervention of soy isoflavones on bone mineral density in women: a meta-analysis of randomized controlled trials. Bone 2009;44:948–53
   PubMed Web of Science ®Google Scholar
• Taku K, Melby MK, Kurzer MS, et al. Effects of soy isoflavone supplements on bone turnover markers in menopausal women: systematic review and meta-analysis of randomized controlled trials. Bone 2010;47:413–23
   PubMed Web of Science ®Google Scholar
• Wei P, Ming L, Chen Y, Chen DC. Systematic review of isoflavone supplements on osteoporosis in women. Asian Pac J Trop Med 2012;5:243–8
   PubMed Web of Science ®Google Scholar