Sains Malaysiana 48(9)(2019):
2007–2019
http://dx.doi.org/10.17576/jsm-2019-4809-22
Osteoporosis: Possible Pathways
Involved and the Role of Natural Phytoestrogens in Bone Metabolism
(Osteoporosis: Laluan
yang Mungkin Terlibat dan Peranan Fitoestrogen Semula Jadi dalam Metabolisme
Tulang)
ZAR
CHI
THENT1,
SRIJIT
DAS2*,
PASUK
MAHAKKANUKRAUH3
& VIRGINIA LANZOTTI4
1Anatomy
Discipline, Basic Medical Science Cluster, Faculty of Medicine,
Sungai Buloh Campus, Universiti Teknologi MARA, 47000 UiTM Sungai
Buloh, Selangor Darul Ehsan, Malaysia
2Department
of Anatomy, Faculty of Medicine, Universiti Kebangsaan Malaysia
Medical Centre, Jalan Yaacob Latif, Bandar Tun Razak, 56000 Cheras,
Kuala Lumpur, Federal Territory, Malaysia
3Forensic Osteology
Research and Training Centre, Excellence Center of Osteology Research and, Training
Center & Department of Anatomy, Faculty of Medicine, Chiang Mai University,
Chiang Mai 50200, Thailand
4Department of
Agricultural Sciences, Università di Napoli Federico II, Napoli, Italy
Received:
17 May 2019/Accepted: 5 July 2019
ABSTRACT
The incidence of
post-menopausal osteoporosis is increasing globally. In post-menopausal
osteoporosis, there is deficiency in oestrogen level resulting in bone loss and
fractures. Bone formation is under the control of different hormones. In the
present review, we highlight few pathways such as RANKL/RANK,
apoptosis and Wnt/β-catenin signalling pathways and phytoestrogens
involved in the bone metabolism. RANKL/RANK signalling is
responsible for regulating the formation and activation of multinucleated
osteoclasts from their precursors which is responsible for the survival of
normal bone remodelling. Apoptosis regulates the development, growth and
maintains the bone tissues. The Wnt pathway is an important pharmacological
target for bone anabolic drugs and its future discovery. In today’s world,
herbal remedies are used to treat post-menopausal osteoporosis as these
products contain phytoestrogens. These phytoestrogens are oestrogen like
compounds which influence bone metabolism. The phytoestrogens provide better
therapeutic effect in reducing the RANKL, osteoclastogenesis,
inflammatory markers, and increase the osteogenic markers in the bone cells or
osteoblasts. We discuss the mechanism of action of few phytoestrogens such as
genistein, daidzein and equol which are beneficial for improvement of the bone
health. Daidzein enhances osteoblast growth via the upregulation of BMP expression
in primary osteoblast cells and it is a potential antiosteoporotic agent.
Genistein also possesses antioestrogenic property by virtue of its competitive
binding to the same receptors as oestradiol. Equol regulates the bone loss via
hemopoiesis and inflammatory cytokine production. Thus, phytoestrogens could be
efficiently used as osteoprotective agents for the treatment of individuals
with post-menopausal osteoporosis.
Keywords: Fracture;
oestrogen; pharmacology; post-menopausal; treatment
ABSTRAK
Kejadian osteoporosis
selepas menopaus meningkat secara global. Dalam osteoporosis selepas menopaus,
terdapat penurunan aras estrogen yang mengakibatkan kehilangan tulang dan patah
tulang. Pembentukan tulang dikawal oleh hormon yang berbeza. Dalam ulasan
kepustakaan ini, kami menyerlahkan beberapa laluan isyarat seperti RANKL/
RANK, apoptosis dan Wnt/β-catenin serta fitoestrogens yang
terlibat dalam metabolisme tulang. Isyarat RANKL/RANK bertanggungjawab
mengawal pembentukan dan pengaktifan osteoklas multinukleus daripada prekursor
mereka yang terlibat dalam proses pembentukan semula tulang yang normal.
Apoptosis mengawal perkembangan, pertumbuhan dan penyelenggaraan tisu tulang.
Laluan Wnt adalah sasaran farmakologi yang penting untuk ubat anabolik tulang
dan penemuan masa depannya. Di dunia hari ini, banyak ubat-ubatan herba
digunakan untuk merawat osteoporosis Osteoporosis:
Possible menopaus kerana produk ini mengandungi fitoestrogen. Fitoestrogen
mempunyai struktur seperti estrogen yang mempengaruhi metabolisme tulang.
Fitoestrogen memberikan kesan terapeutik yang lebih baik dalam mengurangkan RANKL,
osteoklastogenesis, penanda inflamasi dan meningkatkan penanda osteogenik dalam
sel-sel tulang atau pun osteoblas. Kami membincangkan mekanisme tindakan
beberapa fitoestrogen seperti genistein, daidzein dan equol yang bermanfaat
untuk kesihatan tulang. Daidzein meningkatkan pertumbuhan osteoblas melalui
peningkatan ekspresi BMP dalam sel osteoblas primer dan ia
adalah agen antiosteoporotik yang berpotensi. Genistein juga mempunyai harta
antioestrogenik berdasarkan daya saingnya yang kompetitif kepada reseptor yang
sama seperti oestradiol. Equol mengawal kehilangan tulang melalui hemopoiesis
dan penghasilan sitokin inflamasi. Oleh itu, fitoestrogen boleh digunakan
sebagai agen osteoperlindungan untuk rawatan osteoporosis selepas menopaus.
Kata kunci: Estrogen; farmakologi; patah tulang; selepas menopaus;
rawatan
REFERENCES
Adlercreutz,
H. 2002. Phyto-oestrogens and cancer. Lancet. Oncol. 3(6): 364-373.
Adjakly,
M., Ngollo, M., Boiteux, J.P., Bignon, Y.J., Guy, L. & Bernard-Gallon, D.
2013. Genistein and daidzein: Different molecular effects on prostate cancer. Anticancer
Res. 33(1): 39-44.
Ajdžanovic,
V.Z., Trifunovic, S., Miljic, D., Šošic-Jurjevic, B., Filipovic, B., Miler, M.,
Ristic, N., Manojlovic-Stojanoski, M. & Miloševic, V. 2018. Somatopause,
weaknesses of the therapeutic approaches and the cautious optimism based on
experimental ageing studies with soy isoflavones. EXCLI J. 17: 279-301.
Al-Anazi,
A.F., Quresh, V.F., Javaid, K. & Qureshi, S. 2011. Preventive effects of
phytoestrogens against postmenopausal osteoporosis as compared to the available
therapeutic choices: An overview. J. Nat. Sci. Biol. Med. 2(2): 154-163.
Almeida,
M., Iyer, S., Martin-Millan, M., Bartell, S.M., Han, L., Ambrogini,
E., Onal, M., Xiong, J., Weinstein, R.S., Jilka, R.L., O'Brien,
C.A. & Manolagas, S.C. 2013. Estrogen receptor-α signaling
in osteoblast progenitors stimulates cortical bone accrual. J.
Clin. Invest. 123(1): 394-404.
Ambati,
S., Miller, C.N., Bass, E.F., Hohos, N.M., Hartzell, D.L., Kelso, E.W.,
Trunnell, E.R., Yang, J.Y., Della-Fera, M.A., Baile, C.A. & Rayalam, S.
2018. Synergistic phytochemicals fail to protect against ovariectomy induced
bone loss in rats. J. Med. Food 21(10): 1044-1052.
Atmaca,
A., Kleerekoper, M., Bayraktar, M. & Kucuk, O. 2008. Soy isoflavones in the
management of postmenopausal osteoporosis. Menopause 15(4): 748-757.
Ayyanan,
A., Laribi, O., Schuepbach-Mallepell, S., Schrick, C., Gutierrez, M., Tanos,
T., Lefebvre, G., Rougemont, J., Yalcin-Ozuysal, O. & Brisken, C. 2011.
Perinatal exposure to bisphenol a increases adult mammary gland progesterone
response and cell number. Mol. Endocrinol. 25(11): 1915- 1923.
Babu,
P.V.A., Si, H., Fu, Z., Zhen, W. & Liu, D. 2012. Genistein prevents
hyperglycemia induced monocyte adhesion to human aortic endothelial cells
through preservation of the cAMP signaling pathway and ameliorates vascular
inflammation in obese diabetic mice. J. Nutr. 142(4): 724-730.
Bakre,
M.M., Hoi, A., Mong, J.C., Koh, Y.Y., Wong, K.Y. & Stanto, L.W. 2007.
Generation of multipotential mesendodermal progenitors from mouse embryonic
stem cells via sustained Wnt pathway activation. J. Biol. Chem. 282(43):
31703-31712.
Banerjee,
C., Mccabe, L.R., Choi, J., Hiebert, S.W., Stein, J.L., Stein, G.S. & Lian,
J.B. 1997. Runt homology domain proteins in osteoblast differentiation:
AML3/CBFA1 is a major component of a bone-specific complex. J. Cell Biochem. 66(1): 1-8.
Benassayag,
C., Ferre, F. & Perrot-Applanat, M. 2002. Phytoestrogens as modulators of
steroidaction in target cells. J. Chromatogr. B Analyt. Technol. Biomed.
Life Sci. 777(1-2): 233-248.
Bennett,
C.N., Longo, K.A., Wright, W.S., Suva, L.J., Lane, T.F., Hankenson, K.D. &
MacDougald, O.A. 2005. Regulation of osteoblastogenesis and bone mass by
Wnt10b. Proc. Natl. Acad. Sci. USA 102(9): 3324-3329.
Bliuc,
D., Nguyen, N.D., Nguyen, T.V., Eisman, J.A. & Center, J.R. 2013. Compound
risk of high mortality following osteoporotic fracture and refracture in
elderly women and men. J. Bone Miner. Res. 28(11): 2317-2324.
Brown,
S.D., Twells, R.C.J., Hey, P.J., Cox, R.D., Levy, E.R., Soderman, A.R.,
Metzker, M.L., Caskey, C.T., Todd, J.A. & Hess, J.F. 1998. Isolation and
characterization of LRP6, a novel member of the low density lipoprotein
receptor gene family. Biochem. Biophys. Res. Commun. 248(3): 879-888.
Carlsen,
E., Giwercman, A. & Skakkebaek, N.E. 1993. Declining sperm counts and
increasing incidence of testicular cancer and other
gonadal disorders: Is there a connection? Ir. Med. J. 86(3): 85-96.
Cassidy, A., Albertazzi, P., Lise Nielsen, I., Hall, W.,
Williamson, G., Tetens, I., Atkins, S., Cross, H., Manios, Y., Wolk, A.,
Steiner, C. & Branca, F. 2006. Critical review of health effects of
soyabean phytooestrogens in post-menopausal women. Proc. Nutr. Soc. 65(1):
76-92.
Chan, C.Y., Norazlina, M., Ima-Nirwana, S. & Kok, Y.C. 2018.
Attitude of Asians to calcium and vitamin D rich foods and supplements:
A systematic review. Sains Malaysiana 47(8): 1801-1810.
Chang, H.H., Robinson, A.R. & Common, R.H. 1975. Excretion
of radioactive diadzein and equol as monosulfates and disulfates
in the urine of the laying hen. Can. J. Biochem. 53(2):
223-230.
Chen,
Y.M., Ho, S.C., Lam, S.S., Ho, S.S. & Woo, J.L. 2003. 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. 88(10): 4740-4747.
Chen,
Y., Cass, S.L., Kutt, S.K., Yee, E.M.H., Chan, D.S.H., Gardner, C.R., Vittorio,
O., Pasquier, E., Black, D.S. & Kumar, N. 2015. Bioorganic & medicinal
chemistry letters synthesis, biological evaluation and structure - Activity
relationship studies of isoflavene based Mannich bases with potent anticancer
activity. Bioorganic & Medicinal Chemistry Letters 25(22): 5377-5383.
Chiodini,
I., Carnevale, V., Torlontano, M., Fusilli, S., Guglielmi, G., Pileri,
M., Modoni, S., Di Giorgio, A., Liuzzi, A., Minisola, S., Cammisa,
M., Trischitta, V. & Scillitani, A. 1998. Alterations of bone
turnover and bone mass at different skeletal sites due to pure glucocorticoid
excess: Study in eumenorrheic patients with Cushing's Syndrome.
J. Clin. Endocrinol. Metab. 83: 1863-1867.
Christian,
S., Wallaschofski, H., Nauck, M., Völzke, H., Schober, H.C. & Hannemann, A.
2015. Fracture risk and risk factors for osteoporosis: Results from two
representative population-based studies in North East Germany (Study of Health
in Pomerania: SHIP-2 and SHIP-Trend). Dtsch. Arztebl. Int. 112 (21-22):
365-371.
Cornwell,
T., Cohick, W. & Raski, I. 2004. Dietary phytoestrogens and health. Phytochemistry 65(8): 995-1016.
Danciu,
C., Soica, C., Csanyi, E., Ambrus, R., Feflea, S., Peev, C. & Dehelean, C.
2012. Changes in the anti-inflammatory activity of soy isoflavonoid genistein
versus genistein incorporated in two types of cyclodextrin derivatives. Chem.
Cent. J. 6(1): 58.
Delmas,
P.D. 2002. Treatment of postmenopausal osteoporosis. Lancet 359(9322):
2018-2026.
De
Wilde, A., Lieberherr, M., Colin, C. & Pointillart, A. 2004. A low dose of
daidzein acts as an ERβ-selective agonist in trabecular osteoblasts of
young female piglets. J. Cell Physiol. 200(2): 253-262.
Dixon,
R.A. 2004. Phytoestrogens. Annu. Rev. Plant Biol. 55: 225-261.
Ducy,
P., Zhang, R., Geoffroy, V., Ridall, A.L. & Karsenty, G. 1997. Osf2/Cbfa1:
A transcriptional activator of osteoblast differentiation. Cell 89(5):
747-754.
Fritz,
H., Seely, D., Flower, G., Skidmore, B., Fernandes, R., Vadeboncoeur, S.,
Kennedy, D., Cooley, K., Wong, R., Sagar, S., Sabri, E. & Fergusson, D.
2013. Soy, red clover, and isoflavones and breast cancer: A systematic review. PLoS
ONE 8: e81968.
Froyen,
E.B., Reeves, J.L.R., Mitchell, A.E. & Steinberg, F.M. 2009. Regulation of
phase II enzymes by genistein and daidzein in male and female Swiss Webster
mice. J. Med. Food 12(6): 1227-1237.
Fujioka,
M., Uehara, M., Wu, J., Adlercreutz, H., Suzuki, K., Kanazawa, K., Takeda, K.,
Yamada, K. & Ishimi, Y. 2004. Equol, a metabolite of daidzein, inhibits
bone loss in ovariectomized mice. J. Nutr. 134(10): 2623-2627.
Gaur,
T., Lengner, C.J., Hovhannisyan, H., Bhat, R.A., Bodine, P.V., Komm, B.S.,
Javed, A., van Wijnen, A.J., Stein, J.L., Stein, G.S. & Lian, J.B. 2005.
Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2
gene expression. J. Biol. Chem. 280(39): 33132-33140.
Ge,
Y., Chen, D., Xie, L. & Zhang, R. 2006. Enhancing effect of daidzein on the
differentiation and mineralization in mouse osteoblast-like MC3T3-E1 cells. Yakugaku
Zasshi 126(8): 651-656.
Giner,
M., Montoya, M.J., Vázquez, M.A., Miranda, C. & Pérez- Cano, R. 2013.
Differences in osteogenic and apoptotic genes between osteoporotic and
osteoarthritic patients. BMC Musculoskelet Disord 25: 41.
Glass,
D.A., Bialek, P., Ahn, J.D., Starbuck, M., Patel, M.S., Clevers, H., Taketo,
M.M., Long, F., McMahon, A.P., Lang, R.A. & Karsenty, G. 2005. Canonical
Wnt signaling in differentiated osteoblasts controls osteoclast
differentiation. Dev. Cell 8(5): 751-764.
Greenspan,
S.L., Perera, S., Nace, D., Zukowski, K.S., Ferchak, M.A., Lee, C.J., Nayak, S.
& Resnick, N.M. 2012. FRAX or fiction: Determining optimal screening
strategies for treatment of osteoporosis in residents in long-term care
facilities. J. Am. Geriatr. Soc. 60(4): 684-690.
Good,
C.R., O’Keefe, R.J., Puzas, J.E., Schwarz, E.M. & Rosier, R.N. 2002.
Immunohistochemistry study of receptor activator of nuclear kappa-B ligand
(RANK-L) in human osteolytic bone tumors. J. Surg. Oncol. 79(3):
174-179.
Hajirahimkhan,
A., Dietz, B.M. & Bolton, J.L. 2013. Botanical modulation of menopausal symptoms:
Mechanisms of action? Planta. Med. 79(7): 538-553.
Hughes,
D.E. & Boyce, B.F. 1998. Estrogen, transforming growth factor-beta, and the
regulation of bone metabolism in health and disease. The Endocrinologist 8:
55-61.
Hwang,
J.K., Min, K.H., Choi, K.H., Hwang, Y.C., Jeong, I.K., Ahn, K.J., Chung, H.Y.
& Chang, J.S. 2013. Bisphenol A reduces differentiation and stimulates
apoptosis of osteoclasts and osteoblasts. Life Sci. 93(9-11): 367-372.
Ibarreta,
D., Daxenberger, A. & Meyer, H.H. 2001. Possible health impact
of phytoestrogens and xenoestrogens in food. APMIS 109(3):
161-184.
Idrus,
R.B.H., Sainik, N.Q.A.V., Ansari, A.S., Zulfarina, M.S., Razali, R.A., Nordin,
A., Saim, A.B. & Naina-Mohamed, I. 2018. Ficus carica and bone
health: A systematic review. Sains Malaysiana 47(11): 2741-2755.
Jia,
T.L., Wang, H.Z., Xie, L.P., Wang, X.Y. & Zhang, R.Q. 2003. Daidzein
enhances osteoblast growth that may be mediated by increased bone morphogenetic
protein (BMP) production. Biochem. Pharmacol. 65(5): 709-715.
Jin,
D., Wu, X., Yu, H., Jiang, L., Zhou, P., Yao, X., Meng, J., Wang, L., Zhang, M.
& Zhang, Y. 2018. Systematic analysis of lncRNAs, mRNAs, circRNAs and
miRNAs in patients with postmenopausal osteoporosis. Am. J. Transl. Res. 10(5):
1498-1510.
Jou,
H.J., Wu, S.C., Chang, F.W., Ling, P.Y., Chu, K.S. & Wu, W.H. 2008. Effect
of intestinal production of equol on menopausal symptoms in women treated with
soy isoflavones. Int. J. Gynecol. Obstet. 102(1): 44-49.
Kanazawa,
A., Tsukada, S., Sekine, A., Tsunoda, T., Takahashi, A., Kashiwagi, A., Tanaka,
Y., Babazono, T., Matsuda, M., Kaku, K., Iwamoto, Y., Kawamori, R., Kikkawa,
R., Nakamura, Y. & Maeda, S. 2004. Association of the gene encoding
wingless-type mammary tumor virus integration-site family member 5B (WNT5B)
with type 2 diabetes. Am. J. Hum. Genet. 75(5): 832-843.
Kang,
J.S., Yoon, Y.D., Han, M.H., Han, S.B., Lee, K., Park, S.K. & Kim, H.M.
2007. Equol inhibits nitric oxide production and inducible
nitric oxide synthase gene expression through down regulating the activation of
Akt. Int. Immunopharmacol. 7(4): 491-499.
Kawamoto,
E.M., Gleichmann, M., Yshii, L.M., Lima Lde, S., Mattson, M.P. & Scavone,
C. 2012. Effect of activation of canonical Wnt signaling by the Wnt-3a protein
on the susceptibility of PC12 cells to oxidative and apoptotic insults. Braz.
J. Med. Biol. Res. 45(1): 58-67.
Kolios, L., Sehmisch,
S., Daub, F., Rack, T., Tezval, M., Stuermer, K.M. & Stuermer, E.K. 2009.
Equol but not genistein improves early metaphyseal fracture healing in
osteoporotic rats. Planta. Med. 75: 459-465.
Komori, T., Yagi, H.,
Nomura, S., Yamaguchi, A., Sasaki, K., Deguchi, K., Shimizu, Y., Bronson, R.T.,
Gao, Y.H., Inada, M., Sato, M., Okamoto, R., Kitamura, Y., Yoshiki, S. &
Kishimoto, T. 1997. Targeted disruption of Cbfa1 results in a complete lack of
bone formation owing to maturational arrest of osteoblasts. Cell 89(5):
755-764.
Kong, Y.Y., Boyle, W.J.
& Penninger, J.M. 1999. Osteoprotegerin ligand: A common link
between osteoclastogenesis, lymph node formation and lymphocyte
development. Immun. Cell. Biol .77(2): 188-193.
Kwon, Y. 2014. Effect of
soy isoflavones on the growth of human breast tumors: Findings from preclinical
studies. Food Sci. Nutr. 2(6): 613-622.
Lacey, D.L., Timms, E.,
Tan, H.L., Kelley, M.J., Dunstan, C.R., Burgess, T., Elliott, R.,
Colombero, A., Elliott, G., Scully, S., Hsu, H., Sullivan, J., Hawkins,
N., Davy, E., Capparelli, C., Eli, A., Qian, Y.X., Kaufman, S.,
Sarosi, I., Shalhoub, V., Senaldi, G., Guo, J., Delaney, J. &
Boyle, W.J. 1998. Osteoprotegerin ligand is a cytokine that regulates
osteoclast differentiation and activation. Cell 93(2): 165-176.
Lampe, J.W. 2003. Isoflavonoid
and lignan phytoestrogens as dietary biomarkers. J. Nutr. 133(Suppl
3): 956S-964S.
Lane, N.E. 2006.
Epidemiology, etiology, and diagnosis of osteoporosis. Am. J. Obstet.
Gynecol. 1949: S3-S11.
Lee, S.R., Ha, Y.C.,
Kang, H., Park, Y.G., Nam, K.W. & Kim, S.R. 2013. Morbidity and mortality
in Jeju residents over 50-years of age with hip fracture with mean 6-year
follow-up: A prospective cohort study. J. Korean Med. Sci. 28(7):
1089-1094.
Liu, D., Genetos, D.C.,
Shao, Y., Geist, D.J., Li, J., Ke, H.Z., Turner, C.H. & Duncan, R.L. 2008.
Activation of extracellular-signal regulated kinase (ERK1/2) by fluid shear is
Ca (2+) and ATP-dependent in MC3T3-E1 osteoblasts. Bone 42(4): 644-652.
Liu, C.G., Luo, Q.X.,
Ling, T.Y., Mo, Y.Y., Cheng, Z.L., Huang, S.G. & Mo, H. 2013. Effect of
erigeron breviscapus on the expression of OPG/RANKL/RANK in osteoblasts and pre
osteoclasts in vitro. Zhongguo Zhong Xi Yi Jie He Za Zhi 33:
1658-1664.
Liu, X., Jia, H. &
Xia, H. 2017. Reduction of intra-articular adhesion by topical application of
daidzein following knee surgery in rabbits. Afr. J. Tradit. Complement.
Altern. Med. 14: 265-271.
Marrian, G.F. &
Haslewood, G.A. 1932. Equol, a new inactive phenol isolated from the
ketohydroxyoestrin fraction of mares’ urine. Biochem. J. 26: 1227-1232.
Marriott, I. 2004.
Osteoblast responses to bacterial pathogens: A previously unappreciated role
for bone-forming cells in host defense and disease progression. Immunol.
Res. 30(3): 291-308.
Masilamani, M., Wei, J.
& Sampson, H.A. 2012. Regulation of the immune response by soybean
isoflavones. Immunol. Res. 54: 95-110.
Martin, T.J. & Sims,
N.A. 2005. Osteoclast-derived activity in the coupling of bone formation to
resorption. Trends Mol. Med. 11(2): 76-81.
Mense, S.M., Hei, T.K.,
Ganju, R.K. & Bhat, H.K. 2008. Phytoestrogens and breast cancer prevention:
Possible mechanisms of action. Environ. Health Perspect. 116(4):
426-433.
Messina, M.,
McCaskill-Stevens, W. & Lampe, J.W. 2006. Addressing the soy and breast
cancer relationship: Review, commentary, and workshop proceedings. J. Natl.
Cancer Inst. 98(18): 1275-1284.
Miao, Q., Li, J.G.,
Miao, S., Hu, N., Zhang, J. & Zhang, S. 2012. The bone-protective effect of
genistein in the animal model of bilateral ovariectomy: Roles of phytoestrogens
and PTH/ PTHR1 against post-menopausal osteoporosis. Int. J. Mol. Sci. 13:
56-70.
Michel, T., Halabalaki.
& Skaltsounis, A.L. 2013. New concepts, experimental approaches, and
dereplication strategies for the discovery of novel phytoestrogens from natural
sources. Planta Med. 79(7): 514-532.
Miura, M., Chen, X.D.,
Allen, M.R., Bi, Y., Gronthos, S., Seo, B.M., Lakhani, S., Flavell, R.A., Feng,
X.H., Robey, P.G., Young, M. & Shi, S. 2004. A crucial role of caspase-3 in
osteogenic differentiation of bone marrow stromal stem cells. J. Clin.
Invest. 114: 1704-1713.
Mizuno, A., Amizuka, N.,
Irie, K., Murakami, A., Fujise, N., Kanno, T., Sato, Y., Nakagawa, N., Yasuda,
H., Mochizuki, S., Gomibuchi, T., Yano, K., Shima, N., Washida, N., Tsuda, E.,
Morinaga, T., Higashio, K. & Ozawa, H. 1998. Severe osteoporosis in mice
lacking osteoclastogenesis inhibitory factor/osteoprotegerin. Biochem.
Biophys. Res. Commun. 247(3): 610-615.
Moreira, A.C., Silva,
A.M., Santos, M.S. & Sardão, V.A. 2014. Phytoestrogens as alternative
hormone replacement therapy in menopause: What is real, what is unknown. J.
Steroid Biochem. Mol. Biol. 143: 61-71.
Ohtomo, T., Uehara, M.,
Peñalvo, J.L., Adlercreutz, H., Katsumata, S.I., Suzuki, K., Takeda, K.,
Masuyama, R. & Ishimi, Y. 2008. Comparative activities of daidzein
metabolites, equol and O-desmethylangolensin, on bone mineral density and lipid
metabolism in ovariectomized mice and in osteoclast cell cultures. Eur. J.
Nutr. 47(5): 273-279.
Palacios, V.G.,
Robinson, L.J., Borysenko, C.W., Lehmann, T., Kalla, S.E. & Blair, H.C.
2005. Negative regulation of RANKL-induced osteoclastic differentiation in
RAW264.7 cells by estrogen and phytoestrogens. J. Biol. Chem. 280(14):
13720-13727.
Pandur, P., Maurus, D.
& Kuhl, M. 2002. Increasingly complex: New players enter the
Wnt signaling network. BioEssays 24(10): 881-884.
Paterni, I., Granchi, C.,
Katzenellenbogen, J.A. & Minutolo, F. 2014. Estrogen receptors
alpha (ERa) and beta (ERß): Subtype-selective ligands and
clinical potential. Steroids 90: 13-29.
Rietjen, I.M., Sotoca,
A.M., Vervoort, J. & Louisse, J. 2013. Mechanisms underlying the dualistic
mode of action of major soy isoflavones in relation to cell proliferation and
cancer risks. Mol. Nutr. Food Res. 57(1): 100-113.
Saika, M., Inoue, D.,
Kido, S. & Matsumoto, T. 2001. 17 beta-estradiol stimulates expression of
osteoprotegerin by a mouse stromal cell line, ST-2, via estrogen
receptor-alpha. Endocrinology 142(6): 2205-2212.
Saitoh, S., Sato, T.,
Harada, H. & Matsuda, T. 2004. Biotransformation of soy isoflavone
glycosides in laying hens: Intestinal absorption and preferential accumulation
into egg yolk of equol, a more estrogenic metabolite of daidzein. Biochim.
Biophys. Acta Gen. Subj. 1674(2): 122-130.
Seeman,
E. & Delmas, P.D. 2006. Bone quality-The material and structural basis of
bone strength and fragility. N. Engl. J. Med. 354(21): 2250-2261.
Setchell,
K.D.R., Brown, N.M. & Lydeking-Olsen, E. 2002. The clinical importance of
the metabolite equol-a clue to the effectiveness of soy and its isoflavones. J.
Nutr. 132(12): 3577-3584.
Setchell, K.D.
2001. Soy isoflavones-Benefits and risks from nature's selective
estrogen receptor modulators (SERMs). J. Am. Coll. Nutr. 20(5):
354S-362S.
Setchell,
K.R. & Clerici, C. 2010. Equol: History, chemistry, and formation. J.
Nutr. 3: 1355-1362.
Sims, N.A.
& Walsh, N.C. 2012. Intercellular cross-talk among bone cells: New factors
and pathways. Curr. Osteoporos. Rep. 10(2): 109-117.
Simonet,
W.S., Lacey, D.L., Dunstan, C.R., Kelley, M., Chang, M.S., Lüthy, R., Nguyen,
H.Q., Wooden, S., Bennett, L., Boone, T., Shimamoto, G., DeRose, M., Elliott,
R., Colombero, A., Tan, H.L., Trail, G., Sullivan, J., Davy, E., Bucay, N.,
Renshaw-Gegg L, Hughes, T.M., Hill, D., Pattison, W., Campbell, P., Sander, S.,
Van, G., Tarpley, J., Derby, P., Lee, R. & Boyle, W.J. 1997.
Osteoprotegerin: A novel secreted protein involved in the regulation of bone
density. Cell 89(2): 309-319.
Sliwiński,
L., Folwarczna, J., Nowińska, B., Cegieła, U., Pytlik, M.,
Kaczmarczyk-Sedlak, I., Trzeciak, H. & Trzeciak, H.I. 2009. A comparative
study of the effects of genistein, estradiol and raloxifene on the murine
skeletal system. Acta Biochim. Pol. 56(2): 261-270.
Smith, M.G.,
Dunkow, P.& Lang, D.M. 2004. Treatment of osteoporosis: Missed
opportunities in the Hospital fracture clinic. Ann. R. Coll. Surg. of Engl. 86(5):
344-346.
Sözen,
T., Özışık, L. & Başaran, N.Ç.
2017. An overview and management of osteoporosis. Eur. J. Rheumatol.
4(1): 46-56.
Srivastava, S., Toraldo,
G., Weitzmann, M.N., Cenci, S., Ross, F.P. & Pacifici, R. 2001.
Estrogen decreases osteoclast formation by down-regulating receptor
activator of NF-kappa B ligand (RANKL)-induced JNK activation.
J. Biol. Chem. 276(12): 8836-8840.
Stains, J.P.
& Civitelli, R. 2005. Cell-cell interactions in regulating osteogenesis
and osteoblast function. Birth Defects Res. C. Embryo Today 75(1):
72-80.
Streicher,
C., Heyny, A., Andrukhova, O., Haigl, B., Slavic, S., Schüler, C., Kollmann,
K., Kantner, I., Sexl, V., Kleiter, M., Hofbauer, L.C., Kostenuik, P.J. &
Erben, R.G. 2017. Estrogen regulates bone turnover by targeting RANKL
expression in bone lining cells. Sci. Rep. 7(1): 6460.
Strong,
A.L., Jiang, Q., Zhang, Q., Zheng, S., Boue, S.M., Elliott, S., Burow, M.E.,
Bunnell, B.A. & Wang, G. 2014. Design, synthesis, and osteogenic activity
of daidzein analogs on human mesenchymal stem cells. ACS Med. Chem. Lett. 5(2):
143-148.
Tamai, K.,
Semenov, M., Kato, Y., Spokony, R., Liu, C., Katsuyama, Y., Hess, F.,
Saint-Jeannet, J.P. & He, X. 2000. LDL receptor-related proteins in Wnt
signal transduction. Nature 407: 530-535.
Taylor,
J.A., Richter, C.A., Ruhlen, R.L. & vom Saal, F.S. 2011. Estrogenic
environmental chemicals and drugs: Mechanisms for effects on the developing
male urogenital system. J. Steroid Biochem. Mol. Biol. 127(1-2): 83-95.
Teitelbaum,
S.L. 2007. Osteoclasts: What do they do and how do they do it? Am. J.
Pathol. 170(2): 427-435.
Terpos, E.
2003. Soluble receptor activator of nuclear factor B ligand-osteoprotegerin
ratio predicts survival in multiple myeloma: Proposal for a novel prognostic
index. Blood 102(3): 1064-1069.
Theill,
L.E., Boyle, W.J. & Penninger, J.M. 2002. RANK-L and RANK: T cells, bone
loss, and mammalian evolution. Annu. Rev. Immunol. 20: 795-823.
Thirunavukkarasu,
K., Halladay, D.L., Miles, R.R., Yang, X., Galvin, R.J., Chandrasekhar, S.,
Martin, T.J. & Onyia, J.E. 2000. The osteoblast-specific transcription
factor Cbfa1 contributes to the expression of osteoprotegerin, a potent
inhibitor of osteoclast differentiation and function. J. Biol. Chem. 275(33):
25163-25172.
Thomas, P.
& Dong, J. 2006. Binding and activation of the seven-transmembrane estrogen
receptor GPR30 by environmental estrogens: A potential novel mechanism of
endocrine disruption. J. Steroid Biochem. Mol. Biol. 102(1-5): 175-179.
Törmälä, R.,
Appt, S., Clarkson, T.B., Mueck, A.O., Seeger, H., Mikkola, T.S. &
Ylikorkala, O. 2008. Impact of soy supplementation on sex steroids and vascular
inflammation markers in postmenopausal women using tibolone: Role of equol
production capability. Climacteric 11(5): 409-415.
Tousen, Y.,
Wolber, F.M., Chua, W.H., Tadaishi, M., Ishimi, Y. & Kruger, M.C. 2014.
Effects of daidzein and kiwifruit on bone mineral density and equol production
in ovariectomised rats. Int. J. Food Sci. Nutr. 65(3): 360-367.
Tousen, Y.,
Ezaki, J., Fujii, Y., Ueno, T., Nishimuta, M. & Ishimi, Y. 2011. Natural
S-equol decreases bone resorption in postmenopausal, non-equol-producing
Japanese women: A pilot randomized, placebo-controlled trial. Menopause 18(5):
563-574.
Tsuda, E.,
Goto, M., Mochizuki, S.I., Yano, K., Kobayashi, F., Morinaga, T. & Higashio,
K. 1997. Isolation of a novel cytokine from human fibroblasts that specifically
inhibits osteoclastogenesis. Biochem. Biophys. Res. Commun. 234(1):
137-142.
Vatanparast,
H. & Chilibeck, P.D. 2007. Does the effect of soy phytoestrogens on bone in
postmenopausal women depend on the equol-producing phenotype? Nutr. Rev. 65(6):
294-299.
Veeman,
M.T., Axelrod, J.D. & Moon, R.T. 2003. A second canon: Functions and
mechanisms of β-catenin-independent Wnt signaling. Developmental Cell 5(3):
367-377.
Van Pottelbergh,
I., Goemaere, S., Zmierczak, H. & Kaufman, J.M. 2004. Perturbed sex steroid
status in men with idiopathic osteoporosis and their sons. J. Clin.
Endocrinol. Metab. 89(10): 4949-4953.
Vitale,
D.C., Piazza, C., Melilli, B., Drago, F. & Salomone, S. 2013. Isoflavones:
Estrogenic activity, biological effect and bioavailability. Eur J Drug Metab
Pharmacokinet 38(1): 15-25.
Wade, S.W.,
Strader, C., Fitzpatrick, L.A., Anthony, M.S. & O’Malley, C.D. 2014.
Estimating prevalence of osteoporosis: Examples from industrialized countries. Arch.
Osteoporos. 9: 182.
Wang, X.,
Wu, J., Chiba, H., Umegaki, K., Yamada, K. & Ishimi, Y. 2003. Puerariae
radix prevents bone loss in ovariectomized mice. J. Bone Miner. Metab. 21(5):
268-275.
Watkins,
A.J., Lucas, E.S., Wilkins, A., Cagampang, F.R. & Fleming, T.P. 2011.
Maternal periconceptional and gestational low protein diet affects mouse
offspring growth, cardiovascular and adipose phenotype at 1 year of age. PLoS
ONE 6: e28745.
Watts, N.B.
1999. Postmenopausal osteoporosis. Obstet. Gynecol. Surv. 54(8):
532-538.
Williamson-Hughes,
P.S., Flickinger, B.D., Messina, M.J. & Empie, M.W. 2006. Isoflavone
supplements containing predominantly genistein reduce hot flash symptoms: A
critical review of published studies. Menopause 13(5): 831-839.
Wong, K.H., Li, G.Q., Li, K.M., Razmovski-Naumovski, V. &
Chan, K. 2011. Kudzu root: Traditional uses and potential medicinal benefits in
diabetes and cardiovascular diseases. J. Ethnopharmacol. 134(3):
584-607.
Yahaya, M.F., Zainodin,
A., Pupathy, R., Min, E.O.H., Bakar, N.H.A., Zamri, N.A., Ismail, H. & Mohd
Ramli, E.S. 2018. The effect of palm tocotrienol on surface osteoblast and
osteoclast in excess glucocorticoid osteoporotic rat model. Sains Malaysiana 47(11): 2731-2739.
Yasuda, H., Shima, N.,
Nakagawa, N., Yamaguchi, K., Kinosaki, M., Mochizuki, S., Tomoyasu, A., Yano,
K., Goto, M., Murakami, A., Tsuda, E., Morinaga, T., Higashio, K., Udagawa, N.,
Takahashi, N. & Suda, T. 1998. Osteoclast differentiation factor is a
ligand for osteoprotegerin/ osteoclastogenesis inhibitory factor and is
identical to TRANCE/RANKL. Proc. Natl. Acad. Sci. USA 95(7): 3597-3602.
Yuan, J.P., Wang, J.H.
& Liu, X. 2007. Metabolism of dietary soy isoflavones to equol by human
intestinal microflora - Implications for health. Mol. Nutr. Food Res. 51(7):
765-781.
Yoshikata, R., Myint,
K.Z.Y. & Ohta, H. 2018. Effects of equol supplement on bone and cardiovascular
parameters in middle-aged Japanese women: A prospective observational study. J.
Altern. Complement. Med. 24(7): 701-708.
Younes, M.H.N. 2011.
Estrogen receptor. Pathol. Lab. Med. 135: 63-66.
Zhang, H.P., Zhao, J.H.,
Yu, H.X. & Guo, D.X. 2016. Genistein ameliorated endothelial nitric oxidase
synthase uncoupling by stimulating sirtuin-1 pathway in ox-LDL- injured HUVECs. Environ. Toxicol. Pharmacol. 42: 118-124.
Zhang, J., Dai, J., Qi,
Y., Lin, D.L., Smith, P., Strayhorn, C., Mizokami, A., Fu, Z., Westman, J.
& Keller, E.T. 2001. Osteoprotegerin inhibits prostate cancer-induced
osteoclastogenesis and prevents prostate tumor growth in the bone. J. Clin.
Invest. 107(10): 1235-1244.
*Corresponding
author; email: drsrijit@gmail.com
|