Phytoestrogens directly inhibit TNF-α-induced bone resorption in RAW264.7 cells by suppressing c-fos-induced NFATc1 expression

Journal of Cellular Biochemistry

Volumn 112, Issue 2, 2011, Pages 476-487

  Karieb, Sahar ^a   Fox, Simon W ^a  

^a UNIVERSITY OF PLYMOUTH   (United Kingdom)

Author keywords

NFATc1; osteoclast; phytoestrogens; TNF

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; CASPASE 3; CASPASE 7; COUMESTROL; DAIDZEIN; DENDRITIC CELL SPECIFIC TRANSMEMBRANE PROTEIN; FULVESTRANT; GENISTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PHYTOESTROGEN; PROTEIN C FOS; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL FUSION; CELL NUCLEUS; CELL VIABILITY; CONCENTRATION (PARAMETERS); DRUG EFFECT; DRUG MECHANISM; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; GENE EXPRESSION; MONOCYTE; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN TRANSPORT;

ANIMALS; BONE RESORPTION; CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; COUMESTROL; GENISTEIN; ISOFLAVONES; MICE; NFATC TRANSCRIPTION FACTORS; PHYTOESTROGENS; POLYMERASE CHAIN REACTION; PROTO-ONCOGENE PROTEINS C-FOS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79251647528     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22935     Document Type: Article

References (47)

1. Aggarwal BB, Shishodia S,. 2006. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem Pharmacol 71: 1397-1421.
2. Alekel DL, Germain AS, Peterson CT, Hanson KB, Stewart JW, Toda T,. 2000. Isoflavone-rich soy protein isolate attenuates bone loss in the lumbar spine of perimenopausal women. Am J Clin Nutr 72: 844-852.
3. Asagiri M, Sato K, Usami T, Ochi S, Nishina H, Yoshida H, Morita I, Wagner EF, Mak TW, Serfling E, Takayanagi H,. 2005. Autoamplification of NFATc1 expression determines its essential role in bone homeostasis. J Exp Med 202: 1261-1269.
4. Atkinson C, Compston JE, Day NE, Dowsett M, Bingham SA,. 2004. The effects of phytoestrogen isoflavones on bone density in women: A double-blind, randomized, placebo-controlled trial. Am J Clin Nutr 79: 326-333.
5. Bandyopadhyay S, Lion J-M, Mentaverri R, Ricupero DA, Kamel S, Romero JR, Chattopadhyay N,. 2006. Attenuation of osteoclastogenesis and osteoclast function by apigenin. Biochem Pharmacol 72: 184-197.
6. Barnabe C, Hanley DA,. 2009. Effect of tumor necrosis factor alpha inhibition on bone density and turnover markers in patients with rheumatoid arthritis and spondyloarthropathy. Semin Arthritis Rheum 39: 116-122.
7. Bernard-Poenaru O, Roux C, Blanqué R, Gardner C, de Vernejoul MC, Cohen-Solal ME,. 2001. Bone-resorbing cytokines from peripheral blood mononuclear cells after hormone replacement therapy: A longitudinal study. Osteoporos Int 12: 769-776.
8. Boyce BF, Li P, Yao Z, Zhang Q, Badell IR, Schwarz EM, O'Keefe RJ, Xing L,. 2005. TNF-alpha and pathologic bone resorption. Keio J Med 54: 127-131.
9. Burstone MS,. 1958. Histochemical demonstration of acid phosphatases with naphthol AS-phosphates. J Natl Cancer I 21: 523-539.
10. Cenci S, Weitzmann MN, Roggia C, Namba N, Novack D, Woodring J, Pacifici R,. 2000. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-α. J Clin Invest 106: 1229-1237.
11. Chen X, Garner SC, Quarles LD, Anderson JJB,. 2003a. Effects of genistein on expression of bone markers during MC3T3-E1 osteoblastic cell differentiation. J Nutr Biochem 14: 342-349.
12. Chen Y-M, Ho SC, Lam SSH, Ho SSS, Woo JLF,. 2003b. 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: 4740-4747.
13. Cole Z, Dennison E, Cooper C,. 2008. Update on the treatment of post-menopausal osteoporosis. Br Med Bull 86: 129-143.
14. D'Amelio P, Grimaldi A, Pescarmona GP, Tamone C, Roato I, Isaia G,. 2004. Spontaneous osteoclast formation from peripheral blood mononuclear cells in postmenopausal osteoporosis. FASEB J 19: 410-412.
15. Evans K, Fox S,. 2007. Interleukin-10 inhibits osteoclastogenesis by reducing NFATc1 expression and preventing its translocation to the nucleus. BMC Cell Biol 8: 4.
16. Fox SW, Evans KE, Lovibond AC,. 2008. Transforming growth factor-β enables NFATc1 expression during osteoclastogenesis. Biochem Biophys Res Commun 366: 123-128.
17. Fuller K, Murphy C, Kirstein B, Fox SW, Chambers TJ,. 2002. TNF-α potently activates osteoclasts, through a direct action independent of and strongly synergistic with RANKL. Endocrinology 143: 1108-1118.
18. Gallagher JC, Satpathy R, Rafferty K, Haynatzka V,. 2004. The effect of soy protein isolate on bone metabolism. Menopause 11: 290-298.
19. Gao YH, Yamaguchi M,. 2000. Suppressive effect of genistein on rat bone osteoclasts: Involvement of protein kinase inhibition and protein tyrosine phosphatase activation. Int J Mol Med 5: 261-267.
20. Gao YH, Yamouguchi M,. 1999. Inhibitory effect of genistein on osteoclast-like cell formation in mouse marrow cultures. Biochem Pharmacol 58: 767-772.
21. Garcia Palacios V, Robinson LJ, Borysenko CW, Lehmann T, Kalla SE, Blair HC,. 2005. Negative regulation of RANKL-induced osteoclastic differentiation in RAW264.7 cells by estrogen and phytoestrogens. J Biol Chem 280: 13720-13727.
22. Gardner CD, Oelrich B, Liu JP, Feldman D, Franke AA, Brooks JD,. 2009. Prostatic soy isoflavone concentrations exceed serum levels after dietary supplementation. Prostate 69: 719-726.
23. Grassi F, Tell G, Robbie-Ryan M, Gao Y, Terauchi M, Yang X, Romanello M, Jones DP, Weitzmann MN, Pacifici R,. 2007. Oxidative stress causes bone loss in estrogen-deficient mice through enhanced bone marrow dendritic cell activation. Proc Natl Acad Sci USA 104: 15087-15092.
24. Grigoriadis AE, Wang Z-Q, Cecchini MG, Hofstetter W, Felix R, Fleisch HA, Wagner EF,. 1994. c-Fos: A key regulator of osteoclast-macrophage lineage determination and bone remodeling. Science 266: 443-448.
25. Horiuchi T, Onouchi T, Takahashi M, Ito H, Orimo H,. 2000. Effect of soy protein on bone metabolism in postmenopausal Japanese women. Osteoporo Int 11: 721-724.
26. Jeng Y-J, Kochukov M, Watson C,. 2009. Membrane estrogen receptor-α-mediated nongenomic actions of phytoestrogens in GH3/B6/F10 pituitary tumor cells. J Mol Sig 4: 2-13.
27. Kim MK, Chung BC, Yu VY, Nam JH, Lee HC, Huh KB, Lim SK,. 2002. Relationships of urinary phyto-oestrogen excretion to BMD in postmenopausal women. Clin Endocrinol 56: 321-328.
28. Kim H, Kim IY, Lee SY, Jeong D,. 2006. Bimodal actions of reactive oxygen species in the differentiation and bone-resorbing functions of osteoclasts. FEBS Lett 580: 5661-5665.
29. Komine M, Kukita A, Kukita T, Ogata Y, Hotokebuchi T, Kohashi O,. 2001. Tumor necrosis factor-α cooperates with receptor activator of nuclear factor KB ligand in generation of osteoclasts in stromal cell-depleted rat bone marrow cell culture. Bone 28: 474-483.
30. Kudo O, Fujikawa Y, Itonaga I, Sabokbar A, Torisu T, Athanasou NA,. 2002. Proinflammatory cytokine (TNFalpha/IL-1alpha) induction of human osteoclast formation. J Pathol 198: 220-227.
31. Kukita T, Wada N, Kukita A, Kakimoto T, Sandra F, Toh K, Nagata K, Iijima T, Horiuchi M, Matsusaki H, Hieshima K, Yoshie O, Nomiyama H,. 2004. RANKL-induced DC-STAMP is essential for osteoclastogenesis. J Exp Med 200: 941-946.
32. Li B, Yu S,. 2003. Genistein prevents bone resorption diseases by inhibiting bone resorption and stimulating bone formation. Biol Pharm Bull 26: 780-786.
33. Lodder MC, van Pelt PA, Lems WF, Kostense PJ, Koks CH, Dijkmans BA,. 2003. Effects of high dose IV pamidronate on disease activity and bone metabolism in patients with active RA: A randomized, double-blind, placebo-controlled trial. J Rheumatol 30: 2080-2081.
34. Matsuo K, Galson DL, Zhao C, Peng L, Laplace C, Wang KZQ, Bachler MA, Amano H, Aburatani H, Ishikawa H, Wagner EF,. 2004. Nuclear Factor of Activated T-cells (NFAT) rescues osteoclastogenesis in precursors lacking c-Fos. J Biol Chem 279: 26475-26480.
35. Mei J, Yeung SSC, Kung AWC,. 2001. High dietary phytoestrogen intake is associated with higher bone mineral density in postmenopausal but not premenopausal women. J Clin Endocrinol Metab 86: 5217-5221.
36. Miyamoto T,. 2006. The dendritic cell-specific transmembrane protein DC-STAMP is essential for osteoclast fusion and osteoclast bone-resorbing activity. Mod Rheumatol 16: 341-342.
37. Morgenstern JP, Land H,. 1990. Advanced mammalian gene transfer: High titer retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res 18: 3587-3596.
38. Morton MS, Arisaka O, Miyake N, Morgan LD, Evans BAJ,. 2002. Phytoestrogen concentrations in serum from Japanese men and women over forty years of age. J Nutr 132: 3168-3171.
39. Rassi CM, Lieberherr M, Chaumaz G, Pointillart A, Cournot G,. 2002. Down-regulation of osteoclast differentiation by daidzein via caspase 3. J Bone Miner Res 17: 630-638.
40. Robinson LJ, Yaroslavskiy BB, Griswold RD, Zadorozny EV, Guo L, Tourkova IL, Blair HC,. 2009. 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 315: 1287-1301.
41. Roggia C, Gao Y, Cenci S, Weitzmann MN, Toraldo G, Isaia G, Pacifici R,. 2001. Up-regulation of TNF-producing T cells in the bone marrow: A key mechanism by which estrogen deficiency induces bone loss in vivo. Proc Natl Acad Sci USA 98: 13960-13965.
42. Uchiyama S, Yamaguchi M,. 2007. Genistein and zinc synergistically stimulate apoptotic cell death and suppress RANKL signaling-related gene expression in osteoclastic cells. J Cell Biochem 101: 529-542.
43. 41Ca methodology. J Clin Endocrinol Metab 94: 3798-3805.
44. Weitzmann MN, Pacifici R,. 2007. T cells: Unexpected players in the bone loss induced by estrogen deficiency and in basal bone homeostasis. Ann N Y Acad Sci 1116: 360-375.
45. Wu J, Oka J, Tabata I, Higuchi M, Toda T, Fuku N, Ezaki J, Sugiyama F, Uchiyama S, Yamada K, Ishimi Y,. 2006. Effects of isoflavone and exercise on BMD and fat mass in postmenopausal Japanese women: A 1-year randomized placebo-controlled trial. J Bone Miner Res 21: 780-789.
46. Yagi M, Ninomiya K, Fujita N, Suzuki T, Iwasaki R, Morita K, Hosogane N, Matsuo K, Toyama Y, Suda T, Miyamoto T,. 2007. Induction of DC-STAMP by alternative activation and downstream signaling mechanisms. J Bone Miner Res 22: 992-1001.
47. Zhang Q, Badell IR, Schwarz EM, Boulukos KE, Yao Z, Boyce BF, Xing L,. 2005. Tumor necrosis factor prevents alendronate-induced osteoclast apoptosis in vivo by stimulating Bcl-xL expression through Ets-2. Arthritis Rheu 52: 2708-2718.