Homocysteine alters the osteoprotegerin/RANKL system in the osteoblast to promote bone loss: Pivotal role of the redox regulator forkhead O1

Free Radical Biology and Medicine

Volumn 61, Issue , 2013, Pages 72-84

  Vijayan, Viji ^a   Khandelwal, Mayuri ^a   Manglani, Kapil ^a   Singh, Rajiv Ranjan ^a   Gupta, Sarika ^a   Surolia, Avadhesha ^a,b  

^a NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

^b INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

c Jun MAP kinase; Forkhead box; Free radicals; Osteoprotegerin; p38; Protein phosphatase 2 A; Receptor activator of nuclear factor B ligand

Indexed keywords

COLONY STIMULATING FACTOR 1; GAMMA INTERFERON; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HOMOCYSTEINE; INSULIN; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; METHIONINE; MITOGEN ACTIVATED PROTEIN KINASE P38; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR FKHR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HYPERHOMOCYSTEINEMIA; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; OVARIECTOMY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RAT; SIGNAL TRANSDUCTION;

RATTUS;

EID: 84877040655     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.03.004     Document Type: Article

References (39)

1. B.F. Boyce, L. Xing, W. Shakespeare, Y. Wang, D. Dalgarno, J. Iuliucci, and T. Sawyer Regulation of bone remodeling and emerging breakthrough drugs for osteoporosis and osteolytic bone metastases Kidney Int. Suppl. 2003 2 5
2. B.F. Boyce, and L. Xing Biology of RANK, RANKL and osteoprotegerin Arthritis Res. Ther. Suppl. 91 S1 2007
3. L.C. Hofbauer, and M. Schoppet Clinical implications of the osteoprotegerin/RANKL/RANK system for bone and vascular diseases JAMA 292 2004 490 495 (Pubitemid 38988958)
4. B.F. Boyce, and L. Xing Functions of RANKL/RANK/OPG in bone modelling and remodelling Arch. Biochem. Biophys. 473 2008 139 146
5. M. Almeida, L. Han, M. Martin-Millan, L.I. Plotkin, S.A. Stewart, and P.K. Roberson Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids J. Biol. Chem. 282 2007 27285 27297 (Pubitemid 47501960)
6. M. Herrmann, B. Wildemann, L. Claes, S. Klohs, M. Ohnmacht, and O. Taban-Shomal Experimental hyperhomocysteinemia reduces bone quality in rats Clin. Chem. 53 2007 1455 1461 (Pubitemid 47206341)
7. M. Herrmann, A. Tami, B. Wildemann, M. Wolny, A. Wagner, and H. Schorr Hyperhomocysteinemia induces a tissue specific accumulation of homocysteine in bone by collagen binding and adversely affects bone Bone 44 2009 467 475
8. R. Thaler, M. Agsten, S. Spitzer, E.P. Paschalis, H. Karlic, K. Klaushofer, and F. Varga Homocysteine suppresses the expression of the collagen cross-linker lysyl oxidase involving IL-6, Fli1, and epigenetic DNA methylation J. Biol. Chem. 286 2011 5578 5588
9. E. Ambrogini, M. Almeida, M. Millan, J. Paik, R. Depinho, and L. Han FOXO-mediated defense against oxidative stress in osteoblasts is indispensable for skeletal homeostasis in mice Cell Metab. 11 2010 136 157
10. E.L. Greer, and A. Brunet FOXO transcription factors at the interface between longevity and tumor suppression Oncogene 24 2005 7410 7425 (Pubitemid 41637981)
11. M.C. Wang, D. Bohmann, and H. Jasper JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signalling Cell 121 2005 115 125
12. D.A. Salih, and A. Brunet FOXO transcription factors in the maintenance of cellular homeostasis during aging Curr. Opin. Cell Biol. 20 2008 126 136
13. A. Horst, and B.M. Burgering Stressing the role of FOXO proteins in life span and disease Nat. Rev. Mol. Cell Biol. 8 2007 440 450 (Pubitemid 46809159)
14. D. Marinkovic, X. Zhang, S. Yalcin, J.P. Luciano, C. Brugnara, T. Huber, and S. Ghaffari FOXO3 is required for the regulation of oxidative stress in erythropoiesis J. Clin. Invest. 117 2007 2133 2144 (Pubitemid 47219558)
15. S. Yang, H. Xu, S. Yu, H. Cao, J. Fan, C. Ge, R.T. Fransceshi, H.H. Dong, and G. Xio FOXO1 mediates insulin-like growth factor 1 (IGF-1)/insulin regulation of osteocalcin expression by antagonizing Runx2 in osteoblasts J. Biol. Chem. 286 2011 19149 19158
16. H. Okhawa, N. Oshishi, and K. Yag Assay of lipid peroxides in animal tissues by thiobarbituric acid reaction Anal. Biochem. 95 1979 351 357
17. S. Ugi, T. Imamura, H. Maegawa, K. Egava, T. Yoshizaki, and K. Shi Protein phosphatase 2A negatively regulates insulin metabolic signalling pathway by inhibiting AKT (protein kinase B) activity in 3T3-L1 adipocytes 24 2004 8778 8789
18. L. Yan, V.A. Lavin, L.R. Moser, Q. Cui, C. Kanies, and E. Yang PP2A regulates the pro-apoptotic activity of FOXO1 J. Biol. Chem. 283 2008 7411 7420
19. M. Ferron, J. Wei, T. Yoshizawa, A. Del Fattore, R.A. DePinho, and A. Teti Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism Cell 142 2010 296 308
20. K. Fulzele, R.C. Riddle, D.J. DiGirolamo, X. Cao, C. Wan, D. Chen, M.C. Faugere, S. Aja, M.A. Hussain, J.C. Brüning, and T.L. Clemens Insulin receptor signalling in osteoblasts regulates post natal bone acquisition and body composition Cell 142 2010 309 319
21. A.M. Silverstein, C.A. Barrow, A.J. Davis, and M.C. Mumby Actions of PPA on the MAP kinase pathway and apoptosis are regulated by distinct regulatory subunits Proc. Natl. Acad. Sci. USA 99 2002 4221 4226 (Pubitemid 34285967)
22. A. Brunet, A. Bonni, M.J. Zigmond, M.Z. Lin, P. Juo, L.S. Hu, M.J. Anderson, K.C. Arden, J. Blenis, and M.E. Greenberg AKT promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor Cell 96 1999 857 868 (Pubitemid 29165088)
23. C.E. Zhang, Q. Tian, W. Wei, J.H. Peng, G.P. Liu, X.W. Zhou, Q. Wang, D.W. Wang, and J.Z. Wang Homocysteine induces Tau phosphorylation by inactivating protein phosphatase 2A in rat hippocampus Neurobiol. Aging 29 2007 1654 1665
24. S.A. Blaise, E. Nedelec, H. Schroeder, J. Alberto, C. Bossenmever-Pouries, and J. Gueant Gestational vitamin B deficiency leads to homocysteine associated brain apoptosis and alters neurobehavioural development in rats Am. J. Pathol. 170 2007 667 669
25. F. Corallini, C. Celeghini, E. Rimondi, M. Iasio, A. Gonelli, P. Secchiero, and G. Zauli TRAIL downregulates the release of osteoprotegerin by primary cells J. Cell. Physiol. 226 2011 2279 2286
26. T. Nakashima, Y. Kobayashi, S. Yamasaki, A. Kawakami, K. Eguchi, and H. Sasaki Protein expression and functional difference of membrane bound and soluble receptor activator of NF-κB ligand: modulation of the expression by osteotropic factors and cytokines Biochem. Biophys. Res. Commun. 275 2000 768 775
27. F. Ikeda, T. Matsubara, T. Tsurukai, K. Hata, R. Nishimura, and T. Yoneda JNK/c-Jun signaling mediates an anti-apoptotic effect of RANKL in osteoclasts J. Bone Miner. Res. 23 2008 907 911
28. M.S. Nenseter, T. Ueland, K. Retterstol, E. Storm, M.S. Lars Morkrid, and S. Landaas Dysregulated RANK ligand/RANK axis in hyperhomocysteinemic subjects: effect of treatment with vitamins Stroke 40 2009 241 247
29. L. Ginaldi, and M.C. Di Benedetto De Martinis, M. Osteoporosis, inflammation and aging Immun. Ageing 2 2005 14 18
30. Y. Gao, F. Grassi, M.R. Ryan, M. Terauchi, K. Page, X. Yang, M.N. Weitzmann, and R. Pacifici IFN-gamma stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation J. Clin. Invest. 117 2007 122 132 (Pubitemid 46048459)
31. A.C. Hirbe, O. Uluçkan, E.A. Morgan, M.C. Eagleton, J.L. Prior, and D. Piwnica-Worms Granulocyte colony-stimulating factor enhances bone tumor growth in mice in an osteoclast-dependent manner Blood 109 2006 3424 3431
32. C.R. Bebbington, and G.T. Yarranton Methods of treating bone loss disorders using GM-CSF antagonist U.S. Patent Application Publication 0181020A1 2009
33. D.H. Fine, K. Markowitz, D. Furgang, K. Fairlie, J. Ferrandiz, and C. Nasri Macrophage inflammatory protein-1α: a salivary biomarker of bone loss in a longitudinal cohort study of children at risk for aggressive periodontal disease? J Periodontol 80 2009 106 113
34. K. Fuller, J.M. Owens, C.J. Jagger, A. Wilson, R. Moss, and T.J. Chambers Macrophage colony-stimulating factor stimulates survival and chemotactic behavior in isolated osteoclasts J. Exp. Med. 178 1993 1733 1740
35. Y.Y. Kong, H. Yoshida, I. Sarosi, H.L. Tan, E. Timms, and C. Capparelli OPG is a key regulator of osteoclastogenesis, lymphocyte development and lymph node organogenesis Nature 397 1999 315 323
36. K. Henriksen, G. Karsdal, J. Delaisse, and M. Engsig RANKL and vascular endothelial growth factor (VEGF) induce osteoclast chemotaxis through an ERK1/2-dependent mechanism J. Biol. Chem. 278 2003 48745 48753 (Pubitemid 41079516)
37. L.E. Theill, W.J. Boyle, and J.M. Penninger RANK ligand and RANK: T cells, bone loss, and mammalian evolution Annu. Rev. Immunol. 20 2002 795 823 (Pubitemid 34293440)
38. T. Nakashima, and H. Takayanagi Osteoimmunology: crosstalk between the immune and bone systems J. Clin. Immunol. 29 2009 555 567
39. A. Karube-Harada, N. Sugino, S. Kashida, S. Takiguchi, H. Takayama, and Y. Yamagata Induction of manganese superoxide dismutase by tumour necrosis factor-alpha in human endometrial stromal cells Mol. Hum. Reprod. 7 2001 1065 1072 (Pubitemid 33040970)