Apolipoprotein E inhibits osteoclast differentiation via regulation of c-Fos, NFATc1 and NF-κB

Experimental Cell Research

Volumn 319, Issue 4, 2013, Pages 436-446

  Kim, Woo Shin ^a   Kim, Hyung Joon ^a   Lee, Zang Hee ^a   Lee, Youngkyun ^b   Kim, Hong Hee ^a  

^a Seoul National University   (South Korea)

^b Kyungpook National University   (South Korea)

Author keywords

Apolipoprotein E; C Fos; NF B; NFATc1; Osteoclast differentiation

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; APOLIPOPROTEIN E; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEIN C FOS; TRANSCRIPTION FACTOR NFAT; NFATC1 PROTEIN, MOUSE; RECOMBINANT PROTEIN;

ARTICLE; CELL FUSION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENETIC TRANSDUCTION; MOLECULAR CLONING; OSTEOCLAST; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; MOUSE; ONCOGENE; PHYSIOLOGY;

ANIMALS; APOLIPOPROTEINS E; CELL DIFFERENTIATION; CELLS, CULTURED; DOWN-REGULATION; GENE EXPRESSION REGULATION; GENES, FOS; MICE; NF-KAPPA B; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; RANK LIGAND; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

MLCS; MLOWN;

EID: 84875542865     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.12.004     Document Type: Article

References (51)

1. Willnow T.E. The low-density lipoprotein receptor gene family: multiple roles in lipid metabolism. J. Mol. Med. (Berl) 1999, 77:306-315.
2. Fazio S., Linton M.F. Mouse models of hyperlipidemia and atherosclerosis. Front. Biosci. 2001, 6:D515-525.
3. Schneider J.G., Yang Z., Chakravarthy M.V., Lodhi I.J., Wei X., Turk J., Semenkovich C.F. Macrophage fatty-acid synthase deficiency decreases diet-induced atherosclerosis. J. Biol. Chem. 2010, 285:23398-23409.
4. Dove D.E., Linton M.F., Fazio S. ApoE-mediated cholesterol efflux from macrophages: separation of autocrine and paracrine effects. Am. J. Physiol. Cell Physiol. 2005, 288:C586-592.
5. Zerbinatti C.V., Mayer L.P., Audet R.G., Dyer C.A. Apolipoprotein E is a putative autocrine regulator of the rat ovarian theca cell compartment. Biol. Reprod. 2001, 64:1080-1089.
6. H.T. Gan, M. Tham, S. Hariharan, S. Ramasamy, Y.H. Yu, S. Ahmed, Identification of ApoE as an autocrine/paracrine factor that stimulates neural stem cell survival via MAPK/ERK signaling pathway, J. Neurochem. 117 565-578.
7. Laskowitz D.T., Lee D.M., Schmechel D., Staats H.F. Altered immune responses in apolipoprotein E-deficient mice. J. Lipid Res. 2000, 41:613-620.
8. Suda T., Takahashi N., Udagawa N., Jimi E., Gillespie M.T., Martin T.J. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr. Rev. 1999, 20:345-357.
9. Boyle W.J., Simonet W.S., Lacey D.L. Osteoclast differentiation and activation. Nature 2003, 423:337-342.
10. Teitelbaum S.L. Bone resorption by osteoclasts. Science 2000, 289:1504-1508.
11. Lam J., Takeshita S., Barker J.E., Kanagawa O., Ross F.P., Teitelbaum S.L. TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J. Clin. Invest. 2000, 106:1481-1488.
12. Takayanagi H. Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat. Rev. Immunol. 2007, 7:292-304.
13. Grigoriadis A.E., Wang Z.Q., Cecchini M.G., Hofstetter W., Felix R., Fleisch H.A., Wagner E.F. c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling. Science 1994, 266:443-448.
14. Takayanagi H., Kim S., Koga T., Nishina H., Isshiki M., Yoshida H., Saiura A., Isobe M., Yokochi T., Inoue J., Wagner E.F., Mak T.W., Kodama T., Taniguchi T. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev. Cell 2002, 3:889-901.
15. Miyazaki T., Katagiri H., Kanegae Y., Takayanagi H., Sawada Y., Yamamoto A., Pando M.P., Asano T., Verma I.M., Oda H., Nakamura K., Tanaka S. Reciprocal role of ERK and NF-kappaB pathways in survival and activation of osteoclasts. J. Cell Biol. 2000, 148:333-342.
16. Rao A., Luo C., Hogan P.G. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 1997, 15:707-747.
17. Hirotani H., Tuohy N.A., Woo J.T., Stern P.H., Clipstone N.A. The calcineurin/nuclear factor of activated T cells signaling pathway regulates osteoclastogenesis in RAW264.7 cells. J. Biol. Chem. 2004, 279:13984-13992.
18. Teitelbaum S.L., Ross F.P. Genetic regulation of osteoclast development and function. Nat. Rev. Genet. 2003, 4:638-649.
19. Hayman A.R. Tartrate-resistant acid phosphatase (TRAP) and the osteoclast/immune cell dichotomy. Autoimmunity 2008, 41:218-223.
20. Matsumoto M., Kogawa M., Wada S., Takayanagi H., Tsujimoto M., Katayama S., Hisatake K., Nogi Y. Essential role of p38 mitogen-activated protein kinase in cathepsin K gene expression during osteoclastogenesis through association of NFATc1 and PU.1. J. Biol. Chem. 2004, 279:45969-45979.
21. Nemeth K., Schoppet M., Al-Fakhri N., Helas S., Jessberger R., Hofbauer L.C., Goettsch C. The role of osteoclast-associated receptor in osteoimmunology. J. Immunol. 2011, 186:13-18.
22. Yagi M., Miyamoto T., Sawatani Y., Iwamoto K., Hosogane N., Fujita N., Morita K., Ninomiya K., Suzuki T., Miyamoto K., Oike Y., Takeya M., Toyama Y., Suda T. DC-STAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cells. J. Exp. Med. 2005, 202:345-351.
23. Lee S.H., Rho J., Jeong D., Sul J.Y., Kim T., Kim N., Kang J.S., Miyamoto T., Suda T., Lee S.K., Pignolo R.J., Koczon-Jaremko B., Lorenzo J., Choi Y. v-ATPase V0 subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat. Med. 2006, 12:1403-1409.
24. Baeuerle P.A., Henkel T. Function and activation of NF-kappa B in the immune system. Annu. Rev. Immunol. 1994, 12:141-179.
25. DiDonato J.A., Hayakawa M., Rothwarf D.M., Zandi E., Karin M. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 1997, 388:548-554.
26. Yang F., Tang E., Guan K., Wang C.Y. IKK beta plays an essential role in the phosphorylation of RelA/p65 on serine 536 induced by lipopolysaccharide. J. Immunol. 2003, 170:5630-5635.
27. Sakurai H., Chiba H., Miyoshi H., Sugita T., Toriumi W. IkappaB kinases phosphorylate NF-kappaB p65 subunit on serine 536 in the transactivation domain. J. Biol. Chem. 1999, 274:30353-30356.
28. Callister T.Q., Raggi P., Cooil B., Lippolis N.J., Russo D.J. Effect of HMG-CoA reductase inhibitors on coronary artery disease as assessed by electron-beam computed tomography. N. Engl. J. Med. 1998, 339:1972-1978.
29. Mundy G., Garrett R., Harris S., Chan J., Chen D., Rossini G., Boyce B., Zhao M., Gutierrez G. Stimulation of bone formation in vitro and in rodents by statins. Science 1999, 286:1946-1949.
30. Schilling A.F., Schinke T., Munch C., Gebauer M., Niemeier A., Priemel M., Streichert T., Rueger J.M., Amling M. Increased bone formation in mice lacking apolipoprotein E. J. Bone Miner. Res. 2005, 20:274-282.
31. Bartelt A., Beil F.T., Schinke T., Roeser K., Ruether W., Heeren J., Niemeier A. Apolipoprotein E-dependent inverse regulation of vertebral bone and adipose tissue mass in C57Bl/6 mice: modulation by diet-induced obesity. Bone 2010, 47:736-745.
32. Hirasawa H., Tanaka S., Sakai A., Tsutsui M., Shimokawa H., Miyata H., Moriwaki S., Niida S., Ito M., Nakamura T. ApoE gene deficiency enhances the reduction of bone formation induced by a high-fat diet through the stimulation of p53-mediated apoptosis in osteoblastic cells. J. Bone Miner. Res. 2007, 22:1020-1030.
33. Bachner D., Schroder D., Betat N., Ahrens M., Gross G. Apolipoprotein E (ApoE), a Bmp-2 (bone morphogenetic protein) upregulated gene in mesenchymal progenitors (C3H10T1/2), is highly expressed in murine embryonic development. Biofactors 1999, 9:11-17.
34. Lee Z.H., Kim H.H. Signal transduction by receptor activator of nuclear factor kappa B in osteoclasts. Biochem. Biophys. Res. Commun. 2003, 305:211-214.
35. Darnay B.G., Ni J., Moore P.A., Aggarwal B.B. Activation of NF-kappaB by RANK requires tumor necrosis factor receptor-associated factor (TRAF) 6 and NF-kappaB-inducing kinase. Identification of a novel TRAF6 interaction motif. J. Biol. Chem. 1999, 274:7724-7731.
36. Kypreos K.E., Zannis V.I. LDL receptor deficiency or apoE mutations prevent remnant clearance and induce hypertriglyceridemia in mice. J. Lipid Res. 2006, 47:521-529.
37. Lin C.Y., Huang Z.H., Mazzone T. Interaction with proteoglycans enhances the sterol efflux produced by endogenous expression of macrophage apoE. J. Lipid Res. 2001, 42:1125-1133.
38. Mahley R.W. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 1988, 240:622-630.
39. Bornfeldt K.E., Tabas I. Insulin resistance, hyperglycemia, and atherosclerosis. Cell Metab. 2011, 14:575-585.
40. Lammers B., Out R., Hildebrand R.B., Quinn C.M., Williamson D., Hoekstra M., Meurs I., Van Berkel T.J., Jessup W., Van Eck M. Independent protective roles for macrophage Abcg1 and ApoE in the atherosclerotic lesion development. Atherosclerosis 2009, 205:420-426.
41. Bray G.A., Popkin B.M. Dietary fat intake does affect obesity!. Am. J. Clin. Nutr. 1998, 68:1157-1173.
42. Xiao Y., Cui J., Li Y.X., Shi Y.H., Le G.W. Expression of genes associated with bone resorption is increased and bone formation is decreased in mice fed a high-fat diet. Lipids 2010, 45:345-355.
43. Parhami F., Garfinkel A., Demer L.L. Role of lipids in osteoporosis. Arterioscler. Thromb. Vasc. Biol. 2000, 20:2346-2348.
44. Singh K., Chaturvedi R., Barry D.P., Coburn L.A., Asim M., Lewis N.D., Piazuelo M.B., Washington M.K., Vitek M.P., Wilson K.T. The apolipoprotein E-mimetic peptide COG112 inhibits NF-kappaB signaling, proinflammatory cytokine expression, and disease activity in murine models of colitis. J. Biol. Chem. 2011, 286:3839-3850.
45. Singh K., Chaturvedi R., Asim M., Barry D.P., Lewis N.D., Vitek M.P., Wilson K.T. The apolipoprotein E-mimetic peptide COG112 inhibits the inflammatory response to Citrobacter rodentium in colonic epithelial cells by preventing NF-kappaB activation. J. Biol. Chem. 2008, 283:16752-16761.
46. Yamashita T., Yao Z., Li F., Zhang Q., Badell I.R., Schwarz E.M., Takeshita S., Wagner E.F., Noda M., Matsuo K., Xing L., Boyce B.F. NF-kappaB p50 and p52 regulate receptor activator of NF-kappaB ligand (RANKL) and tumor necrosis factor-induced osteoclast precursor differentiation by activating c-Fos and NFATc1. J. Biol. Chem. 2007, 282:18245-18253.
47. Takatsuna H., Asagiri M., Kubota T., Oka K., Osada T., Sugiyama C., Saito H., Aoki K., Ohya K., Takayanagi H., Umezawa K. Inhibition of RANKL-induced osteoclastogenesis by (-)-DHMEQ, a novel NF-kappaB inhibitor, through downregulation of NFATc1. J. Bone Miner. Res. 2005, 20:653-662.
48. C. Goettsch, M. Rauner, K. Sinningen, S. Helas, N. Al-Fakhri, K. Nemeth, C. Hamann, S. Kopprasch, E. Aikawa, S.R. Bornstein, M. Schoppet, L.C. Hofbauer, The osteoclast-associated receptor (OSCAR) is a novel receptor regulated by oxidized low-density lipoprotein in human endothelial cells, Endocrinology 152 4915-4926.
49. Maziere C., Morliere P., Massy Z., Kamel S., Louandre C., Conte M.A., Maziere J.C. Oxidized low-density lipoprotein elicits an intracellular calcium rise and increases the binding activity of the transcription factor NFAT. Free Radical Biol. Med. 2005, 38:472-480.
50. Goettsch C., Rauner M., Hamann C., Sinningen K., Hempel U., Bornstein S.R., Hofbauer L.C. Nuclear factor of activated T cells mediates oxidised LDL-induced calcification of vascular smooth muscle cells. Diabetologia 2011, 54:2690-2701.
51. Kim K., Kim J.H., Lee J., Jin H.M., Lee S.H., Fisher D.E., Kook H., Kim K.K., Choi Y., Kim N. Nuclear factor of activated T cells c1 induces osteoclast-associated receptor gene expression during tumor necrosis factor-related activation-induced cytokine-mediated osteoclastogenesis. J. Biol. Chem. 2005, 280:35209-35216.