N-3 polyunsaturated fatty acids stimulate osteoclastogenesis through PPARγ-mediated enhancement of c-Fos expression, and suppress osteoclastogenesis through PPARγ-dependent inhibition of NFkB activation

Journal of Nutritional Biochemistry

Volumn 26, Issue 11, 2015, Pages 1317-1327

  Nakanishi, Atsuko ^a   Tsukamoto, Ikuyo ^a,b  

^a NARA WOMEN'S UNIVERSITY   (Japan)

^b HIROSHIMA INTERNATIONAL UNIVERSITY   (Japan)

Author keywords

Bone marrow derived monocytes macrophage precursor cells (BMMs); C fos; Docosahexaenoic acid (DHA); Eicosapentaenoic acid (EPA); Osteoclastogenesis; PPAR

Indexed keywords

2 CHLORO 5 NITRO N (4 PYRIDYL)BENZAMIDE; 2 CHLORO 5 NITROBENZANILIDE; ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ARACHIDONIC ACID; CATHEPSIN K; CYCLOOXYGENASE 2; DOCOSAHEXAENOIC ACID; FATTY ACID BINDING PROTEIN 4; ICOSAPENTAENOIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LINOLEIC ACID; MESSENGER RNA; N (2 BENZOYLPHENYL) O [2 (METHYL 2 PYRIDINYLAMINO)ETHYL]TYROSINE; OSTEOCLAST DIFFERENTIATION FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN C FOS; ROSIGLITAZONE; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC1; TRANSCRIPTION FACTOR RUNX2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 2,4 THIAZOLIDINEDIONE DERIVATIVE; BENZOPHENONE DERIVATIVE; NFATC1 PROTEIN, RAT; OMEGA 3 FATTY ACID; PTGS2 PROTEIN, RAT; TRANSCRIPTION FACTOR; TYROSINE;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; GENE EXPRESSION; MALE; MESENCHYMAL STEM CELL; MONOCYTE; NONHUMAN; OSTEOCLASTOGENESIS; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE DEVELOPMENT; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; WISTAR RAT;

ANIMALS; BENZOPHENONES; BONE MARROW CELLS; CELLS, CULTURED; CYCLOOXYGENASE 2; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; FATTY ACIDS, OMEGA-3; GENE EXPRESSION REGULATION; MALE; MESENCHYMAL STROMAL CELLS; NF-KAPPA B; OSTEOGENESIS; PPAR GAMMA; PROTO-ONCOGENE PROTEINS C-FOS; RATS, WISTAR; THIAZOLIDINEDIONES; TRANSCRIPTION FACTORS; TYROSINE;

EID: 84945586799     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.06.007     Document Type: Article

References (52)

1. Frost H.M. Tetracycline bone labeling in anatomy. Am J Phys Anthropol 1968, 29:183-195.
2. Manolagas S.C. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 2000, 21:115-137.
3. Rodan G.A., Martin T.J. Therapeutic approaches to bone diseases. Science 2000, 289:1508-1514.
4. Udagawa N., Takahashi N., Akatsu T., Tanaka H., Sasaki T., Nishihara T., et al. Origin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared by bone marrow-derived stromal cells. Proc Natl Acad Sci U S A 1990, 87:7260-7264.
5. Ross F.P., Christiano A.M. Nothing but skin and bone. J Clin Invest 2006, 116:1140-1149.
6. Nakashima T., Hayashi M., Takayanagi H. New insights into osteoclastogenic signaling mechanisms. Trends Endocrinol Metab 2012, 23:582-590.
7. Asagiri M., Takayanagi H. The molecular understanding of osteoclast differentiation. Bone 2007, 40:251-264.
8. Arai F., Miyamoto T., Ohneda O., Inada T., Sudo T., Brasel K., et al. Commitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor kappaB (RANK) receptors. J Exp Med 1999, 190:1741-1754.
9. Wan Y., Chong L.W., Evans R.M. PPAR-gamma regulates osteoclastogenesis in mice. Nat Med 2007, 13:1496-1503.
10. Wan Y. PPARgamma in bone homeostasis. Trends Endocrinol Metab 2010, 21:722-728.
11. Wei W., Wang X., Yang M., Smith L.C., Dechow P.C., Sonoda J., et al. PGC1beta mediates PPARgamma activation of osteoclastogenesis and rosiglitazone-induced bone loss. Cell Metab 2010, 11:503-516.
12. Wei W., Zeve D., Wang X., Du Y., Tang W., Dechow P.C., et al. Osteoclast progenitors reside in the peroxisome proliferator-activated receptor gamma-expressing bone marrow cell population. Mol Cell Biol 2011, 31:4692-4705.
13. Wu H., Li L., Ma Y., Chen Y., Zhao J., Lu Y., et al. Regulation of selective PPARgamma modulators in the differentiation of osteoclasts. J Cell Biochem 2013, 114:1969-1977.
14. Willson T.M., Lambert M.H., Kliewer S.A. Peroxisome proliferator-activated receptor gamma and metabolic disease. Annu Rev Biochem 2001, 70:341-367.
15. Sun D., Krishnan A., Zaman K., Lawrence R., Bhattacharya A., Fernandes G. Dietary n-3 fatty acids decrease osteoclastogenesis and loss of bone mass in ovariectomized mice. J Bone Miner Res 2003, 18:1206-1216.
16. Bhattacharya A., Rahman M., Sun D., Fernandes G. Effect of fish oil on bone mineral density in aging C57BL/6 female mice. J Nutr Biochem 2007, 18:372-379.
17. Rahman M.M., Bhattacharya A., Banu J., Kang J.X., Fernandes G. Endogenous n-3 fatty acids protect ovariectomy induced bone loss by attenuating osteoclastogenesis. J Cell Mol Med 2009, 13:1833-1844.
18. Nakanishi A., Iitsuka N., Tsukamoto I. Fish oil suppresses bone resorption by inhibiting osteoclastogenesis through decreased expression of M-CSF, PU.1, MITF and RANK in ovariectomized rats. Mol Med Rep 2013, 7:1896-1903.
19. Pascual G., Fong A.L., Ogawa S., Gamliel A., Li A.C., Perissi V., et al. A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma. Nature 2005, 437:759-763.
20. Chapkin R.S., Kim W., Lupton J.R., McMurray D.N. Dietary docosahexaenoic and eicosapentaenoic acid: emerging mediators of inflammation. Prostaglandins Leukot Essent Fat Acids 2009, 81:187-191.
21. Calder P.C. Omega-3 fatty acids and inflammatory processes. Nutrients 2010, 2:355-374.
22. Tontonoz P., Hu E., Spiegelman B.M. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 1994, 79:1147-1156.
23. Brun R.P., Tontonoz P., Forman B.M., Ellis R., Chen J., Evans R.M., et al. Differential activation of adipogenesis by multiple PPAR isoforms. Genes Dev 1996, 10:974-984.
24. Tontonoz P., Spiegelman B.M. Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 2008, 77:289-312.
25. Ali A.A., Weinstein R.S., Stewart S.A., Parfitt A.M., Manolagas S.C., Jilka R.L. Rosiglitazone causes bone loss in mice by suppressing osteoblast differentiation and bone formation. Endocrinology 2005, 146:1226-1235.
26. Rzonca S.O., Suva L.J., Gaddy D., Montague D.C., Lecka-Czernik B. Bone is a target for the antidiabetic compound rosiglitazone. Endocrinology 2004, 145:401-406.
27. Zinman B., Haffner S.M., Herman W.H., Holman R.R., Lachin J.M., Kravitz B.G., et al. Effect of rosiglitazone, metformin, and glyburide on bone biomarkers in patients with type 2 diabetes. J Clin Endocrinol Metab 2010, 95:134-142.
28. Grey A., Bolland M., Gamble G., Wattie D., Horne A., Davidson J., et al. The peroxisome proliferator-activated receptor-gamma agonist rosiglitazone decreases bone formation and bone mineral density in healthy postmenopausal women: a randomized, controlled trial. J Clin Endocrinol Metab 2007, 92:1305-1310.
29. Berberoglu Z., Gursoy A., Bayraktar N., Yazici A.C., Bascil Tutuncu N., Guvener Demirag N. Rosiglitazone decreases serum bone-specific alkaline phosphatase activity in postmenopausal diabetic women. J Clin Endocrinol Metab 2007, 92:3523-3530.
30. Hie M., Tsukamoto I. Vitamin C-deficiency stimulates osteoclastogenesis with an increase in RANK expression. J Nutr Biochem 2011, 22:164-171.
31. Hie M., Yamazaki M., Tsukamoto I. Curcumin suppresses increased bone resorption by inhibiting osteoclastogenesis in rats with streptozotocin-induced diabetes. Eur J Pharmacol 2009, 621:1-9.
32. Hie M., Iitsuka N., Otsuka T., Nakanishi A., Tsukamoto I. Zinc deficiency decreases osteoblasts and osteoclasts associated with the reduced expression of Runx2 and RANK. Bone 2011, 49:1152-1157.
33. Nakanishi A., Hie M., Iitsuka N., Tsukamoto I. A crucial role for reactive oxygen species in macrophage colony-stimulating factor-induced RANK expression in osteoclastic differentiation. Int J Mol Med 2013, 31:874-880.
34. Grigoriadis A.E., Wang Z.Q., Cecchini M.G., Hofstetter W., Felix R., Fleisch H.A., et al. c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling. Science 1994, 266:443-448.
35. Yanai R., Mulki L., Hasegawa E., Takeuchi K., Sweigard H., Suzuki J., et al. Cytochrome P450-generated metabolites derived from omega-3 fatty acids attenuate neovascularization. Proc Natl Acad Sci U S A 2014, 111:9603-9608.
36. Rahman M.M., Bhattacharya A., Fernandes G. Docosahexaenoic acid is more potent inhibitor of osteoclast differentiation in RAW 264.7 cells than eicosapentaenoic acid. J Cell Physiol 2008, 214:201-209.
37. Zhao D., Shi Z., Warriner A.H., Qiao P., Hong H., Wang Y., et al. Molecular mechanism of thiazolidinedione-mediated inhibitory effects on osteoclastogenesis. PLoS One 2014, 9:e102706.
38. Fukunaga T., Zou W., Rohatgi N., Colca J.R., Teitelbaum S.L. An insulin-sensitizing thiazolidinedione, which minimally activates PPARgamma, does not cause bone loss. J Bone Miner Res 2015, 30:481-488.
39. Ahmadian M., Suh J.M., Hah N., Liddle C., Atkins A.R., Downes M., et al. PPARgamma signaling and metabolism: the good, the bad and the future. Nat Med 2013, 19:557-566.
40. Sugii S., Evans R.M. Epigenetic codes of PPARgamma in metabolic disease. FEBS Lett 2011, 585:2121-2128.
41. Akune T., Ohba S., Kamekura S., Yamaguchi M., Chung U.I., Kubota N., et al. PPARgamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. J Clin Invest 2004, 113:846-855.
42. Okazaki R., Toriumi M., Fukumoto S., Miyamoto M., Fujita T., Tanaka K., et al. Thiazolidinediones inhibit osteoclast-like cell formation and bone resorption in vitro. Endocrinology 1999, 140:5060-5065.
43. Cho E.S., Kim M.K., Son Y.O., Lee K.S., Park S.M., Lee J.C. The effects of rosiglitazone on osteoblastic differentiation, osteoclast formation and bone resorption. Mol Cells 2012, 33:173-181.
44. Lazarenko O.P., Rzonca S.O., Hogue W.R., Swain F.L., Suva L.J., Lecka-Czernik B. Rosiglitazone induces decreases in bone mass and strength that are reminiscent of aged bone. Endocrinology 2007, 148:2669-2680.
45. Moerman E.J., Teng K., Lipschitz D.A., Lecka-Czernik B. Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: the role of PPAR-gamma2 transcription factor and TGF-beta/BMP signaling pathways. Aging Cell 2004, 3:379-389.
46. Lecka-Czernik B., Suva L.J. Resolving the two "bony" faces of PPAR-gamma. PPAR Res 2006, 2006:27489.
47. Poulsen R.C., Moughan P.J., Kruger M.C. Long-chain polyunsaturated fatty acids and the regulation of bone metabolism. Exp Biol Med (Maywood) 2007, 232:1275-1288.
48. Salari P., Rezaie A., Larijani B., Abdollahi M. A systematic review of the impact of n-3 fatty acids in bone health and osteoporosis. Med Sci Monit 2008, 14:RA37-RA44.
49. Kruger M.C., Coetzee M., Haag M., Weiler H. Long-chain polyunsaturated fatty acids: selected mechanisms of action on bone. Prog Lipid Res 2010, 49:438-449.
50. Schwartz A.V., Sellmeyer D.E., Vittinghoff E., Palermo L., Lecka-Czernik B., Feingold K.R., et al. Thiazolidinedione use and bone loss in older diabetic adults. J Clin Endocrinol Metab 2006, 91:3349-3354.
51. Kahn S.E., Zinman B., Lachin J.M., Haffner S.M., Herman W.H., Holman R.R., et al. Rosiglitazone-associated fractures in type 2 diabetes: an Analysis from A Diabetes Outcome Progression Trial (ADOPT). Diabetes Care 2008, 31:845-851.
52. Gruntmanis U., Fordan S., Ghayee H.K., Abdullah S.M., See R., Ayers C.R., et al. The peroxisome proliferator-activated receptor-gamma agonist rosiglitazone increases bone resorption in women with type 2 diabetes: a randomized, controlled trial. Calcif Tissue Int 2010, 86:343-349.