Resolvin E1 regulates osteoclast fusion via DC-STAMP and NFATc1

FASEB Journal

Volumn 27, Issue 8, 2013, Pages 3344-3353

  Zhu, Min ^a   Van Dyke, Thomas E ^b   Gyurko, Robert ^a  

^a BOSTON UNIVERSITY   (United States)

^b FORSYTH INSTITUTE   (United States)

Author keywords

Inflammation resolution; Lipid mediator; Osteoimmunology

Indexed keywords

DC STAMP PROTEIN; HYBRID PROTEIN; MEDIATOR COMPLEX; NUCLEAR FACTOR OF ACTIVATED T CELLS C1; RESOLVIN E1 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; 5S,12R,18R-TRIHYDROXY-6Z,8E,10E,14Z,16E-EICOSAPENTAENOIC ACID; DC-STAMP PROTEIN, MOUSE; ICOSAPENTAENOIC ACID; LEUKOTRIENE B4 RECEPTOR; LTB4R1 PROTEIN, MOUSE; MEMBRANE PROTEIN; NERVE PROTEIN; NFATC1 PROTEIN, MOUSE; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEIN BINDING; TNFSF11 PROTEIN, MOUSE; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; ELECTROPHORESIS; IN VITRO STUDY; INFLAMMATION; MALE; MEMBRANE FUSION; MICROSCOPY; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; PRECURSOR; PRIORITY JOURNAL; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL FUSION; CONFOCAL MICROSCOPY; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PROMOTER REGION; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL FUSION; CELLS, CULTURED; EICOSAPENTAENOIC ACID; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RANK LIGAND; RECEPTORS, LEUKOTRIENE B4; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIME-LAPSE IMAGING;

EID: 84881179975     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-220228     Document Type: Article

References (55)

1. Galkina, E., and Ley, K. (2009) Immune and inflammatory mechanisms of atherosclerosis. Annu. Rev. Immunol. 27, 165-197
2. Van Dyke, T. E. (2008) The management of inflammation in periodontal disease. J. Periodontol. 79, 1601-1608
3. El-Gabalawy, H., Guenther, L. C., and Bernstein, C. N. (2010) Epidemiology of immune-mediated inflammatory diseases: incidence, prevalence, natural history, and comorbidities. J. Rheumatol. Suppl. 85, 2-10
4. Hikiji, H., Takato, T., Shimizu, T., and Ishii, S. (2008) The roles of prostanoids, leukotrienes, and platelet-activating factor in bone metabolism and disease. Prog. Lipid Res. 47, 107-126
5. Serhan, C. N., and Savill, J. (2005) Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6, 1191-1197
6. Fierro, I. M., Kutok, J. L., and Serhan, C. N. (2002) Novel lipid mediator regulators of endothelial cell proliferation and migration: aspirin-triggered-15R-lipoxin A(4) and lipoxin A(4). J. Pharmacol. Exp. Ther. 300, 385-392
7. Serhan, C. N., Hong, S., Gronert, K., Colgan, S. P., Devchand, P. R., Mirick, G., and Moussignac, R. L. (2002) Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J. Exp. Med. 196, 1025-1037
8. Ariel, A., Li, P. L., Wang, W., Tang, W. X., Fredman, G., Hong, S., Gotlinger, K. H., and Serhan, C. N. (2005) The docosatriene protectin D1 is produced by TH2 skewing and promotes human T cell apoptosis via lipid raft clustering. J. Biol. Chem. 280, 43079-43086
9. Serhan, C. N., Yang, R., Martinod, K., Kasuga, K., Pillai, P. S., Porter, T. F., Oh, S. F., and Spite, M. (2009) Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions. J. Exp. Med. 206, 15-23
10. Serhan, C. N. (2011) The resolution of inflammation: the devil in the flask and in the details. FASEB J. 25, 1441-1448
11. Serhan, C. N. (2010) Novel lipid mediators and resolution mechanisms in acute inflammation: to resolve or not? Am. J. Pathol. 177, 1576-1591
12. Nathan, C., and Ding, A. (2010) Nonresolving inflammation. Cell 140, 871-882
13. Bannenberg, G. L., Chiang, N., Ariel, A., Arita, M., Tjonahen, E., Gotlinger, K. H., Hong, S., and Serhan, C. N. (2005) Molecular circuits of resolution: formation and actions of resolvins and protectins. J. Immunol. 174, 4345-4355
14. Hasturk, H., Kantarci, A., Ohira, T., Arita, M., Ebrahimi, N., Chiang, N., Petasis, N. A., Levy, B. D., Serhan, C. N., and Van Dyke, T. E. (2006) RvE1 protects from local inflammation and osteoclast-mediated bone destruction in periodontitis. FASEB J. 20, 401-403
15. Haworth, O., Cernadas, M., Yang, R., Serhan, C. N., and Levy, B. D. (2008) Resolvin E1 regulates interleukin 23, interferongamma and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat. Immunol. 9, 873-879
16. Ariel, A., Fredman, G., Sun, Y. P., Kantarci, A., Van Dyke, T. E., Luster, A. D., and Serhan, C. N. (2006) Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nat. Immunol. 7, 1209-1216
17. Arita, M., Bianchini, F., Aliberti, J., Sher, A., Chiang, N., Hong, S., Yang, R., Petasis, N. A., and Serhan, C. N. (2005) Stereochemical assignment, anti-inflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J. Exp. Med. 201, 713-722
18. Nakashima, T., and Takayanagi, H. (2009) Osteoimmunology: crosstalk between the immune and bone systems. J. Clin. Immunol. 29, 555-567
19. Raggatt, L. J., and Partridge, N. C. (2010) Cellular and molecular mechanisms of bone remodeling. J. Biol. Chem. 285, 25103-25108
20. Ishii, M., and Saeki, Y. (2008) Osteoclast cell fusion: mechanisms and molecules. Mod. Rheumatol. 18, 220-227
21. Teitelbaum, S. L. (2000) Bone resorption by osteoclasts. Science 289, 1504-1508
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., and Suda, T. (2005) DC-STAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cells. J. Exp. Med. 202, 345-351
23. Han, X., Sterling, H., Chen, Y., Saginario, C., Brown, E. J., Frazier, W. A., Lindberg, F. P., and Vignery, A. (2000) CD47, a ligand for the macrophage fusion receptor, participates in macrophage multinucleation. J. Biol. Chem. 275, 37984-37992
24. 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., and Choi, Y. (2006) v-ATPase V0 subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat. Med. 12, 1403-1409
25. Kukita, T., Wada, N., Kukita, A., Kakimoto, T., Sandra, F., Toh, K., Nagata, K., Iijima, T., Horiuchi, M., Matsusaki, H., Hieshima, K., Yoshie, O., and Nomiyama, H. (2004) RANKL-induced DC-STAMP is essential for osteoclastogenesis. J. Exp. Med. 200, 941-946
26. Kim, K., Lee, S. H., Ha Kim, J., Choi, Y., and Kim, N. (2008) NFATc1 induces osteoclast fusion via up-regulation of Atp6v0d2 and the dendritic cell-specific transmembrane protein (DCSTAMP). Mol. Endocrinol. 22, 176-185
27. 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., and Taniguchi, T. (2002) Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev. Cell 3, 889-901
28. Herrera, B. S., Ohira, T., Gao, L., Omori, K., Yang, R., Zhu, M., Muscara, M. N., Serhan, C. N., Van Dyke, T. E., and Gyurko, R. (2008) An endogenous regulator of inflammation, resolvin E1, modulates osteoclast differentiation and bone resorption. Br. J. Pharmacol. 155, 1214-1223
29. Gao, L., Faibish, D., Fredman, G., Herrera, B. S., Chiang, N., Serhan, C. N., Van Dyke, T. E., and Gyurko, R. (2013) Resolvin E1 and chemokine-like receptor 1 mediate bone preservation. J. Immunol. 190, 689-694
30. Jacquin, C., Gran, D. E., Lee, S. K., Lorenzo, J. A., and Aguila, H. L. (2006) Identification of multiple osteoclast precursor populations in murine bone marrow. J. Bone Miner. Res. 21, 67-77
31. Helming, L., and Gordon, S. (2009) Molecular mediators of macrophage fusion. Trends Cell Biol. 19, 514-522
32. Negishi-Koga, T., and Takayanagi, H. (2009) Ca2-NFATc1 signaling is an essential axis of osteoclast differentiation. Immunol. Rev. 231, 241-256
33. Aliprantis, A. O., Ueki, Y., Sulyanto, R., Park, A., Sigrist, K. S., Sharma, S. M., Ostrowski, M. C., Olsen, B. R., and Glimcher, L. H. (2008) NFATc1 in mice represses osteoprotegerin during osteoclastogenesis and dissociates systemic osteopenia from inflammation in cherubism. J. Clin. Invest. 118, 3775-3789
34. Cheng, Y. J., Imperatore, G., Caspersen, C. J., Gregg, E. W., Albright, A. L., and Helmick, C. G. (2012) Prevalence of diagnosed arthritis and arthritis-attributable activity limitation among adults with and without diagnosed diabetes: United States, 2008-2010. Diabetes Care 8, 1686-1691
35. Pihlstrom, B. L., Michalowicz, B. S., and Johnson, N. W. (2005) Periodontal diseases. Lancet 366, 1809-1820
36. Bijlsma, J. W., Berenbaum, F., and Lafeber, F. P. (2011) Osteoarthritis: an update with relevance for clinical practice. Lancet 377, 2115-2126
37. Izumi, Y., Aoki, A., Yamada, Y., Kobayashi, H., Iwata, T., Akizuki, T., Suda, T., Nakamura, S., Wara-Aswapati, N., Ueda, M., and Ishikawa, I. (2011) Current and future periodontal tissue engineering. Periodontol. 2000 56, 166-187
38. Serhan, C. N., Chiang, N., and Van Dyke, T. E. (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8, 349-361
39. Schett, G., and David, J. P. (2010) The multiple faces of autoimmune-mediated bone loss. Nature Rev. Endocrinol. 6, 698-706
40. Boyle, W. J., Simonet, W. S., and Lacey, D. L. (2003) Osteoclast differentiation and activation. Nature 423, 337-342
41. Lorenzo, J., Horowitz, M., and Choi, Y. (2008) Osteoimmunology: interactions of the bone and immune system. Endocr. Rev. 29, 403-440
42. Hasturk, H., Kantarci, A., Goguet-Surmenian, E., Blackwood, A., Andry, C., Serhan, C. N., and Van Dyke, T. E. (2007) Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J. Immunol. 179, 7021-7029
43. Hartgers, F. C., Vissers, J. L., Looman, M. W., van Zoelen, C., Huffine, C., Figdor, C. G., and Adema, G. J. (2000) DC-STAMP, a novel multimembrane-spanning molecule preferentially expressed by dendritic cells. Eur. J. Immunol. 30, 3585-3590
44. Yuan, J., Akiyama, M., Nakahama, K., Sato, T., Uematsu, H., and Morita, I. (2010) The effects of polyunsaturated fatty acids and their metabolites on osteoclastogenesis in vitro. Prostaglandins Other Lipid Mediat. 92, 85-90
45. Garcia, C., Boyce, B. F., Gilles, J., Dallas, M., Qiao, M., Mundy, G. R., and Bonewald, L. F. (1996) Leukotriene B4 stimulates osteoclastic bone resorption both in vitro and in vivo. J. Bone Miner. Res. 11, 1619-1627
46. Hikiji, H., Ishii, S., Yokomizo, T., Takato, T., and Shimizu, T. (2009) A distinctive role of the leukotriene B4 receptor BLT1 in osteoclastic activity during bone loss. Proc. Natl. Acad. Sci. U. S. A. 106, 21294-21299
47. Ohira, T., Arita, M., Omori, K., Recchiuti, A., Van Dyke, T. E., and Serhan, C. N. (2010) Resolvin E1 receptor activation signals phosphorylation and phagocytosis. J. Biol. Chem. 285, 3451-3461
48. Takahashi, N., Maeda, K., Ishihara, A., Uehara, S., and Kobayashi, Y. (2011) Regulatory mechanism of osteoclastogenesis by RANKL and Wnt signals. Front. Biosci. 16, 21-30
49. Hwang, S. Y., and Putney, J. W., Jr. (2011) Calcium signaling in osteoclasts. Biochim. Biophys. Acta 1813, 979-983
50. Matsumoto, M., Kogawa, M., Wada, S., Takayanagi, H., Tsujimoto, M., Katayama, S., Hisatake, K., and Nogi, Y. (2004) 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. 279, 45969-45979
51. Yagi, M., Ninomiya, K., Fujita, N., Suzuki, T., Iwasaki, R., Morita, K., Hosogane, N., Matsuo, K., Toyama, Y., Suda, T., and Miyamoto, T. (2007) Induction of DC-STAMP by alternative activation and downstream signaling mechanisms. J. Bone Miner. Res. 22, 992-1001
52. Beals, C. R., Sheridan, C. M., Turck, C. W., Gardner, P., and Crabtree, G. R. (1997) Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275, 1930-1934
53. Martin, T. J., and Sims, N. A. (2005) Osteoclast-derived activity in the coupling of bone formation to resorption. Trends Mol. Med. 11, 76-81
54. Cao, X. (2011) Targeting osteoclast-osteoblast communication. Nat. Med. 17, 1344-1346
55. Feng, X., and McDonald, J. M. (2011) Disorders of bone remodeling. Annu. Rev. Pathol. 6, 121-145