Elevated response to type i IFN enhances rankl-mediated osteoclastogenesis in usp18-knockout mice

Journal of Immunology

Volumn 196, Issue 9, 2016, Pages 3887-3895

  Yim, Hwa Young ^a,b   Park, Cheolkyu ^b   Lee, Yong Deok ^b   Arimoto, Kei Ichiro ^c   Jeon, Raok ^a   Baek, Sung Hee ^b   Zhang, Dong Er ^c   Kim, Hong Hee ^b   Kim, Keun Il ^a  

^a Sookmyung Women's University   (South Korea)

^b Seoul National University   (South Korea)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 6; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEIN USP18; PROTEINASE; STAT1 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NFATC1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; NFATC1 PROTEIN, MOUSE; TNFSF11 PROTEIN, MOUSE; TRANSCRIPTION FACTOR NFAT; UBIQUITIN THIOLESTERASE; USP18 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW DERIVED MACROPHAGE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE RESPONSE; FEMALE; FEMUR; GENE EXPRESSION; IN VITRO STUDY; MALE; MOUSE; MULTINUCLEAR CELL; NONHUMAN; OSTEOCLAST ACTIVITY; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPENIA; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEPLETION; PROTEIN EXPRESSION; 129 MOUSE; ANIMAL; BONE DEVELOPMENT; CELL CULTURE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; OSTEOCLAST; OSTEOPOROSIS; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CHEMOKINE CXCL10; INTERFERON TYPE I; MACROPHAGES; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; OSTEOGENESIS; OSTEOPOROSIS; RANK LIGAND; UBIQUITIN THIOLESTERASE;

EID: 84974803236     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501496     Document Type: Article

References (39)

1. Harada, S., and G. A. Rodan. 2003. Control of osteoblast function and regulation of bone mass. Nature 423: 349-355.
2. Soysa, N. S., N. Alles, K. Aoki, and K. Ohya. 2012. Osteoclast formation and differentiation: an overview. J. Med. Dent. Sci. 59: 65-74.
3. Raggatt, L. J., and N. C. Partridge. 2010. Cellular and molecular mechanisms of bone remodeling. J. Biol. Chem. 285: 25103-25108.
4. Rodan, G. A., and T. J. Martin. 2000. Therapeutic approaches to bone diseases. Science 289: 1508-1514.
5. Takayanagi, H., H. Iizuka, T. Juji, T. Nakagawa, A. Yamamoto, T. Miyazaki, Y. Koshihara, H. Oda, K. Nakamura, and S. Tanaka. 2000. Involvement of receptor activator of nuclear factor kappaB ligand/osteoclast differentiation factor in osteoclastogenesis from synoviocytes in rheumatoid arthritis. Arthritis Rheum. 43: 259-269.
6. Takayanagi, H., S. Kim, and T. Taniguchi. 2002. Signaling crosstalk between RANKL and interferons in osteoclast differentiation. Arthritis Res. 4(Suppl. 3): S227-S232.
7. Yoshida, H., S. Hayashi, T. Kunisada, M. Ogawa, S. Nishikawa, H. Okamura, T. Sudo, L. D. Shultz, and S. Nishikawa. 1990. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345: 442-444.
8. Udagawa, N., N. Takahashi, T. Akatsu, H. Tanaka, T. Sasaki, T. Nishihara, T. Koga, T. J. Martin, and T. Suda. 1990. 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. USA 87: 7260-7264.
9. Ross, F. P., and S. L. Teitelbaum. 2005. alphavbeta3 and macrophage colonystimulating factor: partners in osteoclast biology. Immunol. Rev. 208: 88-105.
10. Asagiri, M., and H. Takayanagi. 2007. The molecular understanding of osteoclast differentiation. Bone 40: 251-264.
11. Theill, L. E., W. J. Boyle, and J. M. Penninger. 2002. RANK-L and RANK: T cells, bone loss, and mammalian evolution. Annu. Rev. Immunol. 20: 795-823.
12. Boyle, W. J., W. S. Simonet, and D. L. Lacey. 2003. Osteoclast differentiation and activation. Nature 423: 337-342.
13. Takayanagi, H. 2005. Mechanistic insight into osteoclast differentiation in osteoimmunology. J. Mol. Med. (Berl.) 83: 170-179.
14. Takayanagi, H., K. Sato, A. Takaoka, and T. Taniguchi. 2005. Interplay between interferon and other cytokine systems in bone metabolism. Immunol. Rev. 208: 181-193.
15. Grigoriadis, A. E., Z. Q. Wang, M. G. Cecchini, W. Hofstetter, R. Felix, H. A. Fleisch, and E. F. Wagner. 1994. c-Fos: a key regulator of osteoclastmacrophage lineage determination and bone remodeling. Science 266: 443-448.
16. Takayanagi, H., S. Kim, T. Koga, H. Nishina, M. Isshiki, H. Yoshida, A. Saiura, M. Isobe, T. Yokochi, J. Inoue, et al. 2002. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev. Cell 3: 889-901.
17. Wagner, E. F., and R. Eferl. 2005. Fos/AP-1 proteins in bone and the immune system. Immunol. Rev. 208: 126-140.
18. Koga, T., M. Inui, K. Inoue, S. Kim, A. Suematsu, E. Kobayashi, T. Iwata, H. Ohnishi, T. Matozaki, T. Kodama, et al. 2004. Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 428: 758-763.
19. Takayanagi, H. 2007. The role of NFAT in osteoclast formation. Ann. N. Y. Acad. Sci. 1116: 227-237.
20. Takayanagi, H., S. Kim, K. Matsuo, H. Suzuki, T. Suzuki, K. Sato, T. Yokochi, H. Oda, K. Nakamura, N. Ida, et al. 2002. RANKL maintains bone homeostasis through c-Fos-dependent induction of interferon-beta. Nature 416: 744-749.
21. Zhang, D., and D. E. Zhang. 2011. Interferon-stimulated gene 15 and the protein ISGylation system. J. Interferon Cytokine Res. 31: 119-130.
22. Morales, D. J., and D. J. Lenschow. 2013. The antiviral activities of ISG15. J. Mol. Biol. 425: 4995-5008.
23. Zhao, C., M. N. Collins, T. Y. Hsiang, and R. M. Krug. 2013. Interferon-induced ISG15 pathway: an ongoing virus-host battle. Trends Microbiol. 21: 181-186.
24. Malakhov, M. P., O. A. Malakhova, K. I. Kim, K. J. Ritchie, and D. E. Zhang. 2002. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J. Biol. Chem. 277: 9976-9981.
25. Malakhova, O. A., M. Yan, M. P. Malakhov, Y. Yuan, K. J. Ritchie, K. I. Kim, L. F. Peterson, K. Shuai, and D. E. Zhang. 2003. Protein ISGylation modulates the JAK-STAT signaling pathway. Genes Dev. 17: 455-460.
26. Ritchie, K. J., C. S. Hahn, K. I. Kim, M. Yan, D. Rosario, L. Li, J. C. de la Torre, and D. E. Zhang. 2004. Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat. Med. 10: 1374-1378.
27. Kim, K. I., O. A. Malakhova, K. Hoebe, M. Yan, B. Beutler, and D. E. Zhang. 2005. Enhanced antibacterial potential in UBP43-deficient mice against Salmonella typhimurium infection by up-regulating type I IFN signaling. J. Immunol. 175: 847-854.
28. Ritchie, K. J., M. P. Malakhov, C. J. Hetherington, L. Zhou, M. T. Little, O. A. Malakhova, J. C. Sipe, S. H. Orkin, and D. E. Zhang. 2002. Dysregulation of protein modification by ISG15 results in brain cell injury. Genes Dev. 16: 2207-2212.
29. Yim, H. Y., Y. Yang, J. S. Lim, M. S. Lee, D. E. Zhang, and K. I. Kim. 2012. The mitochondrial pathway and reactive oxygen species are critical contributors to interferon-a/b-mediated apoptosis in Ubp43-deficient hematopoietic cells. Biochem. Biophys. Res. Commun. 423: 436-440.
30. Malakhova, O. A., K. I. Kim, J. K. Luo, W. Zou, K. G. Kumar, S. Y. Fuchs, K. Shuai, and D. E. Zhang. 2006. UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. EMBO J. 25: 2358-2367.
31. Ketscher, L., R. Hannß, D. J. Morales, A. Basters, S. Guerra, T. Goldmann, A. Hausmann, M. Prinz, R. Naumann, A. Pekosz, et al. 2015. Selective inactivation of USP18 isopeptidase activity in vivo enhances ISG15 conjugation and viral resistance. Proc. Natl. Acad. Sci. USA 112: 1577-1582.
32. Hikata, T., H. Takaishi, J. Takito, A. Hakozaki, M. Furukawa, S. Uchikawa, T. Kimura, Y. Okada, M. Matsumoto, A. Yoshimura, et al. 2009. PIAS3 negatively regulates RANKL-mediated osteoclastogenesis directly in osteoclast precursors and indirectly via osteoblasts. Blood 113: 2202-2212.
33. Wong, P. K., P. J. Egan, B. A. Croker, K. O'Donnell, N. A. Sims, S. Drake, H. Kiu, E. J. McManus, W. S. Alexander, A. W. Roberts, and I. P. Wicks. 2006. SOCS-3 negatively regulates innate and adaptive immune mechanisms in acute IL-1-dependent inflammatory arthritis. J. Clin. Invest. 116: 1571-1581.
34. Kim, J. H., J. K. Luo, and D. E. Zhang. 2008. The level of hepatitis B virus replication is not affected by protein ISG15 modification but is reduced by inhibition of UBP43 (USP18) expression. J. Immunol. 181: 6467-6472.
35. Zupan, J., M. Jeras, and J. Marc. 2013. Osteoimmunology and the influence of pro-inflammatory cytokines on osteoclasts. Biochem. Med. (Zagreb) 23: 43-63.
36. Zou, W., J. H. Kim, A. Handidu, X. Li, K. I. Kim, M. Yan, J. Li, and D. E. Zhang. 2007. Microarray analysis reveals that Type I interferon strongly increases the expression of immune-response related genes in Ubp43 (Usp18) deficient macrophages. Biochem. Biophys. Res. Commun. 356: 193-199.
37. Grassi, F., A. Piacentini, S. Cristino, S. Toneguzzi, C. Cavallo, A. Facchini, and G. Lisignoli. 2003. Human osteoclasts express different CXC chemokines depending on cell culture substrate: molecular and immunocytochemical evidence of high levels of CXCL10 and CXCL12. Histochem. Cell Biol. 120: 391-400.
38. Kwak, H. B., H. Ha, H. N. Kim, J. H. Lee, H. S. Kim, S. Lee, H. M. Kim, J. Y. Kim, H. H. Kim, Y. W. Song, and Z. H. Lee. 2008. Reciprocal cross-talk between RANKL and interferon-gamma-inducible protein 10 is responsible for bone-erosive experimental arthritis. Arthritis Rheum. 58: 1332-1342.
39. Lei, S. F., S. Wu, L. M. Li, F. Y. Deng, S. M. Xiao, C. Jiang, Y. Chen, H. Jiang, F. Yang, L. J. Tan, et al. 2009. An in vivo genome wide gene expression study of circulating monocytes suggested GBP1, STAT1 and CXCL10 as novel risk genes for the differentiation of peak bone mass. Bone 44: 1010-1014.