Bone resorption is regulated by cellautonomous negative feedback loop of Stat5-Dusp axis in the osteoclast

Journal of Experimental Medicine

Volumn 211, Issue 1, 2014, Pages 153-163

  Hirose, Jun ^a   Masuda, Hironari ^a   Tokuyama, Naoto ^a   Omata, Yasunori ^a   Matsumoto, Takumi ^a   Yasui, Tetsuro ^a   Kadono, Yuho ^a   Hennighausen, Lothar ^b   Tanaka, Sakae ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DUAL SPECIFICITY PHOSPHATASE; DUAL SPECIFICITY PHOSPHATASE 2; INTERLEUKIN 3; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; OSTEOCLAST DIFFERENTIATION FACTOR; STAT5 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOCLAST; OSTEOLYSIS; OSTEOPOROSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

ANIMALS; BETA-LACTAMASES; BLOTTING, WESTERN; BONE DENSITY; BONE RESORPTION; DNA PRIMERS; DUAL SPECIFICITY PHOSPHATASE 1; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HISTOLOGICAL TECHNIQUES; IN SITU NICK-END LABELING; INSULIN-LIKE GROWTH FACTOR I; INTERLEUKIN-3; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; OSTEOCALCIN; OSTEOCLASTS; POLYMERASE CHAIN REACTION; REAL-TIME POLYMERASE CHAIN REACTION; STAT5 TRANSCRIPTION FACTOR;

EID: 84892491195     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20130538     Document Type: Article

References (35)

1. Abu-Amer, Y. 2001. IL-4 abrogates osteoclastogenesis through STAT6-dependent inhibition of NF-kappaB. J. Clin. Invest. 107:1375-1385. http://dx.doi.org/10.1172/JCI10530.
2. Akira, S. 1999. Functional roles of STAT family proteins: lessons from knockout mice. Stem Cells. 17:138-146. http://dx.doi.org/10.1002/stem.170138.
3. Baron, R. 1989. Molecular mechanisms of bone resorption by the osteoclast. Anat. Rec. 224:317-324. http://dx.doi.org/10.1002/ar.1092240220.
4. Carlson, J., W.G. Cui, Q. Zhang, X.Q. Xu, F. Mercan, A.M. Bennett, and A. Vignery. 2009. Role of MKP-1 in osteoclasts and bone homeostasis. Am. J. Pathol. 175:1564-1573. http://dx.doi.org/10.2353/ajpath.2009 .090035.
5. Caunt, C.J., C.A. Rivers, B.L. Conway-Campbell, M.R. Norman, and C.A. McArdle. 2008. Epidermal growth factor receptor and protein kinase C signaling to ERK2: spatiotemporal regulation of ERK2 by dual specificity phosphatases. J. Biol. Chem. 283:6241-6252. http://dx.doi.org/10 .1074/jbc.M706624200.
6. Chen, J.R., L.I. Plotkin, J.I. Aguirre, L. Han, R.L. Jilka, S. Kousteni, T. Bellido, and S.C. Manolagas. 2005. Transient versus sustained phosphorylation and nuclear accumulation of ERKs underlie anti-versus pro-apoptotic effects of estrogens. J. Biol. Chem. 280:4632-4638. http://dx.doi.org/10 .1074/jbc.M411530200.
7. Cui, Y., G. Riedlinger, K. Miyoshi, W. Tang, C. Li, C.X. Deng, G.W. Robinson, and L. Hennighausen. 2004. Inactivation of Stat5 in mouse mammary epithelium during pregnancy reveals distinct functions in cell proliferation, survival, and differentiation. Mol. Cell. Biol. 24:8037-8047. http://dx.doi.org/10.1128/MCB.24.18.8037-8047.2004.
8. Gupta, N., A.P. Barhanpurkar, G.B. Tomar, R.K. Srivastava, S. Kour, S.T. Pote, G.C. Mishra, and M.R. Wani. 2010. IL-3 inhibits human osteoclastogenesis and bone resorption through downregulation of c-Fms and diverts the cells to dendritic cell lineage. J. Immunol. 185:2261-2272. http://dx.doi.org/10.4049/jimmunol.1000015.
9. He, Y.Z., K. Staser, S.D. Rhodes, Y.L. Liu, X.H. Wu, S.J. Park, J. Yuan, X.L. Yang, X.H. Li, L. Jiang, et al. 2011. Erk1 positively regulates osteoclast differentiation and bone resorptive activity. PLoS ONE. 6:e24780. http://dx.doi.org/10.1371/journal.pone.0024780.
10. Hennighausen, L., and G.W. Robinson. 2008. Interpretation of cytokine signaling through the transcription factors STAT5A and STAT5B. Genes Dev. 22:711-721. http://dx.doi.org/10.1101/gad.1643908.
11. Hoelbl, A., B. Kovacic, M.A. Kerenyi, O. Simma, W. Warsch, Y.Z. Cui, H. Beug, L. Hennighausen, R. Moriggl, and V. Sexl. 2006. Clarifying the role of Stat5 in lymphoid development and Abelson-induced transformation. Blood. 107:4898-4906. http://dx.doi.org/10.1182/blood-2005-09-3596.
12. Ilaria, R.L. Jr., and R.A. Van Etten. 1996. P210 and P190(BCR/ABL) induce the tyrosine phosphorylation and DNA binding activity of multiple specific STAT family members. J. Biol. Chem. 271:31704-31710. http://dx.doi.org/10.1074/jbc.271.49.31704.
13. Karsenty, G., and E.F. Wagner. 2002. Reaching a genetic and molecular understanding of skeletal development. Dev. Cell. 2:389-406. http://dx.doi .org/10.1016/S1534-5807(02)00157-0.
14. Khapli, S.M., L.S. Mangashetti, S.D. Yogesha, and M.R. Wani. 2003. IL-3 acts directly on osteoclast precursors and irreversibly inhibits receptor activator of NF-kappa B ligand-induced osteoclast differentiation by diverting the cells to macrophage lineage. J. Immunol. 171:142-151.
15. Kitamura, T. 1998. New experimental approaches in retrovirus-mediated expression screening. Int. J. Hematol. 67:351-359. http://dx.doi.org/10 .1016/S0925-5710(98)00025-5.
16. Lacey, D.L., E. Timms, H.L. Tan, M.J. Kelley, C.R. Dunstan, T. Burgess, R. Elliott, A. Colombero, G. Elliott, S. Scully, et al. 1998. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 93:165-176. http://dx.doi.org/10.1016/S0092-8674(00)81569-X.
17. Miyazaki, T., H. Katagiri, Y. Kanegae, H. Takayanagi, Y. Sawada, A. Yamamoto, M.P. Pando, T. Asano, I.M. Verma, H. Oda, et al. 2000. Reciprocal role of ERK and NF-κB pathways in survival and activation of osteoclasts. J. Cell Biol. 148:333-342. http://dx.doi.org/10.1083/jcb.148.2.333.
18. Nakamura, H., A. Hirata, T. Tsuji, and T. Yamamoto. 2003. Role of osteoclast extracellular signal-regulated kinase (ERK) in cell survival and maintenance of cell polarity. J. Bone Miner. Res. 18:1198-1205. http://dx.doi.org/10.1359/jbmr.2003.18.7.1198.
19. Nakamura, T., Y. Imai, T. Matsumoto, S. Sato, K. Takeuchi, K. Igarashi, Y. Harada, Y. Azuma, A. Krust, Y. Yamamoto, et al. 2007. Estrogen prevents bone loss via estrogen receptor alpha and induction of Fas ligand in osteoclasts. Cell. 130:811-823. http://dx.doi.org/10.1016/j.cell.2007.07.025.
20. Patterson, K.I., T. Brummer, P.M. O'Brien, and R.J. Daly. 2009. Dual-specificity phosphatases: critical regulators with diverse cellular targets. Biochem. J. 418:475-489.
21. Roodman, G.D. 2004. Mechanisms of bone metastasis. Discov. Med. 4:144-148.
22. Seeman, E. 2003. Reduced bone formation and increased bone resorption: rational targets for the treatment of osteoporosis. Osteoporos. Int. 14:S2-S8. http://dx.doi.org/10.1007/s00198-002-1340-9.
23. Sommer, B., R. Felix, C. Sprecher, M. Leunig, R. Ganz, and W. Hofstetter. 2005. Wear particles and surface topographies are modulators of osteoclastogenesis in vitro. J. Biomed. Mater. Res. A. 72A:67-76. http://dx.doi .org/10.1002/jbm.a.30202.
24. Suda, T., N. Takahashi, N. Udagawa, E. Jimi, M.T. Gillespie, and T.J. Martin. 1999. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr. Rev. 20:345-357. http://dx.doi.org/10.1210/er.20.3.345.
25. Takahashi, N., T. Akatsu, N. Udagawa, T. Sasaki, A. Yamaguchi, J.M. Moseley, T.J. Martin, and T. Suda. 1988. Osteoblastic cells are involved in osteoclast formation. Endocrinology. 123:2600-2602. http://dx.doi.org/10.1210/endo-123-5-2600.
26. 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. http://dx.doi.org/10.1002/1529-0131(200002)43:2<259::AID-ANR4>3.0.CO;2-W.
27. 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. http://dx.doi.org/10.1038/416744a.
28. Tanaka, S. 2007. Signaling axis in osteoclast biology and therapeutic targeting in the RANKL/RANK/OPG system. Am. J. Nephrol. 27:466-478. http://dx.doi.org/10.1159/000106484.
29. Tanaka, S., T. Takahashi, H. Takayanagi, T. Miyazaki, H. Oda, K. Nakamura, H. Hirai, and T. Kurokawa. 1998. Modulation of osteoclast function by adenovirus vector-induced epidermal growth factor receptor. J. Bone Miner. Res. 13:1714-1720. http://dx.doi.org/10.1359/jbmr.1998.13.11.1714.
30. Teglund, S., C. McKay, E. Schuetz, J.M. van Deursen, D. Stravopodis, D. Wang, M. Brown, S. Bodner, G. Grosveld, and J.N. Ihle. 1998. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell. 93:841-850. http://dx.doi.org/10.1016/S0092-8674(00)81444-0.
31. Van Etten, R.A. 2007. Aberrant cytokine signaling in leukemia. Oncogene. 26:6738-6749. http://dx.doi.org/10.1038/sj.onc.1210758.
32. Villa, A., M.M. Guerrini, B. Cassani, A. Pangrazio, and C. Sobacchi. 2009. Infantile malignant, autosomal recessive osteopetrosis: the rich and the poor. Calcif. Tissue Int. 84:1-12. http://dx.doi.org/10.1007/s00223-008-9196-4.
33. Wakao, H., F. Gouilleux, and B. Groner. 1994. Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J. 13:2182-2191.
34. Yao, Z., Y. Cui, W.T. Watford, J.H. Bream, K. Yamaoka, B.D. Hissong, D. Li, S.K. Durum, Q. Jiang, A. Bhandoola, et al. 2006. Stat5a/b are essential for normal lymphoid development and differentiation. Proc. Natl. Acad. Sci. USA. 103:1000-1005. http://dx.doi.org/10.1073/pnas.0507350103.
35. Yasuda, H., N. Shima, N. Nakagawa, K. Yamaguchi, M. Kinosaki, S. Mochizuki, A. Tomoyasu, K. Yano, M. Goto, A. Murakami, et al. 1998. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesisinhibitory factor and is identical to TRANCE/RANKL. Proc. Natl. Acad. Sci. USA. 95:3597-3602. http://dx.doi.org/10.1073/pnas.95.7.3597.