Siglec-15 protein regulates formation of functional osteoclasts in concert with DNAX-activating protein of 12 kDa (DAP12)

Journal of Biological Chemistry

Volumn 287, Issue 21, 2012, Pages 17493-17502

  Ishida Kitagawa, Norihiro ^a   Tanaka, Kunitaro ^a   Bao, Xilinqiqige ^a   Kimura, Takanori ^a   Miura, Tadashi ^a   Kitaoka, Yoshiki ^a   Hayashi, Kouhei ^a   Sato, Mizuho ^a,b   Maruoka, Masahiro ^a,c   Ogawa, Takuya ^a   Miyoshi, Jun ^d   Takeya, Tatsuo ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c TOHOKU UNIVERSITY   (Japan)

^d OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BONE; CELL PROLIFERATION; CELL SIGNALING; CHEMICAL ACTIVATION; CYTOLOGY; GENE ENCODING; LIGANDS;

CYTOPLASMIC REGIONS; IMMUNORECEPTOR TYROSINE-BASED ACTIVATION MOTIFS; MULTINUCLEATED CELLS; MULTINUCLEATED GIANT CELLS; NUCLEAR FACTOR OF ACTIVATED T-CELLS; OSTEOCLAST FORMATION; RECEPTOR ACTIVATOR; TRANSMEMBRANE REGIONS;

PROTEINS;

ACTIN; KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; LECTIN; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEIN KINASE SYK; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; SIGLEC 15 PROTEIN; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFAT2; UNCLASSIFIED DRUG; VITRONECTIN;

ANIMAL CELL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; GENETIC CODE; INTRACELLULAR SIGNALING; MOUSE; MULTINUCLEAR CELL; MUTATIONAL ANALYSIS; NONHUMAN; OSTEOCLASTOGENESIS; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; STRUCTURE ACTIVITY RELATION;

EID: 84861213722     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.324194     Document Type: Article

References (39)

1. Väänänen, H. K., and Laitala-Leinonen, T. (2008) Osteoclast lineage and function. Arch. Biochem. Biophys. 473, 132-138
2. Suda, T., Takahashi, N., Udagawa, N., Jimi, E., Gillespie, M. T., and Martin, T. J. (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 (Pubitemid 30649812)
3. Boyle, W. J., Simonet, W. S., and Lacey, D. L. (2003) Osteoclast differentiation and activation. Nature 423, 337-342 (Pubitemid 40852708)
4. Boyce, B. F., and Xing, L. (2008) Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch. Biochem. Biophys. 473, 139-146
5. Nakashima, T., and Takayanagi, H. (2009) Osteoclasts and the immune system. J. Bone Miner. Metab. 27, 519-529
6. Kaifu, T., Nakahara, J., Inui, M., Mishima, K., Momiyama, T., Kaji, M., Sugahara, A., Koito, H., Ujike-Asai, A., Nakamura, A., Kanazawa, K., Tan-Takeuchi, K., Iwasaki, K., Yokoyama, W. M., Kudo, A., Fujiwara, M., Asou, H., and Takai, T. (2003) Osteopetrosis and thalamic hypomyelinosis with synaptic degeneration in DAP12-deficient mice. J. Clin. Invest. 111, 323-332 (Pubitemid 36182208)
7. Koga, T., Inui, M., Inoue, K., Kim, S., Suematsu, A., Kobayashi, E., Iwata, T., Ohnishi, H., Matozaki, T., Kodama, T., Taniguchi, T., Takayanagi, H., and Takai, T. (2004) Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 428, 758-763 (Pubitemid 38508286)
8. Mócsai, A., Humphrey, M. B., Van Ziffle, J. A., Hu, Y., Burghardt, A., Spusta, S. C., Majumdar, S., Lanier, L. L., Lowell, C. A., and Nakamura, M. C. (2004) The immunomodulatory adapter proteins DAP12 and Fc receptor γ-chain (FcRγ) regulate development of functional osteoclasts through the Syk tyrosine kinase. Proc. Natl. Acad. Sci. U.S.A. 101, 6158-6163 (Pubitemid 38520544)
9. Aoki, N., Kimura, S., Takiyama, Y., Atsuta, Y., Abe, A., Sato, K., and Katagiri, M. (2000) The role of the DAP12 signal in mouse myeloid differentiation. J. Immunol. 165, 3790-3796 (Pubitemid 32057285)
10. Gingras, M. C., Lapillonne, H., and Margolin, J. F. (2002) TREM-1, MDL-1, and DAP12 expression is associated with a mature stage of myeloid development. Mol. Immunol. 38, 817-824 (Pubitemid 34260883)
11. Humphrey, M. B., Ogasawara, K., Yao, W., Spusta, S. C., Daws, M. R., Lane, N. E., Lanier, L. L., and Nakamura, M. C. (2004) The signaling adapter protein DAP12 regulates multinucleation during osteoclast development. J. Bone Miner. Res. 19, 224-234 (Pubitemid 38116736)
12. Inui, M., Kikuchi, Y., Aoki, N., Endo, S., Maeda, T., Sugahara-Tobinai, A., Fujimura, S., Nakamura, A., Kumanogoh, A., Colonna, M., and Takai, T. (2009) Signal adaptor DAP10 associates with MDL-1 and triggers osteoclastogenesis in cooperation with DAP12. Proc. Natl. Acad. Sci. U.S.A. 106, 4816-4821
13. Ishida, N., Hayashi, K., Hoshijima, M., Ogawa, T., Koga, S., Miyatake, Y., Kumegawa, M., Kimura, T., and Takeya, T. (2002) Large scale gene expression analysis of osteoclastogenesis in vitro and elucidation of NFAT2 as a key regulator. J. Biol. Chem. 277, 41147-41156 (Pubitemid 35215706)
14. Asagiri, M., Sato, K., Usami, T., Ochi, S., Nishina, H., Yoshida, H., Morita, I., Wagner, E. F., Mak, T. W., Serfling, E., and Takayanagi, H. (2005) Autoamplification of NFATc1 expression determines its essential role in bone homeostasis. J. Exp. Med. 202, 1261-1269 (Pubitemid 41586956)
15. Kojima, T., and Kitamura, T. (1999) A signal sequence trap based on a constitutively active cytokine receptor. Nat. Biotechnol. 17, 487-490 (Pubitemid 29217903)
16. Crocker, P. R., Paulson, J. C., and Varki, A. (2007) Siglecs and their roles in the immune system. Nat. Rev. Immunol. 7, 255-266 (Pubitemid 46480955)
17. Angata, T., Tabuchi, Y., Nakamura, K., and Nakamura, M. (2007) Siglec-15. An immune system Siglec conserved throughout vertebrate evolution. Glycobiology 17, 838-846 (Pubitemid 47241821)
18. Takahata, M., Iwasaki, N., Nakagawa, H., Abe, Y., Watanabe, T., Ito, M., Majima, T., and Minami, A. (2007) Sialylation of cell surface glycoconjugates is essential for osteoclastogenesis. Bone 41, 77-86 (Pubitemid 46891898)
19. Ogawa, T., Ishida-Kitagawa, N., Tanaka, A., Matsumoto, T., Hirouchi, T., Akimaru, M., Tanihara, M., Yogo, K., and Takeya, T. (2006) A novel role of serine (L-Ser) for the expression of nuclear factor of activated T cells (NFAT) 2 in receptor activator of nuclear factor κB ligand (RANKL)-induced osteoclastogenesis in vitro. J. Bone Miner. Metab. 24, 373-379 (Pubitemid 44306173)
20. Yogo, K., Mizutamari, M., Mishima, K., Takenouchi, H., Ishida-Kitagawa, N., Sasaki, T., and Takeya, T. (2006) Src homology 2 (SH2)-containing 5′-inositol phosphatase localizes to podosomes, and the SH2 domain is implicated in the attenuation of bone resorption in osteoclasts. Endocrinology 147, 3307-3317 (Pubitemid 43901121)
21. Meiyanto, E., Hoshijima, M., Ogawa, T., Ishida, N., and Takeya, T. (2001) Osteoclast differentiation factor modulates cell cycle machinery and causes a delay in S phase progression in RAW264 cells. Biochem. Biophys. Res. Commun. 282, 278-283 (Pubitemid 32924376)
22. Bao, X., Ogawa, T., Se, S., Akiyama, M., Bahtiar, A., Takeya, T., and Ishida-Kitagawa, N. (2011) Acid sphingomyelinase regulates osteoclastogenesis by modulating sphingosine kinases downstream of RANKL signaling. Biochem. Biophys. Res. Commun. 405, 533-537
23. Akagi, T., Sasai, K., and Hanafusa, H. (2003) Refractory nature of normal human diploid fibroblasts with respect to oncogene-mediated transformation. Proc. Natl. Acad. Sci. U.S.A. 100, 13567-13572 (Pubitemid 37444782)
24. Suzuki, J., Fukuda, M., Kawata, S., Maruoka, M., Kubo, Y., Takeya, T., and Shishido, T. (2006) A rapid protein expression and purification system using Chinese hamster ovary cells expressing retrovirus receptor. J. Biotechnol. 126, 463-474 (Pubitemid 44634811)
25. 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 (Pubitemid 39491590)
26. Matsuo, K., Galson, D. L., Zhao, C., Peng, L., Laplace, C., Wang, K. Z., Bachler, M. A., Amano, H., Aburatani, H., Ishikawa, H., and Wagner, E. F. (2004) Nuclear factor of activated T-cells (NFAT) rescues osteoclastogenesis in precursors lacking c-Fos. J. Biol. Chem. 279, 26475-26480 (Pubitemid 38798801)
27. Ishida, N., Hayashi, K., Hattori, A., Yogo, K., Kimura, T., and Takeya, T. (2006) CCR1 acts downstream of NFAT2 in osteoclastogenesis and enhances cell migration. J. Bone Miner. Res. 21, 48-57 (Pubitemid 43023226)
28. -/- osteoclast phenotype. J. Cell. Biochem. 90, 871-883
29. Zou, W., Zhu, T., Craft, C. S., Broekelmann, T. J., Mecham, R. P., and Teitelbaum, S. L. (2010) Cytoskeletal dysfunction dominates in DAP12-deficient osteoclasts. J. Cell Sci. 123, 2955-2963
30. Zou, W., Reeve, J. L., Liu, Y., Teitelbaum, S. L., and Ross, F. P. (2008) DAP12 couples c-Fms activation to the osteoclast cytoskeleton by recruitment of Syk. Mol. Cell 31, 422-431
31. Zou, W., Kitaura, H., Reeve, J., Long, F., Tybulewicz, V. L., Shattil, S. J., Ginsberg, M. H., Ross, F. P., and Teitelbaum, S. L. (2007) Syk, c-Src, the αvβ3 integrin, and ITAM immunoreceptors, in concert, regulate osteoclastic bone resorption. J. Cell Biol. 176, 877-888 (Pubitemid 46425547)
32. Faccio, R., Teitelbaum, S. L., Fujikawa, K., Chappel, J., Zallone, A., Tybulewicz, V. L., Ross, F. P., and Swat, W. (2005) Vav3 regulates osteoclast function and bone mass. Nat. Med. 11, 284-290 (Pubitemid 40460556)
33. Hiruma, Y., Hirai, T., and Tsuda, E. (2011) Siglec-15, a member of the sialic acid-binding lectin, is a novel regulator for osteoclast differentiation. Biochem. Biophys. Res. Commun. 409, 424-429
34. Humphrey, M. B., Daws, M. R., Spusta, S. C., Niemi, E. C., Torchia, J. A., Lanier, L. L., Seaman, W. E., and Nakamura, M. C. (2006) TREM2, a DAP12-associated receptor, regulates osteoclast differentiation and function. J. Bone Miner. Res. 21, 237-245 (Pubitemid 43265289)
35. Cella, M., Buonsanti, C., Strader, C., Kondo, T., Salmaggi, A., and Colonna, M. (2003) Impaired differentiation of osteoclasts in TREM-2-deficient individuals. J. Exp. Med. 198, 645-651 (Pubitemid 37040398)
36. Paloneva, J., Mandelin, J., Kiialainen, A., Bohling, T., Prudlo, J., Hakola, P., Haltia, M., Konttinen, Y. T., and Peltonen, L. (2003) DAP12/TREM2 deficiency results in impaired osteoclast differentiation and osteoporotic features. J. Exp. Med. 198, 669-675 (Pubitemid 37045349)
37. Paloneva, J., Kestilä, M., Wu, J., Salminen, A., Böhling, T., Ruotsalainen, V., Hakola, P., Bakker, A. B., Phillips, J. H., Pekkarinen, P., Lanier, L. L., Timonen, T., and Peltonen, L. (2000) Loss-of-function mutations in TYROBP (DAP12) result in a presenilin dementia with bone cysts. Nat. Genet. 25, 357-361 (Pubitemid 30437329)
38. Paloneva, J., Manninen, T., Christman, G., Hovanes, K., Mandelin, J., Adolfsson, R., Bianchin, M., Bird, T., Miranda, R., Salmaggi, A., Tranebjaerg, L., Konttinen, Y., and Peltonen, L. (2002) Mutations in two genes encoding different subunits of a receptor signaling complex result in an identical disease phenotype. Am. J. Hum. Genet. 71, 656-662 (Pubitemid 34970138)
39. Colonna, M., Turnbull, I., and Klesney-Tait, J. (2007) The enigmatic function of TREM-2 in osteoclastogenesis. Adv. Exp. Med. Biol. 602, 97-105