DAP12 Couples c-Fms Activation to the Osteoclast Cytoskeleton by Recruitment of Syk

Molecular Cell

Volumn 31, Issue 3, 2008, Pages 422-431

  Zou, Wei ^a   Reeve, Jennifer L ^a   Liu, Yuli ^a   Teitelbaum, Steven L ^a   Ross, F Patrick ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

SIGNALING

Indexed keywords

COLONY STIMULATING FACTOR 1; KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; MUTANT PROTEIN; PROTEIN; PROTEIN C FMS; PROTEIN KINASE SYK;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ENZYME REGULATION; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; WILD TYPE;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; ANIMALS; CYTOSKELETON; ENZYME ACTIVATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROPHAGE COLONY-STIMULATING FACTOR; MICE; OSTEOCLASTS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS PP60(C-SRC); RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS;

EID: 48349105543     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2008.06.023     Document Type: Article

References (42)

1. Barclay A.N., Wright G.J., Brooke G., and Brown M.H. CD200 and membrane protein interactions in the control of myeloid cells. Trends Immunol. 23 (2002) 285-290
2. Boyle W.J., Simonet W.S., and Lacey D.L. Osteoclast differentiation and activation. Nature 423 (2003) 337-342
3. Faccio R., Takeshita S., Zallone A., Ross F.P., and Teitelbaum S.L. c-Fms and the αvβ3 integrin collaborate during osteoclast differentiation. J. Clin. Invest. 111 (2003) 749-758
4. Faccio R., Zou W., Colaianni G., Teitelbaum S.L., and Ross F.P. High dose M-CSF partially rescues the Dap12-/- osteoclast phenotype. J. Cell. Biochem. 90 (2003) 871-883
5. Faccio R., Teitelbaum S.L., Fujikawa K., Chappel J., Zallone A., Tybulewicz V.L., Ross F.P., and Swat W. Vav3 regulates osteoclast function and bone mass. Nat. Med. 11 (2005) 284-290
6. Faccio R., Takeshita S., Colaianni G., Chappel J.C., Zallone A., Teitelbaum S.L., and Ross F.P. M-CSF regulates the cytoskeleton via recruitment of a multimeric signaling complex to c-Fms Tyr-Y559/697/721. J. Biol. Chem. 282 (2007) 18991-18999
7. Feldner J.C., and Brandt B.H. Cancer cell motility-on the road from c-erbB-2 receptor steered signaling to actin reorganization. Exp. Cell Res. 272 (2002) 93-108
8. Feng X., Takeshita S., Namba N., Wei S., Teitelbaum S.L., and Ross F.P. Tyrosines 559 and 807 in the cytoplasmic tail of the M-CSF receptor play distinct roles in osteoclast differentiation and function. Endocrinology 143 (2002) 4868-4874
9. Golden L.H., and Insogna K.L. The expanding role of PI3-kinase in bone. Bone 34 (2004) 3-12
10. Hamerman J.A., Tchao N.K., Lowell C.A., and Lanier L.L. Enhanced Toll-like receptor responses in the absence of signaling adaptor DAP12. Nat. Immunol. 6 (2005) 579-586
11. Hayashi A., Ohnishi H., Okazawa H., Nakazawa S., Ikeda H., Motegi S., Aoki N., Kimura S., Mikuni M., and Matozaki T. Positive regulation of phagocytosis by SIRPbeta and its signaling mechanism in macrophages. J. Biol. Chem. 279 (2004) 29450-29460
12. Insogna K.L., Sahni M., Grey A.B., Tanaka S., Horne W.C., Neff L., Mitnick M., Levy J.B., and Baron R. Colony-stimulating factor-1 induces cytoskeletal reorganization and c-src-dependent tyrosine phosphorylation of selected cellular proteins in rodent osteoclasts. J. Clin. Invest. 100 (1997) 2476-2485
13. Kaifu T., Nakahara J., Inui M., Mishima K., Momiyama T., Kaji M., Sugahara A., Koito H., Ujike-Asai A., Nakamura A., et al. Osteopetrosis and thalamic hypomyelinosis with synaptic degeneration in DAP12-deficient mice. J. Clin. Invest. 111 (2003) 323-332
14. Koga T., Inui M., Inoue K., Kim S., Suematsu A., Kobayashi E., Iwata T., Ohnishi H., Matozaki T., Kodama T., et al. Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 428 (2004) 758-763
15. Lanier L.L., Corliss B.C., Wu J., Leong C., and Phillips J.H. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391 (1998) 703-707
16. Lanier L.L., and Bakker A.B.H. The ITAM-bearing transmembrane adaptor DAP12 in lymphoid and myeloid cell function. Immunol. Today 21 (2000) 611-614
17. Looney M.R., Su X., Van Ziffle J.A., Lowell C.A., and Matthay M.A. Neutrophils and their Fc gamma receptors are essential in a mouse model of transfusion-related acute lung injury. J. Clin. Invest. 116 (2006) 1615-1623
18. McHugh K.P., Hodivala-Dilke K., Zheng M.H., Namba N., Lam J., Novack D., Feng X., Ross F.P., Hynes R.O., and Teitelbaum S.L. Mice lacking β3 integrins are osteosclerotic because of dysfunctional osteoclasts. J. Clin. Invest. 105 (2000) 433-440
19. McVicar D.W., and Burshtyn D.N. Intracellular signaling by the killer immunoglobulin-like receptors and Ly49. Sci. STKE 2001 (2001) RE1 10.1126/stke.2001.75.re1
20. Mocsai A., Zhou M., Meng F., Tybulewicz V.L., and Lowell C.A. Syk is required for integrin signaling in neutrophils. Immunity 16 (2002) 547-548
21. Mocsai 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. The immunomodulatory adapter proteins DAP12 and Fc receptor gamma-chain (FcRgamma) regulate development of functional osteoclasts through the Syk tyrosine kinase. Proc. Natl. Acad. Sci. USA 101 (2004) 6158-6163
22. Mocsai A., Abram C.L., Jakus Z., Hu Y., Lanier L.L., and Lowell C.A. Integrin signaling in neutrophils and macrophages uses adaptors containing immunoreceptor tyrosine-based activation motifs. Nat. Immunol. 7 (2006) 1326-1333
23. Nakahashi C., Tahara-Hanaoka S., Totsuka N., Okoshi Y., Takai T., Ohkohchi N., Honda S., Shibuya K., and Shibuya A. Dual assemblies of an activating immune receptor, MAIR-II, with ITAM-bearing adapters DAP12 and FcRgamma chain on peritoneal macrophages. J. Immunol. 178 (2007) 765-770
24. Obergfell A., Eto K., Mocsai A., Buensuceso C., Moores S.L., Brugge J.S., Lowell C.A., and Shattil S.J. Coordinate interactions of Csk, Src, and Syk kinases with αIIbß3 initiate integrin signaling to the cytoskeleton. J. Cell Biol. 157 (2002) 265-275
25. Onishi M., Nosaka T., Misawa K., Mui A.L.-F., Gorman D., McMahon M., Miyajima A., and Kitamura T. Identification and characterization of a constitutive active STAT5 mutant that promotes cell proliferation. Mol. Cell. Biol. 18 (1998) 3871-3879
26. Pitcher L.A., and van Oers N.S.C. T-cell receptor signal transmission: who gives an ITAM?. Trends Immunol. 24 (2003) 554-560
27. Pixley F.J., and Stanley E.R. CSF-1 regulation of the wandering macrophage: complexity in action. Trends Cell Biol. 14 (2004) 628-638
28. Ravetch J.V., and Kinet J.P. Fc receptors. Annu. Rev. Immunol. 9 (1991) 457-492
29. Ross F.P., and Teitelbaum S.L. αvβ3 and macrophage colony-stimulating factor: partners in osteoclast biology. Immunol. Rev. 208 (2005) 88-105
30. Takahashi K., Rochford C.D., and Neumann H. Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J. Exp. Med. 201 (2005) 647-657
31. Takaki R., Watson S.R., and Lanier L.L. DAP12: an adapter protein with dual functionality. Immunol. Rev. 214 (2006) 118-129
32. Takeshita S., Kaji K., and Kudo A. Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts. J. Bone Miner. Res. 15 (2000) 1477-1488
33. Takeshita S., Faccio R., Chappel J.C., Zheng L., Feng S., Weber J.D., Teitelbaum S.L., and Ross F.P. c-Fms tyrosine 559 Is a major mediator of M-CSF-induced proliferation of primary macrophages. J. Biol. Chem. 282 (2007) 18980-18990
34. Teitelbaum S.L., and Ross F.P. Genetic regulation of osteoclast development and function. Nat. Rev. Genet. 4 (2003) 638-649
35. Tomasello E., Olcese L., Vely F., Geourgeon C., Blery M., Moqrich A., Gautheret D., Djabali M., Mattei M.-G., and Vivier E. Gene structure, expression pattern, and biological activity of mouse killer cell activating receptor-associated protein (KARAP)/DAP-12. J. Biol. Chem. 273 (1998) 34115-34119
36. Tomasello E., Desmoulins P.-O., Chemin K., Guia S., Cremer H., Ortaldo J., Love P., Kaiserlian D., and Vivier E. Combined natural killer cell and dendritic cell functional deficiency in KARAP/DAP12 loss-of-function mutant mice. Immunity 13 (2000) 355-364
37. Turner M., Mee P.J., Costello P.S., Williams O., Price A.A., Duddy L.P., Furlong M.T., Geahlen R.L., and Tybulewicz V.L. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature 378 (1995) 298-302
38. Underhill D.M., and Goodridge H.S. The many faces of ITAMs. Trends Immunol. 28 (2007) 66-73
39. Vines C.M., Potter J.W., Xu Y., Geahlen R.L., Costello P.S., Tybulewicz V.L., Lowell C.A., Chang P.W., Gresham H.D., and Willman C.L. Inhibition of beta 2 integrin receptor and Syk kinase signaling in monocytes by the Src family kinase Fgr. Immunity 15 (2001) 507-519
40. Vivier E., Nunes J.A., and Vely F. Natural killer cell signaling pathways. Science 306 (2004) 1517-1519
41. Wu J., and Luo H. Recent advances on T-cell regulation by receptor tyrosine kinases. Curr. Opin. Hematol. 12 (2005) 292-297
42. Zou W., Kitaura H., Reeve J., Long F., Tybulewicz V.L.J., Shattil S.J., Ginsberg M.H., Ross F.P., and Teitelbaum S.L. Syk, c-Src, the αvβ3 integrin, and ITAM immunoreceptors, in concert, regulate osteoclastic bone resorption. J. Cell Biol. 176 (2007) 877-888