Essential role of DAP12 signaling in macrophage programming into a fusion-competent state

Science Signaling

Volumn 1, Issue 43, 2008, Pages

  Helming, Laura ^a,j   Tomasello, Elena ^b,c,d   Kyriakides, Themis R ^e,f   Martinez, Fernando O ^a   Takai, Toshiyuki ^g,h   Gordon, Siamon ^a   Vivier, Eric ^b,c,d,i  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^c INSERM   (France)

^d CNRS   (France)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g TOHOKU UNIVERSITY   (Japan)

^h JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

ⁱ HÔPITAL DE LA CONCEPTION   (France)

^j TECHNICAL UNIVERSITY OF MUNICH   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN RECEPTOR; MEMBRANE PROTEIN; PROTEIN KINASE SYK; PROTEIN TYROSINE KINASE; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TREM2 PROTEIN, MOUSE; TYROBP PROTEIN, MOUSE; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; C57BL MOUSE; CELL FUSION; GENE EXPRESSION REGULATION; GENETICS; INFLAMMATION; MACROPHAGE; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL FUSION; CYTOKINES; GENE EXPRESSION REGULATION; INFLAMMATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; PROTEIN-TYROSINE KINASES; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION;

EID: 58149195670     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.1159665     Document Type: Article

References (51)

1. T. Langhans, Ueber Riesenzellen mit wandständigen Kernen in Tuberkeln und die fibröse Form des Tuberkels. Virchows Arch. Pathol. Anat. 42, 382-404 (1868).
2. J. M. Anderson, Multinucleated giant cells. Curr. Opin. Hematol. 7, 40-47 (2000).
3. L. Helming, S. Gordon, The molecular basis of macrophage fusion. Immunobiology 212, 785-793 (2008).
4. T. J. Chambers, W. G. Spector, Inflammatory giant cells. Immunobiology 161, 283-289 (1982).
5. E. H. Chen, E. Grote, W. Mohler, A. Vignery, Cell-cell fusion. FEBS Lett. 581, 2181-2193 (2007).
6. B. Huppertz, C. Bartz, M. Kokozidou, Trophoblast fusion: Fusogenic proteins, syncytins and ADAMS, and other prerequisites for syncytial fusion. Micron 37, 509-517 (2006).
7. Q. Zhao, N. Topham, J. M. Anderson, A. Hiltner, G. Lodoen, C. R. Payet, Foreignbody giant cells and polyurethane biostability: In vivo correlation of cell adhesion and surface cracking. J. Biomed. Mater. Res. 25, 177-183 (1991).
8. T. F. Byrd, Multinucleated giant cell formation induced by IFN-gamma/IL-3 is associated with restriction of virulent Mycobacterium tuberculosis cell to cell invasion in human monocyte monolayers. Cell Immunol. 188, 89-96 (1998).
9. X. W. Zhu, N. M. Price, R. H. Gilman, S. Recarvarren, J. S. Friedland, Multinucleate giant cells release functionally unopposed matrix metalloproteinase-9 in vitro and in vivo. J. Infect. Dis. 196, 1076-1079 (2007).
10. A. Vignery, Macrophage fusion: The making of osteoclasts and giant cells. J. Exp. Med. 202, 337-340 (2005).
11. L. Helming, S. Gordon, Macrophage fusion induced by IL-4 alternative activation is a multistage process involving multiple target molecules. Eur. J. Immunol. 37, 33-42 (2007).
12. L. Olcese, A. Cambiaggi, G. Semenzato, C. Bottino, A. Moretta, E. Vivier, Human killer cell activatory receptors for MHC class I molecules are included in a multimeric complex expressed by natural killer cells. J. Immunol. 158, 5083-5086 (1997).
13. E. Tomasello, L. Olcese, F. Vely, C. Geourgeon, M. Blery, A. Moqrich, D. Gautheret, M. Djabali, M. G. Mattei, E. Vivier, Gene structure, expression pattern, and biological activity of mouse killer cell activating receptor-associated protein (KARAP)/DAP-12. J. Biol. Chem. 273, 34115-34119 (1998).
14. L. L. Lanier, B. C. Corliss, J. Wu, C. Leong, J. H. Phillips, Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391, 703-707 (1998).
15. J. Paloneva, J. Mandelin, A. Kiialainen, T. Bohling, J. Prudlo, P. Hakola, M. Haltia, Y. T. Konttinen, L. Peltonen, DAP12/TREM2 deficiency results in impaired osteoclast differentiation and osteoporotic features. J. Exp. Med. 198, 669-675 (2003).
16. T. Kaifu, J. Nakahara, M. Inui, K. Mishima, T. Momiyama, M. Kaji, A. Sugahara, H. Koito, A.Ujike-Asai, A.Nakamura, K.Kanazawa, K.Tan-Takeuchi,K. Iwasaki, W.M.Yokoyama, A. Kudo,M. Fujiwara, H. Asou, T. Takai, Osteopetrosis and thalamic hypomyelinosis with synaptic degeneration in DAP12-deficient mice. J. Clin. Invest. 111, 323-332 (2003).
17. L. L. Lanier, A. B. Bakker, The ITAM-bearing transmembrane adaptor DAP12 in lymphoid and myeloid cell function. Immunol. Today 21, 611-614 (2000).
18. E. Tomasello, E. Vivier, KARAP/DAP12/TYROBP: Three names and a multiplicity of biological functions. Eur. J. Immunol. 35, 1670-1677 (2005).
19. I. R. Turnbull, M. Colonna, Activating and inhibitory functions of DAP12. Nat. Rev. Immunol. 7, 155-161 (2007).
20. E. Vivier, J. A. Nunes, F. Vely, Natural killer cell signaling pathways. Science 306, 1517-1519 (2004).
21. A. S. Tessarz, A. Cerwenka, The TREM-1/DAP12 pathway. Immunol. Lett. 116, 111-116 (2008).
22. J. A. Hamerman, N. K. Tchao, C. A. Lowell, L. L. Lanier, Enhanced Toll-like receptor responses in the absence of signaling adaptor DAP12. Nat. Immunol. 6, 579-586 (2005).
23. J. A. Hamerman, J. R. Jarjoura, M. B. Humphrey, M. C. Nakamura, W. E. Seaman, L. L. Lanier, Cutting edge: Inhibition of TLR and FcR responses in macrophages by triggering receptor expressed on myeloid cells (TREM)-2 and DAP12. J. Immunol. 177, 2051-2055 (2006).
24. A. Mocsai, C. L. Abram, Z. Jakus, Y. Hu, L. L. Lanier, C. A. Lowell, Integrin signaling in neutrophils and macrophages uses adaptors containing immunoreceptor tyrosinebased activation motifs. Nat. Immunol. 7, 1326-1333 (2006).
25. J. Paloneva, M. Kestila, J. Wu, A. Salminen, T. Bohling, V. Ruotsalainen, P. Hakola, A. B. Bakker, J. H. Phillips, P. Pekkarinen, L. L. Lanier, T. Timonen, L. Peltonen, Lossof- function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts. Nat. Genet. 25, 357-361 (2000).
26. A. B. Bakker, R. M. Hoek, A. Cerwenka, B. Blom, L. Lucian, T. McNeil, R. Murray, L. H. Phillips, J. D. Sedgwick, L. L. Lanier, DAP12-deficient mice fail to develop autoimmunity due to impaired antigen priming. Immunity 13, 345-353 (2000).
27. E. Tomasello, P. O. Desmoulins, K. Chemin, S. Guia, H. Cremer, J. Ortaldo, P. Love, D. Kaiserlian, E. Vivier, Combined natural killer cell and dendritic cell functional deficiency in KARAP/DAP12 loss-of-function mutant mice. Immunity 13, 355-364 (2000).
28. S. Nataf, A. Anginot, C. Vuaillat, L. Malaval, N. Fodil, E. Chereul, J. B. Langlois, C. Dumontel, G. Cavillon, C. Confavreux, M. Mazzorana, L. Vico, M. F. Belin, E. Vivier, E. Tomasello, P. Jurdic, Brain and bone damage in KARAP/DAP12 loss-of-function mice correlate with alterations in microglia and osteoclast lineages. Am. J. Pathol. 166, 275-286 (2005).
29. M. B. Humphrey, K.Ogasawara, W. Yao, S. C. Spusta,M. R. Daws, N. E. Lane, L. L. Lanier, M. C. Nakamura, The signaling adapter protein DAP12 regulates multinucleation during osteoclast development. J. Bone Miner. Res. 19, 224-234 (2004).
30. T. Koga, M. Inui, K. Inoue, S. Kim, A. Suematsu, E. Kobayashi, T. Iwata, H. Ohnishi, T. Matozaki, T. Kodama, T. Taniguchi, H. Takayanagi, T. Takai, Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 428, 758-763 (2004).
31. W. Zou, H. Kitaura, J. Reeve, F. Long, V. L. Tybulewicz, S. J. Shattil, M. H. Ginsberg, F. P. Ross, S. L. Teitelbaum, Syk, c-Src, the alphavbeta3 integrin, and ITAM immunoreceptors, in concert, regulate osteoclastic bone resorption. J. Cell Biol. 176, 877-888 (2007).
32. M. Lucas, L. Daniel, E. Tomasello, S. Guia, N. Horschowski, N. Aoki, D. Figarella- Branger, S. Gomez, E. Vivier, Massive inflammatory syndrome and lymphocytic immunodeficiency in KARAP/DAP12-transgenic mice. Eur. J. Immunol. 32, 2653-2663 (2002).
33. N. Aoki, S. Kimura, Y. Takiyama, Y. Atsuta, A. Abe, K. Sato, M. Katagiri, The role of the DAP12 signal in mouse myeloid differentiation. J Immunol. 165, 3790-3796 (2000).
34. A. K. McNally, J. M. Anderson, Beta1 and beta2 integrins mediate adhesion during macrophage fusion and multinucleated foreign body giant cell formation. Am. J. Pathol. 160, 621-630 (2002).
35. S. M. Jay, E. Skokos, F. Laiwalla, M. M. Krady, T. R. Kyriakides, Foreign body giant cell formation is preceded by lamellipodia formation and can be attenuated by inhibition of Rac1 activation. Am. J. Pathol. 171, 632-640 (2007).
36. M. Turner, P. J. Mee, P. S. Costello, O. Williams, A. A. Price, L. P. Duddy, M. T. Furlong, R. L. Geahlen, V. L. Tybulewicz, Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature 378, 298-302 (1995).
37. J. L. Moreno, I. Mikhailenko, M. M. Tondravi, A. D. Keegan, IL-4 promotes the formation of multinucleated giant cells from macrophage precursors by a STAT6- dependent, homotypic mechanism: Contribution of E-cadherin. J. Leukoc. Biol. 82, 1542-1553 (2007).
38. M. Yagi, T. Miyamoto, Y. Sawatani, K. Iwamoto, N. Hosogane, N. Fujita, K. Morita, K. Ninomiya, T. Suzuki, K. Miyamoto, Y. Oike, M. Takeya, Y. Toyama, T. Suda, DCSTAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cells. J. Exp. Med. 202, 345-351 (2005).
39. H. Rosen, S. Gordon, Monoclonal antibody to the murine type 3 complement receptor inhibits adhesion of myelomonocytic cells in vitro and inflammatory cell recruitment in vivo. J. Exp. Med. 166, 1685-1701 (1987).
40. I. Fraser, D. Hughes, S. Gordon, Divalent cation-independent macrophage adhesion inhibited by monoclonal antibody to murine scavenger receptor. Nature 364, 343-346 (1993).
41. S. Mukhopadhyay, Y. Chen, M. Sankala, L. Peiser, T. Pikkarainen, G. Kraal, K. Tryggvason, S. Gordon, MARCO, an innate activation marker of macrophages, is a class A scavenger receptor for Neisseria meningitidis. Eur. J. Immunol. 36, 940-949 (2006).
42. T. R. Kyriakides, M. J. Foster, G. E. Keeney, A. Tsai, C. M. Giachelli, I. Clark-Lewis, B. J. Rollins, P. Bornstein, The CC chemokine ligand, CCL2/MCP1, participates in macrophage fusion and foreign body giant cell formation. Am. J. Pathol. 165, 2157-2166 (2004).
43. H. Jiang, M. B. Harris, P. Rothman, IL-4/IL-13 signaling beyond JAK/STAT. J. Allergy Clin. Immunol. 105, 1063-1070 (2000).
44. M. Terme, E. Tomasello, K. Maruyama, F. Crepineau, N. Chaput, C. Flament, J. P. Marolleau, E. Angevin, E. F. Wagner, B. Salomon, F. A. Lemonnier, H. Wakasugi, M. Colonna, E. Vivier, L. Zitvogel, IL-4 confers NK stimulatory capacity to murine dendritic cells: A signaling pathway involving KARAP/DAP12-triggering receptor expressed on myeloid cell 2 molecules. J. Immunol. 172, 5957-5966 (2004).
45. J. Paloneva, T. Manninen, G. Christman, K. Hovanes, J. Mandelin, R. Adolfsson, M. Bianchin, T. Bird, R. Miranda, A. Salmaggi, L. Tranebjaerg, Y. Konttinen, L. Peltonen, 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 (2002).
46. M. R. Daws, P. M. Sullam, E. C. Niemi, T. T. Chen, N. K. Tchao, W. E. Seaman, Pattern recognition by TREM-2: Binding of anionic ligands. J. Immunol. 171, 594-599 (2003).
47. M. B. Humphrey, M. R. Daws, S. C. Spusta, E. C. Niemi, J. A. Torchia, L. L. Lanier, W. E. Seaman, M. C. Nakamura, TREM2, a DAP12-associated receptor, regulates osteoclast differentiation and function. J. Bone Miner. Res. 21, 237-245 (2006).
48. S. G. Kamel Mohamed, E. Sugiyama, K. Shinoda, H. Hounoki, H. Taki, M. Maruyama, T. Miyahara, M. Kobayashi, Interleukin-4 inhibits RANKL-induced expression of NFATc1 and c-Fos: A possible mechanism for downregulation of osteoclastogenesis. Biochem. Biophys. Res. Commun. 329, 839-845 (2005).
49. H. Karasuyama, F. Melchers, Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4 or 5, using modified cDNA expression vectors. Eur. J. Immunol. 18, 97-104 (1988).
50. D. A. Hume, S. Gordon, Optimal conditions for proliferation of bone marrow-derived mouse macrophages in culture: The roles of CSF-1, serum, Ca2+, and adherence. J. Cell Physiol. 117, 189-194 (1983).
51. G. S. Herron, M. J. Banda, E. J. Clark, J. Gavrilovic, Z.Werb, Secretion of metalloproteinases by stimulated capillary endothelial cells. II. Expression of collagenase and stromelysin activities is regulated by endogenous inhibitors. J. Biol. Chem. 261, 2814-2818 (1986).