Macrophage fusion is controlled by the cytoplasmic protein tyrosine phosphatase PTP-PEST/PTPN12

Molecular and Cellular Biology

Volumn 33, Issue 12, 2013, Pages 2458-2469

  Rhee, Inmoo ^a,b   Davidson, Dominique ^a   Souza, Cleiton Martins ^a   Vacher, Jean ^a,b,c   Veillette, André ^a,b,c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTEGRIN; CD47 ANTIGEN; FOCAL ADHESION KINASE 2; INTERLEUKIN 4; MONOCYTE CHEMOTACTIC PROTEIN 1; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 12; OSTEOCLAST DIFFERENTIATION FACTOR; PAXILLIN; UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FUSION; CELL MIGRATION; CELL PROLIFERATION; CELL SPREADING; CYTOKINE PRODUCTION; FOREIGN BODY; GIANT CELL; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MACROPHAGE FUSION; MOUSE; NONHUMAN; OSTEOCLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; ANTIGENS, CD47; CADHERINS; CELL DIFFERENTIATION; CELL FUSION; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; CHEMOKINE CCL2; FOCAL ADHESION KINASE 2; GIANT CELLS; INTEGRIN BETA CHAINS; INTERLEUKIN-4; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOCLASTS; PAXILLIN; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 12; RANK LIGAND;

EID: 84878971365     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00197-13     Document Type: Article

References (52)

1. Helming L, Gordon S. 2009. Molecular mediators of macrophage fusion. Trends Cell Biol. 19:514-522.
2. Vignery A. 2008. Macrophage fusion: molecular mechanisms. Methods Mol. Biol. 475:149-161.
3. McNally AK, Anderson JM. 2011. Macrophage fusion and multinucleated giant cells of inflammation. Adv. Exp. Med. Biol. 713:97-111.
4. Murphy K, Travers P, Walport M, Janeway C. 2008. Immunobiology, 7th ed. Garland Science, New York, NY.
5. Lay G, Poquet Y, Salek-Peyron P, Puissegur MP, Botanch C, Bon H, Levillain F, Duteyrat JL, Emile JF, Altare F. 2007. Langhans giant cells from M. tuberculosis-induced human granulomas cannot mediate mycobacterial uptake. J. Pathol. 211:76-85.
6. Yang Q, Co D, Sommercorn J, Tonks NK. 1993. Cloning and expression of PTP-PEST. A novel, human, nontransmembrane protein tyrosine phosphatase. J. Biol. Chem. 268:17650.
7. Charest A, Wagner J, Muise ES, Heng HH, Tremblay ML. 1995. Structure of the murine MPTP-PEST gene: genomic organization and chromosomal mapping. Genomics 28:501-507.
8. Veillette A, Rhee I, Souza CM, Davidson D. 2009. PEST family phosphatases in immunity, autoimmunity, and autoinflammatory disorders. Immunol. Rev. 228:312-324.
9. Garton AJ, Flint AJ, Tonks NK. 1996. Identification of p130(cas) as a substrate for the cytosolic protein tyrosine phosphatase PTP-PEST. Mol. Cell. Biol. 16:6408-6418.
10. Davidson D, Cloutier JF, Gregorieff A, Veillette A. 1997. Inhibitory tyrosine protein kinase p50csk is associated with protein-tyrosine phosphatase PTP-PEST in hemopoietic and non-hemopoietic cells. J. Biol. Chem. 272:23455-23462.
11. Cote JF, Charest A, Wagner J, Tremblay ML. 1998. Combination of gene targeting and substrate trapping to identify substrates of protein tyrosine phosphatases using PTP-PEST as a model. Biochemistry 37:13128-13137.
12. Shen Y, Schneider G, Cloutier JF, Veillette A, Schaller MD. 1998. Direct association of protein-tyrosine phosphatase PTP-PEST with paxillin. J. Biol. Chem. 273:6474-6481.
13. Cote JF, Chung PL, Theberge JF, Halle M, Spencer S, Lasky LA, Tremblay ML. 2002. PSTPIP is a substrate of PTP-PEST and serves as a scaffold guiding PTP-PEST toward a specific dephosphorylation of WASP. J. Biol. Chem. 277:2973-2986.
14. Garton AJ, Tonks NK. 1999. Regulation of fibroblast motility by the protein tyrosine phosphatase PTP-PEST. J. Biol. Chem. 274:3811-3818.
15. Sastry SK, Lyons PD, Schaller MD, Burridge K. 2002. PTP-PEST controls motility through regulation of Rac1. J. Cell Sci. 115:4305- 4316.
16. Angers-Loustau A, Cote JF, Charest A, Dowbenko D, Spencer S, Lasky LA, Tremblay ML. 1999. Protein tyrosine phosphatase-PEST regulates focal adhesion disassembly, migration, and cytokinesis in fibroblasts. J. Cell Biol. 144:1019-1031.
17. Sirois J, Cote JF, Charest A, Uetani N, Bourdeau A, Duncan SA, Daniels E, Tremblay ML. 2006. Essential function of PTP-PEST during mouse embryonic vascularization, mesenchyme formation, neurogenesis and early liver development. Mech. Dev. 123:869-880.
18. Souza CM, Davidson D, Rhee I, Gratton JP, Davis EC, Veillette A. 2012. The phosphatase PTP-PEST/PTPN12 regulates endothelial cell migration and adhesion, but not permeability, and controls vascular development and embryonic viability. J. Biol. Chem. 287:43180-43190.
19. Davidson D, Shi X, Zhong MC, Rhee I, Veillette A. 2010. The phosphatase PTP-PEST promotes secondary T cell responses by dephosphorylating the protein tyrosine kinase Pyk2. Immunity 33:167-180.
20. Sun T, Aceto N, Meerbrey KL, Kessler JD, Zhou C, Migliaccio I, Nguyen DX, Pavlova NN, Botero M, Huang J, Bernardi RJ, Schmitt E, Hu G, Li MZ, Dephoure N, Gygi SP, Rao M, Creighton CJ, Hilsenbeck SG, Shaw CA, Muzny D, Gibbs RA, Wheeler DA, Osborne CK, Schiff R, Bentires-Alj M, Elledge SJ, Westbrook TF. 2011. Activation of multiple proto-oncogenic tyrosine kinases in breast cancer via loss of the PTPN12 phosphatase. Cell 144:703-718.
21. Hume DA, Gordon S. 1983. 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.
22. Davidson D, Veillette A. 2001. PTP-PEST, a scaffold protein tyrosine phosphatase, negatively regulates lymphocyte activation by targeting a unique set of substrates. EMBO J. 20:3414-3426.
23. Cloutier JF, Veillette A. 1996. Association of inhibitory tyrosine protein kinase p50csk with protein tyrosine phosphatase PEP in T cells and other hemopoietic cells. EMBO J. 15:4909-4918.
24. Veillette A, Thibaudeau E, Latour S. 1998. High expression of inhibitory receptor SHPS-1 and its association with protein-tyrosine phosphatase SHP-1 in macrophages. J. Biol. Chem. 273:22719-22728.
25. Helming L, Gordon S. 2007. Macrophage fusion induced by IL-4 alternative activation is a multistage process involving multiple target molecules. Eur. J. Immunol. 37:33- 42.
26. Ryan GB, Spector WG. 1970. Macrophage turnover in inflamed connective tissue. Proc. R. Soc. Lond. B Biol. Sci. 174:269-292.
27. Ferron M, Boudiffa M, Arsenault M, Rached M, Pata M, Giroux S, Elfassihi L, Kisseleva M, Majerus PW, Rousseau F, Vacher J. 2011. Inositol polyphosphate 4-phosphatase B as a regulator of bone mass in mice and humans. Cell Metab. 14:466-477.
28. Buckbinder L, Crawford DT, Qi H, Ke HZ, Olson LM, Long KR, Bonnette PC, Baumann AP, Hambor JE, Grasser WA, III, Pan LC, Owen TA, Luzzio MJ, Hulford CA, Gebhard DF, Paralkar VM, Simmons HA, Kath JC, Roberts WG, Smock SL, Guzman-Perez A, Brown TA, Li M. 2007. Proline-rich tyrosine kinase 2 regulates osteoprogenitor cells and bone formation, and offers an anabolic treatment approach for osteoporosis. Proc. Natl. Acad. Sci. U. S. A. 104:10619-10624.
29. Veillette A, Bookman MA, Horak EM, Bolen JB. 1988. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell 55:301-308.
30. Goren I, Allmann N, Yogev N, Schurmann C, Linke A, Holdener M, Waisman A, Pfeilschifter J, Frank S. 2009. A transgenic mouse model of inducible macrophage depletion: effects of diphtheria toxin-driven lysozyme M-specific cell lineage ablation on wound inflammatory, angiogenic, and contractive processes. Am. J. Pathol. 175:132-147.
31. Anderson JM. 2000. Multinucleated giant cells. Curr. Opin. Hematol. 7:40-47.
32. Collin-Osdoby P, Osdoby P. 2012. RANKL-mediated osteoclast formation from murine RAW 264.7 cells. Methods Mol. Biol. 816:187-202.
33. Schindler C, Levy DE, Decker T. 2007. JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282:20059-20063.
34. Gordon S, Martinez FO. 2010. Alternative activation of macrophages: mechanism and functions. Immunity 32:593- 604.
35. Kyriakides TR, Foster MJ, Keeney GE, Tsai A, Giachelli CM, Clark-Lewis I, Rollins BJ, Bornstein P. 2004. The CC chemokine ligand, CCL2/ MCP1, participates in macrophage fusion and foreign body giant cell formation. Am. J. Pathol. 165:2157-2166.
36. McNally AK, Anderson JM. 2002. Beta1 and beta2 integrins mediate adhesion during macrophage fusion and multinucleated foreign body giant cell formation. Am. J. Pathol. 160:621-630.
37. Skokos EA, Charokopos A, Khan K, Wanjala J, Kyriakides TR. 2011. Lack of TNF-alpha-induced MMP-9 production and abnormal Ecadherin redistribution associated with compromised fusion in MCP-1-null macrophages. Am. J. Pathol. 178:2311-2321.
38. Van den Bossche J, Bogaert P, van Hengel J, Guerin CJ, Berx G, Movahedi K, Van den Bergh R, Pereira-Fernandes A, Geuns JM, Pircher H, Dorny P, Grooten J, De Baetselier P, Van Ginderachter JA. 2009. Alternatively activated macrophages engage in homotypic and heterotypic interactions through IL-4 and polyamine-induced E-cadherin/ catenin complexes. Blood 114:4664-4674.
39. Moreno JL, Mikhailenko I, Tondravi MM, Keegan AD. 2007. 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.
40. Frame M, Norman J. 2008. A tal(in) of cell spreading. Nat. Cell Biol. 10:1017-1019.
41. Wells CM, Walmsley M, Ooi S, Tybulewicz V, Ridley AJ. 2004. Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration. J. Cell Sci. 117:1259-1268.
42. Bhavsar PJ, Vigorito E, Turner M, Ridley AJ. 2009. Vav GEFs regulate macrophage morphology and adhesion-induced Rac and Rho activation. Exp. Cell Res. 315:3345-3358.
43. Avraham H, Park SY, Schinkmann K, Avraham S. 2000. RAFTK/Pyk2-mediated cellular signalling. Cell. Signal. 12:123-133.
44. Hagel M, George EL, Kim A, Tamimi R, Opitz SL, Turner CE, Imamoto A, Thomas SM. 2002. The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol. Cell. Biol. 22:901-915.
45. Tse KW, Dang-Lawson M, Lee RL, Vong D, Bulic A, Buckbinder L, Gold MR. 2009. B cell receptor-induced phosphorylation of Pyk2 and focal adhesion kinase involves integrins and the Rap GTPases and is required for B cell spreading. J. Biol. Chem. 284:22865-22877.
46. Bonnette PC, Robinson BS, Silva JC, Stokes MP, Brosius AD, Baumann A, Buckbinder L. 2010. Phosphoproteomic characterization of PYK2 signaling pathways involved in osteogenesis. J. Proteomics 73:1306-1320.
47. Guimaraes CR, Rai BK, Munchhof MJ, Liu S, Wang J, Bhattacharya SK, Buckbinder L. 2011. Understanding the impact of the P-loop conformation on kinase selectivity. J. Chem. Inf. Model. 51:1199-1204.
48. Li X, Earp HS. 1997. Paxillin is tyrosine-phosphorylated by and preferentially associates with the calcium-dependent tyrosine kinase in rat liver epithelial cells. J. Biol. Chem. 272:14341-14348.
49. Helming L, Tomasello E, Kyriakides TR, Martinez FO, Takai T, Gordon S, Vivier E. 2008. Essential role of DAP12 signaling in macrophage programming into a fusion-competent state. Sci. Signal. 1:ra11. doi:10.1126 /scisignal.1159665.
50. Takeda Y, Tachibana I, Miyado K, Kobayashi M, Miyazaki T, Funakoshi T, Kimura H, Yamane H, Saito Y, Goto H, Yoneda T, Yoshida M, Kumagai T, Osaki T, Hayashi S, Kawase I, Mekada E. 2003. Tetraspanins CD9 and CD81 function to prevent the fusion of mononuclear phagocytes. J. Cell Biol. 161:945-956.
51. Honda H, Nakamoto T, Sakai R, Hirai H. 1999. p130(Cas), an assembling molecule of actin filaments, promotes cell movement, cell migration, and cell spreading in fibroblasts. Biochem. Biophys. Res. Commun. 262: 25-30.
52. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, Nomura S, Fujimoto J, Okada M, Yamamoto T. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377:539-544.