A critical role for Syk in signal transduction and phagocytosis mediated by Fcγ receptors on macrophages

Journal of Experimental Medicine

Volumn 186, Issue 7, 1997, Pages 1027-1039

  Crowley, Mary T ^a,c   Costello, Patrick S ^b   Fitzer Attas, Cheryl J ^a   Turner, Martin ^b   Meng, Fanying ^a   Lowell, Clifford ^a   Tybulewicz, Victor L J ^b   DeFranco, Anthony L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CYTOKINE; FC RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MONOCLONAL ANTIBODY; PHOSPHATIDYLINOSITOL 3 KINASE; T LYMPHOCYTE RECEPTOR; WORTMANNIN;

ANIMAL CELL; ARTICLE; ENZYME INHIBITION; ENZYME SUBSTRATE; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANDROSTADIENES; ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CYTOKINES; ENZYME PRECURSORS; ERYTHROCYTES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOPOLYSACCHARIDES; LIVER; MACROPHAGES; MICE; MICE, KNOCKOUT; MICROSPHERES; PHAGOCYTOSIS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RECEPTORS, IGG; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 0030829551     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.186.7.1027     Document Type: Article

References (49)

1. Ravetch, J.V., and J.P. Kinet. 1991. Fc receptors. Ann. Rev. Immunol. 9:457-492.
2. Brooks, D., and J.V. Ravetch. 1994. Fc receptor signaling. Adv. Exp. Med. Biol. 365:185-195.
3. Takai, T., M. Li, D. Sylvestre, R. Clynes, and J.V. Ravetch. 1994. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell. 76:519-529.
4. Takai, T., M. Ono, M. Hikida, H. Ohmori, and J.V. Ravetch. 1996. Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature (Lond.). 379: 346-349.
5. Ravetch, J.V. 1994. Fc receptors: rubor redux. Cell. 78: 553-560.
6. Stockinger, B. 1992. Capacity of antigen uptake by B cells, fibroblasts or macrophages determines efficiency of presentation of a soluble self antigen (C5) to T lymphocytes. Eur. J. Immunol. 22:1271-1278.
7. Greenberg, S., P. Chang, and S. Silverstein. 1993. Tyrosine phosphorylation is required for Fc receptor-mediated phagocytosis in mouse macrophages. J. Exp. Med. 177:529-534.
8. Indik, Z.K., J. Park, S. Hunter, and A. Schreiber. 1995. The molecular dissection of Fcγ receptor mediated phagocytosis. Blood. 86:4389-4399.
9. Hutchinson, M.J., P.T. Harrison, R.A. Floto, and J.M. Allen. 1995. Fc gamma receptor-mediated phagocytosis requires tyrosine kinase activity and is ligand independent. Eur. J. Immunol. 25:481-487.
10. Kiener, P.A., B.M. Rankin, A.L. Burkhardt, G.L. Schieven, L.K. Gilliland, R. Rowley, J.B. Bolen, and J.A. Ledbetter. 1993. Cross-linking of Fc gamma receptor I (Fc gamma RI) and receptor II (Fc gamma RII) on monocytic cells activates a signal transduction pathway common to both Fc receptors that involves the stimulation of p72 Syk protein tyrosine kinase. J. Biol. Chem. 268:24442-24448.
11. Durden, D.L., and Y.B. Liu. 1994. Protein-tyrosine kinase p72syk in Fc gamma RI receptor signaling. Blood. 84:2102-2108.
12. Darby, C., R.L. Geahlen, and A.D. Schreiber. 1994. Stimulation of macrophage Fc gamma RIIIA activates the receptor-associated protein tyrosine kinase Syk and induces phosphorylation of multiple proteins including p95Vav and p62/GAP-associated protein. J. Immunol. 152:5429-5437.
13. Greenberg, S., P. Chang, D. Wang, R. Xavier, and B. Seed. 1996. Clustered syk tyrosine kinase domains trigger phagocytosis. Proc. Natl. Acad. Sci. USA. 93:1103-1107.
14. Gold, M.R., D.A. Law, and A.L. DeFranco. 1990. Stimulation of protein tyrosine phosphorylation by the B-lymphocyte antigen receptor. Nature (Lond.). 345:810-813.
15. Richards, J.D., M.R. Gold, S.L. Hourihane, A.L. DeFranco, and L. Matsuuchi. 1996. Reconstitution of B cell antigen receptor-induced signaling events in a nonlymphoid cell line by expressing the Syk protein-tyrosine kinase. J. Biol. Chem. 271:6458-6466.
16. Hambleton, J., S.L. Weinstein, L. Lem, and A.L. DeFranco. 1996. Activation of c-Jun N-terminal kinase in bacterial lipopolysaccharide-stimulated macrophages. Proc. Natl. Acad. Sci. USA. 93:2774-2778.
17. Turner, M., P.J. Mee, P.S. Costello, O. Williams, A.A. Price, L.P. Duddy, M.T. Furlong, R.L. Geahlen, and V.L. Tybulewicz. 1995. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature (Lond.). 378:298-302.
18. Meng, F., and C.A. Lowell. 1997. Lipopolysaccharide (LPS)-induced macrophage activation and signal transduction in the absence of Src-family kinases Hck, Fgr, and Lyn. J. Exp. Med. 185:1661-1670.
19. Crowley, M.T., S.L. Harmer, and A.L. DeFranco. 1996. Activation-induced association of a 145-kDa tyrosine-phosphorylated protein with shc and syk in B lymphocytes and macrophages. J. Biol. Chem. 271:1145-1152.
20. DeFranco, A.L. 1995. Transmembrane signaling by antigen receptors of B and T lymphocytes. Curr. Biol. 7:163-175.
21. van Oers, N.S., N. Killeen, and A. Weiss. 1996. Lck regulates the tyrosine phosphorylation of the T cell receptor subunits and ZAP-70 in murine thymocytes. J. Exp. Med. 183:1053-1062.
22. Bewarder, N., V. Weinrich, P. Budde, D. Hartmann, H. Flaswinkel, M. Reth, and J. Frey. 1996. In vivo and in vitro specificity of protein tyrosine kinases for immunoglobulin G receptor (Fc gamma RII) phosphorylation. Mol. Cell. Biol. 16:4735-4743.
23. Johnson, S.A., C.M. Pleiman, L. Pao, J. Schneringer, K. Hippen, and J.C. Cambier. 1995. Phosphorylated immunoreceptor signaling motifs (ITAMs) exhibit unique abilities to bind and activate Lyn and Syk tyrosine kinases. J. Immunol. 155: 4596-4603.
24. Bernhard, W., A. Gbarah, and N. Sharon. 1992. Lectinophagocytosis of type 1 fimbriated (mannose-specific) Escherichia coli in the mouse peritoneum. J. Leukocyte Biol. 52:343-348.
25. Yamaya, M., T. Fukushima, K. Sekizawa, T. Ohrui, and H. Sasaki. 1995. Cytoplasmic motility reflects phagocytic activity in alveolar macrophages from dog lungs. Respir. Physiol. 101: 199-205.
26. Tuijnman, W.B., P.J. Capel, and J.G. van de Winkel. 1992. Human low-affinity IgG receptor Fc gamma RIIa (CD32) introduced into mouse fibroblasts mediates phagocytosis of sensitized erythrocytes. Blood. 79:1651-1656.
27. Geng, Y., E. Gulbins, A. Altman, and M. Lotz. 1994. Monocyte deactivation by interleukin 10 via inhibition of tyrosine kinase activity and the Ras signaling pathway. Proc. Natl. Acad. Sci. USA. 91:8602-8606.
28. Ninomiya, N., K. Hazeki, Y. Fukui, T. Seya, T. Okada, O. Hazeki, and M. Ui. 1994. Involvement of phosphatidylinositol 3-kinase in Fc gamma receptor signaling. J. Biol. Chem. 269:22732-22737.
29. Araki, N., M. Johnson, and J. Swanson. 1996. A role for phosphoinositied 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J. Cell Biol. 135: 1249-1260.
30. Suzuki, T. 1991. Signal transduction mechanisms through Fc gamma receptors on the mouse macrophage surface. FASEB J. 5:187-193.
31. Greenberg, S., P. Chang, and S.C. Silverstein. 1994. Tyrosine phosphorylation of the gamma subunit of Fc gamma receptors, p72syk, and paxillin during Fc receptor-mediated phagocytosis in macrophages. J. Biol. Chem. 269:3897-3902.
32. Weinstein, S., M.R. Gold, and A.L. DeFranco. 1991. Bacterial lipopolysaccharide stimulates protein tyrosine phosphorylation in macrophages. Proc. Natl. Acad. Sci. USA. 88:4148-4152.
33. Shapira, L., S. Takashiba, C. Champagne, S. Amar, and T.E. Van Dyke. 1994. Involvement of protein kinase C and protein tyrosine kinase in lipopolysaccharide-induced TNF-alpha and IL-1 beta production by human monocytes. J. Immunol. 153:1818-1824.
34. Chanmugam, P., L. Feng, S. Liou, B.C. Jang, M. Boudreau, G. Yu, J.H. Lee, H.J. Kwon, T. Beppu, and M. Yoshida. 1995. Radicicol, a protein tyrosine kinase inhibitor, suppresses the expression of mitogen-inducible cyclooxygenase in macrophages stimulated with lipopolysaccharide and in experimental glomerulonephritis. J. Biol. Chem. 270:5418-5426.
35. Downward, J. 1994. The GRB2/Sem-5 adaptor protein. FEBS Lett. 338:113-117.
36. Costello, P.S.T., M. Walters, A.E. Cunningham, C.N. Bauer, P.H. Downward, and V.L.J. Tybulewicz. 1996. Critical role for the tyrosine kinase Syk in signalling through the high affinity IgE receptor of mast cells. Oncogene. 13:2595-2605.
37. Gelfand, E.W., K. Weinberg, B.D. Mazer, T.A. Kadlecek, and A. Weiss. 1995. Absence of ZAP-70 prevents signaling through the antigen receptor on peripheral blood T cells but not on thymocytes. J. Exp. Med. 182:1057-1065.
38. Roifman, C.M. 1995. A mutation in zap-70 protein tyrosine kinase results in a selective immunodeficiency. J. Clin. Immunol. 15:52-62.
39. + mobilization through distinct pathways. EMBO J. 13:1341-1349.
40. Keegan, A.D., and W.E. Paul. 1992. Multichain immune recognition receptors: similarities in structure and signaling pathways. Immunol. Today. 13:63-68.
41. Osman, N., H. Turner, S. Lucas, K. Reif, and D.A. Cantrell. 1996. The protein interactions of the immunoglobulin receptor family tyrosine-based activation motifs present in the T cell receptor zeta subunits and the CD3 gamma, delta and epsilon chains. Eur. J. Immunol. 26:1063-1068.
42. Chacko, G.W., J.T. Brandt, K.M. Coggeshall, and C.L. Anderson. 1996. Phosphoinositide 3-kinase and p72syk non-covalently associate with the low affinity Fc gamma receptor on human platelets through an immunoreceptor tyrosine-based activation motif. Reconstitution with synthetic phosphopeptides. J. Biol. Chem. 271:10775-10781.
43. Allen, L.H., and A. Aderem. 1996. Molecular definition of distinct cytoskeletal structures involved in complement-and Fc receptor-mediated phagocytosis in macrophages. J. Exp. Med. 184:627-637.
44. Lennartz, M.R., and E.J. Brown. 1991. Arachidonic acid is essential for IgG Fc receptor-mediated phagocytosis by human monocytes. J. Immunol. 147:621-626.
45. Damen, J.E., L. Liu, P. Rosten, R.K. Humphries, A.B. Jefferson, P.W. Majerus, and G. Krystal. 1996. The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. Proc. Natl. Acad. Sci. USA. 93: 1689-1693.
46. Lioubin, M.N., P.A. Algate, S. Tsai, K. Carlberg, R. Aebersold, and L.R. Rohrschneider. 1996. p150Ship, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev. 10:1084-1095.
47. Nobes, C.D., and A. Hall. 1995. Rho, rac, and cdc42 GTP-ases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 81:53-62.
48. Hawkins, P.T., A. Eguinoa, R.G. Qiu, D. Stokoe, F.T. Cooke, R. Walters, S. Wennstrom, L. Claesson-Welsh, T. Evans, and M. Symons. 1995. PDGF stimulates an increase in GTP-Rac via activation of phosphoinositide 3-kinase. Curr. Biol. 5:393-403.
49. Stephens, L., P.T. Hawkins, A. Eguinoa, and F. Cooke. 1996. A heterotrimeric GTPase-regulated isoform of PI3K and the regulation of its potential effectors. Philos. Trans. R. Soc. Lond. Ser. B. Biol. Sci. 351:211-215.