Differential involvement of Src family kinases in Fcγ receptor-mediated phagocytosis

Journal of Immunology

Volumn 165, Issue 1, 2000, Pages 473-482

  Suzuki, Takeshi ^a   Kono, Hajime ^a   Hirose, Naoto ^a   Okada, Masato ^b   Yamamoto, Tadashi ^c   Yamamoto, Kazuhiko ^a   Honda, Zen Ichiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; CELL MOTILITY; ENZYME ACTIVITY; FLOW CYTOMETRY; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 0034234711     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.165.1.473     Document Type: Article

References (80)

1. Anderson, C. L., L. Shen, D. M. Eicher, M. D. Wewers, and J. K. Gill. 1990. Phagocytosis mediated by three distinct Fc γ receptor classes on human leukocytes. J. Exp. Med. 171:1333.
2. Tuijnman, W. B., P. J. Capel, and J. G. van de Winkel. 1992. Human low-affinity IgG receptor Fc γRlla (CD32) introduced into mouse fibroblasts mediates phagocytosis of sensitized erythrocytes. Blood 79:1651.
3. Ravetch, J. V. 1994. Fc receptors: rubor redux. Cell 78:553.
4. Indik, Z. K., J. G. Park, S. Hunter, and A. D. Schreiber. 1995. The molecular dissection of Fc γ receptor mediated phagocytosis. Blood 86:4389.
5. Daeron, M. 1997. Fc receptor biology. Annu. Rev. Immunol. 1997:15:203.
6. Aderem, A., and D. M. Underhill. 1999. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17:593.
7. Ravelch, J. V., and R. A. Clynes. 1998. Divergent roles for Fc receptors and complement in vivo. Annu. Rev. Immunol. 16:421.
8. Reth, M. 1989. Antigen receptor tail clue. Nature 338:383.
9. Samelson, L. E., and R. D. Klausner. 1992. Tyrosine kinases and tyrosine-based activation motifs: current research on activation via the T cell antigen receptor. J. Biol. Chem. 267:24913.
10. Weiss, A. 1993. T cell antigen receptor signal transduction: a tale of tails and cytoplasmic protein-tyrosine kinases. Cell 73:209.
11. Weiss, A., and D. R. Littman. 1994. Signal transduction by lymphocyte antigen receptors. Cell 76:263.
12. Cambier, J. C. 1995. New nomenclature for the Reth motif (or ARH1/TAM/ ARAM/YXXL). Immunol. Today 16:110.
13. Park, J. G., R. K. Murray, P. Chien, C. Darby, and A. D. Schreiber. 1993. Conserved cytoplasmic tyrosine residues of the γ subunit are required for a phagocytic signal mediated by Fc gamma RIIIA. J. Clin. Invest. 92:2073.
14. Park, J. G., R. E. Isaacs, P. Chien, and A. D. Schreiber. 1993. In the absence of other Fc receptors, FcγRIIIA transmits a phagocytic signal that requires the cytoplasmic domain of its γ subunit. J. Clin. Invest. 92:1967.
15. Park, J. G., and A. D. Schreiber. 1995. Determinants of the phagocytic signal mediated by the type IIIA Fcγ receptor, FcγRIIIA: sequence requirements and interaction with protein-tyrosine kinases. Proc. Natl. Acad. Sci. USA 92:7381.
16. Duchemin, A. M., L. K. Ernst, and C. L. Anderson. 1994. Clustering of the high affinity Fc receptor for immunoglobulin G (FcγRI) results in phosphorylation of its associated gamma-chain. J. Biol. Chem. 269:12111.
17. syk, and paxillin during Fc receptor-mediated phagocytosis in macrophages. J. Biol. Chem. 269:3897.
18. Greenberg, S. 1995. Signal transduction of phagocytosis. Trends Cell Biol. 5:93.
19. 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.
20. Greenberg, S., P. Chang, D. C. Wang, R. Xavier, and B. Seed. 1996. Clustered syk tyrosine kinase domains trigger phagocytosis. Proc. Natl. Acad. Sci. USA 93:1103.
21. Crowley, M. T., P. S. Costello, C. J. Fitzer-Attas, M. Turner, F. Meng, C. Lowell, V. L. Tybulewicz, and A. L. DeFranco. 1997. A critical role for Syk in signal transduction and phagocytosis mediated by Fcγ receptors on macrophages. J. Exp. Med. 186:1027.
22. Amigorena, S., C. Bonnerot, J. R. Drake, D. Choquet, W. Hunziker, J. G. Guillet, P. Webster, C. Sautes, I. Mellman, and W. H. Fridman. 1992. Cytoplasmic domain heterogeneity and functions of IgG Fc receptors in B lymphocytes. Science 256:1808.
23. Muta, T., T. Kurosaki, Z. Misulovin, M. Sanchez, M. C. Nussenzweig, and J. V. Ravetch. 1994. A 13-amino-acid motif in the cytoplasmic domain of Fcγ RIIB modulates B-cell receptor signalling. Nature 369:340.
24. Clynes, R., J. S. Maizes, R. Guinamard, M. Ono, T. Takai, and J. V. Ravetch. 1999. Modulation of immune complex-induced inflammation in vivo by the coordinate expression of activation and inhibitory Fc receptors. J. Exp. Med. 189: 179.
25. Greenberg, S., P. Chang, and S. C. Silverstein. 1993. Tyrosine phosphorylation is required for Fc receptor-mediated phagocytosis in mouse macrophages. J. Exp. Med. 177:529.
26. Allen, L. A., 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.
27. Eiseman, E., and J. B. Bolen. 1992. Engagement of the high-affinity IgE receptor activates src protein-related tyrosine kinases. Nature 355:78.
28. 6lvn protein-tyrosine kinase. Proc. Natl. Acad. Sci. USA 91:11251.
29. Ghazizadeh, S., J. B. Bolen, and H. B. Fleit. 1994. Physical and functional association of Src-related protein tyrosine kinases with Fcγ RII in monocytic THP-1 cells. J. Biol. Chem. 269:8878.
30. lck with Fcγ RIIIA (CD16) in natural killer cells. J. Exp. Med. 177:1475.
31. Kihara, H., and R. P. Siraganian. 1994. Src homology 2 domains of Syk and Lyn bind to tyrosine-phosphorylated subunits of the high affinity IgE receptor. J. Biol. Chem. 269:22427.
32. Lowell, C. A., P. Soriano, and H. E. Varmus. 1994. Functional overlap in the src gene family: inactivation of hck and fgr impairs natural immunity. Genes Dev. 8:387.
33. Nishizumi, H., I. Taniuchi, Y. Yamanashi, D. Kitamura, D. Ilic, S. Mori, T. Watanabe, and T. Yamamoto. 1995. Impaired proliferation of peripheral B cells and indication of autoimmune disease in lyn-deficient mice. Immunity 3:549.
34. Nishizumi, H., K. Horikawa, I. Mlinaric-Rascan, and T. Yamamoto. 1998. A double-edged kinase Lyn: a positive and negative regulator for antigen receptor-mediated signals. J. Exp. Med. 187:1343.
35. 2+ mobilization, but not degranulation, in lyn-deficient bone marrow-derived mast cells. J. Immunol. 158:2350.
36. csk. Nature 365: 156.
37. Honda, Z., T. Suzuki, N. Hirose, M. Aihara, T. Shimizu, S. Nada, M. Okada, C. Ra, Y. Monta, and K. Ito. 1997. Roles of C-terminal Src kinase in the initiation and the termination of the high affinity IgE receptor-mediated signaling. J. Biol. Chem. 272:25753.
38. Suzuki, T., S. Shoji, K. Yamamoto, S. Nada, M. Okada, T. Yamamoto, and Z. Honda. 1998. Essential roles of Lyn in fibronectin-mediated filamentous actin assembly and cell motility in mast cells. J. Immunol. 161:3694.
39. c-src. Nature 351:69.
40. Nada, S., T. Yagi, H. Takeda, T. Tokunaga, H. Nakagawa, Y. Ikawa, M. Okada, and S. Aizawa. 1993. Constitutive activation of Src family kinases in mouse embryos that lack Csk. Cell 73:1125.
41. Imamoto, A., and P. Soriano. 1993. Disruption of the csk gene, encoding a negative regulator of Src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell 73:1117.
42. Cooper, J. A., and B. Howell. 1993. The when and how of Src regulation. Cell 73:1051.
43. Miyazaki, J., S. Takaki, K. Araki, F. Tashiro, A. Tominaga, K. Takatsu, and K. Yamamura. 1989. Expression vector system based on the chicken β-actin promoter directs efficient production of interleukin-5. Gene 79:269.
44. Zhu, Z., Z. Bao, and J. Li. 1995. MacMARCKS mutation blocks macrophage phagocytosis of zymosan. J. Biol. Chem. 270:17652.
45. Grunwald, U., X. Fan, R. S. Jack, G. Workalemahu, A. Kallies, F. Stelter, and C. Schutt. 1996. Monocytes can phagocytose Gram-negative bacteria by a CD14-dependent mechanism. J. Immunol. 157:4119.
46. 2 release in adherent human neutrophils. J. Immunol. 160:5154.
47. Field, K. A., D. Holowka, and B. Baird. 1997. Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J. Biol. Chem. 272:4276.
48. Wessel, D., and U. I. Flugge. 1984. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138:141.
49. Greenberg, S., K. Burridge, and S. C. Silverstein. 1990. Colocalization of F-actin and talin during Fc receptor-mediated phagocytosis in mouse macrophages. J. Exp. Med. 172:1853.
50. Silverstein, S. C., S. Greenberg, F. di Virgilio, and T. H. Steinberg. 1989. Phagocytosis. In Fundamental Immunology, 2nd Ed. W. E. Paul, ed. Raven, New York, p. 703.
51. Speert, D. P., and S. C. Silverstein. 1985. Phagocytosis of unopsonized zymosan by human monocyte-derived macrophages: maturation and inhibition by mannan. J. Leukocyte Biol. 38:655.
52. Kadish, J. L., C. C. Choi, and J. K. Czop. 1986. Phagocytosis of unopsonized zymosan particles by trypsin-sensitive and β-glucan-inhibitable receptors on bone marrow-derived murine macrophages. Immunol. Res. 5:129.
53. Darby, C., R. L. Geahlen, and A. D. Schreiber. 1994. Stimulation of macrophage Fcγ 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.
54. Crespo, P., K. E. Schuebel, A. A. Ostrom, J. S. Gutkind, and X. R. Bustelo. 1997. Phosphotyrosine-dependent activation of Rac-1 GDP/GTP exchange by the vav proto-oncogene product. Nature 385:169.
55. Teramoto, H., P. Salem, K. C. Robbins, X. R. Bustelo, and J. S. Gutkind. 1997. Tyrosine phosphorylation of the vav proto-oncogene product links Fc∈RI to the Rac1-JNK pathway. J. Biol. Chem. 272:10751.
56. Ota, Y., and L. E. Samelson 1997. The product of the proto-oncogene c-cbl: a negative regulator of the Syk tyrosine kinase. Science 276:418.
57. Joazeiro, C. A. P., S. S. Wing, H.-K. Huang, J. D. Leverson, T. Hunter, and Y.-C. Liu. 1999. The tyrosine kinase negative regulator c-Cbl as a RINO-type, E2-dependent ubiquitin-protein ligase. Science 286:309.
58. Ono, M., S. Bolland, P. Tempst, and J. V. Ravetch. 1996. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor Fc(γ)RIIB. Nature 383:263.
59. Takai, T., M. Ono, M. Hikida, H. Ohmori, and J. V. Ravelch. 1996. Augmented humoral and anaphylactic responses in FcγRII-deficient mice. Nature 379:346.
60. Tanaka, S., L. Neff, R. Baron, and J. B. Levy. 1995. Tyrosine phosphorylalion and translocation of the c-cbl protein after activation of tyrosine kinase signaling pathways. J. Biol. Chem. 270:14347.
61. 1 integrin signaling pathway involving Src-family kinases, Cbl and Pl-3 kinase is required for macrophage spreading and migration. EMBO J. 17:4391.
62. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387:569.
63. fyn src homology 4 domain define a motif for immune-receptor tyrosine-based activation motif (ITAM) binding and for plasma membrane localization. J. Cell Biol. 133:1007.
64. Kabouridis, P. S., A. I. Magee, and S. C. Ley. 1997. S-Acylation of LCK protein tyrosine kinase is essential for its signalling function in T lymphocytes. EMBO J. 16:4983.
65. Field, K. A., D. Holowka, and B. Baird. 1999 Structural aspects of the association of FceRI with detergent-resistant membranes. J. Biol. Chem. 274:1753.
66. Montixi, C., C. Langlet, A. M. Bernard, J. Thimonier, C. Dubois, M. A. Wurbel, J. P. Chauvin, M. Pierres, and H. T. He. 1998. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17:5334.
67. Xavier, R., T. Brennan, Q. Li, C. McCormack, and B. Seed. 1998. Membrane compartmentation is required for efficient T cell activation. Immunity 8:723.
68. Bonnerot, C., S. Amigorena, D. Choquet, R. Pavlovich, V. Choukroun, and W. H. Fridman. 1992. Role of associated γ-chain in tyrosine kinase activation via murine Fc gamma RIII. EMBO J. 11:2747.
69. Paolini, R., V. Renard, E. Vivier, K. Ochiai, M. H. Jouvin, B. Malissen, and J. P. Kinet. 1995. Different roles for the Fc∈RIγ chain as a function of the receptor context. J. Exp. Med. 181:247.
70. 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.
71. Sambrano, G. R., and D. Steinberg. 1995. Recognition of oxidatively damaged and apoptotic cells by an oxidized low density lipoprotein receptor on mouse peritoneal macrophages: role of membrane phosphatidylserine. Proc. Natl. Acad. Sci. USA 92:1396.
72. Alvarez, F. J., J. A. Jordan, A. Herraez, J. C. Diez, and M. C. Tejedor. 1998. Hypotonically loaded rat erythrocytes deliver encapsulated substances into peritoneal macrophages. J. Biochem. 123:233.
73. Bratosin, D., J. Mazurier, J. P. Tissier, J. Estaquier, J. J. Huart, J. C. Ameisen, D. Aminoff, and J. Montreuil. 1998. Cellular and molecular mechanisms of senescent erythrocyte phagocytosis by macrophages: a review. Biochimie 80:173.
74. Ofek, I., J. Goldhar, Y. Keisari, and N. Sharon. Nonopsonic phagocytosis of microorganisms. Annu. Rev. Microbiol. 1995:49:239.
75. Resh, M. D. 1994. Myristylation and paimitylation of Src family members: the fats of the matter. Cell 76:411.
76. Honda, Z., T. Suzuki, H. Kono, M. Okada, T. Yamamoto, C. Ra, Y. Morita, and K. Yamamoto. 2000. Sequential requirements of the N-terminal palmitoylation site and SH2 domain of Src family kinases in the initiation and progression of Fc∈ signaling. Mol. Cell. Biol. 20:1759.
77. Rabinowich, H., M. Manciulea, D. Metes, A. Sulica, R. B. Herberman, S. J. Corey, and T. L. Whiteside. 1996. Physical and functional association of Fcμ receptor on human natural killer cells with the ζ- and Fc∈RI γ-chains and with src family protein tyrosine kinases. J. Immunol. 157:1485.
78. Daeron, M., S. Latour, O. Malbec, E. Espinosa, P. Pina, S. Pasmans, and W. H. Fridman. 1995. The same tyrosine-based inhibition motif, in the intracytoplasmic domain of FcγRIIB, regulates negatively BCR-, TCR-, and FcR-dependent cell activation. Immunity 3:635.
79. Ravetch, J. V. 1997. Fc receptors. Curr. Opin. Immunol. 9:121.
80. Fitzer-Attas, C. J., M. Lowry, M. T. Crowley, A. J. Finn, F. Meng, A. L. DeFranco, and C. A. Lowell. 2000. Fcγ receptor-mediated phagocytosis in macrophages lacking the Src family tyrosine kinases Hck, Fgr, and Lyn. J. Exp. Med. 191:669.