Phospholipase Cγ2 is essential for specific functions of FcεR and FcγR

Journal of Immunology

Volumn 169, Issue 12, 2002, Pages 6743-6752

  Wen, Renren ^a   Jou, Shiann Tarng ^b   Chen, Yuhong ^a,c   Hoffmeyer, Angelica ^d   Wang, Demin ^a,e  

^a BLOOD RESEARCH INSTITUTE   (United States)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c NANJING UNIVERSITY   (China)

^d ALTANA PHARMA AG   (Germany)

^e MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; FC RECEPTOR; IMMUNOGLOBULIN E; INOSITOL 1,4,5 TRISPHOSPHATE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA2; UNCLASSIFIED DRUG; CALCIUM; DIVALENT CATION; IMMUNOGLOBULIN E RECEPTOR; ISOENZYME; PHOSPHOLIPASE C GAMMA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; CROSS LINKING; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME DEFICIENCY; MACROPHAGE; MAST CELL; MAST CELL DEGRANULATION; MONOCYTE; MOUSE; MOUSE MUTANT; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SKIN INFLAMMATION; ANIMAL; DEGRANULATION; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PASSIVE SKIN ANAPHYLAXIS; PERITONEUM MACROPHAGE; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; CATIONS, DIVALENT; CELL DEGRANULATION; CYTOKINES; ENZYME ACTIVATION; IMMUNITY, NATURAL; IMMUNOGLOBULIN E; ISOENZYMES; MACROPHAGES, PERITONEAL; MAST CELLS; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASES; PASSIVE CUTANEOUS ANAPHYLAXIS; PHAGOCYTOSIS; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; RECEPTORS, IGE; RECEPTORS, IGG; TRANSCRIPTION, GENETIC;

EID: 0037114147     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.169.12.6743     Document Type: Article

References (88)

1. Ravetch, J. V. 1997. Fc receptors. Curr. Opin. Immunol. 9:121.
2. Ravetch, J. V., and R. A. Clynes. 1998. Divergent roles for Fc receptors and complement in vivo. Annu. Rev. Immunol. 16:421.
3. Daeron, M. 1997. Fc receptor biology. Annu. Rev. Immunol. 15:203.
4. Serafin, W. E., and K. F. Austen. 1987. Mediators of immediate hypersensitivity reactions. N. Engl. J. Med. 317:30.
5. Galli, S. J. 1993. New concepts about the mast cell. N. Engl. J. Med. 328:257.
6. Diamond, B., B. R. Bloom, and M. D. Scharff. 1978. The Fc receptors of primary and cultured phagocytic cells studied with homogeneous antibodies. J. Immunol. 121:1329.
7. Weinshank, R. L., A. D. Luster, and J. V. Ravetch. 1988. Function and regulation of a murine macrophage-specific IgG Fc receptor, FcγR-α. J. Exp. Med. 167:1909.
8. McKenzie, S. E., and A. D. Schreiber. 1998. Fcγ receptors in phagocytes. Curr. Opin. Hematol. 5:16.
9. Nathan, C. F., H. W. Murray, and Z. A. Cohn. 1980. The macrophage as an effector cell. N. Engl. J. Med. 303:622.
10. Takai, T., M. Li, D. Sylvestre, R. Clynes, and J. V. Ravetch. 1994. FcRγ chain deletion results in pleiotrophic effector cell defects. Cell 76:519.
11. Eiseman, E., and J. B. Bolen. 1992. Engagement of the high-affinity IgE receptor activates src protein-related tyrosine kinases. Nature 355:78.
12. Hutchcroft, J. E., R. L. Geahlen, G. G. Deanin, and J. M. Oliver. 1992. FcεRI-mediated tyrosine phosphorylation and activation of the 72-kDa protein-tyrosine kinase. PTK72, in RBL-2H3 rat tumor mast cells. Proc. Natl. Acad. Sci. USA 89:9107.
13. Pignata, C., K. V. Prasad, M. J. Robertson, H. Levine, C. E. Rudd, and J. Ritz. 1993. FcγRIIIA-mediated signaling involves src-family Ick in human natural killer cells. J. Immunol. 151:6794.
14. Durden, D. L., H. M. Kim, B. Calore, and Y. Liu. 1995. The FcγRI receptor signals through the activation of hck and MAP kinase. J. Immunol. 154:4039.
15. Ghazizadeh, S., J. B. Bolen, and H. B. Fleit. 1994. Physical and functional association of Src-related protein tyrosine kinases with FcγRII in monocytic THP-1 cells. J. Biol. Chem. 269:8878.
16. syk in high affinity IgE receptor signaling. Identification as a component of pp72 and association with the receptor γ chain after receptor aggregation. J. Biol. Chem. 268:23318.
17. vav and p62/GAP-associated protein. J. Immunol. 152:5429.
18. Kiener, P. A., B. M. Rankin, A. L. Burkhardt, G. L. Schieven, L. K. Gilliland, R. B. Rowley, J. B. Bolen, and J. A. Ledbetter. 1993. Cross-linking of Fcγ receptor 1 (FcγRI) and receptor II (FcγRII) 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.
19. Rhee, S. G., and Y. S. Bae. 1997. Regulation of phosphoinositide-specific phospholipase C isozymes. J. Biol. Chem. 272:15045.
20. Park, D. J., H. K. Min, and S. G. Rhee. 1991. IgE-induced tyrosine phosphorylation of phospholipase C-γ1 in rat basophilic leukemia cells. J. Biol. Chem. 266:24237.
21. Liao, F., H. S. Shin, and S. G. Rhee. 1993. Cross-linking of FcγRIIIA on natural killer cells results in tyrosine phosphorylation of PLC-γ1 and PLC-γ2. J. Immunol. 150:2668.
22. Ting, A. T., C. J. Dick, R. A. Schoon, L. M. Kamitz, R. T. Abraham, and P. J. Leibson. 1995. Interaction between Ick and syk family tyrosine kinases in Fcγ receptor-initiated activation of natural killer cells. J. Biol. Chem. 270:16415.
23. Xu, X., and A. S. Chong. 1996. Vav in natural killer cells is tyrosine phosphorylated upon cross-linking of FcγRIIIA and is constitutively associated with a serine/threonine kinase. Biochem. J. 318:527.
24. Dusi, S., M. Donini, V. Della Bianca, and F. Rossi. 1994. Tyrosine phosphorylation of phospholipase C-γ2 is involved in the activation of phosphoinositide hydrolysis by Fc receptors in human neutrophils. Biochem. Biophys. Res. Commun. 201:1100.
25. Bonilla, F. A., R. M. Fujita, V. I. Pivniouk, A. C. Chan, and R. S. Geha. 2000. Adapter proteins SLP-76 and BLNK both are expressed by murine, macrophages and are linked to signaling via Fcγ receptors I and II/III. Proc. Natl. Acad. Sci. USA 97:1725.
26. Chao, T. S., D. A. Foster, U. R. Rapp, and M. R. Rosner. 1994. Differential Raf requirement for activation of mitogen-activated protein kinase by growth factors, phorbol esters, and calcium. J. Biol. Chem. 269:7337.
27. Hirasawa, N., F. Santini, and M. A. Beaven. 1995. Activation of the mitogen-activated protein kinase/cytosolic phospholipase A2 pathway in a rat mast cell line: indications of different pathways for release of arachidonic acid and secretory granules. J. Immunol. 154:5391.
28. Roa, M., F. Paumet, J. Le Mao, B. David, and U. Blank. 1997. Involvement of the ras-like GTPase rab3d in RBL-2H3 mast cell exocytosis following stimulation via high affinity IgE receptors (FcεR1). J. Immunol. 159:2815.
29. Jiang, A., A. Craxton, T. Kurosaki, and E. A. Clark. 1998. Different protein tyrosine kinases are required for B cell antigen receptor-mediated activation of extracellular signal-regulated kinase, c-Jun NH2-terminal kinase 1, and p38 mitogen-activated protein kinase. J. Exp. Med. 188:1297.
30. 2-terminal kinase, and p38 mitogen-activated protein kinase activation by the B cell antigen receptor. J. Exp. Med. 188:1287.
31. Marshall, C. J. 1995, Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179.
32. Hirasawa, N., A. Scharenberg, H. Yamamura, M. A. Beaven, and J. P. Kinet. 1995. A requirement for Syk in the activation of the microtubule-associated protein kinase/phospholipase A2 pathway by FcεR1 is not shared by a G protein-coupled receptor. J. Biol. Chem. 270:10960.
33. Zhang, C., N. Hirasawa, and M. A. Beaven. 1997. Antigen activation of mitogen-activated protein kinase in mast cells through protein kinase C-dependent and independent pathways. J. Immunol. 158:4968.
34. Kawakami, Y., S. E. Hartman, P. M. Holland, J. A. Cooper, and T. Kawakami. 1998. Multiple signaling pathways for the activation of JNK in mast cells: involvement of Bruton's tyrosine kinase, protein kinase C, and JNK kinases, SEKI and MKK7. J. Immunol. 161:1795.
35. Campbell, K. S. 1999. Signal transduction from the B cell antigen-receptor. Curr. Opin. Immunol. 11:256.
36. Healy, J. I., R. E. Dolmetsch, L. A. Timmerman, J. G. Cyster. M. L. Thomas, G. R. Crabtree, R. S. Lewis, and C. C. Goodnow. 1997. Different nuclear signals are activated by the B cell receptor during positive versus negative signaling. Immunity 6:419.
37. Jain, J., P. G. McCaffrey, Z. Miner, T. K. Kerppola, J. N, Lambert, G. L. Verdine, T. Curran, and A. Rao. 1993. The T-cell transciption factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature 365:352.
38. Rao, A., C, Luo, and P. G. Hogan. 1997. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15:707.
39. Schlessinger, J. 1997. Phospholipase Cγ activation and phosphoinositide hydrolysis are essential for embryonal development. Proc. Natl. Acad. Sci. USA 94:2798.
40. Ji, Q. S., G. E. Winnier, K. D. Niswender, D. Horstman, R. Wisdom, M. A. Magnuson, and G. Carpenter. 1997. Essential role of the tyrosine kinase substrate phospholipase C-γ1 in mammalian growth and development. Proc. Natl. Acad. Sci. USA 94:2999.
41. Wang, D., J. Feng, R. Wen, J. C. Marine, M. Y. Sangster, E. Parganas, A. Hoffmeyer, C. W. Jackson, J. L. Cleveland, P. J. Murray, et al. 2000. Phospholipase Cγ2 is essential in the functions of B cell and several Fc receptors. Immunity 13:25.
42. Wang, D., D. Stravopodis, S. Teglund, J. Kitazawa, and J. N. Ihle. 1996. Naturally occurring dominant negative variants of Stat5. Mol. Cell. Biol. 16:6141.
43. 2+] with fluorescent indicators. Methods Cell Biol. 40:155.
44. Kurosaki, T. 1999. Genetic analysis of B cell antigen receptor signaling. Annu. Rev. Immunol. 17:555.
45. McLeod, S. J., R. J. Ingham, J. L. Bos, T. Kurosaki, and M. R. Gold, 1998. Activation of the Rap1 GTPase by the B cell antigen receptor. J. Biol. Chem. 273:29218.
46. Plaut, M., J. H. Pierce, C. J. Watson, J. Hanley-Hyde, R. P. Nordan, and W. E. Paul. 1989. Mast cell lines produce lymphokines in response to cross-linkage of FcεRI or to calcium ionophores. Nature 339:64.
47. Wodnar-Filipowicz, A., and C. Moroni. 1990. Regulation of interleukin 3 mRNA expression in mast cells occurs at the posttranscriptional level and is mediated by calcium ions. Proc. Natl. Acad. Sci. USA 87:777.
48. Clipstone, N. A., and G. R. Crabtree. 1992. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357:695.
49. Hutchinson, L. E., and M. A. McCloskey. 1995. FcεRI-mediated induction of nuclear factor of activated T-cells. J. Biol. Chem. 270:16333.
50. Baranes, D., and E. Razin. 1991. Protein kinase C regulates proliferation of mast cells and the expression of the mRNAs of fos and jun proto-oncogenes during activation by IgE-Ag or calcium ionophore A23187. Blood 78:2354.
51. Lewin, I., H, Nechushtan, Q. Ke, and E. Razin. 1993. Regulation of AP-1 expression and activity in antigen-stimulated mast cells: the role played by protein kinase C and the possible involvement of Fos interacting protein. Blood 82:3745.
52. Shaw, J. P., P. J. Utz, D. B. Durand, J. J. Toole, E. A. Emmel, and G. R. Crabtree. 1988. Identification of a putative regulator of early T cell activation genes. Science 241:202.
53. Rao, A. 1994. NF-ATp: a transcription factor required for the co-ordinate induction of several cytokine genes. Immunol. Today 15:274.
54. Turner, H., and D. A. Cantrell. 1997. Distinct Ras effector pathways are involved in FcεRI regulation of the transcriptional activity of Elk-1 and NFAT in mast cells. J. Exp. Med. 185:43.
55. Taniguchi, T. 1988. Regulation of cytokine gene expression. Annu. Rev. Immunol. 6:439.
56. Muegge, K., and S. K. Durum. 1990. Cytokines and transcription factors. Cytokine 2:1.
57. Agarwal, S., and A. Rao. 1998. Long-range transcriptional regulation of cytokine gene expression. Curr. Opin. Immunol. 10:345.
58. Tsuruta, L., N. Arai, and K. Arai. 1998. Transcriptional control of cytokine genes. Int. Rev. Immunol. 16:581.
59. Hazenbos, W. L., J. E. Gessner, F. M. Hofhuis, H. Kuipers, D. Meyer, I. A. Heijnen, R. E. Schmidt, M. Sandor, P. J. Capel, M. Daeron, et al. 1996. Impaired IgG-dependent anaphylaxis and Arthus reaction in FcγRIII (CD16) deficient mice. Immunity 5:181.
60. Barker, S. A., K. K. Caldwell, J. R. Pfeiffer, and B. S. Wilson. 1998. Wortmannin-sensitive phosphorylation, translocation, and activation of PLCγ1, but not PLCγ2, in antigen-stimulated RBL-2H3 mast cells. Mol. Biol. Cell 9:483.
61. Turner, H., and J. P. Kinet. 1999. Signalling through the high-affinity IgE receptor FcεRI. Nature 402:B24.
62. Mohr, F. C., and C. Fewtrell. 1987. The relative contributions of extracellular and intracellular calcium to secretion from tumor mast cells: multiple effects of the proton ionophore carbonyl cyanide m-chlorophenylhydrazone. J. Biol. Chem. 262:10638.
63. Choi, O. H., J. H. Kim, and J. P. Kinet. 1996. Calcium mobilization via sphingosine kinase in signalling by the FcεRI antigen receptor. Nature 380:634.
64. Saitoh, S., R. Arudchandran, T. S. Manetz, W. Zhang, C. L. Sommers, P. E. Love, J. Rivera, and L. E. Samelson. 2000. LAT is essential for FcεRI-mediated mast cell activation. Immunity 12:525.
65. Pivniouk. V. I., T. R. Martin, J. M. Lu-Kuo, H. R. Katz, H. C. Oettgen, and R. S. Geha. 1999. SLP-76 deficiency impairs signaling via the high-affinity IgE receptor in mast cells. J. Clin. Invest. 103:1737.
66. Sanchez-Mejorada, G., and C. Rosales. 1998. Signal transduction by immunoglobulin Fc receptors. J. Leukocyte Biol. 63:521.
67. ras through the formation of a complex of receptor, Grb2 adapter protein, and Sos nucleotide exchange factor. Cell 73:611.
68. Chardin, P., J. H. Camonis, N. W. Gale, L. van Aelst, J. Schlessinger, M. H. Wigler, and D. Bar-Sagi. 1993. Human Sosl: a guanine nucleotide exchange factor for Ras that binds to GRB2. Science 260:1338.
69. Loh, C., K. T. Shaw, J. Carew, J. P. Viola, C. Luo, B. A. Perrino, and A. Rao. 1996. Calcineurin binds the transcription factor NFAT1 and reversibly regulates its activity. J. Biol. Chem. 271:10884.
70. Ruff, V. A., and K. L. Leach. 1995. Direct demonstration of NFATp dephosphorylation and nuclear localization in activated HT-2 cells using a specific NFATp polyclonal antibody. J. Biol. Chem. 270:22602.
71. ras in activated T cells. Eur. J. Immunol. 25:42.
72. Sun, Z., C. W. Arendt, W. Ellmeier, E. M. Schaeffer, M. J. Sunshine, L. Gandhi, J. Annes, D. Petrzilka, A. Kupfer, P. L. Schwartzberg, et al. 2000. PKC-θ is required for TCR-induced NF-κB activation in mature but not immature T lymphocytes. Nature 404:402.
73. syk. J. Biol. Chem. 269:32435.
74. Jouvin, M. H., M. Adamczewski, R. Numerof, O. Letourneur, A. Valle, and J. P. Kinet. 1994. Differential control of the tyrosine kinases Lyn and Syk by the two signaling chains of the high affinity immunoglobulin E receptor. J. Biol. Chem. 269:5918.
75. Tridandapani, S., T. W. Lyden, J. L. Smith, J. E. Carter, K. M. Coggeshall, and C. L. Anderson. 2000. The adapter protein LAT enhances Fcy receptor-mediated signal transduction in myeloid cells. J. Biol. Chem. 275:20480.
76. Wang, A. V., P. R. Scholl, and R. S. Geha. 1994. Physical and functional association of the high affinity immunoglobulin G receptor (FcγRI) with the kinases Hck and Lyn. J. Exp. Med. 180:1165.
77. 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.
78. 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.
79. Kiefer, F., J. Brumell, N. Al-Alawi, S. Latour, A. Cheng, A. Veillette, S. Grinstein, and T. Pawson. 1998. The Syk protein tyrosine kinase is essential for Fcγ receptor signaling in macrophages and neutrophils. Mol. Cell. Biol. 18:4209.
80. 2+ during phagolysosome formation? Cell Calcium 27:33.
81. 2+-independent phagocytosis in human neutrophils. Nature 315:509.
82. Raeder, E. M., P. J. Mansfield, V. Hinkovska-Galcheva, L. Kjeldsen, J. A. Shayman, and L. A. Boxer. 1999. Sphingosine blocks human polymorphonuclear leukocyte phagocytosis through inhibition of mitogen-activated protein kinase activation. Blood 93:686.
83. Karimi, K., T. R. Gemmill, and M. R. Lennartz. 1999. Protein kinase C and a calcium-independent phospholipase are required for IgG-mediated phagocytosis by Mono-Mac-6 cells. J. Leukocyte Biol. 65:854.
84. Breton, A., and A. Descoteaux. 2000. Protein kinase C-α participates in FcγR-mediated phagocytosis in macrophages. Biochem. Biophys. Res. Commun. 276:472.
85. Millard, P. J., T. A. Ryan, W. W. Webb, and C. Fewtrell. 1989. Immunoglobulin E receptor cross-linking induces oscillations in intracellular free ionized calcium in individual tumor mast cells. J. Biol. Chem. 264:19730.
86. 2+ responses and secretion in individual RBL-2H3 mucosal mast cells. J. Biol. Chem. 272:31225.
87. 2+ and purified isozymes in washed permeabilized cells. J. Biol. Chem. 268:1749.
88. Zhang, C., R. A. Baumgartner, K. Yamada, and M. A. Beaven. 1997. Mitogen-activated protein (MAP) kinase regulates production of tumor necrosis factor-α and release of arachidonic acid in mast cells: indications of communication between p38 and p42 MAP kinases. J. Biol. Chem. 272:13397.