Chapter 4 : Fc Receptors and Phagocytosis

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Phagocytosis is a specialized endocytic response of eukaryotic cells to particulate stimuli, such as microbial pathogens. This response is utilized by myeloid cells of the immune system to aid in host defenses. FcγRI is expressed at especially high levels in freshly harvested mouse dendritic cells from spleen, lymph node, and skin. FcγRIIA mediates phagocytosis of IgG-coated particles by human neutrophils and mononuclear phagocytes. FcαRI associates noncovalently with a γ-subunit homodimer common to other Fc receptors. FcγRn, a neonatal Fc receptor complexed to β- microglobulin, is a receptor on intestinal epithelial cells that mediates the transfer of maternal Ig from milk to the bloodstream of newborns. Co-ligation of FcγRIIb with the antigen receptor in B cells (BCR) leads to decreased cellular activation. Several tyrosine phosphatases have been identified that modulate ITAM-mediated responses. These include the membrane-bound tyrosine phosphatase CD45 and SHP-1/ SHP-2. The signaling requirements for endocytosis of monomeric Ig and immune complexes and phagocytosis are distinct. ITAM phosphorylation is accompanied by actin polymerization. The enzymatic steps leading to cytoskeletal assembly during phagocytosis are a matter of debate. Formins comprise a family of actin binding proteins that have the interesting property of weakly capping the barbed ends of actin filaments. Cytosolic transients may be involved in other aspects of phagocytic function, such as chemotactic peptide enhancement of FcR-mediated phagocytosis in neutrophils, arachidonic acid production, phagosome-lysosome fusion, and lysosome-enhanced phagocytosis.

Citation: Greenberg S, Dale B. 2009. Fc Receptors and Phagocytosis, p 71-92. In Russell D, Gordon S (ed), Phagocyte-Pathogen Interactions. ASM Press, Washington, DC. doi: 10.1128/9781555816650.ch4
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Image of FIGURE 1

Domain structures of human FcγRs expressed in phagocytic cells. Ligand binding subunits are labeled. In dark gray are γ-subunit homodimers with white bars representing the two tyrosine residues that are contained within the consensus sequence of ITAMs. In FcγRIIb1 and FcγRIIb2 are the cytosolic domains (light gray), which contain one conserved tyrosine residue (black bar) within the consensus ITIM. FcγRIIIb is a GPI-linked protein expressed in neutrophils and activated eosinophils, but not in monocytes, macrophages, or dendritic cells.

Citation: Greenberg S, Dale B. 2009. Fc Receptors and Phagocytosis, p 71-92. In Russell D, Gordon S (ed), Phagocyte-Pathogen Interactions. ASM Press, Washington, DC. doi: 10.1128/9781555816650.ch4
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1. Aderem, A. A.,, W. A. Scott, and, Z. A. Cohn. 1986. Evidence for sequential signals in the induction of the arachidonic acid cascade in macrophages. J. Exp. Med. 163: 139154.
2. Aderem, A. A.,, S. D. Wright,, S. C. Silverstein, and, Z. A. Cohn. 1985. Ligated complement receptors do not activate the arachidonic acid cascade in resident peritoneal macrophages. J. Exp. Med. 161: 617622.
3. Agarwal, A.,, P. Salem, and, K. C. Robbins. 1993. Involvement of p72 syk, a protein-tyrosine kinase, in Fc γ receptor signaling. J. Biol. Chem. 268: 1590015905.
4. Allen, L. A. 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: 627637.
5. Altieri, D. C.,, and T. S. Edgington. 1988. The saturable high affinity association of factor X to ADP-stimulated monocytes defines a novel function of the Mac-1 receptor. J. Biol. Chem. 263: 70077015.
6. 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: 18081812.
7. Amoui, M.,, L. Draberova,, P. Tolar, and, P. Draber. 1997. Direct interaction of syk and lyn protein tyrosine kinases in rat basophilic leukemia cells activated via type I Fcε receptors. Eur. J. Immunol. 27: 321328.
8. Anderson, C. L.,, P. M. Guyre,, J. C. Whitin,, D. H. Ryan,, R. J. Looney, and, M. W. Fanger. 1986. Soluble circulating Fcγ receptors on human mononuclear phagocytes. Antibody characterization and induction of superoxide production in a monocyte cell line. J. Biol. Chem. 261: 1285612864.
9. 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: 13331345.
10. Anderson, P.,, M. Caliguiri,, C. O’Brien,, T. Manley,, J. Ritz, and, S. F. Schlossman. 1990. Fcγ receptor type III (CD16) is included in the ζ NK receptor complex expressed by human natural killer cells. Proc. Natl. Acad. Sci. USA 87: 22742278.
11. Araki, N.,, M. T. Johnson, and, J. A. Swanson. 1996. A role for phosphoinositide 3-kinase in the completion of macro-pinocytosis and phagocytosis by macrophages. J. Cell Biol. 135: 12491260.
12. Barnes, N.,, A. L. Gavin,, P. S. Tan,, P. Mottram,, F. Koentgen, and, P. M. Hogarth. 2002. FcγRI-deficient mice show multiple alterations to inflammatory and immune responses. Immunity 16: 379389.
13. Barnes, N. C.,, M. S. Powell,, H. M. Trist,, A. L. Gavin,, B. D. Wines, and, P. M. Hogarth. 2006. Raft localisation of FcγRIIa and efficient signaling are dependent on palmitoylation of cysteine 208. Immunol. Lett. 104: 118123.
14. Beekman, J. M.,, J. E. Bakema,, J. G. van de Winkel, and, J. H. Leusen. 2004. Direct interaction between FcγRI (CD64) and periplakin controls receptor endocytosis and ligand binding capacity. Proc. Natl. Acad. Sci. USA 101: 1039210397.
15. Benhamou, M.,, N. J. Ryba,, H. Kihara,, H. Nishikata, and, R. P. Siraganian. 1993. Protein-tyrosine kinase p72 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: 2331823324.
16. Berger, S. A.,, T. W. Mak, and, C. J. Paige. 1994. Leukocyte common antigen (CD45) is required for immunoglobulin E-mediated degranulation of mast cells. J. Exp. Med. 180: 471476.
17. Bergtold, A.,, D. D. Desai,, A. Gavhane, and, R. Clynes. 2005. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 23: 503514.
18. Bijsterbosch, M. K.,, and G. G. Klaus. 1985. Crosslinking of surface immunoglobulin and Fc receptors on B lymphocytes inhibits stimulation of inositol phospholipid breakdown via the antigen receptors. J. Exp. Med. 162: 18251836.
19. Bishop, B.,, and C. M. Lloyd. 2003. CC chemokine ligand 1 promotes recruitment of eosinophils but not Th2 cells during the development of allergic airways disease. J. Immunol. 170: 48104817.
20. Bobak, D. A.,, M. M. Frank, and, A. J. Tenner. 1988. C1q acts synergistically with phorbol dibutyrate to activate CR1-mediated phagocytosis by human mononuclear phagocytes. Eur. J. Immunol. 18: 20012007.
21. Bobak, D. A.,, T. A. Gaither,, M. M. Frank, and, A. J. Tenner. 1987. Modulation of FcR function by complement: subcomponent C1q enhances the phagocytosis of IgG-opsonized targets by human monocytes and culture-derived macrophages. J. Immunol. 138: 11501156.
22. Bodman-Smith, K. B.,, A. J. Melendez,, I. Campbell,, P. T. Harrison,, J. M. Allen, and, J. G. Raynes. 2002. C-reactive protein-mediated phagocytosis and phospholipase D signalling through the high-affinity receptor for immunoglobulin G (FcγRI). Immunology 107: 252260.
23. Bohnsack, J. F.,, H. K. Kleinman,, T. Takahashi,, J. J. O’Shea, and, E. J. Brown. 1985. Connective tissue proteins and phagocytic cell function: laminin enhances complement and Fc-mediated phagocytosis by cultured human phagocytes. J. Exp. Med. 161: 912923.
24. Bolland, S.,, R. N. Pearse,, T. Kurosaki, and, J. V. Ravetch. 1998. SHIP modulates immune receptor responses by regulating membrane association of BTK. Immunity 8: 509516.
25. Bolland, S.,, and J. V. Ravetch. 1999. Inhibitory pathways triggered by ITIM-containing receptors. Adv. Immunol. 72: 149177.
26. Bolland, S.,, and J. V. Ravetch. 2000. Spontaneous autoimmune disease in FcgRIIB-deficient mice results from strain-specific epistasis. Immunity 13: 277285.
27. Booth, J. W.,, M. K. Kim,, A. Jankowski,, A. D. Schreiber, and, S. Grinstein. 2002. Contrasting requirements for ubiquitylation during Fc receptor-mediated endocytosis and phagocytosis. EMBO J. 21: 251258.
28. Botelho, R. J.,, M. Teruel,, R. Dierckman,, R. Anderson,, A. Wells,, J. D. York,, T. Meyer, and, S. Grinstein. 2000. Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151: 13531368.
29. Braun, V.,, V. Fraisier,, G. Raposo,, I. Hurbain,, J. B. Sibarita,, P. Chavrier,, T. Galli, and, F. Niedergang. 2004. TI-VAMP/VAMP7 is required for optimal phagocytosis of opsonised particles in macrophages. EMBO J. 23: 41664176.
30. Brooks, D. G.,, W. Q. Qui,, A. D. Luster, and, J. V. Ravetch. 1989. Structure and expression of human IgG FcRII (CD32). Functional heterogeneity is encoded by the alternatively spliced products of multiple genes. J. Exp. Med. 170: 13691385.
31. Brown, E.,, L. Hooper,, T. Ho, and, H. Gresham. 1990. Integrin-associated protein: a 50 kD plasma membrane antigen physically and functionally associated with integrins. J. Cell Biol. 111: 27852794.
32. Brown, M. T.,, and J. A. Cooper. 1996. Regulation, substrates and functions of src. Biochim. Biophys. Acta 1287: 121149.
33. Brozna, J. P.,, N. F. Hauff,, W. A. Phillips, and, R. B. Johnston, Jr. 1988. Activation of the respiratory burst in macrophages. Phosphorylation specifically associated with Fc receptor-mediated stimulation. J. Immunol. 141: 16421647.
34. Buckle, A. M.,, and N. Hogg. 1989. The effect of IFN-γ and colony-stimulating factors on the expression of neutrophil cell membrane receptors. J. Immunol. 143: 22952301.
35. Canetti, C.,, D. M. Aronoff,, M. Choe,, N. Flamand,, S. Wettlaufer,, G. B. Toews,, G. H. Chen, and, M. Peters-Golden. 2006. Differential regulation by leukotrienes and calcium of Fc γ receptor-induced phagocytosis and Syk activation in dendritic cells versus macrophages. J. Leukoc. Biol. 79: 12341241.
36. Canfield, S. M.,, and S. L. Morrison. 1991. The binding affinity of human IgG for its high affinity Fc receptor is determined by multiple amino acids in the CH2 domain and is modulated by the hinge region. J. Exp. Med. 173: 14831491.
37. Capsoni, F.,, P. Bonara,, F. Minonzio,, A. M. Ongari,, G. Colombo,, G. P. Rizzardi, and, C. Zanussi. 1991. The effect of cytokines on human neutrophil Fc receptor-mediated phagocytosis. J. Clin. Lab. Immunol. 34: 115124.
38. Capsoni, F.,, F. Minonzio,, A. M. Ongari,, V. Carbonelli,, A. Galli, and, C. Zanussi. 1995. IL-10 up-regulates human monocyte phagocytosis in the presence of IL-4 and IFN-γ. J. Leukoc. Biol. 58: 351- 358.
39. Caron, E.,, and A. Hall. 1998. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282: 17171721.
40. Chensue, S. W.,, N. W. Lukacs,, T. Y. Yang,, X. Shang,, K. A. Frait,, S. L. Kunkel,, T. Kung,, M. T. Wiekowski,, J. A. Hedrick,, D. N. Cook,, A. Zingoni,, S. K. Narula,, A. Zlotnik,, F. J. Barrat,, A. O’Garra,, M. Napolitano, and, S. A. Lira. 2001. Aberrant in vivo T helper type 2 cell response and impaired eosinophil recruitment in CC chemokine receptor 8 knockout mice. J. Exp. Med. 193: 573584.
41. Chouchakova, N.,, J. Skokowa,, U. Baumann,, T. Tschernig,, K. M. Philippens,, B. Nieswandt,, R. E. Schmidt, and, J. E. Gessner. 2001. Fc γ RIII-mediated production of TNF-α induces immune complex alveolitis independently of CXC chemokine generation. J. Immunol. 166: 5193- 5200.
42. Clark, M. R.,, S. G. Stuart,, R. P. Kimberly,, P. A. Ory, and, I. M. Goldstein. 1991. A single amino acid distinguishes the high-responder from the low-responder form of Fc receptor II on human monocytes. Eur. J. Immunol. 21: 19111916.
43. Clarkson, S. B.,, R. P. Kimberly,, J. E. Valinsky,, M. D. Witmer,, J. B. Bussel,, R. L. Nachman, and, J. C. Unkeless. 1986. Blockade of clearance of immune complexes by an anti-Fcγ receptor monoclonal antibody. J. Exp. Med. 164: 474489.
44. Cohen-Solal, J. F.,, L. Cassard,, W. H. Fridman, and, C. Sautes-Fridman. 2004. Fc gamma receptors. Immunol. Lett. 92: 199205.
45. Collins, H. L.,, and G. J. Bancroft. 1992. Cytokine enhancement of complement-dependent phagocytosis by macrophages: synergy of tumor necrosis factor-alpha and granulocyte-macrophage colony-stimulating factor for phagocytosis of Cryptococcus neoformans. Eur. J. Immunol. 22: 14471454.
46. Colucci-Guyon, E.,, F. Niedergang,, B. J. Wallar,, J. Peng,, A. S. Alberts, and, P. Chavrier. 2005. A role for mammalian diaphanous-related formins in complement receptor (CR3)-mediated phagocytosis in macrophages. Curr. Biol. 15: 20072012.
47. Cooney, D. S.,, H. Phee,, A. Jacob, and, K. M. Coggeshall. 2001. Signal transduction by human-restricted Fc γ RIIa involves three distinct cytoplasmic kinase families leading to phagocytosis. J. Immunol. 167: 844854.
48. Coppolino, M. G.,, R. Dierckman,, J. Loijens,, R. F. Collins,, M. Pouladi,, J. Jongstra-Bilen,, A. D. Schreiber,, W. S. Trimble,, R. Anderson, and, S. Grinstein. 2002. Inhibition of phosphatidylinositol-4-phosphate 5-kinase Iα impairs localized actin remodeling and suppresses phagocytosis. J. Biol. Chem. 277: 4384943857.
49. Coppolino, M. G.,, M. Krause,, P. Hagendorff,, D. A. Monner,, W. Trimble,, S. Grinstein,, J. Wehland, and, A. S. Sechi. 2001. Evidence for a molecular complex consisting of Fyb/SLAP, SLP-76, Nck, VASP and WASP that links the actin cytoskeleton to Fcγ receptor signalling during phagocytosis. J. Cell Sci. 114: 43074318.
50. Corrotte, M.,, S. Chasserot-Golaz,, P. Huang,, G. Du,, N. T. Ktistakis,, M. A. Frohman,, N. Vitale,, M. F. Bader, and, N. J. Grant. 2006. Dynamics and function of phospholipase D and phosphatidic acid during phagocytosis. Traffic 7: 365377.
51. Cougoule, C.,, S. Hoshino,, A. Dart,, J. Lim, and, E. Caron. 2006. Dissociation of recruitment and activation of the small G-protein Rac during Fcγ receptor-mediated phagocytosis. J. Biol. Chem. 281: 87568764.
52. Cox, D.,, J. S. Berg,, M. Cammer,, J. O. Chinegwundoh,, B. M. Dale,, R. E. Cheney, and, S. Greenberg. 2002. Myosin X is a downstream effector of PI(3)K during phagocytosis. Nat. Cell Biol. 4: 469- 477.
53. Cox, D.,, P. Chang,, T. Kurosaki, and, S. Greenberg. 1996. Syk tyrosine kinase is required for immunoreceptor tyrosine activation motif-dependent actin assembly. J. Biol. Chem. 271: 1659716602.
54. Cox, D.,, P. Chang,, Q. Zhang,, P. G. Reddy,, G. M. Bokoch, and, S. Greenberg. 1997. Requirements for both Rac1 and Cdc42 in membrane ruffling and phagocytosis in leukocytes. J. Exp. Med. 186: 14871494.
55. Cox, D.,, B. M. Dale,, M. Kashiwada,, C. D. Helgason, and, S. Greenberg. 2001. A regulatory role for Src homology 2 domain-containing inositol 5′-phosphatase (SHIP) in phagocytosis mediated by Fc gamma receptors and complement receptor 3 (alpha(M)beta(2); CD11b/CD18). J. Exp. Med. 193: 6171.
56. Cox, D.,, and S. Greenberg. 2001. Phagocytic signaling strategies: Fcγ receptor-mediated phagocytosis as a model system. Semin. Immunol. 13: 339345.
57. Cox, D.,, D. J. Lee,, B. M. Dale,, J. Calafat, and, S. Greenberg. 2000. A Rab11-containing rapidly recycling compartment in macrophages that promotes phagocytosis. Proc. Natl. Acad. Sci. USA 97: 680685.
58. Cox, D.,, C.-C. Tseng,, G. Bjekic, and, S. Greenberg. 1999. A requirement for phosphatidylinositol 3-kinase in pseudopod extension. J. Biol. Chem. 274: 12401247.
59. Crowley, M. T.,, P. S. Costello,, C. J. Fitzer-Attas,, M. Turner,, F. Meng,, C. Lowell,, V. L. J. Tybulewicz, and, A. L. De-Franco. 1997. A critical role for Syk in signal transduction and phagocytosis mediated by Fc γ receptors on macrophages. J. Exp. Med. 186: 10271039.
60. Czibener, C.,, N. M. Sherer,, S. M. Becker,, M. Pypaert,, E. Hui,, E. R. Chapman,, W. Mothes, and, N. W. Andrews. 2006. Ca 2+ and synaptotagmin VII-dependent delivery of lysosomal membrane to nascent phagosomes. J. Cell Biol. 174: 9971007.
61. Daeron, M. 1996. Building up the family of ITIM-bearing negative coreceptors. Immunol. Lett. 54: 7376.
62. Daeron, M.,, and R. Lesourne. 2006. Negative signaling in Fc receptor complexes. Adv Immunol 89: 3986.
63. Davis, W.,, P. T. Harrison,, M. J. Hutchinson, and, J. M. Allen. 1995. Two distinct regions of Fc γ RI initiate separate signalling pathways involved in endocytosis and phagocytosis. EMBO J. 14: 432441.
64. Debets, J. M.,, J. G. van de Winkel,, J. L. Ceuppens,, I. E. Dieteren, and, W. A. Buurman. 1990. Cross-linking of both FcγRI and FcγRII induces secretion of tumor necrosis factor by human monocytes, requiring high affinity Fc-FcγR interactions. Functional activation of FcγRII by treatment with proteases or neuraminidase. J. Immunol. 144: 13041310.
65. Debets, J. M.,, C. J. Van der Linden,, I. E. Dieteren,, J. F. Leeuwenberg, and, W. A. Buurman. 1988. Fc-receptor cross-linking induces rapid secretion of tumor necrosis factor (cachectin) by human peripheral blood monocytes. J. Immunol. 141: 11971201.
66. Della Bianca, V.,, M. Grzeskowiak,, S. Dusi, and, F. Rossi. 1993. Formation of inositol (1,4,5) trisphosphate and increase of cytosolic Ca 2+ mediated by Fc receptors in human neutrophils. Biochem. Biophys. Res. Comm. 196: 12331239.
67. Della Bianca, V.,, M. Grzeskowiak, and, F. Rossi. 1990. Studies on molecular regulation of phagocytosis and activation of the NADPH oxidase in neutrophils-IgG- and C3b- mediated ingestion and associated respiratory burst independent of phospholipid turnover and Ca 2+ transients. J. Immunol. 144: 14111417.
68. Denu, J. M.,, and K. G. Tanner. 1998. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 37: 56335642.
69. de Waal Malefyt, R.,, C. G. Figdor,, R. Huijbens,, S. Mohan-Peterson,, B. Bennett,, J. Culpepper,, W. Dang,, G. Zurawski, and, J. E. de Vries. 1993. Effects of IL-13 on phenotype, cytokine production, and cytotoxic function of human monocytes. Comparison with IL-4 and modulation by IFN-γ or IL-10. J. Immunol. 151: 63706381.
70. Diamond, M. S.,, R. Alon,, C. A. Parkos,, M. T. Quinn, and, T. A. Springer. 1995. Heparin is an adhesive ligand for the leukocyte integrin Mac-1 (CD11b/CD18). J. Cell Biol. 130: 14731482.
71. Drechsler, Y.,, S. Chavan,, D. Catalano,, P. Mandrekar, and, G. Szabo. 2002. FcγR cross-linking mediates NF-kB activation, reduced antigen presentation capacity, and decreased IL-12 production in monocytes without modulation of myeloid dendritic cell development. J. Leukoc. Biol. 72: 657667.
72. Duchemin, A.-M.,, and C. L. Anderson. 1997. Association of non-receptor protein tyrosine kinases with the FcγRI/γ-chain complex in monocytic cells. J. Immunol. 158: 865871.
73. 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 γ-chain. J. Biol. Chem. 269: 1211112117.
74. Duits, A. J.,, H. Bootsma,, R. H. Derksen,, P. E. Spronk,, L. Kater,, C. G. Kallenberg,, P. J. Capel,, N. A. Westerdaal,, G. T. Spierenburg,, F. H. Gmelig-Meyling, et al. 1995. Skewed distribution of IgG Fc receptor IIa (CD32) polymorphism is associated with renal disease in systemic lupus erythematosus patients. Arthritis Rheum. 38: 18321836.
75. Durden, D. L.,, H. M. Kim,, B. Calore, and, Y. B. Liu. 1995. The FcγRI receptor signals through the activation of hck and MAP kinase. J. Immunol. 154: 40394047.
76. Dusi, S.,, M. Donini,, B. V. Della, 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: 11001108.
77. Ernst, L. K.,, J. G. J. van de Winkel,, I.-M. Chiu, and, C. L. Anderson. 1992. Three genes for the human high affinity Fc receptor for IgG (FcγRI) encode four distinct transcription products. J. Biol. Chem. 267: 1569215700.
78. Fahy, R. J.,, P. T. Diaz,, J. Hart, and, M. D. Wewers. 2001. BAL and serum IgG levels in healthy asymptomatic HIV-infected patients. Chest 119: 196203.
79. Fallman, M.,, K. Andersson,, S. Hakansson,, K.-E. Magnusson,, O. Stendahl, and, H. Wolf-Watz. 1995. Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells. Infect. Immun. 63: 31173124.
80. Fanger, N. A.,, D. Voigtlaender,, C. Liu,, S. Swink,, K. Ward-well,, J. Fisher,, R. F. Graziano,, L. C. Pfefferkorn, and, P. M. Guyre. 1997. Characterization of expression, cytokine regulation, and effector function of the high affinity IgG receptor Fc γ RI (CD64) expressed on human blood dendritic cells. J. Immunol. 158: 30903098.
81. Fernandes, M. J.,, E. Rollet-Labelle,, G. Pare,, S. Marois,, M. L. Tremblay,, J. L. Teillaud, and, P. H. Naccache. 2006. CD16b associates with high-density, detergent-resistant membranes in human neutrophils. Biochem. J. 393: 351359.
82. Gagnon, E.,, S. Duclos,, C. Rondeau,, E. Chevet,, P. H. Cameron,, O. Steele-Mortimer,, J. Paiement,, J. J. Bergeron, and, M. Desjardins. 2002. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110: 119131.
83. Galon, J.,, J. F. Gauchat,, N. Mazieres,, R. Spagnoli,, W. Storkus,, M. Lotze,, J. Y. Bonnefoy,, W. H. Fridman, and, C. Sautes. 1996. Soluble Fcγ receptor type III (FcγRIII, CD16) triggers cell activation through interaction with complement receptors. J. Immunol. 157: 11841192.
84. Ganesan, L. P.,, H. Fang,, C. B. Marsh, and, S. Tridandapani. 2003. The protein-tyrosine phosphatase SHP-1 associates with the phosphorylated immunoreceptor tyrosine-based activation motif of Fc γ RIIa to modulate signaling events in myeloid cells. J. Biol. Chem. 278: 3571035717.
85. Garcia-Garcia, E.,, E. J. Brown, and, C. Rosales. 2007. Trans-membrane mutations to FcγRIIA alter its association with lipid rafts: implications for receptor signaling. J. Immunol. 178: 30483058.
86. Gessner, J. E.,, H. Heiken,, A. Tamm, and, R. E. Schmidt. 1998. The IgG Fc receptor family. Ann. Hematol. 76: 231248.
87. Gewirtz, A. T.,, and E. R. Simons. 1997. Phospholipase D mediates Fcγ receptor activation of neutrophils and provides specificity between high-valency immune complexes and fMLP signaling pathways. J. Leukoc. Biol. 61: 522- 528.
88. 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: 88788884.
89. Ghazizadeh, S.,, J. B. Bolen, and, H. B. Fleit. 1995. Tyrosine phosphorylation and association of Syk with Fcγ RII in monocytic THP-1 cells. Biochem. J. 305: 669674.
90. Ghazizadeh, S.,, and H. B. Fleit. 1994. Tyrosine phosphorylation provides an obligatory early signal for Fcγ RII-mediated endocytosis in the monocytic cell line THP-1. J. Immunol. 152: 3041.
91. Girard, M. T.,, S. Hjaltadottir,, A. N. Fejes-Toth, and, P. M. Guyre. 1987. Glucocorticoids enhance the γ-interferon augmentation of human monocyte immunoglobulin G Fc receptor expression. J. Immunol. 138: 32353241.
92. Gold, E. S.,, D. M. Underhill,, N. S. Morrissette,, J. Guo,, M. A. McNiven, and, A. Aderem. 1999. Dynamin 2 is required for phagocytosis in macrophages. J. Exp. Med. 190: 18491856.
93. Green, J. M.,, A. D. Schreiber, and, E. J. Brown. 1997. Role for a glycan phosphoinositol anchor in Fcγ receptor synergy. J. Cell Biol. 139: 12091217.
94. Greenberg, S. 1999. Fc receptor-mediated phagocytosis, p. 149-191. In S. Gordon (ed.), Phagocytosis: The Host, vol. 5. JAI Press, Stamford, CT.
95. 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: 18531856.
96. Greenberg, S.,, P. Chang, and, S. C. Silverstein. 1993. Tyro-sine phosphorylation is required for Fc receptor-mediated phagocytosis in mouse macrophages. J. Exp. Med. 177: 529534.
97. Greenberg, S.,, P. Chang, and, S. C. Silverstein. 1994. Tyro-sine phosphorylation of the γ subunit of Fc γ receptors, p72 syk, and paxillin during Fc receptor-mediated phagocytosis in macrophages. J. Biol. Chem. 269: 38973902.
98. 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: 11031107.
99. Gresham, H. D.,, B. M. Dale,, J. W. Potter,, P. W. Chang,, C. M. Vines,, C. A. Lowell,, C. F. Lagenaur, and, C. L. Will-man. 2000. Negative regulation of phagocytosis in murine macrophages by the Src kinase family member, Fgr. J. Exp. Med. 191: 515528.
100. Gu, H.,, R. J. Botelho,, M. Yu,, S. Grinstein, and, B. G. Neel. 2003. Critical role for scaffolding adapter Gab2 in Fc γ R-mediated phagocytosis. J. Cell Biol. 161: 1151- 1161.
101. Gupta, N.,, A. M. Scharenberg,, D. N. Burshtyn,, N. Wagt-mann,, M. N. Lioubin,, L. R. Rohrschneider,, J. P. Kinet, and, E. O. Long. 1997. Negative signaling pathways of the killer cell inhibitory receptor and Fc γ RIIb1 require distinct phosphatases. J. Exp. Med. 186: 473478.
102. Gupta, R. K.,, and G. R. Siber. 1995. Method for quantitation of IgG subclass antibodies in mouse serum by enzyme-linked immunosorbent assay. J. Immunol. Methods 181: 7581.
103. Guriec, N.,, C. Daniel,, K. Le Ster,, E. Hardy, and, C. Berthou. 2006. Cytokine-regulated expression and inhibitory function of FcγRIIB1 and -B2 receptors in human dendritic cells. J. Leukoc. Biol. 79: 5970.
104. Hackam, D. J.,, O. D. Rotstein,, A. Schreiber,, W. J. Zhang, and, S. Grinstein. 1997. Rho is required for the initiation of calcium signaling and phagocytosis by Fcγ receptors in macrophages. J. Exp. Med. 186: 955966.
105. Hall, A. B.,, M. A. Gakidis,, M. Glogauer,, J. L. Wilsbacher,, S. Gao,, W. Swat, and, J. S. Brugge. 2006. Requirements for Vav guanine nucleotide exchange factors and Rho GTPases in FcγR- and complement-mediated phagocytosis. Immunity 24: 305316.
106. Hallett, M. B. 2006. Phagocytosis of optically-trapped particles: delivery of the pure phagocytic signal. Cell Res. 16: 852854.
107. Hamada, F.,, M. Aoki,, T. Akiyama, and, K. Toyoshima. 1993. Association of immunoglobulin G Fc receptor II with Srclike protein-tyrosine kinase Fgr in neutrophils. Proc. Natl. Acad. Sci. USA 90: 63056309.
108. Hamerman, J. A.,, and L. L. Lanier. 2006. Inhibition of immune responses by ITAM-bearing receptors. Sci. STKE 2006: re1.
109. Hartwig, J. H.,, G. M. Bokoch,, C. L. Carpenter,, P. A. Janmey,, L. A. Taylor,, A. Toker, and, T. P. Stossel. 1995. Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell 82: 643653.
110. Hauschildt, S.,, and B. Kleine. 1995. Bacterial stimulators of macrophages. Int. Rev. Cytol. 161: 263331.
111. 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,, J. G. van de Winkel, and, J. S. Verbeek. 1996. Impaired IgG-dependent anaphylaxis and Arthus reaction in Fc γ RIII (CD16) deficient mice. Immunity 5: 181188.
112. Herr, A. B.,, E. R. Ballister, and, P. J. Bjorkman. 2003. Insights into IgA-mediated immune responses from the crystal structures of human FcαRI and its complex with IgA1-Fc. Nature 423: 614620.
113. Hibbs, M. L.,, P. Selvaraj,, O. Carpen,, T. A. Springer,, H. Kuster,, M. E. Jouvin, and, J. Kinet. 1989. Mechanisms for regulating expression of membrane isoforms of FcγRIII (CD16). Science 246: 16081611.
114. 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 A 2 pathway by Fc ΣR1 is not shared by a G protein-coupled receptor. J. Biol. Chem. 270: 1096010967.
115. Hirata, Y.,, and T. Suzuki. 1987. Protein kinase activity associated with Fcγ 2a receptor of a murine macrophage like cell line, P388D 1. Biochemistry 26: 81898195.
116. Hitomi, T.,, S. Yanagi,, R. Inatome,, J. Ding,, T. Takano, and, H. Yamamura. 2001. Requirement of Syk-phospholipase C-γ2 pathway for phorbol ester-induced phospholipase D activation in DT40 cells. Genes Cells 6: 475485.
117. Hitomi, T.,, S. Yanagi,, R. Inatome, and, H. Yamamura. 1999. Cross-linking of the B cell receptor induces activation of phospholipase D through Syk, Btk and phospholipase C-γ2. FEBS Lett. 445: 371374.
118. Hogarth, P. M. 2002. Fc receptors are major mediators of antibody based inflammation in autoimmunity. Curr. Opin. Immunol. 14: 798802.
119. Hoppe, A. D.,, and J. A. Swanson. 2004. Cdc42, Rac1, and Rac2 display distinct patterns of activation during phagocytosis. Mol. Biol. Cell 15: 35093519.
120. Hostoffer, R. W.,, I. Krukovets, and, M. Berger. 1994. Enhancement by tumor necrosis factor-α of Fc α receptor expression and IgA-mediated superoxide generation and killing of Pseudomonas aeruginosa by polymorphonuclear leukocytes. J. Infect. Dis. 170: 8287.
121. Hostoffer, R. W.,, I. Krukovets, and, M. Berger. 1993. Increased FcαR expression and IgA-mediated function on neutrophils induced by chemoattractants. J. Immunol. 150: 45324540.
122. Huang, Z. Y.,, D. R. Barreda,, R. G. Worth,, Z. K. Indik,, M. K. Kim,, P. Chien, and, A. D. Schreiber. 2006. Differential kinase requirements in human and mouse Fc-γ receptor phagocytosis and endocytosis. J. Leukoc. Biol. 80: 15531562.
123. Huang, Z. Y.,, S. Hunter,, M. K. Kim,, Z. K. Indik, and, A. D. Schreiber. 2003. The effect of phosphatases SHP-1 and SHIP-1 on signaling by the ITIM- and ITAM-containing Fcγ receptors FcγRIIB and FcγRIIA. J. Leukoc. Biol. 73: 823829.
124. Huizinga, T. W. J.,, C. E. van der Schoot,, C. Jost,, R. Klaassen,, M. Kleijer,, A. E. G. K. von dem Borne,, D. Roos, and, P. A. T. Tetteroo. 1988. The PI-linked receptor FcRIII is released on stimulation of neutrophils. Nature 333: 667669.
125. Huizinga, T. W. J.,, F. van Kemenade,, L. Koenderman,, K. M. Dolman,, A. E. G. Von den Borne,, P. A. T. Tetteroo, and, R. Roos. 1989. The 40-kDa Fc γ receptor (FcRII) on human neutrophils is essential for the IgG-induced respiratory burst and IgG-induced phagocytosis. J. Immunol. 142: 23652369.
126. Hulett, M. D.,, and P. M. Hogarth. 1994. Molecular basis of Fc receptor function. Adv. Immunol. 57: 1127.
127. Hulett, M. D.,, N. Osman,, I. F. McKenzie, and, P. M. Hogarth. 1991. Chimeric Fc receptors identify functional domains of the murine high affinity receptor for IgG. J. Immunol. 147: 18631868.
128. Ioan-Facsinay, A.,, S. J. de Kimpe,, S. M. Hellwig,, P. L. van Lent,, F. M. Hofhuis,, H. H. van Ojik,, C. Sedlik,, S. A. da Silveira,, J. Gerber,, Y. F. de Jong,, R. Roozendaal,, L. A. Aarden,, W. B. van den Berg,, T. Saito,, D. Mosser,, S. Amigorena,, S. Izui,, G. J. van Ommen,, M. van Vugt,, J. G. van de Winkel, and, J. S. Verbeek. 2002. FcγRI (CD64) contributes substantially to severity of arthritis, hypersensitivity responses, and protection from bacterial infection. Immunity 16: 391402.
129. Israel, E. J.,, D. F. Wilsker,, K. C. Hayes,, D. Schoenfeld, and, N. E. Simister. 1996. Increased clearance of IgG in mice that lack β2-microglobulin: possible protective role of FcRn. Immunology 89: 573578.
130. Jaconi, M. E. E.,, D. P. Lew,, J.-L. Carpentier,, K. E. Magnusson,, M. Sjogren, and, O. Stendahl. 1990. Cytosolic free calcium elevation mediates the phagosome-lysosome fusion during phagocytosis in human neutrophils. J. Cell Biol. 110: 15551564.
131. Ji, J. D.,, I. Tassiulas,, K. H. Park-Min,, A. Aydin,, I. Mecklenbrauker,, A. Tarakhovsky,, L. Pricop,, J. E. Salmon, and, L. B. Ivashkiv. 2003. Inhibition of interleukin 10 signaling after Fc receptor ligation and during rheumatoid arthritis. J. Exp. Med. 197: 15731583.
132. Jones, S. L.,, and E. J. Brown. 1996. FcγRII-mediated adhesion and phagocytosis induce L-plastin phosphorylation in human neutrophils. J. Biol. Chem. 271: 1462314630.
133. Joshi, T.,, L. P. Ganesan,, X. Cao, and, S. Tridandapani. 2006. Molecular analysis of expression and function of hFcγRIIbl and b2 isoforms in myeloid cells. Mol. Immunol. 43: 839850.
134. 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: 59185925.
135. Junghans, R. P.,, and C. L. Anderson. 1996. The protection receptor for IgG catabolism is the β2-microglobulin-containing neonatal intestinal transport receptor. Proc. Natl. Acad. Sci. USA 93: 55125516.
136. Kant, A. M.,, P. De,, X. Peng,, T. Yi,, D. J. Rawlings,, J. S. Kim, and, D. L. Durden. 2002. SHP-1 regulates Fcγ receptor-mediated phagocytosis and the activation of RAC. Blood 100: 18521859.
137. 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: 42094220.
138. 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 I (Fcγ RI) and receptor II (Fcγ 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: 2444224448.
139. Kimberly, R. P.,, J. W. Ahlstrom,, M. E. Click, and, J. C. Edberg. 1990. The glycosyl phosphatidylinositol-linked FcγRIII PMN mediates transmembrane signaling events distinct from FcγRII. J. Exp. Med. 171: 12391255.
140. Kimura, T.,, H. Sakamoto,, E. Appella, and, R. P. Siraganian. 1996. Conformational changes induced in the protein tyro-sine kinase p72 syk by tyrosine phosphorylation or by binding of phosphorylated immunoreceptor tyrosine-based activation motif peptides. Mol. Cell Biol. 16: 14711478.
141. Kimura, T.,, J. Zhang,, K. Sagawa,, K. Sakaguchi,, E. Appella, and, R. P. Siraganian. 1997. Syk-independent tyrosine phosphorylation and association of the protein tyrosine phosphatases SHP-1 and SHP-2 with the high affinity IgE receptor. J. Immunol. 159: 44264434.
142. Klebanoff, S. J.,, M. A. Vadas,, J. M. Harlan,, L. H. Sparks,, J. R. Gamble,, J. M. Agosti, and, A. M. Waltersdorph. 1986. Stimulation of neutrophils by tumor necrosis factor. J. Immunol. 136: 42204225.
143. Kleinau, S.,, P. Martinsson, and, B. Heyman. 2000. Induction and suppression of collagen-induced arthritis is dependent on distinct fcγ receptors. J. Exp. Med. 191: 16111616.
144. Kono, H.,, C. Kyogoku,, T. Suzuki,, N. Tsuchiya,, H. Honda,, K. Yamamoto,, K. Tokunaga, and, Z. Honda. 2005. FcγRIIB Ile232Thr transmembrane polymorphism associated with human systemic lupus erythematosus decreases affinity to lipid rafts and attenuates inhibitory effects on B cell receptor signaling. Hum. Mol. Genet. 14: 28812892.
145. Koval, M.,, K. Preiter,, C. Adles,, P. D. Stahl, and, T. H. Steinberg. 1998. Size of IgG-opsonized particles determines macrophage response during internalization. Exp. Cell Res. 242: 265273.
146. Kuhlman, M.,, K. Joiner, and, R. A. B. Ezekowitz. 1989. The human mannose-binding protein functions as an opsonin. J. Exp. Med. 169: 17331745.
147. Kumar, V.,, S. R. Ali,, S. Konrad,, J. Zwirner,, J. S. Verbeek,, R. E. Schmidt, and, J. E. Gessner. 2006. Cell-derived anaphylatoxins as key mediators of antibody-dependent type II autoimmunity in mice. J. Clin. Invest. 116: 512520.
148. Kurosaki, T.,, and J. V. Ravetch. 1989. A single amino acid in the glycosyl phosphatidyl inositol attachment domain determines the membrane topology of FcγRIII. Nature 342: 805807.
149. Kurosaki, T.,, M. Takata,, Y. Yamanashi,, T. Inazu,, T. Taniguchi,, T. Yamamoto, and, H. Yamamura. 1994. Syk activation by the Src-family tyrosine kinase in the B cell receptor signaling. J. Exp. Med. 179: 17251729.
150. Kusner, D. J.,, C. F. Hall, and, S. Jackson. 1999. Fcγ receptor-mediated activation of phospholipase D regulates macrophage phagocytosis of IgG-opsonized particles. J. Immunol. 162: 22662274.
151. Lanier, L. L.,, S. Cwirla,, G. Yu,, R. Testi, and, J. H. Phillips. 1989. Membrane anchoring of a human IgG Fc receptor (CD16) determined by a single amino acid. Science 246: 16111613.
152. Larsen, E. C.,, T. Ueyama,, P. M. Brannock,, Y. Shirai,, N. Saito,, C. Larsson,, D. Loegering,, P. B. Weber, and, M. R. Lennartz. 2002. A role for PKC-e in FcγR-mediated phagocytosis by RAW 264.7 cells. J. Cell Biol. 159: 939944.
153. Laudanna, C.,, J. J. Campbell, and, E. C. Butcher. 1996. Role of Rho in chemoattractant-activated leukocyte adhesion through integrins. Science 271: 981983.
154. Law, D. A.,, V. W. F. Chan,, S. K. Datta, and, A. L. DeFranco. 1993. B-cell antigen receptor motifs have redundant signalling capabilities and bind the tyrosine kinases PTK72, Lyn and Fyn. Curr. Biol. 3: 645657.
155. Lee, J. H.,, Y. M. Kim,, N. W. Kim,, J. W. Kim,, E. Her,, B. K. Kim,, J. H. Kim,, S. H. Ryu,, J. W. Park,, D. W. Seo,, J. W. Han,, M. A. Beaven, and, W. S. Choi. 2006. Phospholipase D2 acts as an essential adaptor protein in the activation of Syk in antigen-stimulated mast cells. Blood 108: 956964.
156. Lee, J. S.,, W. M. Nauseef,, A. Moeenrezakhanlou,, L. M. Sly,, S. Noubir,, K. G. Leidal,, J. M. Schlomann,, G. Krystal, and, N. E. Reiner. 2007. Monocyte p110α phosphatidylinositol 3-kinase regulates phagocytosis, the phagocyte oxidase, and cytokine production. J. Leukoc. Biol. 81: 15481561.
157. Lee, W. L.,, G. Cosio,, K. Ireton, and, S. Grinstein. 2007. Role of CrkII in Fcγ receptor-mediated phagocytosis. J. Biol. Chem. 282: 1113511143.
158. Lencer, W. I.,, and R. S. Blumberg. 2005. A passionate kiss, then run: exocytosis and recycling of IgG by FcRn. Trends Cell Biol 15: 59.
159. Lennartz, M. R.,, and E. J. Brown. 1991. Arachidonic acid is essential for IgG Fc receptor-mediated phagocytosis by human monocytes. J. Immunol. 147: 621626.
160. Lennartz, M. R.,, A. F. C. Yuen,, S. M. Masi,, D. G. Russell,, K. F. Buttle, and, J. J. Smith. 1997. Phospholipase A 2 inhibition results in sequestration of plasma membrane into electron-lucent vesicles during IgG-mediated phagocytosis. J. Cell Sci. 110: 20412052.
161. Lerm, M.,, V. P. Brodin,, I. Ruishalme,, O. Stendahl, and, E. Sarndahl. 2007. Inactivation of cdc42 is necessary for depolymerization of phagosomal f-actin and subsequent phagosomal maturation. J. Immunol. 178: 73577365.
162. Leverrier, Y.,, K. Okkenhaug,, C. Sawyer,, A. Bilancio,, B. Vanhaesebroeck, and, A. J. Ridley. 2003. Class I phosphoinositide 3-kinase p110β is required for apoptotic cell and Fcγ receptor-mediated phagocytosis by macrophages. J. Biol. Chem. 278: 3843738442.
163. Li, X.,, J. Wu,, R. H. Carter,, J. C. Edberg,, K. Su,, G. S. Cooper, and, R. P. Kimberly. 2003. A novel polymorphism in the Fcγ receptor IIB (CD32B) transmembrane region alters receptor signaling. Arthritis Rheum. 48: 32423252.
164. Liang, L.,, and C.-K. Huang. 1995. Activation of multiple protein kinase induced by cross-linking of FcγRII in human neutrophils. J. Leukoc. Biol. 57: 326331.
165. Lim, J.,, A. Wiedemann,, G. Tzircotis,, S. J. Monkley,, D. R. Critchley, and, E. Caron. 2007. An essential role for talin during α Mβ 2-mediated phagocytosis. Mol. Biol. Cell 18: 976985.
166. Lin, P. M.,, and J. R. Wright. 2006. Surfactant protein A binds to IgG and enhances phagocytosis of IgG-opsonized erythrocytes. Am. J. Physiol. Lung Cell. Mol. Physiol. 291: L1199L1206.
167. Lin, S. Q.,, C. Cicala,, A. M. Scharenberg, and, J. P. Kinet. 1996. The FcεRI β subunit functions as an amplifier of FcεRI γ-mediated cell activation signals. Cell 85: 985995.
168. Lindberg, F. P.,, D. C. Bullard,, T. E. Caver,, H. D. Gresham,, A. L. Beaudet, and, E. J. Brown. 1996. Decreased resistance to bacterial infection and granulocyte defects in IAPdeficient mice. Science 274: 795798.
169. Lindberg, F. P.,, H. D. Gresham,, E. Schwarz, and, E. J. Brown. 1993. Molecular cloning of integrin-associated protein: an immunoglobulin family member with multiple membrane-spanning domains implicated inα vβ 3-dependent ligand binding. J. Cell Biol. 123: 485496.
170. Lioubin, M. N.,, P. A. Algate,, S. Tsai,, K. Carlberg,, A. Aebersold, and, L. R. Rohrschneider. 1996. p150 Ship, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev. 10: 10841095.
171. Liu, Y.,, E. Masuda,, M. C. Blank,, K. A. Kirou,, X. Gao,, M. S. Park, and, L. Pricop. 2005. Cytokine-mediated regulation of activating and inhibitory Fc γ receptors in human monocytes. J. Leukoc. Biol. 77: 767776.
172. Lorenzi, R.,, P. M. Brickell,, D. R. Katz,, C. Kinnon, and, A. J. Thrasher. 2000. Wiskott-Aldrich syndrome protein is necessary for efficient IgG-mediated phagocytosis. Blood 95: 29432946.
173. Lubeck, M. D.,, Z. Steplewski,, F. Baglia,, M. H. Klein,, K. D. Dorrington, and, H. Koprowski. 1985. The interaction of murine IgG subclass proteins with human monocyte Fc receptors. J. Immunol. 135: 12991304.
174. Majeed, M.,, E. Caveggion,, C. A. Lowell, and, G. Berton. 2001. Role of Src kinases and Syk in Fcγ receptor-mediated phagocytosis and phagosome-lysosome fusion. J. Leukoc. Biol. 70: 801811.
175. Maliszewski, C. R.,, C. J. March,, M. A. Schoenborn,, S. Gimpel, and, L. Shen. 1990. Expression cloning of a human Fc receptor for IgA. J. Exp. Med. 172: 16651672.
176. Marcilla, A.,, O. M. Riverolezcano,, A. Agarwal, and, K. C. Robbins. 1995. Identification of the major tyrosine kinase substrate in signaling complexes formed after engagement of Fcγ receptors. J. Biol. Chem. 270: 91159120.
177. Massol, P.,, P. Montcourrier,, J.-C. Guillemot, and, P. Chavrier. 1998. Fc receptor-mediated phagocytosis requires CDC42 and Rac1. EMBO J. 17: 62196229.
178. Matsuda, M.,, J. G. Park,, D. C. Wang,, S. Hunter,, P. Chien, and, A. D. Schreiber. 1996. Abrogation of the Fcγ receptor IIA-mediated phagocytic signal by stem-loop Syk antisense oligonucleotides. Mol. Biol. Cell 7: 10951106.
179. Matsuo, T.,, K. Hazeki,, O. Hazeki,, T. Katada, and, M. Ui. 1996. Specific association of phosphatidylinositol 3-kinase with the protooncogene product Cbl in Fcγ receptor signaling. FEBS Lett. 382: 1114.
180. May, R. C.,, E. Caron,, A. Hall, and, L. M. Machesky. 2000. Involvement of the Arp2/3 complex in phagocytosis mediated by FcγR or CR3. Nat. Cell Biol. 2: 246248.
181. Mayorga, L. S.,, M. I. Colombo,, M. Lennartz,, E. J. Brown,, K. H. Rahman,, R. Weiss,, P. J. Lennon, and, P. D. Stahl. 1993. Inhibition of endosome fusion by phospholipase A 2 (PLA 2) inhibitors points to a role for PLA 2 in endocytosis. Proc. Natl. Acad. Sci. USA 90: 1025510259.
182. Means, T. K.,, E. Latz,, F. Hayashi,, M. R. Murali,, D. T. Golenbock, and, A. D. Luster. 2005. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. J. Clin. Invest. 115: 407417.
183. Melendez, A.,, R. A. Floto,, D. J. Gillooly,, M. M. Harnett, and, J. M. Allen. 1998. FcγRI coupling to phospholipase D initiates sphingosine kinase-mediated calcium mobilization and vesicular trafficking. J. Biol. Chem. 273: 93939402.
184. Mero, P.,, C. Y. Zhang,, Z. Y. Huang,, M. K. Kim,, A. D. Schreiber,, S. Grinstein, and, J. W. Booth. 2006. Phosphorylation-independent ubiquitylation and endocytosis of Fc γRIIA. J. Biol. Chem. 281: 3324233249.
185. Meyer, D.,, C. Schiller,, J. Westermann,, S. Izui,, W. L. Hazenbos,, J. S. Verbeek,, R. E. Schmidt, and, J. E. Gessner. 1998. FcγRIII (CD16)-deficient mice show IgG isotype-dependent protection to experimental autoimmune hemolytic anemia. Blood 92: 39974002.
186. Miettinen, H. M.,, J. K. Rose, and, I. Mellman. 1989. Fc receptor isoforms exhibit distinct abilities for coated pit localization as a result of cytoplasmic domain heterogeneity. Cell 58: 317327.
187. Missy, K.,, V. VanPoucke,, P. Raynal,, C. Viala,, G. Mauco,, M. Plantavid,, H. Chap, and, B. Payrastre. 1998. Lipid products of phosphoinositide 3-kinase interact with rad GTPase and stimulate GDP dissociation. J. Biol. Chem. 273: 3027930286.
188. Mocsai, A.,, M. Zhou,, F. Meng,, V. L. Tybulewicz, and, C. A. Lowell. 2002. Syk is required for integrin signaling in neutrophils. Immunity 16: 547558.
189. Monteiro, R. C.,, and J. G. Van De Winkel. 2003. IgA Fc receptors. Annu. Rev. Immunol. 21: 177204.
190. Moxey-Mims, M. M.,, H. H. Simms,, M. M. Frank,, E. Y. Lin, and, T. A. Gaither. 1991. The effects of IL-1, IL-2, and tumor necrosis factor on polymorphonuclear leukocyte Fcγ receptor-mediated phagocytosis. J. Immunol. 147: 18231830.
191. Munugalavadla, V.,, J. Borneo,, D. A. Ingram, and, R. Kapur. 2005. p85α subunit of class IA PI-3 kinase is crucial for macrophage growth and migration. Blood 106: 103109.
192. 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 Fc γRIIB modulates B-cell receptor signalling. Nature 368: 7073.
193. Nagarajan, S.,, K. Venkiteswaran,, M. Anderson,, U. Sayed,, C. Zhu, and, P. Selvaraj. 2000. Cell-specific, activation-dependent regulation of neutrophil CD32A ligand-binding function. Blood 95: 10691077.
194. Neel, B. G. 1997. Role of phosphatases in lymphocyte activation. Curr. Opin. Immunol. 9: 405420.
195. Niedergang, F.,, and P. Chavrier. 2005. Regulation of phagocytosis by Rho GTPases. Curr. Top. Microbiol. Immunol. 291: 4360.
196. Niedergang, F.,, E. Colucci-Guyon,, T. Dubois,, G. Raposo, and, P. Chavrier. 2003. ADP ribosylation factor 6 is activated and controls membrane delivery during phagocytosis in macrophages. J. Cell Biol. 161: 11431150.
197. Nimmerjahn, F.,, P. Bruhns,, K. Horiuchi, and, J. V. Ravetch. 2005. FcγRIV: a novel FcR with distinct IgG subclass specificity. Immunity 23: 4151.
198. Nitta, T.,, and T. Suzuki. 1982. Fc γ2b receptor-mediated prostaglandin synthesis by a murine macrophage cell line P388D 1. J. Immunol. 128: 25272532.
199. Odin, J. A.,, J. C. Edberg,, C. J. Painter,, R. P. Kimberly, and, J. C. Unkeless. 1991. Regulation of phagocytosis and [Ca 2+] i flux by distinct regions of an Fc receptor. Science 254: 17851788.
200. Ofek, I.,, J. Goldhar,, Y. Keisari, and, N. Sharon. 1995. Nonopsonic phagocytosis of microorganisms. Annu. Rev. Microbiol. 49: 239276.
201. Okayama, Y.,, A. S. Kirshenbaum, and, D. D. Metcalfe. 2000. Expression of a functional high-affinity IgG receptor, Fcγ RI, on human mast cells: up-regulation by IFN-γ. J. Immunol. 164: 43324339.
202. Olazabal, I. M.,, E. Caron,, R. C. May,, K. Schilling,, D. A. Knecht, and, L. M. Machesky. 2002. Rho-kinase and myosinII control phagocytic cup formation during CR, but not FcγR, phagocytosis. Curr. Biol. 12: 14131418.
203. Olcese, L.,, P. Lang,, F. Vely,, A. Cambiaggi,, D. Marguet,, M. Blery,, K. L. Hippen,, R. Biassoni,, A. Moretta,, L. Moretta,, J. C. Cambier, and, E. Vivier. 1996. Human and mouse killer-cell inhibitory receptors recruit PTP1C and PTP1D protein tyrosine phosphatases. J. Immunol. 156: 45314534.
204. 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 FcγRIIB. Nature 383: 263266.
205. Ono, M.,, H. Okada,, S. Bolland,, S. Yanagi,, T. Kurosaki, and, J. V. Ravetch. 1997. Deletion of SHIP or SHP-1 reveals two distinct pathways for inhibitory signaling. Cell 90: 293301.
206. Osborne, M. A.,, G. Zenner,, M. Lubinus,, X. L. Zhang,, Z. Songyang,, L. C. Cantley,, P. Majerus,, P. Burn, and, J. P. Kochan. 1996. The inositol 5′-phosphatase SHIP binds to immunoreceptor signaling motifs and responds to high affinity IgE receptor aggregation. J. Biol. Chem. 271: 2927129278.
207. Oster, G. 1987. The physics of cell motility. J. Cell Sci. 8: 3554.
208. Ota, Y.,, and L. E. Samelson. 1997. The product of the protooncogene c-cbl: a negative regulator of the Syk tyrosine kinase. Science 276: 418420.
209. Paolini, R.,, M. H. Jouvin, and, J. P. Kinet. 1991. Phosphorylation and dephosphorylation of the high-affinity receptor for immunoglobulin E immediately after receptor engagement and disengagement. Nature 353: 855858.
210. Park, R. K.,, Y. B. Liu, and, D. L. Durden. 1996. A role for Shc, Grb2, and Raf-1 in FcγRI signal relay. J. Biol. Chem. 271: 1334213348.
211. Parren, P. W.,, P. A. Warmerdam,, L. C. Boeije,, J. Arts,, N. A. Westerdaal,, A. Vlug,, P. J. Capel,, L. A. Aarden, and, J. G. van de Winkel. 1992. On the interaction of IgG subclasses with the low affinity FcγRIIa (CD32) on human monocytes, neutrophils, and platelets. Analysis of a functional polymorphism to human IgG2. J. Clin. Invest. 90: 15371546.
212. Pasquier, B.,, P. Launay,, Y. Kanamaru,, I. C. Moura,, S. Pfirsch,, C. Ruffie,, D. Henin,, M. Benhamou,, M. Pretolani,, U. Blank, and, R. C. Monteiro. 2005. Identification of FcαRI as an inhibitory receptor that controls inflammation: dual role of FcRγ ITAM. Immunity 22: 3142.
213. Perez, C.,, E. Coeffier,, F. Moreau-Gachelin,, J. Wietzerbin, and, P. D. Benech. 1994. Involvement of the transcription factor PU.1/Spi-1 in myeloid cell-restricted expression of an interferon-inducible gene encoding the human high-affinity Fc gamma receptor. Mol. Cell. Biol. 14: 50235031.
214. Perry, D. G.,, G. L. Daugherty, and, W. J. Martin. 1999. Clathrin-coated pit-associated proteins are required for alveolar macrophage phagocytosis. J. Immunol. 162: 380386.
215. Perussia, B.,, M. Kobayashi,, M. E. Rossi,, I. Anegon, and, G. Trinchieri. 1987. Immune interferon enhances functional properties of human granulocytes: role of Fc receptors and effect of lymphotoxin, tumor necrosis factor, and granulocyte-macrophage colony-stimulating factor. J. Immunol. 138: 765774.
216. Perussia, B.,, G. Trinchieri,, A. Jackson,, N. L. Warner,, J. Faust,, H. Rumpold,, D. Kraft, and, L. L. Lanier. 1984. The Fc receptor for IgG on human natural killer cells: phenotypic, functional, and comparative studies with monoclonal antibodies. J. Immunol. 133: 180189.
217. Pfefferkorn, L. C.,, and G. R. Yeaman. 1994. Association of IgA-Fc receptors (FcαR) with FcεRI γ2 subunits in U937 cells: aggregation induces the tyrosine phosphorylation of γ2. J. Immunol. 153: 32283236.
218. Phillips, N. E.,, and D. C. Parker. 1983. Cross-linking of B lymphocyte Fc gamma receptors and membrane immunoglobulin inhibits anti-immunoglobulin-induced blastogenesis. J. Immunol. 132: 627632.
219. Pollard, T. D. 2007. Regulation of actin filament assembly by arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 36: 451477.
220. Pommier, C. G.,, S. Inada,, L. F. Fries,, T. Takahashi,, M. M. Frank, and, E. J. Brown. 1983. Plasma fibronectin enhances phagocytosis of opsonized particles by human peripheral blood monocytes. J. Exp. Med. 157: 18441854.
221. Poo, H.,, J. C. Krauss,, L. Mayo-Bond,, R. Todd, III, and, H. R. Petty. 1995. Interaction of Fc γ receptor type IIIB with complement receptor type 3 in fibroblast transfectants: evidence from lateral diffusion and resonance energy transfer studies. J. Mol. Biol. 247: 597603.
222. Qin, S.,, T. Inazu, and, H. Yamamura. 1995. Activation and tyrosine phosphorylation of p72 syk as well as calcium mobilization after hydrogen peroxide stimulation in peripheral blood lymphocytes. Biochem. J. 308: 347352.
223. Rabinovitch, M.,, S. I. Hamburg, and, H. B. Fleit. 1980. Interferon-induced enhancement of Fc receptor-mediated macrophage phagocytosis. J. Reticuloendothel. Soc. 28: 27s28s.
224. Regnault, A.,, D. Lankar,, V. Lacabanne,, A. Rodriguez,, C. Thery,, M. Rescigno,, T. Saito,, S. Verbeek,, C. Bonnerot,, P. Ricciardi-Castagnoli, and, S. Amigorena. 1999. Fcγ receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J. Exp. Med. 189: 371380.
225. Relman, D.,, T. E.,, S. Falkow,, D. T. Golenbock,, K. Saukkonen, and, S. D. Wright. 1990. Recognition of a bacterial adhesion by an integrin: macrophage CR3(α Mβ 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell 61: 13751382.
226. Reterink, T. J.,, E. W. Levarht,, M. N. Klar,, L. A. Van Es, and, M. R. Daha. 1996. Transforming growth factor-β1 (TGF-β1) down-regulates IgA Fc-receptor (CD89) expression on human monocytes. Clin. Exp. Immunol. 103: 161166.
227. Reth, M. 1989. Antigen receptor tail clue. Nature 338: 383384.
228. Rollag, H.,, M. Degre, and, G. Sonnenfeld. 1984. Effects of interferon-α/β and interferon-γ preparations on phagocytosis by mouse peritoneal macrophages. Scand. J. Immunol. 20: 149155.
229. Rosales, C.,, and E. J. Brown. 1991. Two mechanisms for IgG Fc-receptor-mediated phagocytosis by human neutrophils. J. Immunol. 146: 39373944.
230. Rose, D. M.,, B. W. Winston,, E. D. Chan,, D. W. H. Riches,, P. Gerwins,, G. L. Johnson, and, P. M. Henson. 1997. Fcγ receptor cross-linking activates p42, p38, and JNK/SAPK mitogen-activated protein kinases in murine macrophages: role for p42 MAPK in Fcγ receptor-stimulated TNF-α synthesis. J. Immunol. 158: 34333438.
231. Ross, G. D.,, J. A. Cain, and, P. J. Lachmann. 1985. Membrane complement receptor type three (CR 3) has lectin-like properties analogous to bovine conglutinin and functions as a receptor for zymosan and rabbit erythrocytes as well as a receptor for iC3b. J. Immunol. 134: 33073315.
232. Rossman, M. D.,, E. Chen,, P. Chien,, M. Rotten,, A. Cprek, and, A. D. Schreiber. 1989. Fcγ receptor recognition of IgG ligand by human monocytes and macrophages. Am. J. Respir. Cell Mol. Biol. 1: 211220.
233. Rowley, R. B.,, A. L. Burkhardt,, H. G. Chao,, G. R. Matsueda, and, J. B. Bolen. 1995. Syk protein-tyrosine kinase is regulated by tyrosine-phosphorylated Igα/Igβ immunoreceptor tyrosine activation motif binding and autophosphorylation. J. Biol. Chem. 270: 1159011594.
234. Ruppert, J.,, D. Friedrichs,, H. Xu, and, J. H. Peters. 1991. IL-4 decreases the expression of the monocyte differentiation marker CD14, paralleled by an increasing accessory potency. Immunobiology 182: 449464.
235. Salcedo, T. W.,, T. Kurosaki,, P. Kanakaraj,, J. V. Ravetch, and, B. Perussia. 1993. Physical and functional association of p56 lck with Fc γ RIIIA (CD16) in natural killer cells. J. Exp. Med. 177: 14751480.
236. Salmon, J. E.,, N. L. Brogle,, J. C. Edberg, and, R. P. Kimberly. 1991. Fc γ receptor III induces actin polymerization in human neutrophils and primes phagocytosis mediated by Fc γ receptor II. J. Immunol. 146: 9971004.
237. Salmon, J. E.,, J. C. Edberg, and, R. P. Kimberly. 1990. Fcγ receptor III on human neutrophils. Allelic variants have functionally distinct capacities. J. Clin. Invest. 85: 12871295.
238. Salmon, J. E.,, S. Kapur, and, R. P. Kimberly. 1987. Opsonin-independent ligation of Fcγ receptors. The 3G8-bearing receptors on neutrophils mediate the phagocytosis of concanavalin A-treated erythrocytes and nonopsonized Escherichia coli. J. Exp. Med. 166: 17981813.
239. Salmon, J. E.,, S. Millard,, L. A. Schachter,, F. C. Arnett,, E. M. Ginzler,, M. F. Gourley,, R. Ramsey Goldman,, M. G. Peterson, and, R. P. Kimberly. 1996. FcγRIIA alleles are heritable risk factors for lupus nephritis in African Americans. J. Clin. Invest. 97: 13481354.
240. Salmon, J. E.,, S. S. Millard,, N. L. Brogle, and, R. P. Kimberly. 1995. Fcγ receptor IIIb enhances Fcγ receptor IIa function in an oxidant-dependent and allele-sensitive manner. J. Clin. Invest. 95: 28772885.
241. Sampson, L. L.,, J. Heuser, and, E. J. Brown. 1991. Cytokine regulation of complement receptor-mediated ingestion by mouse peritoneal macrophages. M-CSF and IL-4 activate phagocytosis by a common mechanism requiring autostimulation by IFN-β. J. Immunol. 146: 10051013.
242. Samuelsson, A.,, T. L. Towers, and, J. V. Ravetch. 2001. Anti-inflammatory activity of IVIG mediated through the inhibitory Fc receptor. Science 291: 484486.
243. Sano, H.,, D. K. Hsu,, J. R. Apgar,, L. Yu,, B. B. Sharma,, I. Kuwabara,, S. Izui, and, F. T. Liu. 2003. Critical role of galectin-3 in phagocytosis by macrophages. J. Clin. Invest. 112: 389397.
244. Sarmay, G.,, I. Pecht, and, J. Gergely. 1994. Protein-tyrosine kinase activity tightly associated with human type II Fcγ receptors. Proc. Natl. Acad. Sci. USA 91: 41404144.
245. Sawyer, D. W.,, J. A. Sullivan, and, G. L. Mandell. 1985. Intracellular free calcium localization in neutrophils during phagocytosis. Science 230: 663666.
246. Schauer, U.,, F. Stemberg,, C. H. Rieger,, M. Borte,, S. Schubert,, F. Riedel,, U. Herz,, H. Renz,, M. Wick,, H. D. Carr-Smith,, A. R. Bradwell, and, W. Herzog. 2003. IgG subclass concentrations in certified reference material 470 and reference values for children and adults determined with the binding site reagents. Clin. Chem. 49: 19241929.
247. Schieven, G. L.,, J. M. Kirihara,, D. L. Burg,, R. L. Geahlen, and, J. A. Ledbetter. 1993. p72 syk tyrosine kinase is activated by oxidizing conditions that induce lymphocyte tyrosine phosphorylation and Ca 2+ signals. J. Biol. Chem. 268: 1668816692.
248. Schmidt, R. E.,, and J. E. Gessner. 2005. Fc receptors and their interaction with complement in autoimmunity. Immunol. Lett. 100: 5667.
249. Scholl, P. R.,, D. Ahern, and, R. S. Geha. 1992. Protein tyrosine phosphorylation induced via the IgG receptors FcγRI and FcγRII in the human monocytic cell line THP-1. J. Immunol. 149: 17511757.
250. Scott, C. C.,, W. Dobson,, R. J. Botelho,, N. Coady-Osberg,, P. Chavrier,, D. A. Knecht,, C. Heath,, P. Stahl, and, S. Grin-stein. 2005. Phosphatidylinositol-4,5-bisphosphate hydrolysis directs actin remodeling during phagocytosis. J. Cell Biol. 169: 139149.
251. Sears, D. W.,, N. Osman,, B. Tate,, I. F. McKenzie, and, P. M. Hogarth. 1990. Molecular cloning and expression of the mouse high affinity Fc receptor for IgG. J. Immunol. 144: 371378.
252. Sedlik, C.,, D. Orbach,, P. Veron,, E. Schweighoffer,, F. Colucci,, R. Gamberale,, A. Ioan-Facsinay,, S. Verbeek,, P. Ricciardi-Castagnoli,, C. Bonnerot,, V. L. Tybulewicz,, J. Di Santo, and, S. Amigorena. 2003. A critical role for Syk protein tyrosine kinase in Fc receptor-mediated antigen presentation and induction of dendritic cell maturation. J. Immunol. 170: 846852.