The coordination of signaling during Fc receptor-mediated phagocytosis

Journal of Leukocyte Biology

Volumn 76, Issue 6, 2004, Pages 1093-1103

  Swanson, Joel A ^a   Hoppe, Adam D ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Actin; Cdc42; Macrophage; PI 3 kinase; Rac

Indexed keywords

ACTIN; CELL PROTEIN; FC RECEPTOR; IMMUNOGLOBULIN G; MYOSIN; PHOSPHATIDYLINOSITIDE; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANTIGEN BINDING; CELL MEMBRANE; COMPLEX FORMATION; ENZYME INACTIVATION; FLUORESCENCE MICROSCOPY; INTERNALIZATION; MACROPHAGE; MEMBRANE BINDING; MEMBRANE FUSION; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEIN PHOSPHORYLATION; RECEPTOR INTRINSIC ACTIVITY; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL MEMBRANE; DIFFUSION; ENZYME ACTIVATION; HUMANS; IMMUNOGLOBULIN G; MACROPHAGES; PHAGOCYTOSIS; PROTEIN TRANSPORT; RECEPTORS, FC; SIGNAL TRANSDUCTION;

EID: 10044234242     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0804439     Document Type: Review

References (117)

1. May, R. C., Machesky, L. M. (2001) Phagocytosis and the actin cytoskeleton. J. Cell Sci. 114, 1061-1077.
2. Araki, N., Hatae, T., Furukawa, A., Swanson, J. A. (2003) Phosphoinositide-3-kinase-independent contractile activities associated with Fcγ-receptor-mediated phagocytosis and macropinocytosis in macrophages. J. Cell Sci. 116, 247-257.
3. Henry, R.M., Hoppe, A.D., Joshi, N., Swanson, J. A. (2004) The uniformity of phagosome maturation in macrophages. J. Cell Biol. 164, 185-194.
4. Hoppe, A. D., Swanson, J. A. (2004) Cdc42, Rac1 and Rac2 display distinct patterns of activation during phagocytosis. Mol. Biol. Cell 15, 3509-3519.
5. Di, A., Nelson, D. J., Bindokas, V., Brown, M. E., Libunao, F., Palfrey, H. C. (2003) Dynamin regulates focal exocytosis in phagocytosing macrophages. Mol. Biol. Cell 14, 2016-2028.
6. Bajno, L., Peng, X-R., Schreiber, A. D., Moore, H-P., Trimble, W. S., Grinstein, S. (2000) Focal exocytosis of VAMP3-containing vesicles at sites of phagosome formation. J. Cell Biol. 149, 697-705.
7. Hackam, D. J., Rotstein, O. D., Sjolin, C., Schreiber, A. D., Trimble, W. S., Grinstein, S. (1998) v-SNARE-dependent secretion is required for phagocytosis. Proc. Natl. Acad. Sci. USA 95, 11691-11696.
8. Gagnon, E., Duclos, S., Rondeau, C., Chevet, E., Cameron, P. H., Steele-Mortimer, O., Paiement, J., Bergeron, J. J. M., Desjardins, M. (2002) Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110, 119-131.
9. Segal, A. W., Wientjes, F., Stockley, R. W., Dekker, L. V. (1999) Components and organization of the NADPH oxidase of phagocytic cells: its role in microbial killing and in the molecular pathology of chronic granulomatous disease. In Phagocytosis: The Host (S. Gordon, ed.), Stamford, CT, JAI, 441.
10. Diebold, B. A., Bokoch, G. M. (2001) Molecular basis for Rac2 regulation of phagocyte NADPH oxidase. Nat. Immunol. 2, 211-215.
11. Babior, B. M. (2000) Phagocytes and oxidative stress. Am. J. Med. 109, 33-44.
12. Greenberg, S. (1999) Modular components of phagocytosis. J. Leukoc. Biol. 66, 712-717.
13. Suzuki, T., Kono, H., Hirose, N., Okada, M., Yamamoto, T., Yamamoto, K., Honda, Z-i. (2000) Differential involvement of Src family kinases in Fcγ receptor-mediated phagocytosis. J. Immunol. 165, 473-482.
14. Crowley, M. T., Costello, P. S., Fitzer-Attas, C. J., Turner, M., Meng, F., Lowell, C., Tybulewicz, V. L. J., DeFranco, A. L. (1997) A critical role for Syk in signal transduction and phagocytosis mediated by Fcγ receptors on macrophages. J. Exp. Med. 186, 1027-1039.
15. Leverrier, Y., Okkenhaug, K., Sawyer, C., Bilancio, A., Vanhaesebroeck, B., Ridley, A. J. (2003) Class I phosphoinositide 3-kinase p110β is required for apoptotic cell and Fcγ receptor-mediated phagocytosis by macrophages. J. Biol. Chem. 278, 38437-38442.
16. Kant, A. M., De, P., Peng, X., Yi, T., Rawlings, D. J., Kim, J. S., Durden, D. L. (2002) SHP-1 regulates Fcγ receptor-mediated phagocytosis and the activation of RAC. Blood 100, 1852-1859.
17. Huang, Z-Y., Hunter, J., Kim, M-K., Indik, Z. K., Schreiber, A. D. (2003) The effect of phosphatases SHP-1 and SHIP-1 on signaling by the ITIM- and ITAM-contaiing Fcγ receptors FcγRIIB and FcγRIIA. J. Leukoc. Biol. 73, 823-829.
18. Gu, H., Botelho, R. J., Yu, M., Grinstein, S., Neel, B. G. (2003) Critical role for scaffolding adapter Gab2 in FcγR-mediated phagocytosis. J. Cell Biol. 161, 1151-1161.
19. Coppolino, M. G., Krause, M., Hagendorff, P., Monner, D. A., Trimple, W., Grinstein, S., Wehland, J., Sechi, A. S. (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, 4307-4318.
20. Izadi, K. D., Erdreich-Epstein, A., Liu, Y., Durden, D. L. (1998) Characterization of Cbl-Nck and Nck-Pak1 interactions in myeloid FcγRII signaling. Exp. Cell Res. 245, 330-342.
21. 2; CD11b/CD18). J. Exp. Med. 193, 61-71.
22. Booth, J. W., Kim, M-K., Jankowski, A., Schreiber, A. D., Grinstein, S. (2002) Contrasting requirements for ubiquitylation during Fc receptor-mediated endocytosis and phagocytosis. EMBO J. 21, 251-258.
23. Castellano, F., Chavrier, P., Caron, E. (2001) Actin dynamics during phagocytosis. Semin. Immunol. 13, 347-355.
24. Desjardins, M. (2003) ER-mediated phagocytosis: a new membrane for new functions. Nat. Rev. Immunol. 3, 280-291.
25. Chimini, G., Chavrier, P. (2000) Function of Rho family proteins in actin dynamics during phagocytosis and engulfment. Nat. Cell Biol. 2, E191-E196.
26. Bokoch, G. M., Diebold, B. A. (2002) Current molecular models for NADPH oxidase regulation by Rac GTPase. Blood 100, 2692-2696.
27. Caron, E., Hall, A. (1998) Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282, 1717-1721.
28. Cox, D., Chang, P., Zhang, Q., Reddy, P. G., Bokoch, G. M., Greenberg, S. (1997) Requirements for both Rac1 and Cdc42 in membrane ruffling and phagocytosis in leukocytes. J. Exp. Med. 186, 1487-1494.
29. Lorenzi, R., Brickell, P. M., Katz, D. R., Kinnon, C., Thrasher, A. J. (2000) Wiskott-Aldrich syndrome protein is necessary for efficient IgG-mediated phagocytosis. Blood 95, 2943-2946.
30. May, R. C., Caron, E., Hall, A., Machesky, L. M. (2000) Involvement of the Arp2/3 complex in phagocytosis mediated by FcγR and CR3. Nat. Cell Biol. 2, 246-248.
31. Diakonova, M., Bokoch, G., Swanson, J. A. (2002) Dynamics of cytoskeletal proteins during Fcγ receptor-mediated phagocytosis in macrophages. Mol. Biol. Cell 13, 402-411.
32. Defacque, H., Egeberg, M., Habermann, A., Diakonova, M., Roy, C., Mangeat, P., Voelter, W., Marriott, G., Pfannsteil, J., Faulstich, H., Griffiths, G. (2000) Involvement of ezrin/moesin in de novo actin assembly on phagosomal membranes. EMBO J. 19, 199-212.
33. Morrissette, N. S., Gold, E. S., Guo, J., Hamerman, J. A., Ozinsky, A., Bedian, V., Aderem, A. A. (1999) Isolation and characterization of monoclonal antibodies directed against novel components of macrophage phagosomes. J. Cell Sci. 112, 4705-4713.
34. Botelho, R. J., Teruel, M., Dierckman, R., Anderson, R., Wells, A., York, J. D., Meyer, T., Grinstein, S. (2000) Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151, 1353-1367.
35. Dharmawardhane, S., Brownson, D., Lennartz, M., Bokoch, G. M. (1999) Localization of p21-activated kinase 1 (PAK1) to pseudopodia, membrane ruffles, and phagocytic cups in activated human neutrophils. J. Leukoc. Biol. 66, 521-527.
36. Swanson, J. A., Johnson, M. T., Beningo, K., Post, P., Mooseker, M., Araki, N. (1999) A contractile activity that closes phagosomes in macrophages. J. Cell Sci. 112, 307-316.
37. Cox, D., Berg, J. S., Cammer, M., Chinegwundoh, J. O., Dale, B. M., Cheney, R. E., Greenberg, S. (2002) Myosin X is a downstream effector of PI(3)K during phagocytosis. Nat. Cell Biol. 4, 469-477.
38. Hackam, D. J., Rotstein, O. D., Schreiber, A., Zhang, W-J., Grinstein, S. (1997) Rho is required for the initiation of calcium signaling and phagocytosis by Fcγ receptors in macrophages. J. Exp. Med. 186, 955-966.
39. Gold, E. S., Underhill, D. M., Morrissette, N. S., Guo, J., McNiven, M. A., Aderem, A. (1999) Dynamin 2 is required for phagocytosis in macrophages. J. Exp. Med. 190, 1849-1856.
40. Gold, E. S., Morrissette, N. S., Underhill, D. M., Guo, J., Bassetti, M., Aderem, A. (2000) Amphiphysin IIm, a novel amphiphysin II isoform, is required for macrophage phagocytosis. Immunity 12, 285-292.
41. Zhang, Q., Cox, D., Tseng, C-C., Donaldson, J. G., Greenberg, S. (1998) A requirement for ARF6 in Fcγ receptor-mediated phagocytosis in macrophages. J. Biol. Chem. 273, 19977-19981.
42. Niedergang, F., Colucci-Guyon, E., Dubois, T., Raposo, G., Chavrier, P. (2003) ADP ribosylation factor 6 is activated and controls membrane delivery during phagocytosis in macrophages. J. Cell Biol. 161, 1143-1150.
43. Roberts, R. L., Barbieri, M. A., Ullrich, J., Stahl, P. D. (2000) Dynamics of rab5 activation in endocytosis and phagocytosis. J. Leukoc. Biol. 68, 627-632.
44. Duclos, S., Diez, R., Garin, J., Papadopoulou, B., Descoteaux, A., Stenmark, H., Desjardins, M. (2000) Rab5 regulates the kiss and run fusion between phagosomes and endosomes and the acquisition of phagosome leishmanicidal properties in RAW 264.7 macrophages. J. Cell Sci. 113, 3531-3541.
45. Cox, D., Lee, D. J., Dale, B. M., Calafat, J., Greenberg, S. (2000) A Rab11-containing rapidly recycling compartment in macrophages that promotes phagocytosis. Proc. Natl. Acad. Sci. USA 97, 680-685.
46. Lennartz, M. R. (1999) Phospholipases and phagocytosis: the role of phospholipid-derived second messengers in phagocytosis. Int. J. Biochem. Cell Biol. 31, 415-430.
47. phox cells, and the level of superoxide production is exchange factor-dependent. J. Biol. Chem. 277, 19220-19228.
48. Bokoch, G. M. (2003) Biology of the p21-activated kinases. Annu. Rev. Biochem. 72, 743-781.
49. Allen, L-A. H., Aderem, A. (1995) A role for MARCKS, the a isozyme of protein kinase C and myosin 1 in zymosan phagocytosis by macrophages. J. Exp. Med. 182, 829-840.
50. Larsen, E. C., Ueyama, T., Brannock, P. M., Shirai, Y., Saito, N., Larsson, C., Loegering, D., Weber, P. B., Lennartz, M. R. (2002) A role for PKC-ε in FcγR-mediated phagocytosis by RAW 264.7 cells. J. Cell Biol. 159, 939-944.
51. phox activity by site-specific phosphorylation: Akt-dependent activation of the NADPH oxidase. Proc. Natl. Acad. Sci. USA 100, 5130-5135.
52. Takai, Y., Sasaki, T., Matozaki, T. (2001) Small GTP-binding proteins. Physiol. Rev. 81, 153-208.
53. Patel, J. C., Hall, A., Caron, E. (2002) Vav regulates activation of Rac but not Cdc42 during FcγR-mediated phagocytosis. Mol. Biol. Cell 13, 1215-1226.
54. Hall, A. B., Gakidis, M. A. M., Gao, S., Wilsbacher, J. L., Swat, W., Brugge, J. S. (2003) Vav family proteins play a critical role in multiple macrophage functions. Mol. Biol. Cell 14, 212a.
55. Kitamura, Y., Shibagaki, K., Takata, K., Tsuchiya, D., Taniguchi, T., Gebicke-Haerter, P. J., Miki, H., Takenawa, T., Shimohama, S. (2003) Involvement of Wiskott-Aldrich syndrome protein family verprolin-homologous protein (WAVE) and Rac1 in the phagocytosis of amyloid-β(1-42) in rat microglia. J. Pharmacol. Sci. 92, 115-123.
56. Etienne-Manneville, S., Hall, A. (2002) Rho GTPases in cell biology. Nature 420, 629-635.
57. Bishop, A. L., Hall, A. (2000) Rho GTPases and their effector proteins. Biochem. J. 348, 241-255.
58. Castellano, F., Montcourrier, P., Guillemot, J. C., Gouin, E., Machesky, L., Cossart, P., Chavrier, P. (1999) Inducible recruitment of Cdc42 or WASP to a cell-surface receptor triggers actin polymerization and filopodium formation. Curr. Biol. 9, 351-360.
59. Castellano, F., Montcourrier, P., Chavrier, P. (2000) Membrane recruitment of Rac1 triggers phagocytosis. J. Cell Sci. 113, 2955-2961.
60. Diebold, B. A., Fowler, B., Lu, J., Dinauer, M. C., Bokoch, G. M. (2004) Antagonistic cross-talk between Rac and Cdc42 GTPases regulates generation of reactive oxygen species. J. Biol. Chem. 279, 28136-28142.
61. Dharmawardhane, S., Brownson, D., Lennartz, M., Bokoch, G. M. (1999) Localization of p21-activated kinase 1 (PAK1) to pseudopodia, membrane ruffles, and phagocytic cups in activated human neutrophils. J. Leukoc. Biol. 66, 521-527.
62. Diakonova, M., Bokoch, G., Swanson, J. A. (2002) Dynamics of cytoskeletal proteins during Fcγ receptor-mediated phagocytosis in macrophages. Mol. Biol. Cell 13, 402-411.
63. Ghosh, M., Song, X., Mouneimne, G., Sidani, M., Lawrence, D. S., Condeelis, J. S. (2004) Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304, 743-746.
64. Sanders, L. C., Matsumura, F., Bokoch, G. M., deLanerolle, P. (1999) Inhibition of myosin light chain kinase by p21-activated kinase. Science 283, 2083-2085.
65. DerMardirossian, C., Schnelzer, A., Bokoch, G. M. (2004) Phosphorylation of RhoGD1 by Pak1 mediates dissociation of Rac GTPase. Mol. Cell 15, 117-127.
66. Larsen, E. C., DiGennaro, J. A., Saito, N., Mehta, S., Loegering, D. J., Mazurkiewicz, J. E., Lennartz, M. R. (2000) Differential requirement for classic and novel PKC isoforms in respiratory burst and phagocytosis in RAW 264.7 cells. J. Immunol. 165, 2809-2817.
67. Araki, N., Johnson, M. T., Swanson, J. A. (1996) A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis in macrophages. J. Cell Biol. 135, 1249-1260.
68. 2 inhibition results in sequestration of plasma membrane into electronlucent vesicles during IgG-mediated phagocytosis. J. Cell Sci. 110, 2041-2052.
69. Kusner, D. J., Hall, C. F., Jackson, S. (1999) Fc γ receptor-mediated activation of phospholipase D regulates macrophage phagocylosis of IgG-opsonized particles. J. Immunol. 162, 2266-2274.
70. Cao, X., Wei, G., Fang, H., Guo, J., Weinstein, M., Marsh, C. B., Ostrowski, M. C., Tridandapani, S. (2004) The inositol 3-phosphatase PTEN negatively regulates Fc γ receptor signaling, but supports Toll-like receptor 4 signaling in murine peritoneal macrophages. J. Immunol. 172, 4851-4857.
71. Kim, J. S., Peng, X., De, P. K., Geahlen, R. L., Durden, D. L. (2002) PTEN controls immunoreceptor (immunoreceptor tyrosine-based activation motif) signaling and the activation of Rac. Blood 99, 694-697.
72. Cantrell, D. A. (2001) Phosphoinositide 3-kinase signalling pathways. J. Cell Sci. 114, 1439-1445.
73. Sechi, A. S., Wehland, J. (2000) The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P2 influences cytoskeletal protein activity at the plasma membrane. J. Cell Sci. 113, 3685-3695.
74. Canetti, C., Hu, B., Curtis, J. L., Peters-Golden, M. (2003) Syk activation is a leukotriene B4-regulated event involved in macrophage phagocytosis of IgG-coated targets but not apoptotic cells. Blood 102, 1877-1883.
75. Galbiati, F., Razani, B., Lisanti, M. P. (2001) Emerging themes in lipid rafts and caveolae. Cell 106, 403-411.
76. Kwiatkowska, K., Frey, J., Sobota, A. (2003) Phosphorylation of FcγRIIA is required for the receptor-induced actin rearrangement and capping: the role of membrane rafts. J. Cell Sci. 116, 537-550.
77. Kono, H., Suzuki, T., Yamamoto, K., Okada, M., Yamamoto, T., Honda, Z. (2002) Spatial raft coalescence represents an initial step in Fcγ R signaling. J. Immunol. 169, 193-203.
78. Abdel Shakor, A. B., Kwiatkowska, K., Sobota, A. (2004) Cell surface ceramide generation precedes and controls FcγRII clustering and phosphorylation in rafts. J. Biol. Chem. 279, 36778-36787.
79. Baumeister, M. A., Martinu, L., Rossman, K. L., Sondek, J., Lemmon, M. A., Chou, M. M. (2003) Loss of phosphatidylinositol 3-phosphate binding by the C-terminal Tiam-1 pleckstrin homology domain prevents in vivo Rac1 activation without affecting membrane targeting. J. Biol. Chem. 278, 11457-11464.
80. Venkateswarlu, K., Cullen, P. J. (2000) Signalling via ADP-ribosylation factor 6 lies downstream of phosphatidylinositide 3-kinase. Biochem. J. 345, 719-724.
81. Srinivasan, S., Wang, F., Glavas, S., Ott, A., Hofmann, F., Aktories, K., Kalman, D., Bourne, H. R. (2003) Rac and Cdc42 play distinct roles in regulating PI(3,4,5)P-3 and polarity during neutrophil chemotaxis. J. Cell Biol. 160, 375-385.
82. Maehama, T., Taylor, G. S., Dixon, J. E. (2001) PTEN and myotubularin: novel phosphoinositide phosphatases. Annu. Rev. Biochem. 70, 247-279.
83. Vieira, O. V., Botelho, R. J., Rameh, L., Brachmann, S. M., Matsuo, T., Davidson, H. W., Schreiber, A., Backer, J. M., Cantley, L. C., Grinstein, S. (2001) Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J. Cell Biol. 155, 19-25.
84. Fratti, R. A., Backer, J. M., Gruenberg, J., Corvera, S., Deretic, V. (2001) Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J. Cell Biol. 154, 631-644.
85. Gillooly, D. J., Simonsen, A., Stenmark, H. (2001) Phosphoinositides and phagocytosis. J. Cell Biol. 155, 15-17.
86. Kanai, F., Liu, H., Field, S. J., Akbary, H., Matsuo, T., Brown, G. E., Cantley, L. C., Yaffe, M. B. (2001) The PX domain of p47phox and p40phox bind to lipid products of PI(3)K. Nat. Cell Biol. 3, 675-678.
87. Cox, D., Tseng, C-C., Bjekic, G., Greenberg, S. (1999) A requirement for phosphatidylinositol 3-kinase in pseudopod extension. J. Biol. Chem. 274, 1240-1247.
88. 2+ levels. J. Cell Biol. 106, 657-666.
89. Myers, J. T., Swanson, J. A. (2002) Calcium spikes in activated macrophages during Fcγ receptor-mediated phagocytosis. J. Leukoc. Biol. 72, 677-684.
90. Iyer, S. S., Barton, J. A., Bourgoin, S., Kusner, D. J. (2004) Phospholipases D1 and D2 coordinately regulate macrophage phagocytosis. J. Immunol. 173, 2615-2623.
91. Marshall, J. G., Booth, J. W., Stambolic, V., Mak, T., Balla, T., Schreiber, A. D., Meyer, T., Grinstein, S. (2001) Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomain during Fcγ receptor-mediated phagocytosis. J. Cell Biol. 153, 1369-1380.
92. Ravetch, J. V., Clynes, R. A. (1998) Divergent roles for Fc receptors and complement in vivo. Annu. Rev. Immunol. 16, 421-432.
93. Ganesan, L. P., Fang, H., Marsh, C. B., Tridandipani, S. (2003) The protein-tyrosine phosphatase SHP-1 associates with the phosphorylated immunoreceptor tyrosine-based activation motif of FcγRIIa to modulate signaling events in myeloid cells. J. Biol. Chem. 278, 35710-35717.
94. Bottomley, M. J., Salim, K., Panayotou, G. (1998) Phospholipid-binding protein domains. Biochim. Biophys. Acta 1436, 165-183.
95. Clarke, J. H. (2003) Lipid signalling: picking out the PIPs. Curr. Biol. 13, R815-R817.
96. phox PX domains of NADPH oxidase target cell membranes via direct and indirect recruitment by phosphoinositides. J. Biol. Chem. 277, 4512-4518.
97. Kavran, J. M., Klein, D. E., Lee, A., Falasca, M., Isakoff, S. J., Skolnik, E. Y., Lemmon, M. A. (1998) Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains. J. Biol. Chem. 273, 30497-30508.
98. Wishart, M. J., Taylor, G. S., Dixon, J. E. (2001) Phoxy lipids: revealing PX domains as phosphoinositide-binding molecules. Cell 105, 817-820.
99. Bustelo, X. R. (2001) Vav proteins, adaptors and cell signaling. Oncogene 20, 6372-6381.
100. Han, J., Luby-Phelps, K., Das, B., Shu, X., Xia, Y., Mosteller, R. D., Krishna, U. M., Falck, J. R., White, M. A., Broek, D. (1998) Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav. Science 279, 558-560.
101. Desjardins, M., Huber, L. A., Parton, R. G., Griffiths, G. (1994) Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124, 677-688.
102. Vieira, O. V., Bucci, C., Harrison, R. E., Trimble, W. S., Lanzetti, L., Gruenberg, J., Schreiber, A. D., Stahl, P. D., Grinstein, S. (2003) Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase. Mol. Cell. Biol. 23, 2501-2514.
103. Rabinowitz, S., Horstmann, H., Gordon, S., Griffiths, G. (1992) Immunocytochemical characterization of the endocytic and phagosomal compartments in peritoneal macrophages. J. Cell Biol. 116, 95-112.
104. Allen, L-A. H., DeLeo, F., Gallois, A., Toyoshima, S., Suzuki, K., Nauseef, W. M. (1999) Transient association of the nicotinamide adenine dinucleotide phosphate oxidase subunits p47phox and p67phox with phagosomes in neutrophils from patients with X-linked chronic granulomatous disease. Blood 93, 3521-3530.
105. Teruel, M. N., Meyer, T. (2000) Translocation and reversible localization of signaling proteins: a dynamic future for signal transduction. Cell 103, 181-184.
106. Griffin, F. M., Silverstein, S. C. (1974) Segmental response of the macrophage plasma membrane to a phagocytic stimulus. J. Exp. Med. 139, 323-336.
107. Griffin, F. M., Griffin, J. A., Leider, J. E., Silverstein, S. C. (1975) Studies on the mechanism of phagocytosis. I. Requirements for circumferential attachment of particle-bound ligands to specific receptors on the macrophage plasma membrane. J. Exp. Med. 142, 1263-1282.
108. Koval, M., Preiter, K., Adles, C., Stahl, P. D., Steinberg, T. H. (1998) Size of IgG-opsonized particles determines macrophage response during internalization. Exp. Cell Res. 242, 265-273.
109. Ukkonen, P., Lewis, V., Marsh, M., Helenius, A., Mellman, I. (1986) Transport of macrophage Fc receptors and Fc receptor-bound ligands to lysosomes. J. Exp. Med. 163, 952-971.
110. Reynolds, A. R., Tischer, C., Verveer, P. J., Rocks, O., Bastiaens, P. I. (2003) EGFR activation coupled to inhibition of tyrosine phosphatases causes lateral signal propagation. Nat. Cell Biol. 5, 447-453.
111. Sawano, A., Takayama, S., Matsuda, M., Miyawaki, A. (2002) Lateral propagation of EGF signaling after local stimulation is dependent on receptor density. Dev. Cell 3, 245-257.
112. Beningo, K. A., Wang, Y-L. (2002) Fc-receptor-mediated phagocytosis is regulated by mechanical properties of the target. J. Cell Sci. 115, 849-856.
113. Greenberg, S. (1999) Fc receptor-mediated phagocytosis. In Phagocytosis: The Host (S. Gordon, ed.), Stamford, CT, JAI, 149-191.
114. Gresham, H. D., Dale, B. M., Potter, J. W., Chang, P. W., Vines, C. M., Lowell, C. A., Lagenaur, C. F., Willman, C. L. (2000) Negative regulation of phagocytosis in murine macrophages by the Src kinase family member, Fgr. J. Exp. Med. 191, 515-528.
115. Katso, R., Okkenhaug, K., Ahmadi, K., While, S., Timms, J., Waterfield, M. D. (2001) Cellular function of phosphoinositide 3-kinases: implications for development, immunity, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 17, 615-675.
116. Alvarez, B., Garrido, E., Garcia-Sanz, J. A., Carrera, A. C. (2003) Phosphoinositide 3-kinase activation regulates cell division time by coordinated control of cell mass and cell cycle progression rate. J. Biol. Chem. 278, 26466-26473.
117. Swanson, J. A., Watts, C. (1995) Macropinocytosis. Trends Cell Biol. 5, 424-428.