Studies on the mechanism of phagocytosis. I. Requirements for circumferential attachment of particle-bound ligands to specific receptors on the macrophage plasma membrane

doi:10.1084/jem.142.5.1263

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Studies on the mechanism of phagocytosis. I. Requirements for circumferential attachment of particle-bound ligands to specific receptors on the macrophage plasma membrane

FM Griffin Jr, JA Griffin, JE Leider and SC Silverstein

These experiments were designed to evaluate the role of macrophage plasma membrane receptors for the third component of complement (C) and for the Fc portion of IgG in the ingestion phase of phagocytosis. Sheep erythrocyte (E) were coated with anti-E IgG [E(IgG)]; these E(IgG) were then attached to cultivated monolayers of mouse peritoneal macrophages under conditions which reversibly inhibit ingestion of E(IgG). The E(IgG)-macrophage complexes were further incubated under similar conditions with an antimacrophage IgG fraction which blocks Fc receptor- mediated ingestion but has no effect upon ingestion mediated by other phagocytic receptors. When these cultures were subsequently incubated under conditions optimal for particle ingestion, phagocytosis of the IgG-coated erythrocytes did not occur; the erythrocytes remained bound to the Fc receptors of the macrophage plasma membrane. To determine whether ligands must cover the entire surface of an attached particle to permit ingestion of that particle, C-coated E [E(IgM)C] were bound to the C receptors of thioglycollate-induced (activated) macrophages at 4 degrees C. E(IgM)C-macrophage complexes were then trypsinized at 4 degrees C, a procedure which resulted in cleavage of erythrocyte-bound C3b molecules to a form of C3 not recognized by the macrophage receptors for C3b. Under the conditions used, trypsin did not affect the attachment of E(IgM)C to the macrophage surface or the macrophage receptors for C3b. When these trypsin treated E(IgM)C-macrophage complexes were incubated at 37 degrees C, the bound E(IgM)C were not ingested; the erythrocytes remained attached to the macrophage plasma membrane via the macrophage's C receptors. These results indicate that attachment of a particle to specific receptors on the macrophage plasma membrane is not sufficient to trigger ingestion of that particle. Rather, ingestion requires the sequential, circumferential interaction of particle-bound ligands with specific plasma membrane receptors not involved in the initial attachment process.
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Finnemann, S. C., Rodriguez-Boulan, E. (1999). Macrophage and Retinal Pigment Epithelium Phagocytosis: Apoptotic Cells and Photoreceptors Compete for {alpha}v{beta}3 and {alpha}v{beta}5 Integrins, and Protein Kinase C Regulates {alpha}v{beta}5 Binding and Cytoskeletal Linkage. JEM 190: 861-874 [Abstract] [Full Text]
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Mukherjee, J., Kozel, T. R., Casadevall, A. (1998). Monoclonal Antibodies Reveal Additional Epitopes of Serotype D Cryptococcus neoformans Capsular Glucuronoxylomannan that Elicit Protective Antibodies. J. Immunol. 161: 3557-3568 [Abstract] [Full Text]
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Rittig, M. G., Schroppel, K., Seack, K.-H., Sander, U., N'Diaye, E.-N., Maridonneau-Parini, I., Solbach, W., Bogdan, C. (1998). Coiling Phagocytosis of Trypanosomatids and Fungal Cells. Infect. Immun. 66: 4331-4339 [Abstract] [Full Text]
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Reinagel, M. L., Gezen, M., Ferguson, P. J., Kuhn, S., Martin, E. N., Taylor, R. P. (1997). The Primate Erythrocyte Complement Receptor (CR1) as a Privileged Site: Binding of Immunoglobulin G to Erythrocyte CR1 Does Not Target Erythrocytes for Phagocytosis. Blood 89: 1068-1077 [Abstract] [Full Text]
Lennartz, M., Yuen, A., Masi, S., Russell, D., Buttle, K., Smith, J. (1997). Phospholipase A2 inhibition results in sequestration of plasma membrane into electronlucent vesicles during IgG-mediated phagocytosis. J. Cell Sci. 110: 2041-2052 [Abstract]
Jones, S. L., Brown, E. J. (1996). Fcgamma RII-mediated Adhesion and Phagocytosis Induce L-Plastin Phosphorylation in Human Neutrophils. J. Biol. Chem. 271: 14623-14630 [Abstract] [Full Text]
Zhu, Z., Bao, Z., Li, J. (1995). MacMARCKS Mutation Blocks Macrophage Phagocytosis of Zymosan. J. Biol. Chem. 270: 17652-17655 [Abstract] [Full Text]
Morisaki, J., Heuser, J., Sibley, L. (1995). Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J. Cell Sci. 108: 2457-2464 [Abstract]
Nagumo, M., Sakurada, S., Enomoto, S. (1982). Clinical Science: Membrane Receptors on Human Neutrophils in Oral Bacterial Infections. JDR 61: 962-966 [Abstract]
Di, A., Krupa, B., Nelson, D. J. (2001). Calcium-G Protein Interactions in the Regulation of Macrophage Secretion. J. Biol. Chem. 276: 37124-37132 [Abstract] [Full Text]
Patel, J. C., Hall, A., Caron, E. (2002). Vav Regulates Activation of Rac but Not Cdc42 during Fcgamma R-mediated Phagocytosis. Mol. Biol. Cell 13: 1215-1226 [Abstract] [Full Text]