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. 1981 Aug 1;154(2):291–305. doi: 10.1084/jem.154.2.291

Augmentation of macrophage complement receptor function in vitro. III. C3b receptors that promote phagocytosis migrate within the plane of the macrophage plasma membrane

PMCID: PMC2186406  PMID: 7264560

Abstract

We have previously reported that treatment with a unique lymphokine enables resident mouse peritoneal macrophages to phagocytize via their complement receptors and we have presented evidence that the lymphokine act by enabling complement receptor engagement by C3b ligands to generate a phagocytic signal, thereby linking the cell surface binding event with the intracellular phagocytic machinery. In the present experiments, we used immobilized immune complexes to study the topography of C3b receptors of resident mouse peritoneal macrophages treated with the lymphokine. Our results indicate that lymphokine treatment enables the macrophages' C3b receptors to migrate within the plane of the cells' plasma membrane and that manipulations of macrophages that abrogate one response to the lymphokine, complement receptor mobility, also abrogate the other response, complement receptor-mediated phagocytosis. These findings strongly suggest that lateral mobility of a ligand-bound receptor within the macrophage plasma membrane is an essential component of the phagocytic signal. Moreover, our results indicate that the difference in complement receptor function among various populations of macrophages is not due to the expression of different types of complement receptors by the different macrophage populations but rather to a difference in the relationship of the C3b receptor with other plasma membrane or intracellular components.

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Selected References

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  1. Ash J. F., Louvard D., Singer S. J. Antibody-induced linkages of plasma membrane proteins to intracellular actomyosin-containing filaments in cultured fibroblasts. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5584–5588. doi: 10.1073/pnas.74.12.5584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ash J. F., Singer S. J. Concanavalin-A-induced transmembrane linkage of concanavalin A surface receptors to intracellular myosin-containing filaments. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4575–4579. doi: 10.1073/pnas.73.12.4575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bianco C., Griffin F. M., Jr, Silverstein S. C. Studies of the macrophage complement receptor. Alteration of receptor function upon macrophage activation. J Exp Med. 1975 Jun 1;141(6):1278–1290. doi: 10.1084/jem.141.6.1278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Crossin K. L., Carney D. H. Evidence that microtubule depolymerization early in the cell cycle is sufficient to initiate DNA synthesis. Cell. 1981 Jan;23(1):61–71. doi: 10.1016/0092-8674(81)90270-1. [DOI] [PubMed] [Google Scholar]
  5. Douglas S. D. Human monocyte spreading in vitro--inducers and effects on Fc and C3 receptors. Cell Immunol. 1976 Feb;21(2):344–349. doi: 10.1016/0008-8749(76)90062-9. [DOI] [PubMed] [Google Scholar]
  6. Edelman G. M. Surface modulation in cell recognition and cell growth. Science. 1976 Apr 16;192(4236):218–226. doi: 10.1126/science.769162. [DOI] [PubMed] [Google Scholar]
  7. Ehlenberger A. G., Nussenzweig V. The role of membrane receptors for C3b and C3d in phagocytosis. J Exp Med. 1977 Feb 1;145(2):357–371. doi: 10.1084/jem.145.2.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Flanagan J., Koch G. L. Cross-linked surface Ig attaches to actin. Nature. 1978 May 25;273(5660):278–281. doi: 10.1038/273278a0. [DOI] [PubMed] [Google Scholar]
  9. Frye L. D., Edidin M. The rapid intermixing of cell surface antigens after formation of mouse-human heterokaryons. J Cell Sci. 1970 Sep;7(2):319–335. doi: 10.1242/jcs.7.2.319. [DOI] [PubMed] [Google Scholar]
  10. Griffin F. M., Jr, Bianco C., Silverstein S. C. Characterization of the macrophage receptro for complement and demonstration of its functional independence from the receptor for the Fc portion of immunoglobulin G. J Exp Med. 1975 Jun 1;141(6):1269–1277. doi: 10.1084/jem.141.6.1269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Griffin F. M., Jr Effects of soluble immune complexes on Fc receptor- and C3b receptor-mediated phagocytosis by macrophages. J Exp Med. 1980 Oct 1;152(4):905–919. doi: 10.1084/jem.152.4.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Griffin F. M., Jr, Griffin J. A. Augmentation of macrophage complement receptor function in vitro. II. Characterization of the effects of a unique lymphokine upon the phagocytic capabilities of macrophages. J Immunol. 1980 Aug;125(2):844–849. [PubMed] [Google Scholar]
  13. Griffin J. A., Griffin F. M., Jr Augmentation of macrophage complement receptor function in vitro. I. Characterization of the cellular interactions required for the generation of a T-lymphocyte product that enhances macrophage complement receptor function. J Exp Med. 1979 Sep 19;150(3):653–675. doi: 10.1084/jem.150.3.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Haigler H. T., McKanna J. A., Cohen S. Direct visualization of the binding and internalization of a ferritin conjugate of epidermal growth factor in human carcinoma cells A-431. J Cell Biol. 1979 May;81(2):382–395. doi: 10.1083/jcb.81.2.382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ishizaka K., Ishizaka T. Immune mechanisms of reversed type reaginic hypersensitivity. J Immunol. 1969 Sep;103(3):588–595. [PubMed] [Google Scholar]
  16. Johnston R. B., Jr, Lehmeyer J. E., Guthrie L. A. Generation of superoxide anion and chemiluminescence by human monocytes during phagocytosis and on contact with surface-bound immunoglobulin G. J Exp Med. 1976 Jun 1;143(6):1551–1556. doi: 10.1084/jem.143.6.1551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kaplan G., Eskeland T., Seljelid R. Difference in the effect of immobilized ligands on the Fc and C3 receptors of mouse peritoneal macrophages in vitro. Scand J Immunol. 1978;7(1):19–24. doi: 10.1111/j.1365-3083.1978.tb00422.x. [DOI] [PubMed] [Google Scholar]
  18. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  19. Mantovani B., Rabinovitch M., Nussenzweig V. Phagocytosis of immune complexes by macrophages. Different roles of the macrophage receptor sites for complement (C3) and for immunoglobulin (IgG). J Exp Med. 1972 Apr 1;135(4):780–792. doi: 10.1084/jem.135.4.780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Michl J., Pieczonka M. M., Unkeless J. C., Silverstein S. C. Effects of immobilized immune complexes on Fc- and complement-receptor function in resident and thioglycollate-elicited mouse peritoneal macrophages. J Exp Med. 1979 Sep 19;150(3):607–621. doi: 10.1084/jem.150.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Passwell J. H., Dayer J. M., Merler E. Increased prostaglandin production by human monocytes after membrane receptor activation. J Immunol. 1979 Jul;123(1):115–120. [PubMed] [Google Scholar]
  22. Rabinovitch M., Manejias R. E., Nussenzweig V. Selective phagocytic paralysis induced by immobilized immune complexes. J Exp Med. 1975 Oct 1;142(4):827–838. doi: 10.1084/jem.142.4.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ragsdale C. G., Arend W. P. Loss of Fc receptor activity after culture of human monocytes on surface-bound immune complexes. Mediation by cyclic nucleotides. J Exp Med. 1980 Jan 1;151(1):32–44. doi: 10.1084/jem.151.1.32. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ragsdale C. G., Arend W. P. Neutral protease secretion by human monocytes. Effect of surface-bound immune complexes. J Exp Med. 1979 Apr 1;149(4):954–968. doi: 10.1084/jem.149.4.954. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schiff P. B., Fant J., Horwitz S. B. Promotion of microtubule assembly in vitro by taxol. Nature. 1979 Feb 22;277(5698):665–667. doi: 10.1038/277665a0. [DOI] [PubMed] [Google Scholar]
  26. Schiff P. B., Horwitz S. B. Taxol stabilizes microtubules in mouse fibroblast cells. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1561–1565. doi: 10.1073/pnas.77.3.1561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schlessinger J., Elson E. L., Webb W. W., Yahara I., Rutishauser U., Edelman G. M. Receptor diffusion on cell surfaces modulated by locally bound concanavalin A. Proc Natl Acad Sci U S A. 1977 Mar;74(3):1110–1114. doi: 10.1073/pnas.74.3.1110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schlessinger J., Koppel D. E., Axelrod D., Jacobson K., Webb W. W., Elson E. L. Lateral transport on cell membranes: mobility of concanavalin A receptors on myoblasts. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2409–2413. doi: 10.1073/pnas.73.7.2409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schlessinger J., Shechter Y., Willingham M. C., Pastan I. Direct visualization of binding, aggregation, and internalization of insulin and epidermal growth factor on living fibroblastic cells. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2659–2663. doi: 10.1073/pnas.75.6.2659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schlessinger J., Webb W. W., Elson E. L., Metzger H. Lateral motion and valence of Fc receptors on rat peritoneal mast cells. Nature. 1976 Dec 9;264(5586):550–552. doi: 10.1038/264550a0. [DOI] [PubMed] [Google Scholar]
  31. Schramm M. Transfer of glucagon receptor from liver membranes to a foreign adenylate cyclase by a membrane fusion procedure. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1174–1178. doi: 10.1073/pnas.76.3.1174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shaw D. R., Griffin F. M., Jr Phagocytosis requires repeated triggering of macrophage phagocytic receptors during particle ingestion. Nature. 1981 Jan 29;289(5796):409–411. doi: 10.1038/289409a0. [DOI] [PubMed] [Google Scholar]
  33. Singer S. J., Nicolson G. L. The fluid mosaic model of the structure of cell membranes. Science. 1972 Feb 18;175(4023):720–731. doi: 10.1126/science.175.4023.720. [DOI] [PubMed] [Google Scholar]
  34. Stossel T. P., Hartwig J. H. Interactions of actin, myosin, and a new actin-binding protein of rabbit pulmonary macrophages. II. Role in cytoplasmic movement and phagocytosis. J Cell Biol. 1976 Mar;68(3):602–619. doi: 10.1083/jcb.68.3.602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Walter R. J., Berlin R. D., Pfeiffer J. R., Oliver J. M. Polarization of endocytosis and receptor topography on cultured macrophages. J Cell Biol. 1980 Jul;86(1):199–211. doi: 10.1083/jcb.86.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wilson L., Friedkin M. The biochemical events of mitosis. I. Synthesis and properties of colchicine labeled with tritium in its acetyl moiety. Biochemistry. 1966 Jul;5(7):2463–2468. doi: 10.1021/bi00871a042. [DOI] [PubMed] [Google Scholar]
  37. Wilson L. Microtubules as drug receptors: pharmacological properties of microtubule protein. Ann N Y Acad Sci. 1975 Jun 30;253:213–231. doi: 10.1111/j.1749-6632.1975.tb19201.x. [DOI] [PubMed] [Google Scholar]
  38. Yin H. L., Stossel T. P. Control of cytoplasmic actin gel-sol transformation by gelsolin, a calcium-dependent regulatory protein. Nature. 1979 Oct 18;281(5732):583–586. doi: 10.1038/281583a0. [DOI] [PubMed] [Google Scholar]

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