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J Exp Med. Sep 1, 1976; 144(3): 788–809.
PMCID: PMC2190417

Studies on the mechanism of phagocytosis. II. The interaction of macrophages with anti-immunoglobulin IgG-coated bone marrow-derived lymphocytes

Abstract

We have examined the effect of the distribution of anti-immunoglobulin IgG molecules on the surface of bone marrow-derived lymphocytes upon the interaction of these cells with macrophages. Lymphocytes which were diffusely coated with antibodies to surface immunoglogulin were ingested by macrophages. Lymphocytes which had the same number of anti- immunoglobulin IgG molecules redistributed to one pole of the surface bound to the macrophages' Fc receptors but were not ingested. These results confirm our previous hypothesis that ingestion of an immunologically coated particle requires the sequential, circumferential binding of specific receptors on the plasma membrane of a phagocytic cell to immunologic ligands distributed over the entire particle surface. Macrophages which had bound capped lymphocytes by the macrophages' Fc receptors removed the immune complex caps from the lymphocyte surface without destroying the lymphocytes. These lymphocytes remained attached to the macrophage surface. The finding that macrophages can phagocytize immune complexes from the surface of a cell without destroying the cell to which these complexes are attached may be important in understanding the effects of antigens and antibodies on cells participating in a humoral immune response, in identifying the mechanisms by which chronic viral infections are established, and in defining the roles of blocking antibodies in tumor immunity.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Berken A, Benacerraf B. Properties of antibodies cytophilic for macrophages. J Exp Med. 1966 Jan 1;123(1):119–144. [PMC free article] [PubMed]
  • Huber H, Fudenberg HH. Receptor sites of human monocytes for IgG. Int Arch Allergy Appl Immunol. 1968;34(1):18–31. [PubMed]
  • Huber H, Polley MJ, Linscott WD, Fudenberg HH, Müller-Eberhard HJ. Human monocytes: distinct receptor sites for the third component of complement and for immunoglobulin G. Science. 1968 Dec 13;162(3859):1281–1283. [PubMed]
  • Lay WH, Nussenzweig V. Receptors for complement of leukocytes. J Exp Med. 1968 Nov 1;128(5):991–1009. [PMC free article] [PubMed]
  • Henson PM. The adherence of leucocytes and platelets induced by fixed IgG antibody or complement. Immunology. 1969 Jan;16(1):107–121. [PMC free article] [PubMed]
  • Messner RP, Jelinek J. Receptors for human gamma G globulin on human neutrophils. J Clin Invest. 1970 Dec;49(12):2165–2171. [PMC free article] [PubMed]
  • Phillips-Quagliata JM, Levine BB, Quagliata F, Uhr JW. Mechanisms underlying binding of immune complexes to macrophages. J Exp Med. 1971 Mar 1;133(3):589–601. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Arend WP, Mannik M. The macrophage receptor for IgG: number and affinity of binding sites. J Immunol. 1973 Jun;110(6):1455–1463. [PubMed]
  • Gigli I, Nelson RA., Jr Complement dependent immune phagocytosis. I. Requirements for C'1, C'4, C'2, C'3. Exp Cell Res. 1968 Jul;51(1):45–67. [PubMed]
  • Huber H, Douglas SD. Receptor sites on human monocytes for complement: binding of red cells sensitized by cold autoantibodies. Br J Haematol. 1970 Jul;19(1):19–26. [PubMed]
  • Logue GL, Rosse WF, Adams JP. Complement-dependent immune adherence measured with human granulocytes: changes in the antigenic nature of red cell-bound C3 produced by incubation in human serum. Clin Immunol Immunopathol. 1973 Apr;1(3):398–407. [PubMed]
  • Griffin FM, Jr, Bianco C, Silverstein SC. 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. [PMC free article] [PubMed]
  • Bianco C, Griffin FM, Jr, Silverstein SC. Studies of the macrophage complement receptor. Alteration of receptor function upon macrophage activation. J Exp Med. 1975 Jun 1;141(6):1278–1290. [PMC free article] [PubMed]
  • Ross GD, Polley MJ. Specificity of human lymphocyte complement receptors. J Exp Med. 1975 May 1;141(5):1163–1180. [PMC free article] [PubMed]
  • Griffin FM, Jr, Griffin JA, Leider JE, Silverstein SC. 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. 1975 Nov 1;142(5):1263–1282. [PMC free article] [PubMed]
  • COHN ZA, BENSON B. THE DIFFERENTIATION OF MONONUCLEAR PHAGOCYTES. MORPHOLOGY, CYTOCHEMISTRY, AND BIOCHEMISTRY. J Exp Med. 1965 Jan 1;121:153–170. [PMC free article] [PubMed]
  • Holland P, Holland NH, Cohn ZA. The selective inhibition of macrophage phagocytic receptors by anti-membrane antibodies. J Exp Med. 1972 Mar 1;135(3):458–475. [PMC free article] [PubMed]
  • Griffin FM, Jr, Silverstein SC. Segmental response of the macrophage plasma membrane to a phagocytic stimulus. J Exp Med. 1974 Feb 1;139(2):323–336. [PMC free article] [PubMed]
  • March SC, Parikh I, Cuatrecasas P. A simplified method for cyanogen bromide activation of agarose for affinity chromatography. Anal Biochem. 1974 Jul;60(1):149–152. [PubMed]
  • DULBECCO R, VOGT M. Plaque formation and isolation of pure lines with poliomyelitis viruses. J Exp Med. 1954 Feb;99(2):167–182. [PMC free article] [PubMed]
  • Avrameas S, Ternynck T. Peroxidase labelled antibody and Fab conjugates with enhanced intracellular penetration. Immunochemistry. 1971 Dec;8(12):1175–1179. [PubMed]
  • Graham RC, Jr, Karnovsky MJ. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. [PubMed]
  • Hirsch JG, Fedorko ME. Ultrastructure of human leukocytes after simultaneous fixation with glutaraldehyde and osmium tetroxide and "postfixation" in uranyl acetate. J Cell Biol. 1968 Sep;38(3):615–627. [PMC free article] [PubMed]
  • LUFT JH. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. [PMC free article] [PubMed]
  • LOWRY OH, ROSEBROUGH NJ, FARR AL, RANDALL RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed]
  • Takahashi T, Old LJ, McIntire KR, Boyse EA. Immunoglobulin and other surface antigens of cells of the immune system. J Exp Med. 1971 Oct 1;134(4):815–832. [PMC free article] [PubMed]
  • Rabinovitch M, Manejias RE, Nussenzweig V. Selective phagocytic paralysis induced by immobilized immune complexes. J Exp Med. 1975 Oct 1;142(4):827–838. [PMC free article] [PubMed]
  • Allison AC, Davies P, De Petris S. Role of contractile microfilaments in macrophage movement and endocytosis. Nat New Biol. 1971 Aug 4;232(31):153–155. [PubMed]
  • Allison AC, Davies P. Mechanisms of endocytosis and exocytosis. Symp Soc Exp Biol. 1974;(28):419–446. [PubMed]
  • Boxer LA, Hedley-Whyte ET, Stossel TP. Neutrophil action dysfunction and abnormal neutrophil behavior. N Engl J Med. 1974 Nov 21;291(21):1093–1099. [PubMed]
  • Pollard TD, Weihing RR. Actin and myosin and cell movement. CRC Crit Rev Biochem. 1974 Jan;2(1):1–65. [PubMed]
  • Stossel TP, Hartwig JH. Interactions between actin, myosin, and an actin-binding protein from rabbit alveolar macrophages. Alveolar macrophage myosin Mg-2+-adenosine triphosphatase requires a cofactor for activation by actin. J Biol Chem. 1975 Jul 25;250(14):5706–5712. [PubMed]
  • Stossel TP, Hartwig JH. 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. [PMC free article] [PubMed]
  • Boxer LA, Stossel TP. Interactions of actin, myosin, and an actin-binding protein of chronic myelogenous leukemia leukocytes. J Clin Invest. 1976 Apr;57(4):964–976. [PMC free article] [PubMed]
  • Reaven EP, Axline SG. Subplasmalemmal microfilaments and microtubules in resting and phagocytizing cultivated macrophages. J Cell Biol. 1973 Oct;59(1):12–27. [PMC free article] [PubMed]
  • Spudich JA, Lin S. Cytochalasin B, its interaction with actin and actomyosin from muscle (cell movement-microfilaments-rabbit striated muscle). Proc Natl Acad Sci U S A. 1972 Feb;69(2):442–446. [PMC free article] [PubMed]
  • Axline SG, Reaven EP. Inhibition of phagocytosis and plasma membrane mobility of the cultivated macrophage by cytochalasin B. Role of subplasmalemmal microfilaments. J Cell Biol. 1974 Sep;62(3):647–659. [PMC free article] [PubMed]
  • Rutishauser U, Sachs L. Receptor mobility and the mechanism of cell-cell binding induced by concanavalin A. Proc Natl Acad Sci U S A. 1974 Jun;71(6):2456–2460. [PMC free article] [PubMed]
  • Evans R, Cox H, Alexander P. Immunologically specific activation of macrophages armed with the specific macrophage arming factor (SMAF). Proc Soc Exp Biol Med. 1973 May;143(1):256–259. [PubMed]
  • Diener E, Paetkau VH. Antigen recognition: early surface-receptor phenomena induced by binding of a tritium-labeled antigen. Proc Natl Acad Sci U S A. 1972 Sep;69(9):2364–2368. [PMC free article] [PubMed]
  • Raff MC, Feldmann M, De Petris S. Monospecificity of bone marrow-derived lymphocytes. J Exp Med. 1973 Apr 1;137(4):1024–1030. [PMC free article] [PubMed]
  • DeLuca D, Miller A, Sercarz E. Antigen binding to lymphoid cells from unimmunized mice. IV. Shedding and reappearance of multiple antigen binding Ig receptors of T- and B-lymphocytes. Cell Immunol. 1975 Aug;18(2):286–303. [PubMed]
  • Nossal GJ, Layton JE. Antigen-induced aggregation and modulation of receptors on hapten-specific B lymphocytes. J Exp Med. 1976 Mar 1;143(3):511–528. [PMC free article] [PubMed]
  • Lausch RN, Rapp F. Tumor-specific antigens and reexpression of fetal antigens in mammalian cells. Prog Exp Tumor Res. 1974;19:45–58. [PubMed]
  • Old LJ, Stockert E, Boyse EA, Kim JH. Antigenic modulation. Loss of TL antigen from cells exposed to TL antibody. Study of the phenomenon in vitro. J Exp Med. 1968 Mar 1;127(3):523–539. [PMC free article] [PubMed]
  • Joseph BS, Oldstone MB. Immunologic injury in measles virus infection. II. Suppression of immune injury through antigenic modulation. J Exp Med. 1975 Oct 1;142(4):864–876. [PMC free article] [PubMed]
  • Lampert PW, Joseph BS, Oldstone MB. Antibody-induced capping of measles virus antigens on plasma membrane studied by electron microscopy. J Virol. 1975 May;15(5):1248–1255. [PMC free article] [PubMed]

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