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. 1980 Oct;66(4):773–781. doi: 10.1172/JCI109915

Reversible and irreversible loss of Fc receptor function of human monocytes as a consequence of interaction with immunoglobulin G.

R J Kurlander
PMCID: PMC371652  PMID: 6968321

Abstract

The effects of IgG in different configurations on the Fc receptor function of human monocytes were studied. Receptor function was assessed by quantitating immune adherence and/or ingestion of human erythrocytes coated with IgG anti-D antibody. Monomeric IgGl in solution inhibited the Fc receptor function of monocytes, but this function was restored completely after washing. In contrast, monomeric IgG that was adsorbed nonspecifically to a plastic surface inhibited the Fc receptor function of monocytes even after washing away unbound IgGl. This loss of function could be blocked by sodium azide and was reversed when the IgG adsorbed to plastic was degraded by trypsin, suggesting that loss of function was the reversible consequence of localized binding of most of the monocyte's receptors at the point of contact with immobilized IgGl. Fluid-phase aggregates of IgGl also reduced the Fc receptor function of monocytes as a consequence of direct binding to the monocyte surface. High concentrations of purified aggregates rapidly reduced Fc receptor function but function was reversed by trypsin even after incubation for 18 h. Lower concentrations of aggregates reduced Fc receptor function more slowly, but after 18 h of incubation, lost function was not restored by trypsin treatment. Because the transition from reversible to irreversible loss was blocked by sodium azide, an energy-dependent process of ingestion, shedding or denaturation of receptors is responsible for this irreversible loss of Fc receptor function. Rabbit IgG anti-human IgG bound to IgG adsorbed to the surface of monocytes also mediated a loss of Fc receptor function as a result of the binding of Fc receptors to the Fc portion of the rabbit IgG molecule, a process analogous to the binding of aggregated IgG. After irreversible depletion of Fc receptor function by anti-IgG, partial recovery of function was detectable within 12-24 h of incubation in vitro, and this recovery was blocked by cycloheximide, suggesting that new receptor synthesis was required for restoration of function.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abramson N., Gelfand E. W., Jandl J. H., Rosen F. S. The interaction between human monocytes and red cells. Specificity for IgG subclasses and IgG fragments. J Exp Med. 1970 Dec 1;132(6):1207–1215. doi: 10.1084/jem.132.6.1207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson C. L., Grey H. M. Receptors for aggregated IgG on mouse lymphocytes: their presence on thymocytes, thymus-derived, and bone marrow-derived lymphocytes. J Exp Med. 1974 May 1;139(5):1175–1188. doi: 10.1084/jem.139.5.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968;97:77–89. [PubMed] [Google Scholar]
  4. Cooper S. M. Fc-receptor dysfunction in lupus. N Engl J Med. 1979 Jun 28;300(26):1486–1486. doi: 10.1056/NEJM197906283002611. [DOI] [PubMed] [Google Scholar]
  5. Davey M. J., Asherson G. L. Cytophilic antibody. I. Nature of the macrophage receptor. Immunology. 1967 Jan;12(1):13–20. [PMC free article] [PubMed] [Google Scholar]
  6. Dickler H. B., Kunkel H. G. Interaction of aggregated -globulin with B lymphocytes. J Exp Med. 1972 Jul 1;136(1):191–196. doi: 10.1084/jem.136.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dixon R., Rosse W., Ebbert L. Quantitative determination of antibody in idiopathic thrombocytopenic purpura. Correlation of serum and platelet-bound antibody with clinical response. N Engl J Med. 1975 Jan 30;292(5):230–236. doi: 10.1056/NEJM197501302920503. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Frank M. M., Hamburger M. I., Lawley T. J., Kimberly R. P., Plotz P. H. Defective reticuloendothelial system Fc-receptor function in systemic lupus erythematosus. N Engl J Med. 1979 Mar 8;300(10):518–523. doi: 10.1056/NEJM197903083001002. [DOI] [PubMed] [Google Scholar]
  10. Henson P. M. The adherence of leucocytes and platelets induced by fixed IgG antibody or complement. Immunology. 1969 Jan;16(1):107–121. [PMC free article] [PubMed] [Google Scholar]
  11. Huber H., Douglas S. D., Fudenberg H. H. The IgG receptor: an immunological marker for the characterization of mononuclear cells. Immunology. 1969 Jul;17(1):7–21. [PMC free article] [PubMed] [Google Scholar]
  12. Johnson W. D., Jr, Mei B., Cohn Z. A. The separation, long-term cultivation, and maturation of the human monocyte. J Exp Med. 1977 Dec 1;146(6):1613–1626. doi: 10.1084/jem.146.6.1613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kaplan J., Nielsen M. L. Analysis of macrophage surface receptors. II. Internalization of alpha-macroglobulin . trypsin complexes by rabbit alveolar macrophages. J Biol Chem. 1979 Aug 10;254(15):7329–7335. [PubMed] [Google Scholar]
  14. Knutson D. W., Kijlstra A., Van Es L. A. Association and dissociation of aggregated IgG from rat peritoneal macrophages. J Exp Med. 1977 May 1;145(5):1368–1381. doi: 10.1084/jem.145.5.1368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kurlander R. J., Rosse W. F., Logue G. L. Quantitative influence of antibody and complement coating of red cells on monocyte-mediated cell lysis. J Clin Invest. 1978 May;61(5):1309–1319. doi: 10.1172/JCI109048. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. LoBuglio A. F., Cotran R. S., Jandl J. H. Red cells coated with immunoglobulin G: binding and sphering by mononuclear cells in man. Science. 1967 Dec 22;158(3808):1582–1585. doi: 10.1126/science.158.3808.1582. [DOI] [PubMed] [Google Scholar]
  17. Lockwood C. M., Worlledge S., Nicholas A., Cotton C., Peters D. K. Reversal of impaired splenic function in patients with nephritis or vasculitis (or both) by plasma exchange. N Engl J Med. 1979 Mar 8;300(10):524–530. doi: 10.1056/NEJM197903083001003. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Mollison P. L., Hughes-Jones N. C. Clearance of Rh-positive red cells by low concentrations of Rh antibody. Immunology. 1967 Jan;12(1):63–73. [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Rosse W. F., Logue G. L., Adams J., Crookston J. H. Mechanisms of immune lysis of the red cells in hereditary erythroblastic multinuclearity with a positive acidified serum test and paroxysmal nocturnal hemoglobinuria. J Clin Invest. 1974 Jan;53(1):31–43. doi: 10.1172/JCI107551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schmidt M. E., Douglas S. D. Disappearance and recovery of human monocyte IgG receptor activity after phagocytosis. J Immunol. 1972 Oct;109(4):914–917. [PubMed] [Google Scholar]
  24. Schreiber A. D., Frank M. M. Role of antibody and complement in the immune clearance and destruction of erythrocytes. I. In vivo effects of IgG and IgM complement-fixing sites. J Clin Invest. 1972 Mar;51(3):575–582. doi: 10.1172/JCI106846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Segal D. M., Hurwitz E. Binding of affinity cross-linked oligomers of IgG to cells bearing Fc receptors. J Immunol. 1977 Apr;118(4):1338–1337. [PubMed] [Google Scholar]
  26. Slease R. B., Wistar R., Jr, Scher I. Surface immunoglobulin density on human peripheral blood mononuclear cells. Blood. 1979 Jul;54(1):72–87. [PubMed] [Google Scholar]
  27. Walker W. S. Separate Fc-receptors for immunoglogulins IgG2a and IgG2b on an established cell line of mouse macrophages. J Immunol. 1976 Apr;116(4):911–914. [PubMed] [Google Scholar]

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