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In vitro studies on the Fc-receptor function of mononuclear phagocytes in rheumatoid arthritis: Relation between the Fc-receptor blockade and the concanavalin A-binding capacity of autologous immunoglobulin G

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Abstract

The Fc-receptor (Fc-R) function of monocytes isolated from 19 control subjects and from 30 patients presenting with a rheumatoid arthritis (RA) was assessedin vitro by a classical rosette assay using IgG-coated sheep red blood cells. In RA patients, the percentage of monocytes forming rosettes was significantly lower than in controls (34.4±20.4 versus 67.4±4.5%;P<0.001). The blockade observed was reversed by a prior trypsin treatment of RA monocytes, the percentage of recovery being correlated with the IgG plasma levels. Besides, IgG purified from the serum of four RA patients bound a mean of 7.3, 5.2, 1.6, and 1.6 times more than normal IgG did onto concanavalin A (Con A), peanut agglutinin (PNA), phytohemagglutinin (PHA), and pokeweed mitogen (PWM), respectively. Although similar amounts of125I-labeled normal and RA IgG were bound to normal monocytes, RA IgG inhibited more efficiently than normal IgG the Fc-R function of normal monocytes, for all concentrations tested (10 to 100 µg/100 µl). A prior treatment of RA IgG by α-mannosidase, but not by β-galactosidase, significantly reduced their inhibitory properties. The incubation of monocytes withD-mannose or mannan reduced their capacity to form rosettes. The percentage of monocytes forming rosettes in the presence of both mannan and normal IgG was significantly lower than that measured in the presence of normal IgG only. On the contrary, the rosetting capacity of monocytes in the presence of both RA IgG and mannan was the same as that calculated in the presence of RA IgG only. The inhibitory effect of RA IgG was not related to their abnormal circular dichroism. Our data suggest that the greater ability of RA IgG to block the Fc-R function of monocytes probably depends on the presence of a greater number of accessible mannosyl residues on the glycosidic side chains located in the Fc domain of the molecules.

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References

  1. Lobuglio AF, Cotran RS, Jandl JH: Red cells with immunoglobulin G: binding and sphering by mononuclear cells in man. Science 158:1582–1584, 1967

    Google Scholar 

  2. Huber H, Douglas SD, Fudenberg HH: The IgG receptor: An immunological marker for the characterization of mononuclear cells. Immunology 17:7–20, 1969

    Google Scholar 

  3. Ciccimarra F, Rosen FS, Merler E: Localization of the IgG effector site for monocyte receptors. Proc Natl Acad Sci USA 72:2081–2083, 1975

    Google Scholar 

  4. Davey MJ, Asherton GL: Cytophilic antibody. I. Nature of the macrophage receptor. Immunology 12:13–20, 1967

    Google Scholar 

  5. Wilson JG, Fearon DT: Altered expression of complement receptors as a pathogenic factor in systemic lupus erythematosus. Arth Rheum 27:1321–1328, 1984

    Google Scholar 

  6. Snyderman R: Structure and function of monocytes and macrophages.In Arthritis and Allied Conditions, DJ McCarty (ed). Philadelphia, Lea & Febiger, 1985, pp 287–308

    Google Scholar 

  7. Sharon N: Surface carbohydrates and surface lectins are recognition determinants in phagocytosis. Immunology Today 5:143–147, 1984

    Google Scholar 

  8. Czop JK, Austen KF: Generation of leukotrienes by human monocytes upon stimulation of their β-glucan receptor during phagocytosis. Proc Natl Acad Sci USA 82:2751–2755, 1985

    Google Scholar 

  9. Sun-Sang JS, Nelson RS, Silverstein C: Mouse peritoneal macrophages plated on mannan- and horseradish peroxidase-coated substrates lose the ability to phagocytose by their Fc receptors. J Immunol 134:3712–3717, 1985

    Google Scholar 

  10. Kurlander RJ: Reversible and irreversible loss of Fc-receptor function of human monocytes as a consequence of interaction with immunoglobulin G. J Clin Invest 66:773–781, 1980

    Google Scholar 

  11. Norris DA, Morris RM, Sanderson RJ, Kohler PF: Isolation of functional subsets of human peripheral blood monocyte. J Immunol 123:166–172, 1979

    Google Scholar 

  12. Ragsdale CG, Arend WP: Neutral protease secretion by human monocytes. Effect of surface-bound immune complexes. J Exp Med 149:954–968, 1977

    Google Scholar 

  13. Hoch S, Schur P: Monocyte receptor function in patients with rheumatoid arthritis. Arth Rheum 24:1268–1277, 1981

    Google Scholar 

  14. Temple A, Loewi G: The effect of sera from patients with connective tissue diseases on red cell binding and phagocytosis by monocytes. Immunology 33:109–114, 1977

    Google Scholar 

  15. Cooperating Clinic Committee of American Rheumatism Association. Arth Rheum 8:302–310, 1976

    Google Scholar 

  16. Malaise MG, Hauwaert C, Franchimont P, Danneskiold-Samsöe B, Bach-Andersen R, Gross D, Gerber H, Gerschpacher H, Stocker H, Bolla K: Treatment of active rheumatoid arthritis with slow intravenous injections of thymopentin. A double-blind placebo-controlled randomised study. Lancet 1:832–836, 1985

    Google Scholar 

  17. Ritchie DM, Boyle JA, McInnes JM, Jasani MK, Dalakos IG, Griveson P, Buchanan W: Clinical studies with an articular index for the assessment of joint tenderness in patients with rheumatoid arthritis. Q J Med 37:393–406, 1968

    Google Scholar 

  18. Hoyoux C, Foidart JB, Rigo P, Mahieu P, Geubelle F: Effect of methylprednisolone on the Fc-receptor function of human reticuloendothelial system in vivo. Eur J Clin Invest 14:60–66, 1984

    Google Scholar 

  19. Malaise MG, Foidart JB, Hauwaert C, Mahieu PH, Franchimont P: In vivo studies on the mononuclear phagocyte system Fc receptor function in rheumatoid arthritis. Correlations with clinical and immunological variables. J Rheum 12:33–42, 1985

    Google Scholar 

  20. Snedecor GW: Queries. Biometrics 8:85–95, 1952

    Google Scholar 

  21. Dubois CH, Goffinet G, Foidart JB, Dechenne CA, Foidart JM, Mahieu PR: Evidence for a particular binding capacity of rat peritoneal macrophages to rat glomerular mesangial cells in vitro. Eur J Clin Invest 12:239–246, 1982

    Google Scholar 

  22. Sober HA, Peterson EA: Protein chromatography on ion exchanges cellulose. Fed Proc 17:1116–1123, 1958

    Google Scholar 

  23. Kinet JP, Bensinger WI, Bolland N, Saint-Remy M, Frankenne F, Hennen G, Mahieu PR: Ex vivo perfusion of plasma over protein A columns in human mammary adenocarcinoma. Role of the Fc-binding capacity of protein A in the side-effects and tumouricidal response. Eur J Clin Invest 16:43–49, 1986

    Google Scholar 

  24. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275, 1951

    Google Scholar 

  25. Scheidegger JJ: Une microméthode de l'immunoélectrophorèse. Int Arch Allergy Appl Immunol 7:103–110, 1955

    Google Scholar 

  26. Casali P, Bossus A, Carpentier NA, Lambert PH: Solid-phase enzyme immunoassay or radioimmunoassay for the detection of immune complexes based on their recognition by conglutinin: conglutinin binding test. Clin Exp Immunol 29:342–346, 1977

    Google Scholar 

  27. Laemmli UK: Cleavage of structural proteins during the assembly of the head of Bacteriophage T4. Nature 227:680–685, 1970

    Google Scholar 

  28. Mahieu PR, Winand RJ: Carbohydrate and amino-acid composition of human glomerular-basement-membrane fractions purified by affinity chromatography. Eur J Biochem 37:157–163, 1973

    Google Scholar 

  29. Yphantis DA: Equilibrium ultracentrifugation of dilute solutions. Biochemistry 3:297–305, 1965

    Google Scholar 

  30. Stanworth DR, Turner MW: Immunochemical analysis of immunoglobulins and their subunits.In Handbook of Experimental Immunology: Immunochemistry, Vol. 1, DM Weir (ed). Oxford, Blackwell Scientific, 1978, pp 1–102

    Google Scholar 

  31. McConahey PF, Dixon FJ: A method of trace iodination of proteins for immunological studies. Int Arch Allergy Appl Immunol 29:185–192, 1966

    Google Scholar 

  32. Warren L: Sialic acid in human semen and in the male genital tract. J Clin Invest 38:755–761, 1959

    Google Scholar 

  33. Koide N, Nose M, and Muramatsu T: Recognition of IgG by Fc receptor and complement: Effects of glycosidase digestion. Biochem Biophys Res Commun 75:838–844, 1977

    Google Scholar 

  34. Zubler RH, Lange G, Lambert PH, Miescher PA: Detection of immune complexes in unheated sera by a modified125I-C1q binding test. J Immunol 116:232–235, 1976

    Google Scholar 

  35. Zubler RH, Nydegger U, Perrin LH, Fehr K, McCormick J, Lambert PH, Miescher PA: Circulating and intraarticular immune complexes in patients with rheumatoid arthritis. Correlation of125I-C1q binding activity with clinical and biological features of the disease. J Clin Invest 57:1308–1319, 1976

    Google Scholar 

  36. Schreiber AD, Parsons J, McDermott P, Cooper RA: Effect of corticosteroids on the human monocyte IgG and complement receptor. J Clin Invest 56:1189–1197, 1975

    Google Scholar 

  37. Lipsky PE, Ziff M: The mechanism of action of gold and d-penicillamine in rheumatoid arthritis.In Advances in Inflammation Research, Vol. 3, Rheumatoid Arthritis, M Ziff, GP Velo, S Gorini (eds). New York, Raven Press, 1982, pp 219–235

    Google Scholar 

  38. Hoyoux P, Malaise MG, Foidart JB, Rigo P, Halleux R, Hauwaert C, Mahieu PR, Franchimont P: Effect of plasma separation by membranes on the Fc-receptor function in patients with severe rheumatoid arthritis. Proc Int Soc Art Organs 1:144–150, 1981

    Google Scholar 

  39. Lambert PH, Dixon FJ, Zubler RH: A WHO collaborative study for evaluation of 18 methods for detecting immune complexes in serum. J Lab Clin Immunol 1:1–15, 1978

    Google Scholar 

  40. Carter SD, Leslie RGQ, Reeves WG: Human monocyte binding of homologous monomer and complexed IgG. Immunology 46:793–800, 1982

    Google Scholar 

  41. Alexander MD, Andrews JA, Leslie RQG, Wood NJ: The binding of human and guinea-pig IgG subclasses to homologous macrophage and monocyte Fc receptors. Immunology 35:115–123, 1978

    Google Scholar 

  42. Parekh RB, Dwek RA, Sutton BJ, Fernandes DL, Leung A, Stanworth D, Rademacher TW, Mizuochi T, Taniguchi T, Matsuta K, Takeuchi F, Nagano Y, Miyamoto T, Kobata A: Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosilation pattern of total serum IgG. Nature 316:452–457, 1985

    Google Scholar 

  43. Ashman RF: Lymphocyte activation.In Fundamental Immunology, WE Paul (ed). New York, Raven Press, 1984, pp 267–300

    Google Scholar 

  44. Huber R, Deisenhofer J, Colman PM, Matsushima M: Crystallographic structure studies of an IgG molecule and an Fc fragment. Nature 264:415–420, 1976

    Google Scholar 

  45. Johnson PM, Watkins J, Scopes PM, Tracey BM: Differences in serum IgG structure in health and rheumatoid disease. Ann Rheum Dis 33:366–370, 1974

    Google Scholar 

  46. Nose M, Wigzell H: Biological significance of carbohydrate chains on monoclonal antibodies. Proc Natl Acad Sci USA 80:6632–6636, 1983

    Google Scholar 

  47. Shepherd VL, Campbel EJ, Senior RM, Stahl PD: Characterization of the mannose/fucose receptor on human mononuclear phagocytes. J Reticuloendothel Soc 32:423–431, 1982

    Google Scholar 

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Malaise, M.G., Franchimont, P., Houssier, C. et al. In vitro studies on the Fc-receptor function of mononuclear phagocytes in rheumatoid arthritis: Relation between the Fc-receptor blockade and the concanavalin A-binding capacity of autologous immunoglobulin G. J Clin Immunol 6, 442–456 (1986). https://doi.org/10.1007/BF00915250

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