Evidence that exposure to fibrinogen or to antibodies directed against Mac-1 (CD11b/CD18; CR3) modulates human monocyte effector functions
F. E. Maly
Clinical Immunology, University of Berne, Berne, Switzerland
Institutes of Veterinary Virology, Switzerland
Search for more papers by this authorCorresponding Author
T. W. Jungi
Institutes of Veterinary Virology, Switzerland
Dr T. W. Jungi, Institute of Veterinary Virology, Langgass-Str. 122, CH-3012 Berne, Switzerland.Search for more papers by this authorF. E. Maly
Clinical Immunology, University of Berne, Berne, Switzerland
Institutes of Veterinary Virology, Switzerland
Search for more papers by this authorCorresponding Author
T. W. Jungi
Institutes of Veterinary Virology, Switzerland
Dr T. W. Jungi, Institute of Veterinary Virology, Langgass-Str. 122, CH-3012 Berne, Switzerland.Search for more papers by this authorThis work was supported by grants from the Swiss National Science Fund (T.W.J, and F.E.M.), from the Central Laboratory of the Swiss Red Cross Blood Transfusion Service (T.W.J.). and from the Arbeitsgemeinschaft für Osteosynthese (T.W.J.). The generous gift of monoclonal antibodies by Ortho Pharmaceutical, Raritan, N.J. (Dr P. Rao) and Dr K. Blaser. Swiss Institute of Asthma and Allergy Research, Davos, and the excellent technical assistance by Mrs M. BrčicA and H. Pfister is gratefully acknowledged.
Abstract
Summary. We have recently shown that the treatment of fibrinogen-coated monocytes (MO) with anti-fibrinogen as well as the exposure of MO to surface-bound fibrinogen (Fg) or to albumin haptenized with the Fg C-gamma-terminal pentadecapeptide, induces an oxidative burst. Using chemiluminescence (CL) for indicating an oxidative burst, and the ingestion of IgG-coated erythrocytes as a test of phagocytosis, we have now studied the impact of Fg on MO effector functions. MO that had been either pretreated with Fg and washed, or that were exposed to surface-adsorbed Fg, exhibited impaired Fc receptor-mediated phagocytosis. A similar impairment was observed when MO were pretreated with activating agents such as phorbol myristate acetate, n-formyl-methionyl-leucyl-phenylalanine (fMLP) or the calcium ionophore A23187. Moreover, following exposure to Fg or IgG, MO exhibited a reduced oxidative burst upon stimulation with a variety of agents. Similarly, MO pretreated or coincubated with anti-Mac-1 exhibited a reduced oxidative burst upon stimulation. Our results raise the possibility that inflammatory mononuclear phagocytes experience a functional modulation upon encountering fibrin by interacting with specific receptors for fibrin(ogen). This type of modulation is analogous to effects induced by the triggering of Fcγ receptors. MO showed a decreased oxidative burst when either pretreated or coincubated with anti-Mac-1 antibodies, whereas antibodies directed against other MO surface constitutents had no, or a weak effect only. This is compatible with the suggestion that Mac-1 acts as a fibrin(ogen) receptor.
REFERENCES
- Akiyama, Y., Griffith, R., Miller, P., Stevenson, G.W., Lund, S., Kanapa, D.J. & Stevenson, H.C. (1988) Effects of adherence, activation and distinct serum proteins on the in vitro human monocyte maturation process. Journal of Leukocyte Biology, 43, 224–231.
- Altieri, D.C., Morrissey, J.H. & Edgington, T.S. (1988a) Adhesive receptor Mac-1 coordinates the activation of factor X on stimulated cells of monocytic and myeloid differentiation: an alternative initiation of the coagulation protease cascade. Proceedings of the National Academy of Sciences of the United States of America, 85, 7462–7466.
- Alteri, D.C., Bader, R., Mannucci, P.M. & Edgington, T.S. (1988b) Oligospeciflcity of the cellular adhesion receptor Mac-1 encompasses an inducible recognition specificity for fibrinogen. Journal of Cell Biology, 107, 1893–1900.
- Asch, A.S., Barnwell, J., Silverstein, R.L. & Nachman, R.L. (1987) Isolation of the thrombospondin membrane receptor. Journal of Clinical Investigation, 79, 1054–1061.
- Barnwell, J.W., Ockenhouse, C.F. & Knowles, D.M. (1985) Monoclonal antibody OKM5 inhibits the in vitro binding of Plasmodium falciparum-infected erythrocytes to monocytes, endothelial cells, and C32 melanoma cells. Journal of Immnology, 135, 3494–3497.
- Bartolini, G., Orlandi, M., Chiricolo, M., Minghetti, L., Guerrini, F., Franceschi, C. & Tomasi, V. (1986) Regulation of thromboxane A2 biosynthesis in platelet-free human monocytes and the possible role of polypeptide growth factor(s) in the induction of cyclooxygenase system. Biochimica et Biophysica Acta, 876, 486–493.
- Beutler, B. & Cerami, A. (1986) Cachectin and tumor necrosis factor as two sides of the same biological coin. Nature, 320, 584.
- Bevilacqua, M.P., Pober, J.S., Wheeler, M.E., Cotran, R.S. & Gimbrone, M.A., Jr (1985) Interleukin-1 activation of vascular endothelium. Effects on procoagulant activity and leukocyte adhesion. American Journal of Pathology, 121, 394–403.
- Braquet, P. & Rola Pleszczynski, M. (1987) Platelet-activating factor and cellular immune responses. Immunology Today, 8, 345–351.
- Brestel, E.P. (1985) Co-oxidation by hypochlorite and hydrogen peroxide---implications for neutrophil chemiluminescence. Biophysical and Biochemical Research Communications, 126, 482–488.
- Brown, E.J., Bohnsack, J.F. & Gresham, H.D. (1988) Mechanism of inhibition of immunoglobulin G-mediated phagocytosis by monoclonal antibodies that recognize the Mac-1 antigen. Journal of Clinical Investigation, 81, 365–375.
- Camussi, G., Bussolino, F., Salvidio, G. & Baglioni, C. (1987) Tumor necrosis factor/cachectin stimulates peritoneal macrophages, polymorphonuclear neutrophils, and vascular endothelial cells to synthesize and release platelet, activating factor. Journal of Experimental Medicine, 166, 1390–1404.
- Colvin, R.B. & Dvorak, H.F. (1975) Fibrinogen/fibrin on the surface of macrophages: detection, distribution, binding requirements, and possible role in macrophage adherence phenomena. Journal of Experimental Medicine, 142, 1377–1390.
- Da Silva, R.P., Hall, B.F., Joiner, K.A. & Sacks, D.L. (1989) CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. Journal of Immunology, 143, 617–642.
- Dechatelet, L.R., Long, G.D., Shirley, P.S., Bass, D.A., Thomas, M.J., Henderson, F.W. & Cohen, M.S. (1982) Mechanism of the luminol-dependent chemiluminescence of human neutrophils. Journal of Immunology, 129, 1589–1593.
- Dougherty, S.H. (1988) Pathobiology of infection in prosthetic devices. Reviews of Infectious Diseases, 10, 1102–1117.
- Dougherty, G.J., Selvendran, Y., Murdoch, S., Palmer, D.G. & Hogg, N. (1987) The human mononuclear phagocyte high-affinity Fc receptor, FcRI, defined by a monoclonal antibody, 10.1. European Journal of Immunology, 17, 1453–1459.
- Edwards, R.L. & Rickles, F.R. (1984) Macrophage procoagulants. Progress in Hemostasis and Thrombosis, 7, 183–209.
- Gregory, S.A. & Edgington, T.S. (1985) Tissue factor induction in human monocytes. Two distinct mechanisms displayed by different alloantigen-responsive T cell clones. Journal of Clinical Investigation, 76, 2440–2445.
- Gustafson, E.J., Lukasiewicz, H., Wachtfogel, Y.T., Norton, K.J., Schmaier, A.H., Niewarowski, S. & Colman, R.W. (1989) High molecular weight kininogen inhibits fibrinogen binding to cytoadhesins of neutrophils and platelets. Journal of Cell Biology, 109, 377–387.
- Hopper, K.E., Geczy, C.L. & Davies, W.A. (1981) A mechanism of migration inhibition in delayed-type hypersensitivity reactions. I. Fibrin deposition on the surface of elicited peritoneal macrophages in vivo. Journal of Immunology, 126, 1052–1058.
- Hynes, R.O. (1990) Integrins: a family of cell surface receptors. Cell, 48, 549–554.
- Jack, R.M. & Fearon, D.T. (1984) Altered surface distribution of both C3b receptors and Fc receptors on neutrophils induced by anti-C3b receptor or aggregated IgG. Journal of Immunology, 132, 3028–3033.
- Johnston, R.B., Jr., Lehmeyer, J.E. & Guthrie, L.A. (1976) Generation of superoxide anion and chemiluminescence by human monocytes during phagocytosis and on contact with surface-bound immunoglobulin G. Journal of Experimental Medicine, 143, 1551–1556.
- Jungi, T.W. (1985) A rapid and sensitive method allowing photometric determination of erythrophagocytosis by mononuclear phagocytes. Journal of Immunological Methods, 82, 141–153.
- Jungi, T.W. & Barandun, S. (1985) Estimation of the degree of opsonisation of homologous erythrocytes by IgG for intravenous and intramuscular use. Vox Sanguinis, 49, 9–19.
- Jungi, T.W. & Hafner, S. (1986) Quantitative assessment of Fc receptor expression and function during in vitro differentiation of human monocytes to macrophages. Immunology, 58, 131–137.
- Jungi, T.W., Spycher, M.O., Nydegger, U.E. & Barandun, S. (1986) Platelet-leukocyte interaction: selective binding of thrombin-stimulated platelets to human monocytes, polymorphonuclear leukocytes and related cell lines. Blood, 67, 629–636.
- Jungi, T.W., von Below, G., Lerch, P.G. & Spaeth, P.J. (1987) Modulation of human monocyte Fc receptor function by surface-adsorbed IgG. Immunology, 60, 261–268.
- Jungi, T.W. & Peterhans, E. (1988) Change in the chemiluminescence reactivity pattern during in vitro differentiation of human monocytes to macrophages. Blut, 56, 213–220.
- Jungi, T.W., Kuhnert, P. & Nydegger, U.E. (1989a) Evidence for human monocyte activation by IgG for IV use. Proceedings of the 7th International Congress of Immunology, Berlin, 1989 (ed. by F. Melchers), p. 424. Springer, New York .
- Jungi, T.W., Rüegg, S.J. & Morell, A. (1989b) Interferon gamma-treated human macrophages display enhanced cytolysis and generation of reactive oxygen metabolites but reduced ingestion upon Fc receptor triggering. Human Immunology, 24, 77–93.
- Jungi, T.W., Peterhans, E., Pfister, H. & Fey, H. (1989c) The interaction of ruminant IgG with receptor type II for IgG on human phagocytes. Immunology, 66, 143–148.
- Krishnamurti, C., Wahl, L.M. & Alving, B.M. (1989) Stimulation of plasminogen activator inhibitor activity in human monocytes infected with dengue virus. American Journal of Tropical Medicine and Hygiene, 40, 102–107.
- Maly, F.E., Vittoz, M., Urwyler, A., Koshikawa, K. & De Weck, A.L. (1989) A dual microtiter plate (192 samples) luminometer employing computer-aided single-photon imaging applicable to cellular luminescence and luminescence immunoassay, Journal of Immunological Methods, 122, 91–96.
- McGregor, J.L., Catimel, B., Parmentier, S., Clezardin, P., Dechavanne, M. & Leung, L.L. (1989) Rapid purification and partial characterization of human platelet glycoprotein IIIb. Interaction with thrombospondin and its role in platelet aggregation. Journal of Biological Chemistry, 264, 501–506.
- Mosser, D.M. & Edelson, P.J. (1987) The third component of complement is responsible for the intracellular survival of Leishmania major. Nature, 327, 329–331.
- Nakagawara, A. & Nathan, C.F. (1983) A simple method of counting adherent cells: application to cultured human monocytes, macrophages and multinucleated giant cells. Journal of Immunological Methods, 56, 261–268.
- Nathan, C., Srimal, S., Farber, C., Sanchez, E., Kabbash, L., Asch, A., Gailit, J. & Wright, S.D. (1989) Cytokine-induced respiratory burst of human neutrophils: dependence on extracellular matrix proteins and CD11/CD18 integrins. Journal of Cell Biology, 109, 1341–1349.
- Nawroth, P.P. & Stern, D.M. (1985) Modulation of endothelial cell hemostatic properties by tumor necrosis factor. Journal of Experimental Medicine, 163, 740–745.
- Ockenhouse, C.F., Magowan, C. & Chulay, J.D. (1989) Activation of monocytes and platelets by monoclonal antibodies or malaria-infected erythrocytes binding to the CD36 surface receptor in vitro. Journal of Clinical Investigation, 84, 468–475.
- Oquendo, P., Hundt, E., Lawler, J. & Seed, B. (1989) CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell, 58, 95–101.
- Peterhans, E., Jungi, T.W. & Stacker, R. (1988) Autotoxicity and reactive oxygen in viral disease. Oxy-Radicals in Molecular Biology and Pathology (ed. by P. A. Cerutti, I. Fridovich and J. M. McCord), p. 543. Allan R. Liss, New York .
- Ross, G.D., Cain, J.A. & Lachmann, P.J. (1985) Membrane complement receptor type three (CR3) has lectin-like properties analogous to bovine conglutinin and functions as a receptor for zymosan and rabbit erythrocytes as well as a receptor for iC3b. Journal of Immunology, 134, 3307–3315.
- Schwartz, B.S. & Monroe, M.C. (1986) Human platelet aggregation is initiated by peripheral blood mononuclear cells exposed to bacterial lipopolysaccharide in vitro. Journal of Clinical Investigation, 78, 1136–1141.
- Segal, D.M., Dower, S.K. & Titus, J.A. (1983) The FcR-mediated endocytosis of model immune complexes by cells from the P338D1 mouse macrophage line. I. Internalization of small, nonaggregating oligomers of IgG. Journal of Immunology, 130, 130–137.
- Sitrin, R.G., Brubaker, P.G., Shellito, J.E. & Kaltreider, H.B. (1986) The distribution of procoagulant and plasminogen activator activities among density fractions of normal rabbit alveolar macrophages. American Review of Respiratory Diseases, 133, 468–472.
- Sugarman, B. & Young, E.J. (1984) Infections Associated with Prosthetic Devices. CRC Press, Boca Raton , Fla .
- Sung, S.S., Nelson, R.S. & Silverstein, S.C. (1985) Mouse peritoneal macrophages plated on mannan- and horseradish peroxidasecoated substrates lose the ability to phagocytose by their Fc receptors. Journal of Immunology, 134, 3712–3717.
- Takemura, R. & Werb, Z. (1984) Regulation of elastase and plasminogen activator secretion in resident and inflammatory macrophages by receptors for the Fc domain of immunoglobulin G. Journal of Experimental Medicine, 159, 152–166.
- Trezzini, C., Jungi, T.W., Kuhnert, P. & Peterhans, E. (1988) Fibrinogen association with human monocytes: evidence for constitutive expression of fibrinogen receptors and for involvement of Mac-1 (CD18, CR3) in the binding. Biophysical and Biochemical Research Communications, 156, 477–484.
- Trezzini, C., Jungi, T.W., Maly, F.E., Vittoz, M. & Peterhans, E. (1989) Low-affinity interaction of fibrinogen carboxy-gamma terminus with human monocytes induces an oxidative burst and modulates effector functions. Biophysical and Biochemical Research Communications, 165, 7–14.
- Trezzini, C., Jungi, T.W., Spycher, M.O., Maly, F.E. & Rao, P. (1990a) Human monocyte CD36 and CD16 are signaling molecules. Evidence from studies using antibody-induced chemiluminescence as a tool to probe signal transduction. Immunology, 71, 29–37.
- Trezzini, C., Scholch, L. & Jungi, T.W. (1990b) The triggering of fibrinogen receptors on mononuclear phagocytes of healthy subjects and of a thrombosthenia Glanzmann patient promotes the generation of reactive oxygen species. Blood Coagulation and Fibrinolysis, in press.
- Wasi, S., Burrowes, C.E., Hay, J.B. & Movat, H.Z. (1983) Plasminogen activator and thromboplastin activity from sheep alveolar macrophages. Thrombosis Research, 30, 27–45.
- Winder, N.C., Grünig, G., Hermann, M. & von Fellenberg, R. (1990) Fibrin/fibrinogen in lungs and respiratory secretions of horses with chronic pulmonary disease. American Journal of Veterinary Research, 51, 945–949.
- Wright, S.D., Weitz, J.I., Huang, A.J., Levin, S.M., Silverstein, S.C. & Loike, J.D. (1988) Complement receptor type three (CD11 b/CD18) of human polymorphonuclear leukocytes recognizes fibrinogen. Proceedings of the National Academy of Sciences of the United States of America, 85, 7734–7738.
- Wymann, M.P., von Tscharner, V., Deranleau, D.A. & Baggiolini, M. (1987) The onset of the respiratory burst in human neutrophils. Real-time studies of H2O2 formation reveal a rapid agonist-induced transduction process. Journal of Biological Chemistry, 262, 12048–12053.
- Yagawa, K., Kaku, M., Ichinose, Y., Aida, Y. & Tomoda, A. (1985) Fc receptor-mediated desensitization of superoxide (O2-) generation response of guinea-pig macrophages and polymorphonuclear leucocytes. Immunology, 55, 629–638.