Tolerance is dependent on complement C3 fragment iC3b binding to antigen-presenting cells

Nature Medicine

Volumn 9, Issue 2, 2003, Pages 206-212

  Sohn, Jeong Hyeon ^a   Bora, Puran S ^a   Suk, Hye Jung ^a   Molina, Hector ^b   Kaplan, Henry J ^a   Bora, Nalini S ^a  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C3B RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 12; MONOCLONAL ANTIBODY; TRANSFORMING GROWTH FACTOR BETA2;

ANIMAL CELL; ANTERIOR EYE CHAMBER; ANTIGEN PRESENTING CELL; ARTICLE; COMPLEMENT ACTIVATION; COMPLEMENT FIXATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DELAYED HYPERSENSITIVITY; IMMUNOLOGICAL TOLERANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD; ANTIGENS, CD147; ANTIGENS, NEOPLASM; ANTIGENS, SURFACE; AVIAN PROTEINS; BLOOD PROTEINS; COMPLEMENT C3B; HYPERSENSITIVITY, DELAYED; IMMUNE TOLERANCE; INTERLEUKIN-10; INTERLEUKIN-12; MEMBRANE GLYCOPROTEINS; RATS; RATS, INBRED LEW; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2;

ANIMALIA;

EID: 0037324434     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm814     Document Type: Article

References (45)

1. Frank, M.M. & Fries, L.F. The role of complement in inflammation and phagocytosis. Immunol. Today 12, 322-326 (1991).
2. Thomlinson, S. Complement defense mechanisms. Curr. Opin. Immunol. 5, 83-89 (1993).
3. Carroll, M.C. The role of complement and complement receptors in induction and regulation of immunity. Annu. Rev. Immunol. 16, 545-568 (1998).
4. Nielsen, C.H., Fischer, E.M. & Leslie, R.G.Q. The role of complement in the acquired immune response. Immunology 100, 4-12 (2000).
5. Arvieux, J., Yssel, H. & Colomb, M.G. Antigen-bound C3b and C4b enhance antigen-presenting cell function in activation of human T-cell clones. Immunology 65, 229-235 (1988).
6. Dempsey, P.W., Allison, M.E.D., Akkaraju, S., Goodnow, C.C. & Fearon, D.T. C3d of complement as a molecular adjuvant: Bridging innate and acquired immunity. Science 271, 348-350 (1996).
7. Jacquier-Sarlin, M.R., Gabert, F.M., Villiers, M.-B. & Colomb, M.G. Modulation of antigen processing and presentation by covalently linked complement C3b fragment. Immunology 84, 164-170 (1995).
8. Streilein, J.W. Immunologic privilege of the eye. Springer Semin. Immunopathol. 21, 95-111 (1999).
9. Kaplan, H.J. & Streilein, J.W. Immune response to immunization via the anterior chamber of the eye. I. F1 lymphocyte-induced immune deviation. J. Immunol. 118, 809-814 (1977).
10. Kaplan, H.J. & Streilein, J.W. Immune response to immunization via the anterior chamber of the eye. II. F1 lymphocyte-induced immune deviation. J. Immunol. 120, 689-693 (1978).
11. Streilein, J.W. & Niederkorn, I.Y. Induction of anterior chamber-associated immune deviation requires an intact, functional spleen. J. Exp. Med. 153, 1058-1067 (1981).
12. Wilbanks, G.A. & Streilein, J.W. Macrophages capable of inducing anterior chamber associated immune deviation demonstrate spleen-seeking migratory properties. Reg. Immunol. 4, 130-137 (1992).
13. Wilbanks, G.A. & Streilein J.W. Characterization of suppressor cells in anterior chamber-associated immune deviation (ACAID) induced by soluble antigen. Evidence of two functionally and phenotypically distinct T-suppressor cell populations. Immunology 71, 383-389 (1990).
14. Sonoda, K.-H., Exley, M., Snapper, S., Balk, S.P. & Stein-Streilein, J. CD1-reactive natural killer T cells are required for development of systemic tolerance through an immune-privileged site. J. Exp. Med. 190, 1215-1225 (1999).
15. Wilbanks, G.A., Mammolenti, M. & Streilein, J.W. Studies on the induction of anterior chamber-associated immune deviation (ACAID). III. Induction of ACAID depends upon intraocular transforming growth factor-β. Eur. J. Immunol. 22, 165-173 (1992).
16. D'orazio, T.J. & Niederkorn, J.Y. Splenic B cells are required for tolerogenic antigen presentation in the induction of anterior chamber-associated immune deviation (ACAID). Immunology 95, 47-55 (1998).
17. Streilein, J.W. Immune privilege as the result of local tissue barriers and immunosuppressive microenvironments. Curr. Opin. Immunol. 5, 428-432 (1993).
18. Hara, Y., Okamoto, S., Rouse, B. & Streilein, J.W. Evidence that peritoneal exudates cells cultured with eye-derived fluids are the proximate antigen-presenting cells in immune deviation of the ocular type. J. Immunol. 151, 5162-5170 (1993).
19. Sohn, J.-H., Kaplan, H.J., Suk, H.-J., Bora, P.S. & Bora, N.S. Chronic low level complement activation within the eye is controlled by intraocular complement regulatory proteins. Invest. Ophthalmol. Vis. Sci. 41, 3492-3502 (2000).
20. Kabat, E.A. & Mayer, M.M. in Experimental Immunohistochemistry (ed. Thomas, C.C.) 133-239 (Springfield, IL, 1961).
21. Diamond, M.S., Garcia-Aguilar, J., Bickford, I.K., Corbi, A.L. & Springer, T.A. The I domain is a major recognition site on the leukocyte integrin Mac-1 (CD11b/CD18) for four distinct adhesion ligands. J. Cell Biol. 120, 1031-1043 (1993).
22. Foris, G., Fust, G. & Medgyesi, G.A. The effect of oligopeptides on the C3b receptor-mediated functions of rat macrophages. Immunol. Lett. 6, 7-11 (1983).
23. Simpson, A.E.C.M., Tomkins, P.T. & Cooper, K.L. An investigation of the temporal induction of cytokine mRNAs in LPS-challenged thioglycollate-elicited murine peritoneal macrophages using the reverse transcription polymerase chain reaction. Inflamm. Res. 46, 65-71 (1997).
24. Fritzinger, D.C., Bredehorst, R. & Vogel, C.W. Molecular cloning and derived primary structure of cobra venom factor. Proc. Natl. Acad. Sci. USA 91, 12775-12779 (1994).
25. Wessels, M.R. et al. Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc. Natl. Acad. Sci. USA 92, 11490-11494 (1995).
26. Robinson, A.P., White, T.M. & Mason, D.W. Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. Immunology 57, 239-247 (1986).
27. Ross, G.D. & Lambris, J.D. Identification of a C3bi-specific membrane complement receptor that is expressed on lymphocytes, monocytes, neutrophils, and erythrocytes. J. Exp. Med. 155, 96-110 (1982).
28. Ross, G.D. & Vetvicka, V. CR3 (CD11b, CD18): A phagocyte and NK cell membrane receptor with multiple ligand specificities and functions. Clin. Exp. Immunol. 92, 181-184 (1993).
29. Taylor, A.W., Streilein, J.W. & Cousins, S.W. Identification of α-melanocyte stimulating hormone as a potential immunosuppressive factor in aqueous humor. Curr. Eye Res. 11, 1199-1206 (1992).
30. Taylor, A.W., Streilein, J.W. & Cousins, S.W. Immunoreactive vasoactive intestinal peptide contributes to the immunosuppressive activity of normal aqueous humor. J. Immunol. 153, 1080-1086 (1994).
31. Cousins, S.W., McCabe, M.M., Danielpour, D. & Streilein, J.W. Identification of transforming growth factor-β as an immunosuppressive factor in aqueous humor. Invest. Ophthalmol. Vis. Sci. 32, 2201-2211 (1991).
32. Streilein, J.W. Unraveling immune privilege. Science 270, 1158-1159 (1995).
33. Griffith, T.S., Brunner, T., Fletcher, S.M., Green, D.R. & Ferguson, T.A. Fas ligand-induced apoptosis as a mechanism of immune privilege. Science 270, 1189-1192 (1995).
34. Hammerberg, C., Duraiswamy, N. & Cooper, K.D. Reversal of immunosuppression inducible through ultraviolet-exposed skin by in vivo anti-CD11b treatment. J. Immunol. 157, 5254-5262 (1996).
35. Hammerberg, C., Katiyar, S.K., Carroll, M.C. & Cooper, K.D. Activated complement component 3 (C3) is required for ultraviolet induction of immunosuppression and antigenic tolerance. J. Exp. Med. 187, 1133-1138 (1998).
36. Tsuji, R.F. et al. Requried early complement activation in contact sensitivity with generation of local C5-dependent chemotactic activity, and late T cell interferon γ. A possible initiating role of B cells. J. Exp. Med. 186, 1015-1026 (1997).
37. D'orazio, T.J. & Niederkorn, J.Y. A novel role for TGF-β and IL-10 in the induction of immune privilege. J. Immunol. 160, 2089-2098 (1998).
38. Karp, C.L. et al. Mechanism of suppression of cell-mediated immunity by measles virus. Science 273, 228-231 (1996).
39. Yoshida, Y. et al. Monocyte induction of IL-10 and down-regulation of IL-12 by iC3b deposited in ultraviolet-exposed human skin. J. Immunol. 161, 5873-5979 (1998).
40. Kosiewicz, M., Alard, P. & Streilein, J.W. Alteration in cytokine production following intraocular injection of soluble protein antigen: impairment in IFN-γ and induction of TGF-β and IL-4 production. J. Immunol. 161, 5382-5390 (1998).
41. Miller, A., Lider, O., Roberts, A.B., Sporn, M.B. & Weiner, H.L. Suppressor T cells generated by oral tolerization to myelin basic protein suppress both in vitro and in vivo immune responses by the release of transforming growth factor β after antigen-specific triggering. Proc. Natl. Acad. Sci. USA 89, 421-425 (1992).
42. Shankland, S.J. et al. Differential expression of transforming growth factor-β isoforms and receptors in experimental membranous nephropathy. Kidney Int. 50, 116-124 (1996).
43. Kalli, K.R., Ahearn, J.M. & Fearon, D.T. Interaction of iC3b with recombinant isotypic and chimeric forms of CR2. J. Immunol. 147, 590-594 (1991).
44. Ross, G. D. Analysis of the different types of leukocyte membrane complement receptors and their interaction with the complement system. J. Immunol. Methods 37, 197-211 (1980).
45. McQuillen, D.P. et al. Complement processing and immunoglobulin binding to Neisseria gonorrhoeae determined in vitro simulates in vivo effects. J. Infect. Dis. 179, 124-135 (1995).