C3d binding to the myelin oligodendrocyte glycoprotein results in an exacerbated experimental autoimmune encephalomyelitis

Journal of Immunology

Volumn 178, Issue 5, 2007, Pages 3323-3331

  Jégou, Jean François ^a   Chan, Philippe ^a   Schouft, Marie Thérèse ^a   Griffiths, Mark R ^b   Neal, James W ^b   Gasque, Philippe ^b,c   Vaudry, Hubert ^a   Fontaine, Marc ^a  

^a UNIVERSITÉ DE ROUEN   (France)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSITÉ DE LA RÉUNION   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3D; MYELIN OLIGODENDROCYTE GLYCOPROTEIN;

ADAPTIVE IMMUNITY; ADOLESCENT; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; COMPLEMENT ACTIVATION; COMPLEMENT FIXATION; COMPLEMENT SYSTEM; CONTROLLED STUDY; DEMYELINATION; DISEASE EXACERBATION; DISEASE SEVERITY; FEMALE; GERMINAL CENTER; HUMORAL IMMUNITY; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL;

EID: 33847398000     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.5.3323     Document Type: Article

References (56)

1. Egg, R., M. Reindl, F. Deisenhammer, C. Linington, and T. Berger. 2001. Anti-MOG and anti-MBP antibody subclasses in multiple sclerosis. Mult. Scler. 1: 285-289.
2. Reindl, M., C. Linington, U. Brehm, R. Egg, E. Dilitz, F. Deisenhammer, W. Poewe, and T. Berger. 1999. Antibodies against the myelin oligodendrocyte glycoprotein and the myelin basic protein in multiple sclerosis and other neurological diseases: a comparative study. Brain 122: 2047-2056.
3. Compston, D. A., B. P. Morgan, A. K. Campbell, P. Wilkins, G. Cole, N. D. Thomas, and B. Jasani. 1989. Immunocytochemical localization of the terminal complement complex in multiple sclerosis. Neuropathol. Appl. Neurobiol. 15:307-316.
4. Linington, C., B. P. Morgan, N. J. Scolding, P. Wilkins, S. Piddlesden, and D. A. Compston. 1989. The role of complement in the pathogenesis of experimental allergic encephalomyelitis. Brain 112: 895-911.
5. Piddlesden, S. J., H. Lassmann, F. Zimprich, B. P. Morgan, and C. Linington. 1993. The demyelinating potential of antibodies to myelin oligodendrocyte glycoprotein is related to their ability to fix complement. Am. J. Pathol. 143: 555-564.
6. Vanguri, P., C. L. Koski, B. Silverman, and M. L. Shin. 1982. Complement activation by isolated myelin: activation of the classical pathway in the absence of myelin-specific antibodies. Proc. Natl. Acad. Sci. USA 79: 3290-3294.
7. Iglesias, A., J. Bauer, T. Litzenburger, A. Schubart, and C. Linington. 2001. T- and B-cell responses to myelin oligodendrocyte glycoprotein in experimental autoimmune encephalomyelitis and multiple sclerosis. Glia 36: 220-234.
8. Johns, T. G., and C. C. Bernard. 1997. Binding of complement component Clq to myelin oligodendrocyte glycoprotein: a novel mechanism for regulating CNS inflammation. Mol. Immunol. 34: 33-38.
9. Johns, T. G., and C. C. Bernard. 1999. The structure and function of myelin oligodendrocyte glycoprotein. J. Neurochem. 72: 1-9.
10. Piddlesden, S. J., M. K. Storch, M. Hibbs, A. M. Freeman, H. Lassmann, and B. P. Morgan. 1994. Soluble recombinant complement receptor 1 inhibits inflammation and demyelination in antibody-mediated demyelinating experimental allergic encephalomyelitis. J. Immunol. 152: 5477-5484.
11. Nataf, S., S. L. Carroll, R. A. Wetsel, A. J. Szalai, and S. R. Barnum. 2000. Attenuation of experimental autoimmune demyelination in complement-deficient mice. J. Immunol. 165: 5867-5873.
12. Boos, L., I. L. Campbell, R. Ames, R. A. Wetsel, and S. R. Barnum. 2004. Deletion of the complement anaphylatoxin C3a receptor attenuates, whereas ectopic expression of C3a in the brain exacerbates, experimental autoimmune encephalomyelitis. J. Immunol. 173: 4708-4714.
13. Rotshenker, S. 2003. Microglia and macrophage activation and the regulation of complement-receptor-3 (CR3/MAC-1)-mediated myelin phagocytosis in injury and disease. J. Mol. Neurosci. 21: 65-72.
14. Brink, B. P., R. Veerhuis, E. C. Breij, P. van der Valk, C. D. Dijkstra, and L. Bo. 2005. The pathology of multiple sclerosis is location-dependent: no significant complement activation is detected in purely cortical lesions. J. Neuropathol. Exp. Neurol. 64: 147-155.
15. Rickert, R. C. 2005. Regulation of B lymphocyte activation by complement C3 and the B cell coreceptor complex. Curr. Opin. Immunol. 17: 237-243.
16. Mitchell, J. A., T. D. Green, R. A. Bright, and T. M. Ross. 2003. Induction of heterosubtypic immunity to influenza A virus using a DNA vaccine expressing hemagglutinin-C3d fusion proteins. Vaccine 21: 902-914.
17. Villiers, M. B., C. L. Villiers, A. M. Laharie, and P. N. Marche. 1999. Amplification of the antibody response by C3b complexed to antigen through an ester link. J. Immunol. 162: 3647-3652.
18. Dempsey, P. W., M. E. Allison, S. Akkaraju, C. C. Goodnow, and D. T. Fearon. 1996. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 271: 348-350.
19. Carter, R. H., and D. T. Fearon. 1992. CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science 256: 105-107.
20. Tedder, T. F., L. J. Zhou, and P. Engel. 1994. The CD19/CD21 signal transduction complex of B lymphocytes. Immunol. Today 15: 437-442.
21. Fang, Y., C. Xu, Y. X. Fu, V. M. Holers, and H. Molina. 1998. Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a strong antigen-specific IgG response. J. Immunol. 160: 5273-5279.
22. Fischer, M. B., S. Goerg, L. Shen, A. P. Prodeus, C. C. Goodnow, G. Kelsoe, and M. C. Carroll. 1998. Dependence of germinal center B cells on expression of CD21/CD35 for survival. Science 280: 582-585.
23. Ahearn, J. M., M. B. Fischer, D. Croix, S. Goerg, M. Ma, J. Xia, X. Zhou, R. G. Howard, T. L. Rothstein, and M. C. Carroll. 1996. Disruption of the Cr2 locus results in a reduction in B-1a cells and in an impaired B cell response to T-dependent antigen. Immunity 4: 251-262.
24. Croix, D. A., J. M. Ahearn, A. M. Rosengard, S. Han, G. Kelsoe, M. Ma, and M. C. Carroll. 1996. Antibody response to a T-dependent antigen requires B cell expression of complement receptors. J. Exp. Med. 183: 1857-1864.
25. Kopf, M., B. Abel, A. Gallimore, M. Carroll, and M. F. Bachmann. 2002. Complement component C3 promotes T-cell priming and lung migration to control acute influenza virus infection. Nat. Med. 8: 373-378.
26. Mitsuyoshi, J. K., Y. Hu, and S. T. Test. 2005. Role of complement receptor type 2 and endogenous complement in the humoral immune response to conjugates of complement C3d and pneumococcal serotype 14 capsular polysaccharide. Infect. Immun. 73: 7311-7316.
27. Molina, H., V. M. Holers, B. Li, Y. Fung, S. Mariathasan, J. Goellner, J. Strauss-Schoenberger, R. W. Karr, and D. D. Chaplin. 1996. Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. Proc. Natl. Acad. Sci. USA 93: 3357-3361.
28. Ochsenbein, A. F., D. D. Pinschewer, B. Odermatt, M. C. Carroll, H. Hengartner, and R. M. Zinkernagel. 1999. Protective T cell-independent antiviral antibody responses are dependent on complement. J. Exp. Med. 190: 1165-1174.
29. Green, T. D., B. R. Newton, P. A. Rota, Y. Xu, H. L. Robinson, and T. M. Ross. 2001. C3d enhancement of neutralizing antibodies to measles hemagglutinin. Vaccine 20: 242-248.
30. Bower, J. F., T. D. Green, and T. M. Ross. 2004. DNA vaccines expressing soluble CD4-envelope proteins fused to C3d elicit cross-reactive neutralizing antibodies to HIV-1. Virology 328: 292-300.
31. Bower, J. F., X. Yang, J. Sodroski, and T. M. Ross. 2004. Elicitation of neutralizing antibodies with DNA vaccines expressing soluble stabilized human immunodeficiency virus type 1 envelope glycoprotein trimers conjugated to C3d. J. Virol. 78: 4710-4719.
32. Test, S. T., J. Mitsuyoshi, C. C. Connolly, and A. H. Lucas. 2001. Increased immunogenicity and induction of class switching by conjugation of complement C3d to pneumococcal serotype 14 capsular polysaccharide. Infect. Immun. 69: 3031-3040.
33. Domdey, H., K. Wiebauer, M. Kazmaier, V. Muller, K. Odink, and G. Fey. 1982. Characterization of the mRNA and cloned cDNA specifying the third component of mouse complement. Proc. Natl. Acad. Sci. USA 79: 7619-7623.
34. Linares, D., I. Echevarria, and P. Mana. 2004. Single-step purification and refolding of recombinant mouse and human myelin oligodendrocyte glycoprotein and induction of EAE in mice. Protein Expression Purif. 34: 249-256.
35. Linnington, C., M. Webb, and P. L. Woodhams. 1984. A novel myelin-associated glycoprotein defined by a mouse monoclonal antibody. J. Neuroimmunol. 6: 387-396.
36. Piddlesden, S., H. Lassmann, I. Laffafian, B. P. Morgan, and C. Linington. 1991. Antibody-mediated demyelination in experimental allergic encephalomyelitis is independent of complement membrane attack complex formation. Clin. Exp. Immunol. 83: 245-250.
37. -/- mice is rescued by adjuvants without improvement in germinal center development. J. Immunol. 165: 3119-3127.
38. Hietala, M. A., I. M. Jonsson, A. Tarkowski, S. Kleinau, and M. Pekna. 2002. Complement deficiency ameliorates collagen-induced arthritis in mice. J. Immunol. 169: 454-459.
39. Calida, D. M., C. Constantinescu, E. Purev, G. X. Zhang, E. S. Ventura, E. Lavi, and A. Rostami. 2001. Cutting edge: C3, a key component of complement activation, is not required for the development of myelin oligodendrocyte glycoprotein peptide-induced experimental autoimmune encephalomyelitis in mice. J. Immunol. 166: 723-726.
40. Lyons, J. A., M. San, M. P. Happ, and A. H. Cross. 1999. B cells are critical to induction of experimental allergic encephalomyelitis by protein but not by a short encephalitogenic peptide. Eur. J. Immunol. 29: 3432-3439.
41. Linton, S. M., and B. P. Morgan. 1999. Complement activation and inhibition in experimental models of arthritis. Mol. Immunol. 36: 905-914.
42. Stad, R. K., D. J. van Gijlswijk-Janssen, L. A. van Es, and M. R. Dana. 1994. Complement depletion abolishes IgA-mediated glomerular inflammation in rats. Exp. Nephrol. 2: 182-189.
43. Del Nagro, C. J., R. V. Kolla, and R. C. Rickert. 2005. A critical role for complement C3d and the B cell coreceptor (CD19/CD21) complex in the initiation of inflammatory arthritis. J. Immunol. 175: 5379-5389.
44. Jacquier-Sarlin, M. R., F. M. Gabert, M. B. Villiers, and M. G. Colomb. 1995. Modulation of antigen processing and presentation by covalently linked complement C3b fragment. Immunology 84: 164-170.
45. Lyons, J. A., M. J. Ramsbottom, and A. H. Cross. 2002. Critical role of antigen-specific antibody in experimental autoimmune encephalomyelitis induced by recombinant myelin oligodendrocyte glycoprotein. Eur. J. Immunol. 32: 1905-1913.
46. Oliver, A. R., G. M. Lyon, and N. H. Ruddle. 2003. Rat and human myelin oligodendrocyte glycoproteins induce experimental autoimmune encephalomyelitis by different mechanisms in C57BL/6 mice. J. Immunol. 171: 462-468.
47. Delarasse, C., P. Daubas, L. T. Mars, C. Vizler, T. Litzenburger, A. Iglesias, J. Bauer, B. Della Gaspera, A. Schubart, L. Decker, et al. 2003. Myelin/oligodendrocyte glycoprotein-deficient (MOG-deficient) mice reveal lack of immune tolerance to MOG in wild-type mice. J. Clin. Invest. 112: 544-553.
48. Marta, C. B., A. R. Oliver, R. A. Sweet, S. E. Pfeiffer, and N. H. Ruddle. 2005. Pathogenic myelin oligodendrocyte glycoprotein antibodies recognize glycosylated epitopes and perturb oligodendrocyte physiology. Proc. Natl. Acad. Sci. USA 102: 13992-13997.
49. Kroepfl, J. F., L. R. Viise, A. J. Charron, C. Linington, and M. V. Gardinier. 1996. Investigation of myelin/oligodendrocyte glycoprotein membrane topology. J. Neurochem. 67: 2219-2222.
50. t Hart, B. A., and Y. van Kooyk. 2004. Yin-Yang regulation of autoimmunity by DCs. Trends Immunol. 25: 353-359.
51. Brehm, U., S. J. Piddlesden, M. V. Gardinier, and C. Linington. 1999. Epitope specificity of demyelinating monoclonal autoantibodies directed against the human myelin oligodendrocyte glycoprotein (MOG). J. Neuroimmunol. 97: 9-15.
52. von Budingen, H. C., S. L. Hauser, A. Fuhrmann, C. B. Nabavi, J. I. Lee, and C. P. Genain. 2002. Molecular characterization of antibody specificities against myelin/oligodendrocyte glycoprotein in autoimmune demyelination. Proc. Natl. Acad. Sci. USA 99: 8207-8212.
53. Barrington, R. A., O. Pozdnyakova, M. R. Zafari, C. D. Benjamin, and M. C. Carroll. 2002. B lymphocyte memory: role of stromal cell complement and FCγRIIB receptors. J. Exp. Med. 196: 1189-1199.
54. Cherukuri, A., P. C. Cheng, and S. K. Pierce. 2001. The role of the CD19/CD21 complex in B cell processing and presentation of complement-tagged antigens. J. Immunol. 167: 163-172.
55. Hess, M. W., M. G. Schwendinger, E. L. Eskelinen, K. Pfaller, M. Pavelka, M. P. Dierich, and W. M. Prodinger. 2000. Tracing uptake of C3dg-conjugated antigen into B cells via complement receptor type 2 (CR2, CD21). Blood 95: 2617-2623.
56. Kozono, Y., R. Abe, H. Kozono, R. G. Kelly, T. Azuma, and V. M. Holers. 1998. Cross-linking CD21/CD35 or CD19 increases both B7-1 and B7-2 expression on murine splenic B cells. J. Immunol. 160: 1565-1572.