The B cell receptor itself can activate complement to provide the complement receptor 1/2 ligand required to enhance B cell immune responses in vivo

Journal of Experimental Medicine

Volumn 198, Issue 4, 2003, Pages 591-602

  Rossbacher, Joerg ^a   Shlomchik, Mark J ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Box 208035 ^*  (United States)

Author keywords

C1q; CD19; CD35; Germinal center; IgM

Indexed keywords

B LYMPHOCYTE RECEPTOR; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C3B RECEPTOR; COMPLEMENT COMPONENT C3D RECEPTOR; COMPLEMENT RECEPTOR; HUMAN SERUM ALBUMIN; IMMUNOGLOBULIN; IMMUNOGLOBULIN M ANTIBODY; LIGAND;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DETECTION; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; COMPLEMENT ACTIVATION; COMPLEMENT DEPOSITION; COMPLEMENT FIXATION; CONTROLLED STUDY; GERMINAL CENTER; HUMORAL IMMUNITY; IMMUNE RESPONSE; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS; B-LYMPHOCYTES; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; GERMINAL CENTER; HUMANS; IMMUNIZATION; IMMUNOGLOBULIN M; LIGANDS; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, B-CELL; RECEPTORS, COMPLEMENT;

EID: 0042422053     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20022042     Document Type: Article

References (54)

1. Carter, R.H., M.O. Spycher, Y.C. Ng, R. Hoffman, and D.T. Fearon. 1988. Synergistic interaction between complement receptor type 2 and membrane IgM on B lymphocytes. J. Immunol. 141:457-463.
2. Eden, A., G.W. Miller, and V. Nussenzweig. 1973. Human lymphocytes bear membrane receptors for C3b and C3d. J. Clin. Invest. 32:3239-3242.
3. Ross, G.D., M.J. Polley, E.M. Rabellino, and H.M. Grey. 1973. Two different complement receptors on human lymphocytes. One specific for C3b and one specific for C3b inactivator-cleaved C3b. J. Exp. Med. 138:798-811.
4. Pepys, M.B. 1972. Role of complement in induction of the allergic response. Nat. New Biol. 237:157-159.
5. Chen, Z., S.B. Koralov, M. Gendelman, M.C. Carroll, and G. Kelsoe. 2000. Humoral immune responses in Cr2-/mice: enhanced affinity maturation but impaired antibody persistence. J. Immunol. 164:4522-4532.
6. 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.
7. Molina, H., V.M. Holers, B. Li, Y.-F. Fang, 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.
8. Applequist, S.E., J. Dahlstrom, N. Jiang, H. Molina, and B. Heyman. 2000. Antibody production in mice deficient for complement receptors 1 and 2 can Be induced by IgG/Ag and IgE/Ag, but not IgM/Ag complexes. J. Immunol. 165:2398-2403.
9. 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.
10. 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.
11. Carter, R.H., D.A. Tuveson, D.J. Park, S.G. Rhee, and D.T. Fearon. 1991. The CD19 complex of B lymphocytes. Activation of phospholipase C by a protein tyrosine kinase-dependent pathway that can be enhanced by the membrane IgM complex. J. Immunol. 147:3663-3671.
12. Bradbury, L.E., G.S. Kansas, S. Levy, R.L. Evans, and T.F. Tedder. 1992. The CD19/CD21 signal transducing complex of human B lymphocytes includes the target of antiproliferative antibody-1 and Leu-13 molecules. J. Immunol. 149:2841-2850.
13. Kansas, G.S., and T.F. Tedder. 1991. Transmembrane signals generated through MHC class II, CD19, CD20, CD39, and CD40 antigens induce LFA-1-dependent and independent adhesion in human B cells through a tyrosine kinase-dependent pathway. J. Immunol. 147:4094-4102.
14. Fearon, D.T., and R.H. Carter. 1995. The CD19/CR2/ TAPA-1 complex of B lymphocytes: Linking natural to acquired immunity. Annu. Rev. Immunol. 13:127-149.
15. Carter, R.H., and D.T. Fearon. 1992. CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science. 256:105-107.
16. Weiss, A., and D.R. Littman. 1994. Signal transduction by lymphocyte antigen receptors. Cell. 76:263-274.
17. Tedder, T.F., L.J. Zhou, and P. Engel. 1994. The CD19/CD21 signal transduction complex of B lymphocytes. Immunol. Today. 15:437-442.
18. Dykstra, M., A. Cherukuri, and S.K. Pierce. 2001. Rafts and synapses in the spatial organization of immune cell signaling receptors. J. Leukoc. Biol. 70:699-707.
19. Dykstra, M.L., R. Longnecker, and S.K. Pierce. 2001. Epstein-Barr virus coopts lipid rafts to block the signaling and antigen transport functions of the BCR. Immunity. 14:57-67.
20. Stoddart, A., M.L. Dykstra, B.K. Brown, W. Song, S.K. Pierce, and F.M. Brodsky. 2002. Lipid rafts unite signaling cascades with Clathrin to regulate BCR internalization. Immunity. 17:451-462.
21. Pierce, S.K. 2002. Lipid rafts and B-cell activation. Nat. Rev. Immunol. 2:96-105.
22. Cheng, P.C., M.L. Dykstra, R.N. Mitchell, and S.K. Pierce. 1999. A role for lipid rafts in B cell antigen receptor signaling and antigen targeting. J. Exp. Med. 190:1549-1560.
23. Cheng, P.C., B.K. Brown, W. Song, and S.K. Pierce. 2001. Translocation of the B cell antigen receptor into lipid rafts reveals a novel step in signaling. J. Immunol. 166:3693-3701.
24. Cherukuri, A., P.C. Cheng, H.W. Sohn, and S.K. Pierce. 2001. The CD19/CD21 complex functions to prolong B cell antigen receptor signaling from lipid rafts. Immunity. 14:169-179.
25. Bottger, E.C., T. Hoffmann, U. Hadding, and D. Bitter-Suermann. 1985. Influence of genetically inherited complement deficiencies on humoral immune response in guinea pigs. J. Immunol. 135:4100-4107.
26. Fischer, M.B., M. Ma, S. Goerg, X. Zhou, J. Xia, O. Finco, S. Han, G. Kelsoe, R.G. Howard, T.L. Rothstein, et al. 1996. Regulation of the B cell response to T-dependent antigens by classical pathway complement. J. Immunol. 157:549-556.
27. Petry, F., M. Botto, R. Holtappels, M.J. Walport, and M. Loos. 2001. Reconstitution of the complement function in C1q-deficient (C1qa-/-) mice with wild-type bone marrow cells. J. Immunol. 167:4033-4037.
28. Botto, M., C. Dell'Agnola, A.E. Bygrave, E.M. Thompson, H.T. Cook, F. Perry, M. Loos, P.P. Pandolfi, and M.J. Walport. 1998. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19:56-59.
29. Cutler, A.J., M. Botto, D. van Essen, R. Rivi, K.A. Davies, D. Gray, and M.J. Walport. 1998. T cell-dependent immune response in C1q-deficient mice: defective interferon gamma production by antigen-specific T cells. J. Exp. Med. 187:1789-1797.
30. Matsumoto, M., W. Fukuda, A. Circolo, J. Goellner, J. Strauss-Schoenberger, X. Wang, S. Fujita, T. Hidvegi, D.D. Chaplin, and H.R. Colten. 1997. Abrogation of the alternative complement pathway by targeted deletion of murine factor B. Proc. Natl. Acad. Sci. USA. 94:8720-8725.
31. Klaus, G.G.B., J.H. Humphrey, A. Kunkl, and D.W. Dongworth. 1980. The follicular dendritic cell: Its role in antigen presentation in the generation of immunological memory. Immunol. Rev. 53:3-28.
32. Thornton, B.P., V. Vetvicka, and G.D. Ross. 1994. Natural antibody and complement-mediated antigen processing and presentation by B lymphocytes. J. Immunol. 152:1727-1737.
33. Hannum, L.G., A.M. Haberman, S.M. Anderson, and M.J. Shlomchik. 2000. Germinal center initiation, variable gene region hypermutation, and mutant B cell selection without detectable immune complexes on follicular dendritic cells. J. Exp. Med. 192:931-942.
34. Chan, O.T., L.G. Hannum, A.M. Haberman, M.P. Madaio, and M.J. Shlomchik. 1999. A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. J. Exp. Med. 189:1639-1648.
35. Arya, S., F. Chen, S. Spycher, D.E. Isenman, M.J. Shulman, and R.H. Painter. 1994. Mapping of amino acid residues in the C mu 3 domain of mouse IgM important in macromolecular assembly and complement-dependent cytolysis. J. Immunol. 152:1206-1212.
36. Wright, J.F., M.J. Shulman, D.E. Isenman, and R.H. Painter. 1988. C1 binding by murine IgM. The effect of a Pro-to-Ser exchange at residue 436 of the mu-chain. J. Biol. Chem. 263:11221-11226.
37. Lynes, M.A., L.L. Lanier, G.F. Babcock, P.J. Wettstein, and G. Haughton. 1978. Antigen-induced murine B cell lymphomas. I. Induction and characterization of CH1 and CH2. J. Immunol. 121:2352-2357.
38. Shlomchik, M.J., D. Zharhary, T. Saunders, S.A. Camper, and M.G. Weigert. 1993. A rheumatoid factor transgenic mouse model of autoantibody regulation. Int. Immunol. 5:1329-1341.
39. Jacob, J., R. Kassir, and G. Kelsoe. 1991. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J. Exp. Med. 173:1165-1175.
40. Jacob, J., and G. Kelsoe. 1992. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. II. A common clonal origin for periarteriolar lymphoid sheath-associated foci and germinal centers. J. Exp. Med. 176:679-687.
41. Borso, T., and M. Cooper. 1961. On the hemolytic activity of mouse complement. Prc. Soc. Exp. Biol. Med. 107:227-237.
42. Klaus, G.G., M.B. Pepys, K. Kitajima, and B.A. Askonas. 1979. Activation of mouse complement by different classes of mouse antibody. Immunology. 38:687-695.
43. Johnson, A.A., A. Mirowski Rosengard, K. Skjodt, J.M. Ahearn, and R.G. Leslie. 1999. The structural basis for complement receptor type 2 (CR2, CD21)-mediated alternative pathway activation of complement: studies with CR2 deletion mutants and vaccinia virus complement-control protein-CR2 chimeras. Eur. J. Immunol. 29:3837-3844.
44. Marquart, H.V., S.E. Svehag, and R.G. Leslie. 1994. CR2 is the primary acceptor site for C3 during alternative pathway activation of complement on human peripheral B lymphocytes. J. Immunol. 153:307-315.
45. Nielsen, C.H., H.V. Marquart, W.M. Prodinger, and R.G. Leslie. 2001. CR2-mediated activation of the complement alternative pathway results in formation of membrane attack complexes on human B lymphocytes. Immunology. 104:418-422.
46. Nielsen, C.H., M.L. Pedersen, H.V. Marquart, W.M. Prodinger, and R.G. Leslie. 2002. The role of complement receptors type 1 (CR1, CD35) and 2 (CR2, CD21) in promoting C3 fragment deposition and membrane attack complex formation on normal peripheral human B cells. Eur. J. Immunol. 32:1359-1367.
47. Nielsen, C.H., and R.G. Leslie. 2002. Complement's participation in acquired immunity. J. Leukoc. Biol. 72:249-261.
48. Olesen, E.H., A.A. Johnson, G. Damgaard, and R.G. Leslie. 1998. The requirement of localized, CR2-mediated, alternative pathway activation of complement for covalent deposition of C3 fragments on normal B cells. Immunology. 93:177-183.
49. Ehrenstein, M.R., T.L. O'Keefe, S.L. Davies, and M.S. Neuberger. 1998. Targeted gene disruption reveals a role for natural secretory IgM in the maturation of the primary immune response. Proc. Natl. Acad. Sci. USA. 95:10089-10093.
50. Boes, M., C. Esau, M.B. Fischer, T. Schmidt, M. Carroll, and J. Chen. 1998. Enhanced B-1 cell development, but impaired IgG antibody responses in mice deficient in secreted IgM. J. Immunol. 160:4776-4787.
51. Heyman, B. 1990. The immune complex: possible ways of regulating the antibody response. Immunol. Today. 11:310-313.
52. Heyman, B., L. Pilstrom, and M.J. Shulman. 1988. Complement activation is required for IgM-mediated enhancement of the antibody response. J. Exp. Med. 167:1999-2004.
53. Klaus, G.G.B. 1978. The generation of memory cells II. Generation of B memory cells with preformed antigen-antibody complexes. Immunology. 34:643-652.
54. Klaus, G.G.B. 1979. The generation of memory cells III. Antibody class requirements for the generation of B-memory cells by antigen-antibody complexes. Immunology. 37:345-351.