CR1/CR2 Deficiency Alters IgG3 Autoantibody Production and IgA Glomerular Deposition in the MRL/lpr Model of SLE

References

• Andrews, B.S., Eisenberg, RA., Theofilopoulos, AN., Izui, S., Wilson, C.B., McConahey, P.J., Murphy, ED., Roths, J.B. and Dixon, F.J. (1978) "Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains", J. Exp. Med. 148, 1198–1215.
   PubMed Web of Science ®Google Scholar
• Watson, ML., Rao, J.K., Gilkeson, G.S., Ruiz, E, Eicher, EM., Pisetsky, D.S., Matsuzawa, A., Rochelle, J.M. and Seldin, M.F. (1992) "Genetic analysis of MRL//pr mice: relationship of the Fas apoptosis gene to disease manifestations and renal disease-modifying loci", J. Exp. Med. 176, 1645–1656.
   PubMed Web of Science ®Google Scholar
• Watanabe-Fukunaga, R., Brannan, CI, Copeland, N.G., Jenkins, N.A. and Nagata, S. (1992) "Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis", Nature 356, 314–317.
   PubMed Web of Science ®Google Scholar
• Theofilopoulos, A.N. and Dixon, F.J. (1985) "Murine models of systemic lupus erythematosus", Adv. Immunol. 37, 269–390.
   PubMed Web of Science ®Google Scholar
• Theofilopoulos, AN., Kofler, R., Singer, RA. and Dixon, F.J. (1989) "Molecular genetics of murine lupus models", Adv. Immunol. 46, 61–109.
   PubMed Web of Science ®Google Scholar
• Lloyd, CM., Gonzalo, J.A., Salant, D.J., Just, J. and Gutierrez-Ramos, J.C. (1997) "Intercellular adhesion molecule-1 deficiency prolongs survival and protects against the development of pulmonary inflammation during murine lupus", J. aim Invest. 100, 963–971.
   Google Scholar
• Reininger, L, Berney, T., Shibata, T., Spertini, F., Merino, R. and Izui, S. (1990) "Cryoglobulinemia induced by a murine IgG3 rheumatoid factor: skin vasculitis and glomerulonephritis arise from distinct pathogenic mechanisms", Proc. Natl Acad. Sci. USA 87, 10038–10042.
   PubMed Web of Science ®Google Scholar
• Morse, H.C., M, Davidson, WE, Yetter, R.A., Murphy, ED., Roths, LB. and Coffman, R.L. (1982) "Abnormalities induced by the mutant gene 1pr expansion of a unique lymphocyte subset", J. Immunol. 129, 2612–2615.
   Google Scholar
• Nemazee, D.A., Studer, S., Steinmetz, M., Dembic, Z. and Kiefer, M. (1985) "The lymphoproliferating cells of MRL-IprIlpr mice are a polyclonal population that bear the T lymphocyte receptor for antigen", Eur. J. Immunol. 15, 760–764.
   PubMed Web of Science ®Google Scholar
• Katagiri, T., Cohen, EL. and Eisenberg, R.A. (1988) "The 1pr gene causes an intrinsic T cell abnormality that is required for hyperproliferation", J. Exp. Med. 167, 741–751.
   PubMed Web of Science ®Google Scholar
• Perkins, DL, Glaser, R.M., Mahon, CA., Michaelson, J. and Marshak-Rothstein, A. (1990) "Evidence for an intrinsic B cell defect in IprIlpr mice apparent in neonatal chimeras", J. Immunol. 145, 549–555.
   PubMed Web of Science ®Google Scholar
• Nemazee, D., Guiet, C., Buerki, K. and Marshak-Rothstein, A. (1991) "B lymphocytes from the autoimmune-prone mouse strain MRL//pr manifest an intrinsic defect in tetraparental MRL//pr:DBA/2 chimeras", J. Immunol. 147, 2536–2539.
   PubMed Web of Science ®Google Scholar
• Sobel, ES., Kakkanaiah, V.N., Kakkanaiah, M., Cheek, R.L., Cohen, EL. and Eisenberg, R.A. (1994) "T-B collaboration for autoantibody production in 1pr mice is cognate and MHC-restricted", J. Immunol. 152, 6011–6016.
   PubMed Web of Science ®Google Scholar
• Shlomchik, Mi., Madaio, M.P., Ni, D., Trounstein, M. and Huszar, D. (1994) "The role of B cells in /pr//pr-induced autoimmunity", J. Exp. Med. 180, 1295–1306.
   PubMed Web of Science ®Google Scholar
• Chan, 0.T.M., Hannum, L.G., Haberman, A.M., Madaio, my. and Shlomchik, M.J. (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, 1639–1647.
   PubMed Web of Science ®Google Scholar
• Walport, M.J., Davies, K.A., Morley, B.J. and Bono, M. (1997) "Complement deficiency and autoimmunity", Ann. N. Y. Acad. Sci. 815, 267 — 281.
   Web of Science ®Google Scholar
• Mevorach, D., Thou, J.L., Song, X. and Elkon, KB. (1998) "Systemic exposure to irradiated apoptotic cells induces autoanti-body production", J. Exp. Med. 188, 387–392.
   PubMed Web of Science ®Google Scholar
• Mitchell, D.A., Pickering, M.C., Warren, J., Fossati-Jimack, L., Cortes-Hemandez, J., Cook, H.T., Botto, M. and Walport, M.J. (2002) "Clq deficiency and autoimmunity: the effects of genetic background on disease expression", J. Immunol. 168, 2538–2543.
   PubMed Web of Science ®Google Scholar
• Watanabe, H., Gamier, G., Circolo, A., Wetsel, R.A., Ruiz, P., Holers, V.M., Boackle, S.A., Cohen, RR. and Gilkeson, G.S. (2000) "Modulation of renal disease in MRL//pr mice genetically deficient in the alternative complement pathway factor B", J. Immunol. 164, 786–794.
   PubMed Web of Science ®Google Scholar
• Elliott, M.K., Jarmi, T., Ruiz, P., Xu, Y, Holers, V.M. and Gilkeson, G.S. (2004) "Effects of complement factor D deficiency on the renal disease of MRL//pr mice", Kidney Int. 65, 129–138.
   PubMed Web of Science ®Google Scholar
• Molina, H., Kinoshita, T., Inoue, K., Carel, J.C. and Holers, V.M. (1990) "A molecular and immunochemical characterization of mouse CR2: evidence for a single gene model of mouse complement receptors 1 and 2", J. Immunol. 145, 2974–2983.
   PubMed Web of Science ®Google Scholar
• Kurtz, C.B., O'Toole, E., Christensen, S.M. and Weis, J.H. (1990) "The murine complement receptor gene family. IV. Alternative splicing of Cr2 gene transcripts predicts two distinct gene products that share homologous domains with both human CR2 and CR1", J. Immunol. 144, 3581–3591.
   PubMed Web of Science ®Google Scholar
• Gonunerman, J.L., Oh, D.Y., Thou, X., Tedder, T.F., Maurer, M., Galli, S.J. and Carroll, M.C. (2000) "A role for CD21/CD35 and CD19 in responses to acute septic peritonitis: a potential mechanism for mast cell activation", J. Immunol. 165, 6915–6921.
   PubMed Web of Science ®Google Scholar
• Kaya, Z., Afanasyeva, M., Wang, Y, Dohmen, KM., Schlichting, J., Tretter, T., Fairweather, D., Holers, V.M. and Rose, N.R. (2001) "Contribution of the innate immune system to autoimmune myocarditis: a role for complement", Nature Immunol. 2, 739–745.
   PubMed Web of Science ®Google Scholar
• Carter, R.H., Spycher, no., Ng, Y.C., Hoffman, R. and Fearon, D.T. (1988) "Synergistic interaction between complement receptor type 2 and membrane IgM on B lymphocytes", J. Immunol. 141, 457–463.
   PubMed Web of Science ®Google Scholar
• Fingeroth, J.D., Heath, M.E. and Ambrosino, D.M. (1989) "Proliferation of resting B cells is modulated by CR2 and CR1", Immunol. Lett. 21, 291–302.
   PubMed Web of Science ®Google Scholar
• Luxembourg, A.T. and Cooper, N.R. (1994) "Modulation of signaling via the B cell antigen receptor by CD21, the receptor for C3dg and EBV", J. Immunol. 153, 4448–4457.
   PubMed Web of Science ®Google Scholar
• Kozono, Y, Duke, R.C., Schleicher, M.S. and Holers, V.M. (1995) "Co-ligation of mouse complement receptors 1 and 2 with surface IgM rescues splenic B cells and WEHI-231 cells from anti-surface IgM-induced apoptosis", Eur. J. Immunol. 25, 1013–1017.
   PubMed Web of Science ®Google Scholar
• Arvieux, J., Yssel, H. and Colomb, M.G. (1988) "Antigen-bound C3b and C4b enhance antigen-presenting cell function in activation of human T-cell clones", Immunology 65, 229–235.
   PubMed Web of Science ®Google Scholar
• Boackle, S.A., Holers, V.M. and Karp, D.R. (1997) "CD21 augments antigen presentation in immune individuals", Eur. J. Immunol. 27, 122–130.
   PubMed Web of Science ®Google Scholar
• Boackle, S.A., Morris, MA., Holers, V.M. and Karp, D.R. (1998) "Complement opsonization is required for the presentation of immune complexes by resting peripheral blood B cells", J. Immunol. 161, 6537–6543.
   PubMed Web of Science ®Google Scholar
• Lanzavecchia, A., Abrignani, S., Scheidegger, D., Obrist, R., Dorken, B. and Moldenhauer, G. (1988) "Antibodies as antigens: the use of mouse monoclonal antibodies to focus human T cells against selected targets", J. Exp. Med. 167, 345–352.
   PubMed Web of Science ®Google Scholar
• Thornton, BR, Vetvicka, V. and Ross, G.D. (1994) "Natural antibody and complement-mediated antigen processing and presentation by B lymphocytes", J. Immunol. 152, 1727 —1737.
   PubMed Web of Science ®Google Scholar
• Kozono, Y, Abe, R., Kozono, H., Kelly, R.G., Azuma, T. and Holers, V.M. (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.
   PubMed Web of Science ®Google Scholar
• Cherukuri, A., Cheng, P.C., Sohn, H.W. and Pierce, S.K. (2001) "The CD19/CD21 complex functions to prolong B cell antigen receptor signaling from lipid rafts", Immunity 14, 169–179.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Papamichai, M., Gutierrez, C., Embling, P., Johnson, P., Holborow, E.J. and Pepys, MB. (1975) "Complement dependence of localization of aggregated IgG in germinal centers", Scand. J. Immunol. 4, 343–347.
   PubMed Web of Science ®Google Scholar
• Bradbury, L.E., Kansas, G.S., Levy, S., Evans, RI. and Tedder, T.F. (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.
   PubMed Web of Science ®Google Scholar
• Matsumoto, AK., Kopicky-Burd, J., Carter, R.H., Tuveson, D.A., Tedder, T.F. and Fearon, D.T. (1991) "Intersection of the complement and immune systems: a signal transduction complex of the B lymphocyte-containing complement receptor type 2 and CD19", J. Exp. Med. 173, 55–64.
   PubMed Web of Science ®Google Scholar
• Molina, H., Holers, V.M., Li, B., Fang, Y.F., Mariathasan, S., Goellner, J., Strauss-Schoenberger, J., Karr, R.W. and Chaplin, D.D. (1996) "Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2", Proc. Natl Acad. Sci. USA 93, 3357–3361.
   PubMed Web of Science ®Google Scholar
• Croix, D.A., Ahearn, J.M., Rosengard, A.M., Han, S., Kelsoe, G., Ma, M. and Carroll, M.C. (1996) "Antibody response to a T-dependent antigen requires B cell expression of complement receptors", J. Exp. Med. 183, 1857–1864.
   PubMed Web of Science ®Google Scholar
• Ahearn, J.M., Fischer, MB., Croix, D., Goerg, S., Ma, M., Xia, J., Zhou, X., Howard, R.G., Rothstein, T.L. and Carroll, M.C. (1996) "Disruption of the Cr2 locus results in a reduction in B-la cells and in an impaired B cell response to T-dependent antigen", Immunity 4, 251–262.
   PubMed Web of Science ®Google Scholar
• Haas, KM., Hasegawa, M., Steeber, D.A., Poe, J.C., Zabel, M.D., Bock, C.B., Karp, D.R., Briles, D.E., Weis, J.H. and Tedder, T.F. (2002) "Complement receptors CD21/35 link innate and protective immunity during Streptococcus pneumoniae infection by regulating IgG3 antibody responses", Immunity 17, 713–723.
   PubMed Web of Science ®Google Scholar
• Wu, X., Jiang, N., Fang, Y.F., Xu, C., Mao, D., Singh, J., Fu, Y.X. and Molina, H. (2000) "Impaired affinity maturation in Cr2 — /—mice is rescued by adjuvants without improvement in germinal center development", J. Immunol. 165, 3119–3127.
   PubMed Web of Science ®Google Scholar
• Barrington, R.A., Pozdnyakova, 0., Zafari, MR., Benjamin, C.D. and Carroll, M.C. (2002) "B lymphocyte memory: role of stromal cell complement and FcgRBB receptors", J. Exp. Med. 196, 1189–1199.
   PubMed Web of Science ®Google Scholar
• Fleming, S.D., Shea-Donohue, T., Guthridge, J.M., Kulik, L., Waldschmidt, T.J., Gipson, M.G., Tsokos, G.C. and Holers, V.M. (2002) "Mice deficient in complement receptors 1 and 2 lack a tissue injury-inducing subset of the natural antibody repertoire", J. Immunol. 169, 2126–2133.
   PubMed Web of Science ®Google Scholar
• Prodeus, A.P., Georg, S., Shen, L.M., Pozdnyakova, 0.0., Chu, L., Alicot, EM., Goodnow, C.C. and Carroll, M.C. (1998) "A critical role for complement in the maintenance of self-tolerance", Immunity 9, 721 —731.
   Web of Science ®Google Scholar
• Wu, X., Jiang, N., Deppong, C., Singh, J., Dolecki, G., Mao, D., Morel, L. and Molina, H.D. (2002) "A role for the Cr2 gene in modifying autoantibody production in systemic lupus erythe-matosus", J. Immunol. 169, 1587–1592.
   PubMed Web of Science ®Google Scholar
• Boackle, S.A., Holers, V.M., Chen, X., Szakonyi, G., Karp, D.R., Wakeland, E.K. and Morel, L. (2001) "Cr2, a candidate gene in the murine Slelc lupus susceptibility locus, encodes a dysfunctional protein", Immunity 15, 775–785.
   PubMed Web of Science ®Google Scholar
• Wilson, J.G., Ratnoff, W.D., Schur, PH. and Fearon, D.T. (1986) "Decreased expression of the C3b/C4b receptor (CR1) and the C3d receptor (CR2) on B lymphocytes and of CR1 on neutrophils of patients with systemic lupus erythematosus", Arthritis Rheum. 29, 739–747.
   PubMedGoogle Scholar
• Levy, E., Ambrus, J., Kahl, L., Molina, H., Tung, K. and Holers, V.M. (1992) "T lymphocyte expression of complement receptor 2 (CR2/CD21): a role in adhesive cell—cell interactions and dysregulation in a patient with systemic lupus erythematosus (SLE)", Clin. Exp. Immunol. 90, 235–244.
   PubMed Web of Science ®Google Scholar
• Marquart, H.V., Svendsen, A., Rasmussen, J.M., Nielsen, C.H., Junker, P., Svehag, S.E. and Leslie, R.G.Q. (1995) "Complement receptor expression and activation of the complement cascade on B lymphocytes from patients with systemic lupus erythematosus (SLE)", Clin. Exp. Immunol. 101, 60–65.
   PubMed Web of Science ®Google Scholar
• Takahashi, K., Kozono, Y., Waldschmidt, T.J., Quigg, R.J., Baron, A. and Holers, V.M. (1997) "Mouse complement receptors type 1 (CR1; CD35) and type 2 (CR2; CD21): expression on normal B cell subpopulations and decreased levels during development of autoimmunity in MRL//pr mice", J. Immunol. 159, 1557–1569.
   PubMed Web of Science ®Google Scholar
• Reap, E.A., Piecyk, ML., Oliver, A., Sobel, ES., Waldschmidt, T., Cohen, P.L. and Eisenberg, R.A. (1996) "Phenotypic abnormalities of splenic and bone marrow B cells in lpr and gld mice", Clin. Exp. Immunopathol. 78, 21–29.
   PubMedGoogle Scholar
• Feuerstein, N., Chen, F., Madaio, M.P., Maldonado, MA. and Eisenberg, R.A. (1999) "Induction of autoimmunity in a transgenic model of B cell receptor peripheral tolerance: changes in coreceptors and B cell receptor-induced tyrosine-phosphoproteins", J. Immunol. 163, 5287–5297.
   PubMed Web of Science ®Google Scholar
• Quigg, R.J., Lim, A., Haas, M., Alexander, J.J., He, C. and Carroll, MC. (1998) "Immune complex glomerulonephritis in C4- and C3-deficient mice", Kidney Int. 53, 320–330.
   PubMed Web of Science ®Google Scholar
• Passwell, J., Schreiner, GE, Nonaka, M., Beuscher, H.U. and Cohen, RR. (1988) "Local extrahepatic expression of complement genes C3, factor B, C2 and C4 is increased in murine lupus nephritis", J. Clin. Invest. 82, 1676–1684.
   PubMed Web of Science ®Google Scholar
• Fulpius, T., Spertini, F., Reininger, L. and Izui, S. (1993) "Inununoglobulin heavy chain constant region determines the pathogenicity and the antigen-binding activity of rheumatoid factor", Proc. Natl Acad. Sci. USA 90, 2345–2349.
   PubMed Web of Science ®Google Scholar
• Guinamard, R., Okigaki, M., Schlessinger, J. and Ravetch, J.V. (2000) "Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral responses", Nat. Immunol. 1, 31–36.
   PubMed Web of Science ®Google Scholar
• Abdelmoula, M., Spertini, F., Shibata, T., Gyotoku, Y, Luzuy, S., Lambert, PH. and Izui, S. (1989) "IgG3 is the major source of cryoglobulins in mice", J. Immunol. 143, 526–532.
   PubMed Web of Science ®Google Scholar
• da Silveira, S.A., Kikuchi, S., Fossati-Jimack, L., Moll, T., Saito, T., Verbeek, J.S., Botto, M., Walport, M.J., Carroll, M. and Izui, S. (2002) "Complement activation selectively potentiates the patho-genicity of the IgG2b and IgG3 isotypes of a high affinity anti-erythrocyte autoantibody", J. Exp. Med. 195, 665–672.
   PubMed Web of Science ®Google Scholar
• de Stahl, T.D., Dahlstrom, J., Carroll, MC. and Heyman, B. (2003) "A role for complement in feedback enhancement of antibody responses by IgG3", J. Exp. Med. 197, 1183–1190.
   PubMed Web of Science ®Google Scholar
• Stad, R.K., van Gijlswijk-Janssen, D.J., Van Es, L.A. and Daha, M.R. (1994) "Complement depletion abolishes IgA-mediated glomerular inflammation in rats", Exp. Nephrol. 2, 182–189.
   PubMedGoogle Scholar
• Schaapherder, A.F., Gooszen, HG., te Bulte, UT. and Daha, MR. (1995) "Human complement activation via the alternative pathway on porcine endothelium initiated by IgA antibodies", Transplan-tation 60, 287–291.
   PubMed Web of Science ®Google Scholar
• Hisano, S., Matsushita, M., Fujita, T., Endo, Y. and Takebayashi, S. (2001) "Mesangial IgA2 deposits and lectin pathway-mediated complement activation in IgA glomerulonephritis", Am. J. Kidney Dis. 38, 1082–1088.
   PubMed Web of Science ®Google Scholar
• Roos, A., Bouwman, L.H., van Glilswijk-Janssen, D.J., Faber-Krol, MC., Stahl, G.L. and Daha, M.R. (2001) "Human IgA activates the complement system via the mannan-binding lectin pathway", J. Immunol. 167, 2861–2868.
   PubMed Web of Science ®Google Scholar
• Oyama, A., Muso, E., Ono, T., Matsushima, H., Yashiro, M., Suyama, K., Kamata, T., Nogaki, F., Kobayashi, I., Miyawaki, S., Yoshida, H. and Sasayama, S. (2001) "Up-regulated TGF-I3 mRNA expression in splenic T cells of high IgA-prone mice: a murine model of IgA nephropathy with glomerulosclerosis", Nephron 88, 368–375.
   PubMed Web of Science ®Google Scholar
• Hale, G.M., McIntosh, S.L., Hiki, Y, Clarkson, A.R. and Woodroffe, A.J. (1986) "Evidence for IgA-specific B cell hyperactivity in patients with IgA nephropathy", Kidney Int. 29, 718–724.
   PubMed Web of Science ®Google Scholar
• Schena, F.P., Pastore, A. and Montinaro, V. (1988) "The role of polymeric IgA in complement-mediated solubilization of IgG and IgA immune complexes", Am. J. Kidney Dis. 12, 433–436.
   PubMed Web of Science ®Google Scholar
• Lindorfer, M.A., Jinivizian, H.B., Foley, P.L., Kennedy, A.D., Solga, M.D. and Taylor, R.P. (2003) "B cell complement receptor 2 transfer reaction", J. Immunol. 170, 3671–3678.
   PubMed Web of Science ®Google Scholar
• Meryhew, N.L. and Messner, RP. (1993) "Murine complement-mediated immune clearance dysfunction is associated with the lymphoproliferative (lpr) gene", Clin. Immunol. Immunopathol. 69, 324–332.
   PubMedGoogle Scholar
• Meryhew, N.L., Tam, P.E., Seim, J.K. and Messner, R.P. (1996) "Abnormal complement-mediated immune clearance in MRL-Iprl+ heterozygote mice: dose-dependent effect of the Fas antigen mutation", Clin. Immunol. Immunopathol. 78, 236–244.
   PubMedGoogle Scholar
• Fukuyama, H., Adachi, M., Suematsu, S., Miwa, K., Suda, T., Yoshida, N. and Nagata, S. (1998) "Transgenic expression of Fos in T cells blocks lymphoproliferation but not autoimmune disease in MRL-/pr mice", J. Immunol. 160, 3805–3811.
   PubMed Web of Science ®Google Scholar
• Walport, M.J., Davies, K.A. and Botto, M. (1998) "Clq and systemic lupus erythematosus", Immunobiology 199, 265–285.
   PubMed Web of Science ®Google Scholar