Activation-induced deaminase contributes to the antibody-independent role of B cells in the development of autoimmunity

References

• Weigert MG, Cesari IM, Yonkovich SJ, Cohn M. Variability in the lambda light chain sequences of mouse antibody. Nature. 1970; 228:1045–1047.
   PubMed Web of Science ®Google Scholar
• Berek C, Berger A, Apel M. Maturation of the immune response in germinal centers. Cell. 1991; 67:1121–1129.
   PubMed Web of Science ®Google Scholar
• Eisen HN, Siskind GW. Variations in affinities of antibodies during the immune response. Biochemistry. 1964; 3:996–1008.
   PubMed Web of Science ®Google Scholar
• Klinman NR. The mechanism of antigenic stimulation of primary and secondary clonal precursor cells. J Exp Med. 1972; 136:241–260.
   PubMed Web of Science ®Google Scholar
• Clarke SH, Huppi K, Ruezinsky D, Staudt L, Gerhard W, Weigert M. Inter- and intraclonal diversity in the antibody response to influenza hemagglutinin. J Exp Med. 1985; 161:687–704.
   PubMed Web of Science ®Google Scholar
• Crews S, Griffin J, Huang H, Calame K, Hood L. A single VH gene segment encodes the immune response to phosphorylcholine: somatic mutation is correlated with the class of the antibody. Cell. 1981; 25:59–66.
   PubMed Web of Science ®Google Scholar
• Shlomchik MJ, Marshak-Rothstein A, Wolfowicz CB, Rothstein TL, Weigert MG. The role of clonal selection and somatic mutation in autoimmunity. Nature. 1987; 328:805–811.
   PubMed Web of Science ®Google Scholar
• Radic MZ, Mascelli MA, Erikson J, Shan H, Shlomchik M, Weigert M. Structural patterns in anti-DNA antibodies from MRL/lpr mice. Cold Spring Harb Symp Quant Biol. 1989; 54 Pt 2:933–946.
   PubMedGoogle Scholar
• Shlomchik M, Mascelli M, Shan H, Radic MZ, Pisetsky D, Marshak-Rothstein A, . Anti-DNA antibodies from autoimmune mice arise by clonal expansion and somatic mutation. J Exp Med. 1990; 171:265–292.
   PubMed Web of Science ®Google Scholar
• van Es JH, Gmelig Meyling FH, van de Akker WR, Aanstoot H, Derksen RH, Logtenberg T. Somatic mutations in the variable regions of a human IgG anti-double-stranded DNA autoantibody suggest a role for antigen in the induction of systemic lupus erythematosus. J Exp Med. 1991; 173:461–470.
   PubMed Web of Science ®Google Scholar
• Winkler TH, Fehr H, Kalden JR. Analysis of immunoglobulin variable region genes from human IgG anti-DNA hybridomas. Eur J Immunol. 1992; 22:1719–1728.
   PubMed Web of Science ®Google Scholar
• Radic MZ, Mascelli MA, Erikson J, Shan H, Weigert M. Ig H and L chain contributions to autoimmune specificities. J Immunol. 1991; 146:176–182.
   PubMed Web of Science ®Google Scholar
• Radic MZ, Mackle J, Erikson J, Mol C, Anderson WF, Weigert M. Residues that mediate DNA binding of autoimmune antibodies. J Immunol. 1993; 150:4966–4977.
   PubMed Web of Science ®Google Scholar
• Wellmann U, Letz M, Herrmann M, Angermuller S, Kalden JR, Winkler TH. The evolution of human anti-double-stranded DNA autoantibodies. Proc Natl Acad Sci USA. 2005; 102:9258–9263.
   PubMed Web of Science ®Google Scholar
• Shlomchik MJ, Aucoin AH, Pisetsky DS, Weigert MG. Structure and function of anti-DNA autoantibodies derived from a single autoimmune mouse. Proc Natl Acad Sci USA. 1987; 84:9150–9154.
   PubMed Web of Science ®Google Scholar
• Vuyyuru R, Mohan C, Manser T, Rahman ZS. The lupus susceptibility locus Sle1 breaches peripheral B cell tolerance at the antibody-forming cell and germinal center checkpoints. J Immunol. 2009; 183:5716–5727.
   PubMed Web of Science ®Google Scholar
• Guo W, Smith D, Aviszus K, Detanico T, Heiser RA, Wysocki LJ. Somatic hypermutation as a generator of antinuclear antibodies in a murine model of systemic autoimmunity. J Exp Med. 2010; 207:2225–2237.
   PubMed Web of Science ®Google Scholar
• Ait-Azzouzene D, Kono DH, Gonzalez-Quintial R, McHeyzer-Williams LJ, Lim M, Wickramarachchi D, . Deletion of IgG-switched autoreactive B cells and defects in Fas(lpr) lupus mice. J Immunol. 2010; 185:1015–1027.
   PubMed Web of Science ®Google Scholar
• Eisenberg R. Why can't we find a new treatment for SLE?. J Autoimmun. 2009; 32:223–230.
   PubMed Web of Science ®Google Scholar
• Jiang C, Zhao ML, Diaz M. Activation-induced deaminase heterozygous MRL/lpr mice are delayed in the production of high-affinity pathogenic antibodies and in the development of lupus nephritis. Immunology. 2009; 126:102–113.
   PubMed Web of Science ®Google Scholar
• Jiang C, Foley J, Clayton N, Kissling G, Jokinen M, Herbert R, . Abrogation of lupus nephritis in activation-induced deaminase-deficient MRL/lpr mice. J Immunol. 2007; 178:7422–7431.
   PubMed Web of Science ®Google Scholar
• Chan O, Shlomchik MJ. A new role for B cells in systemic autoimmunity: B cells promote spontaneous T cell activation in MRL-lpr/lpr mice. J Immunol. 1998; 160:51–59.
   PubMed Web of Science ®Google Scholar
• Chan OT, Hannum LG, Haberman AM, Madaio MP, Shlomchik MJ. A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. J Exp Med. 1999; 189:1639–1648.
   PubMed Web of Science ®Google Scholar
• Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell. 2000; 102:553–563.
   PubMed Web of Science ®Google Scholar
• Revy P, Muto T, Levy Y, Geissmann F, Plebani A, Sanal O, . Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell. 2000; 102:565–575.
   PubMed Web of Science ®Google Scholar
• Jiang C, Zhao ML, Scearce RM, Diaz M. Activation-induced deaminase-deficient MRL/lpr mice secrete high levels of protective antibodies against lupus nephritis. Arthritis Rheum. 2011; 63:1086–1096.
   PubMed Web of Science ®Google Scholar
• Hazenbos WL, Gessner JE, Hofhuis FM, Kuipers H, Meyer D, Heijnen IA, . Impaired IgG-dependent anaphylaxis and Arthus reaction in Fc gamma RIII (CD16) deficient mice. Immunity. 1996; 5:181–188.
   PubMed Web of Science ®Google Scholar
• Takai T, Ono M, Hikida M, Ohmori H, Ravetch JV. Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature. 1996; 379:346–349.
   PubMed Web of Science ®Google Scholar
• Ravetch JV, Bolland S. IgG Fc receptors. Annu Rev Immunol. 2001; 19:275–290.
   PubMed Web of Science ®Google Scholar
• Boes M, Schmidt T, Linkemann K, Beaudette BC, Marshak-Rothstein A, Chen J. Accelerated development of IgG autoantibodies and autoimmune disease in the absence of secreted IgM. Proc Natl Acad Sci USA. 2000; 97:1184–1189.
   PubMed Web of Science ®Google Scholar
• Melamed D, Miri E, Leider N, Nemazee D. Unexpected autoantibody production in membrane Ig-mu-deficient/lpr mice. J Immunol. 2000; 165:4353–4358.
   PubMed Web of Science ®Google Scholar
• Liang Z, Xie C, Chen C, Kreska D, Hsu K, Li L, . Pathogenic profiles and molecular signatures of antinuclear autoantibodies rescued from NZM2410 lupus mice. J Exp Med. 2004; 199:381–398.
   PubMed Web of Science ®Google Scholar
• Sims GP, Shiono H, Willcox N, Stott DI. Somatic hypermutation and selection of B cells in thymic germinal centers responding to acetylcholine receptor in myasthenia gravis. J Immunol. 2001; 167:1935–1944.
   PubMed Web of Science ®Google Scholar
• Stott DI, Hiepe F, Hummel M, Steinhauser G, Berek C. Antigen-driven clonal proliferation of B cells within the target tissue of an autoimmune disease. The salivary glands of patients with Sjogren's syndrome. J Clin Invest. 1998; 102:938–946.
   PubMed Web of Science ®Google Scholar
• Diamond B, Katz JB, Paul E, Aranow C, Lustgarten D, Scharff MD. The Role of Somatic Mutation in the Pathogenic Anti-DNA Response. Annual Rev Immunol. 1992; 10:731–757.
   PubMed Web of Science ®Google Scholar
• Li Z, Schettino EW, Padlan EA, Ikematsu H, Casali P. Structure-function analysis of a lupus anti-DNA autoantibody: central role of the heavy chain complementarity-determining region 3 Arg in binding of double- and single-stranded DNA. Eur J Immunol. 2015; 30:2015–2026.
   Google Scholar
• Qin H, Suzuki K, Nakata M, Chikuma S, Izumi N. Activation-induced cytidine deaminase expression in CD4+T Cells is associated with a unique IL-10-producing subset that increases with age. PLoS ONE. 2011; 6:e29141.
   PubMed Web of Science ®Google Scholar
• Lee SB, Kalluri R. Mechanistic connection between inflammation and fibrosis. Kidney Int Suppl. 2010S22–S26.
   Google Scholar