The role of somatic hypermutation in the generation of pathogenic antibodies in SLE

References

• Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997; 40:1725.
   PubMed Web of Science ®Google Scholar
• Tan EM, Cohen AS, Fries JF, . The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1982; 25:1271–1277.
   PubMed Web of Science ®Google Scholar
• ter Borg E, Horst G, Hummel E, Limburg P, Kallenberg C. Measurement of increases in anti-double-stranded DNA antibody levels as a predictor of disease exacerbation in systemic lupus erythematosus. A long-term, prospective study. Arthritis Rheum. 1990; 33:634–643.
   PubMed Web of Science ®Google Scholar
• Ebling F, Hahn B. Restricted subpopulations of DNA antibodies in kidneys of mice with systemic lupus. Comparison of antibodies in serum and renal eluates. Arthritis Rheum. 1980; 23:392–403.
   PubMed Web of Science ®Google Scholar
• Ehrenstein MR, Katz DR, Griffiths MH, . Human IgG anti-DNA antibodies deposit in kidneys and induce proteinuria in SCID mice. Kidney Int. 1995; 48:705–711.
   PubMed Web of Science ®Google Scholar
• Vlahakos D, Foster M, Adams S, . Anti-DNA antibodies form immune deposits at distinct glomerular and vascular sites. Kidney Int. 1992; 41:1690–1700.
   PubMed Web of Science ®Google Scholar
• Berland R, Fernandez L, Kari E, . Toll-like receptor 7-dependent loss of B cell tolerance in pathogenic autoantibody knockin mice. Immunity. 2006; 25:429–440.
   PubMed Web of Science ®Google Scholar
• Hahn BH. Antibodies to DNA. N. Engl. J. Med. 1998; 338:1359–1368.
   PubMed Web of Science ®Google Scholar
• Deocharan B, Qing X, Lichauco J, Putterman C. Alpha-actinin is a cross-reactive renal target for pathogenic anti-DNA antibodies. J. Immunol. 2002; 168:3072–3078.
   PubMed Web of Science ®Google Scholar
• Faaber P, Rijke TP, van-de-Putte LB, Capel PJ, Berden JH. Cross-reactivity of human and murine anti-DNA antibodies with heparan sulfate. The major glycosaminoglycan in glomerular basement membranes. J. Clin. Invest. 1986; 77:1824–1830.
   PubMed Web of Science ®Google Scholar
• Sabbaga J, Line SR, Potocnjak P, Madaio MP. A murine nephritogenic monoclonal anti-DNA autoantibody binds directly to mouse laminin, the major non-collagenous protein component of the glomerular basement membrane. Eur. J. Immunol. 1989; 19:137–143.
   PubMed Web of Science ®Google Scholar
• Mortensen ES, Fenton KA, Rekvig OP. Lupus nephritis: the central role of nucleosomes revealed. Am. J. Pathol. 2008; 172:275–283.
   PubMed Web of Science ®Google Scholar
• Kalaaji M, Mortensen E, Jørgensen L, Olsen R, Rekvig OP. Nephritogenic lupus antibodies recognize glomerular basement membrane-associated chromatin fragments released from apoptotic intraglomerular cells. Am. J. Pathol. 2006; 168:1779–1792.
   PubMed Web of Science ®Google Scholar
• Munoz LE, Lauber K, Schiller M, Manfredi AA, Herrmann M. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat. Rev. Rheumatol. 2010; 6:280–289.
   PubMed Web of Science ®Google Scholar
• Munoz LE, Janko C, Grossmayer GE, . Remnants of secondarily necrotic cells fuel inflammation in systemic lupus erythematosus. Arthritis Rheum. 2009; 60:1733–1742.
   PubMed Web of Science ®Google Scholar
• Notkins AL. Polyreactivity of antibody molecules. Trends Immunol. 2004; 25:174–179.
   PubMed Web of Science ®Google Scholar
• Naparstek J, Andra-Schwartz J, Mauser T, . A single germ-line VH gene segment of normal A/J mice encodes auto-antibodies characteristic of systemic lupus erythematosus. J. Exp. Med. 1986; 164:614–626.
   PubMed Web of Science ®Google Scholar
• Cairns E, Kwong PC, Misener V, . Analysis of variable region genes encoding a human anti-DNA antibody of normal origin. Implications for the molecular basis of human autoimmune responses. J. Immunol. 1989; 143:685–691.
   PubMedGoogle Scholar
• Dersimonian H, McAdam KP, Mackworth-Young C, Stollar BD. The recurrent expression of variable region segments in human IgM anti-DNA autoantibodies. J. Immunol. 1989; 142:4027–4033.
   PubMedGoogle Scholar
• Wardemann H, Yurasov S, Schaefer A, . Predominant autoantibody production by early human B cell precursors. Science. 2003; 301:1374–1377.
   PubMed Web of Science ®Google Scholar
• Tiller T, Tsuiji M, Yurasov S, . Autoreactivity in human IgG+ memory B cells. Immunity. 2007; 26:205–213.
   PubMed Web of Science ®Google Scholar
• Shlomchik M, Mascelli M, Shan H, . 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
• 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
• 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
• Tillman DM, Jou NT, Hill RJ, Marion TN. Both IgM and IgG anti-DNA antibodies are the products of clonally selective B cell stimulation in (NZB x NZW)F1 mice. J. Exp. Med. 1992; 176:761–779.
   PubMed Web of Science ®Google Scholar
• Eilat D, Fischel R. Recurrent utilization of genetic elements in V regions of antinucleic acid antibodies from autoimmune mice. J. Immunol. 1991; 147:361–368.
   PubMedGoogle Scholar
• Bloom DD, Davignon JL, Retter MW, . V region gene analysis of anti-Sm hybridomas from MRL/Mp-lpr/lpr mice. J. Immunol. 1993; 150:1591–1610.
   PubMedGoogle Scholar
• Losman MJ, Fasy TM, Novick KE, Monestier M. Monoclonal autoantibodies to subnucleosomes from a MRL/Mp( − )+/+mouse. Oligoclonality of the antibody response and recognition of a determinant composed of histones H2A, H2B, and DNA. J. Immunol. 1992; 148:1561–1569.
   PubMed Web of Science ®Google Scholar
• Liang Z, Xie C, Chen C, . 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
• 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
• van Es JH, Gmelig Meyling FH, van de Akker WR, . 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
• Radic MZ, Weigert M. Genetic and structural evidence for antigen selection of anti-DNA antibodies. Annu. Rev. Immunol. 1994; 12:487–520.
   PubMed Web of Science ®Google Scholar
• Radic MZ, Mackle J, Erikson J, . Residues that mediate DNA binding of autoimmune antibodies. J. Immunol. 1993; 150:4966–4977.
   PubMed Web of Science ®Google Scholar
• Haley J, Mason LJ, Nagl S, . Somatic mutations to arginine residues affect the binding of human monoclonal antibodies to DNA, histones, SmD and Ro antigen. Mol. Immunol. 2004; 40:745–758.
   PubMedGoogle Scholar
• Siekevitz M, Kocks C, Rajewsky K, Dildrop R. Analysis of somatic mutation and class switching in naive and memory B cells generating adoptive primary and secondary responses. Cell. 1987; 48:757–770.
   PubMed Web of Science ®Google Scholar
• Caton AJ, Brownlee GG, Staudt LM, Gerhard W. Structural and functional implications of a restricted antibody response to a defined antigenic region on the influenza virus hemagglutinin. EMBO J. 1986; 5:1577–1587.
   PubMedGoogle Scholar
• Clarke SH, Huppi K, Ruezinsky D, . Inter- and intraclonal diversity in the antibody response to influenza hemagglutinin. J. Exp. Med. 1985; 161:687–704.
   PubMed Web of Science ®Google Scholar
• Liu YJ, Joshua DE, Williams GT, . Mechanism of antigen-driven selection in germinal centres. Nature. 1989; 342:929–931.
   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
• Kuppers R, Zhao M, Hansmann ML, Rajewsky K. Tracing B cell development in human germinal centres by molecular analysis of single cells picked from histological sections. EMBO J. 1993; 12:4955–4967.
   PubMed Web of Science ®Google Scholar
• Herlands RA, William J, Hershberg U, Shlomchik MJ. Anti-chromatin antibodies drive in vivo antigen-specific activation and somatic hypermutation of rheumatoid factor B cells at extrafollicular sites. Eur. J. Immunol. 2007; 37:3339–3351.
   PubMed Web of Science ®Google Scholar
• William J, Euler C, Christensen S, Shlomchik MJ. Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science. 2002; 297:2066–2070.
   PubMed Web of Science ®Google Scholar
• Tiller T, Kofer J, Kreschel C, . Development of self-reactive germinal center B cells and plasma cells in autoimmune Fc gammaRIIB-deficient mice. J. Exp. Med. 2010; 207:2767–2778.
   PubMed Web of Science ®Google Scholar
• Wellmann U, Letz M, Herrmann M, . The evolution of human anti-double-stranded DNA autoantibodies. Proc Natl Acad Sci USA. 2005; 102:9258–9263.
   PubMed Web of Science ®Google Scholar
• Mietzner B, Tsuiji M, Scheid J, . Autoreactive IgG memory antibodies in patients with systemic lupus erythematosus arise from nonreactive and polyreactive precursors. Proc Natl Acad Sci USA. 2008; 105:9727–9732.
   PubMed Web of Science ®Google Scholar
• Guo W, Smith D, Aviszus K, . 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
• Di Zenzo G, Di Lullo G, Corti D, . Pemphigus autoantibodies generated through somatic mutations target the desmoglein-3 cis-interface. J. Clin. Invest. 2012; 122:3781–3790.
   PubMed Web of Science ®Google Scholar
• Schulze C, Munoz LE, Franz S, . Clearance deficiency—A potential link between infections and autoimmunity. Autoimmun. Rev. 2008; 8:5–8.
   PubMed Web of Science ®Google Scholar
• Diamond B, Scharff MD. Somatic mutation of the T15 heavy chain gives rise to an antibody with autoantibody specificity. Proc. Natl. Acad. Sci. USA. 1984; 81:5841–5844.
   PubMed Web of Science ®Google Scholar
• Ray SK, Putterman C, Diamond B. Pathogenic autoantibodies are routinely generated during the response to foreign antigen: a paradigm for autoimmune disease. Proc. Natl. Acad. Sci. USA. 1996; 93:2019–2024.
   PubMed Web of Science ®Google Scholar
• Rogozin IB, Kolchanov NA. Somatic hypermutagenesis in immunoglobulin genes. II. Influence of neighbouring base sequences on mutagenesis. Biochim. Biophys. Acta. 1992; 1171:11–18.
   PubMedGoogle Scholar
• Martin A, Scharff MD. Somatic hypermutation of the AID transgene in B and non-B cells. Proc Natl Acad Sci USA. 2002; 99:12304–12308.
   PubMed Web of Science ®Google Scholar
• Jiang C, Foley J, Clayton N, . Abrogation of lupus nephritis in activation-induced deaminase-deficient MRL/lpr mice. J. Immunol. 2007; 178:7422–7431.
   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
• Zan H, Zhang J, Ardeshna S, . Lupus-prone MRL/faslpr/lpr mice display increased AID expression and extensive DNA lesions, comprising deletions and insertions, in the immunoglobulin locus: concurrent upregulation of somatic hypermutation and class switch DNA recombination. Autoimmunity. 2009; 42:89–103.
   PubMed Web of Science ®Google Scholar
• Casciola-Rosen LA, Anhalt G, Rosen A. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 1994; 179:1317–1330.
   PubMed Web of Science ®Google Scholar
• Baumann I, Kolowos W, Voll RE, . Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum. 2002; 46:191–201.
   PubMed Web of Science ®Google Scholar
• Napirei M, Karsunky H, Zevnik B, . Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet. 2000; 25:177–181.
   PubMed Web of Science ®Google Scholar
• Al-Mayouf SM, Sunker A, Abdwani R, . Loss-of-function variant in DNASE1L3 causes a familial form of systemic lupus erythematosus. Nat. Genet. 2011; 43:1186–1188.
   PubMed Web of Science ®Google Scholar
• Hanayama R, Tanaka M, Miyasaka K, . Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science. 2004; 304:1147–1150.
   PubMed Web of Science ®Google Scholar
• Kranich J, Krautler N, Heinen E, . Follicular dendritic cells control engulfment of apoptotic bodies by secreting Mfge8. J. Exp. Med. 2008; 205:1293–1302.
   PubMed Web of Science ®Google Scholar
• Taylor PR, Carugati A, Fadok VA, . A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J. Exp. Med. 2000; 192:359–366.
   PubMed Web of Science ®Google Scholar
• Cohen PL, Caricchio R, Abraham V, . Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med. 2002; 196:135–140.
   PubMed Web of Science ®Google Scholar
• Munoz LE, Janko C, Chaurio RA, . IgG opsonized nuclear remnants from dead cells cause systemic inflammation in SLE. Autoimmunity. 2010; 43:232–235.
   PubMed Web of Science ®Google Scholar
• Crotty S. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol.. 2011; 29:621–663.
   PubMed Web of Science ®Google Scholar
• Vinuesa CG, Cook MC, Angelucci C, . A RING-type ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity. Nature. 2005; 435:452–458.
   PubMed Web of Science ®Google Scholar
• Simpson N, Gatenby PA, Wilson A, . Expansion of circulating T cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of severe systemic lupus erythematosus. Arthritis Rheum. 2010; 62:234–244.
   PubMed Web of Science ®Google Scholar
• Zinkernagel RM, Cooper S, Chambers J, . Virus-induced autoantibody response to a transgenic viral antigen. Nature. 1990; 345:68–71.
   PubMedGoogle Scholar
• Hou B, Saudan P, Ott G, . Selective utilization of toll-like receptor and MyD88 signaling in B cells for enhancement of the antiviral germinal center response. Immunity. 2011; 34:375–384.
   PubMed Web of Science ®Google Scholar
• Eilat D, Wabl M. B cell tolerance and positive selection in lupus. J. Immunol. 2012; 189:503–509.
   PubMedGoogle Scholar