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

Autoimmunity

Volumn 46, Issue 2, 2013, Pages 121-127

  Schroeder, Kristin ^a,b   Herrmann, Martin ^a   Winkler, Thomas H ^b  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Anti DNA antibodies; Germinal center; Somatic mutation; Systemic lupus erythematosus

Indexed keywords

AUTOANTIBODY; DOUBLE STRANDED DNA ANTIBODY;

ANTIBODY PRODUCTION; GENETIC RISK; GERMINAL CENTER; HUMAN; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGICAL TOLERANCE; LUPUS VULGARIS; NONHUMAN; PATHOGENESIS; REVIEW; SOMATIC HYPERMUTATION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIBODIES, ANTINUCLEAR; ANTIBODY FORMATION; AUTOANTIBODIES; DNA; GERMINAL CENTER; HUMANS; IMMUNE TOLERANCE; IMMUNOGLOBULIN VARIABLE REGION; LUPUS ERYTHEMATOSUS, SYSTEMIC; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

EID: 84873666705     PISSN: 08916934     EISSN: 1607842X     Source Type: Journal    
DOI: 10.3109/08916934.2012.748751     Document Type: Review

References (70)

1. Hochberg, MC. 1997. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40: 1725
2. Tan, EM, AS Cohen, JF Fries, et al. 1982. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25: 1271-1277
3. ter Borg, E, G Horst, E Hummel, P Limburg, and C Kallenberg. 1990. Measurement of increases in antidouble-stranded DNA antibody levels as a predictor of disease exacerbation in systemic lupus erythematosus. A long-term, prospective study. Arthritis Rheum 33: 634-643
4. Ebling, F, and B Hahn. 1980. Restricted subpopulations of DNA antibodies in kidneys of mice with systemic lupus. Comparison of antibodies in serum and renal eluates. Arthritis Rheum 23: 392-403
5. Ehrenstein, MR, DR Katz, MH Griffiths, et al. 1995. Human IgG anti-DNA antibodies deposit in kidneys and induce proteinuria in SCID mice. Kidney Int 48: 705-711
6. Vlahakos, D, M Foster, S Adams, et al. 1992. Anti-DNA antibodies form immune deposits at distinct glomerular and vascular sites. Kidney Int 41: 1690-1700
7. Berland, R, L Fernandez, E Kari, et al. 2006. Toll-like receptor 7-dependent loss of B cell tolerance in pathogenic autoantibody knockin mice. Immunity 25: 429-440
8. Hahn, BH. 1998. Antibodies to DNA. N. Engl. J. Med 338: 1359-1368
9. Deocharan, B, X Qing, J Lichauco, and C Putterman. 2002. Alpha-actinin is a cross-reactive renal target for pathogenic anti-DNA antibodies. J. Immunol 168: 3072-3078
10. Faaber, P, TP Rijke, LB van-de-Putte, PJ Capel, and JH Berden. 1986. Cross-reactivity of human and murine anti-DNA antibodies with heparan sulfate. The major glycosaminoglycan in glomerular basement membranes. J. Clin. Invest 77: 1824-1830
11. Sabbaga, J, SR Line, P Potocnjak, and MP Madaio. 1989. 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 19: 137-143
12. Mortensen, ES, KA Fenton, and OP Rekvig. 2008. Lupus nephritis: the central role of nucleosomes revealed. Am. J. Pathol 172: 275-283
13. Kalaaji, M, E Mortensen, L Jørgensen, R Olsen, and OP Rekvig. 2006. Nephritogenic lupus antibodies recognize glomerular basement membrane-associated chromatin fragments released from apoptotic intraglomerular cells. Am. J. Pathol 168: 1779-1792
14. Munoz, LE, K Lauber, M Schiller, AA Manfredi, and M Herrmann. 2010. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat. Rev. Rheumatol 6: 280-289
15. Munoz, LE, C Janko, GE Grossmayer, et al. 2009. Remnants of secondarily necrotic cells fuel inflammation in systemic lupus erythematosus. Arthritis Rheum 60: 1733-1742
16. Notkins, AL. 2004. Polyreactivity of antibody molecules. Trends Immunol 25: 174-179
17. Naparstek, J, J Andra-Schwartz, T Mauser, et al. 1986. A single germ-line VH gene segment of normal A/J mice encodes auto-antibodies characteristic of systemic lupus erythematosus. J. Exp. Med 164: 614-626
18. Cairns, E, PC Kwong, V Misener, et al. 1989. 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 143: 685-691
19. Dersimonian, H, KP McAdam, C Mackworth-Young, and BD Stollar. 1989. The recurrent expression of variable region segments in human IgM anti-DNA autoantibodies. J. Immunol 142: 4027-4033
20. Wardemann, H, S Yurasov, A Schaefer, et al. 2003. Predominant autoantibody production by early human B cell precursors. Science 301: 1374-1377
21. Tiller, T, M Tsuiji, S Yurasov, et al. 2007. Autoreactivity in human IgG memory B cells. Immunity 26: 205-213
22. Shlomchik, M, M Mascelli, H Shan, et al. 1990. Anti-DNA antibodies from autoimmune mice arise by clonal expansion and somatic mutation. J. Exp. Med 171: 265-292
23. Shlomchik, MJ, AH Aucoin, DS Pisetsky, and MG Weigert. 1987. Structure and function of anti-DNA autoantibodies derived from a single autoimmune mouse. Proc Natl Acad Sci USA 84: 9150-9154
24. Shlomchik, MJ, A Marshak-Rothstein, CB Wolfowicz, TL Rothstein, and MG Weigert. 1987. The role of clonal selection and somatic mutation in autoimmunity. Nature 328: 805-811
25. Tillman, DM, NT Jou, RJ Hill, and TN Marion. 1992. 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 176: 761-779
26. Eilat, D, and R Fischel. 1991. Recurrent utilization of genetic elements in V regions of antinucleic acid antibodies from autoimmune mice. J. Immunol 147: 361-368
27. Bloom, DD, JL Davignon, MW Retter, et al. 1993. V region gene analysis of anti-Sm hybridomas from MRL/Mp-lpr/lpr mice. J. Immunol 150: 1591-1610
28. Losman, MJ, TM Fasy, KE Novick, and M Monestier. 1992. Monoclonal autoantibodies to subnucleosomes from a MRL/Mp(2) /mouse. Oligoclonality of the antibody response and recognition of a determinant composed of histones H2A, H2B, and DNA. J. Immunol 148: 1561-1569
29. Liang, Z, C Xie, C Chen, et al. 2004. Pathogenic profiles and molecular signatures of antinuclear autoantibodies rescued from NZM2410 lupus mice. J. Exp. Med 199: 381-398
30. Winkler, TH, H Fehr, and JR Kalden. 1992. Analysis of immunoglobulin variable region genes from human IgG anti-DNA hybridomas. Eur. J. Immunol 22: 1719-1728
31. van Es, JH, FH Gmelig Meyling, WR van de Akker, et al. 1991. 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 173: 461-470
32. Radic, MZ, and M Weigert. 1994. Genetic and structural evidence for antigen selection of anti-DNA antibodies. Annu. Rev. Immunol 12: 487-520
33. Radic, MZ, J Mackle, J Erikson, et al. 1993. Residues that mediate DNA binding of autoimmune antibodies. J. Immunol 150: 4966-4977
34. Haley, J, LJ Mason, S Nagl, et al. 2004. Somatic mutations to arginine residues affect the binding of human monoclonal antibodies to DNA, histones, SmD and Ro antigen. Mol. Immunol 40: 745-758
35. Siekevitz, M, C Kocks, K Rajewsky, and R Dildrop. 1987. Analysis of somatic mutation and class switching in naive and memory B cells generating adoptive primary and secondary responses. Cell 48: 757-770
36. Caton, AJ, GG Brownlee, LM Staudt, and W Gerhard. 1986. Structural and functional implications of a restricted antibody response to a defined antigenic region on the influenza virus hemagglutinin. EMBO J 5: 1577-1587
37. Clarke, SH, K Huppi, D Ruezinsky, et al. 1985. Inter-and intraclonal diversity in the antibody response to influenza hemagglutinin. J. Exp. Med 161: 687-704
38. Liu, YJ, DE Joshua, GT Williams, et al. 1989. Mechanism of antigen-driven selection in germinal centres. Nature 342: 929-931
39. Berek, C, A Berger, and M Apel. 1991. Maturation of the immune response in germinal centers. Cell 67: 1121-1129
40. Kuppers, R,MZhao, ML Hansmann, and K Rajewsky. 1993. Tracing B cell development in human germinal centres by molecular analysis of single cells picked from histological sections. EMBO J 12: 4955-4967
41. Herlands, RA, J William, U Hershberg, and MJ Shlomchik. 2007. Anti-chromatin antibodies drive in vivo antigen-specific activation and somatic hypermutation of rheumatoid factor B cells at extrafollicular sites. Eur. J. Immunol 37: 3339-3351
42. William, J, C Euler, S Christensen, and MJ Shlomchik. 2002. Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science 297: 2066-2070
43. Tiller, T, J Kofer, C Kreschel, et al. 2010. Development of self-reactive germinal center B cells and plasma cells in autoimmune Fc gammaRIIB-deficient mice. J. Exp.Med 207: 2767-2778
44. Wellmann, U, M Letz, M Herrmann, et al. 2005. The evolution of human anti-double-stranded DNA autoantibodies. Proc Natl Acad Sci USA 102: 9258-9263
45. Mietzner, B, M Tsuiji, J Scheid, et al. 2008. Autoreactive IgG memory antibodies in patients with systemic lupus erythematosus arise from nonreactive and polyreactive precursors. Proc Natl Acad Sci USA 105: 9727-9732
46. Guo, W, D Smith, K Aviszus, et al. 2010. Somatic hypermutation as a generator of antinuclear antibodies in a murine model of systemic autoimmunity. J. Exp. Med 207: 2225-2237
47. Di Zenzo, G, G Di Lullo, D Corti, et al. 2012. Pemphigus autoantibodies generated through somatic mutations target the desmoglein-3 cis-interface. J. Clin. Invest 122: 3781-3790
48. Schulze, C, LE Munoz, S Franz, et al. 2008. Clearance deficiency-A potential link between infections and autoimmunity. Autoimmun. Rev 8: 5-8
49. Diamond, B, and MD Scharff. 1984. Somatic mutation of the T15 heavy chain gives rise to an antibody with autoantibody specificity. Proc. Natl. Acad. Sci. USA 81: 5841-5844
50. Ray, SK, C Putterman, and B Diamond. 1996. Pathogenic autoantibodies are routinely generated during the response to foreign antigen: a paradigm for autoimmune disease. Proc. Natl. Acad. Sci. USA 93: 2019-2024
51. Rogozin, IB, and NA Kolchanov. 1992. Somatic hypermutagenesis in immunoglobulin genes. II. Influence of neighbouring base sequences on mutagenesis. Biochim. Biophys. Acta 1171: 11-18
52. Martin, A, and MD Scharff. 2002. Somatic hypermutation of the AID transgene in B and non-B cells. Proc Natl Acad Sci USA 99: 12304-12308
53. Jiang, C, J Foley, N Clayton, et al. 2007. Abrogation of lupus nephritis in activation-induced deaminase-deficient MRL/lpr mice. J. Immunol 178: 7422-7431
54. Jiang, C, ML Zhao, and M Diaz. 2009. 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 126: 102-113
55. Zan, H, J Zhang, S Ardeshna, et al. 2009. 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 42: 89-103
56. Casciola-Rosen, LA, G Anhalt, and A Rosen. 1994. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med 179: 1317-1330
57. Baumann, I, W Kolowos, RE Voll, et al. 2002. Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum 46: 191-201
58. Napirei, M, H Karsunky, B Zevnik, et al. 2000. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet 25: 177-181
59. Al-Mayouf, SM, A Sunker, R Abdwani, et al. 2011. Loss-offunction variant in DNASE1L3 causes a familial form of systemic lupus erythematosus. Nat. Genet 43: 1186-1188
60. Hanayama, R, M Tanaka, K Miyasaka, et al. 2004. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 304: 1147-1150
61. Kranich, J, N Krautler, E Heinen, et al. 2008. Follicular dendritic cells control engulfment of apoptotic bodies by secreting Mfge8. J. Exp. Med 205: 1293-1302
62. Taylor, PR, A Carugati, VA Fadok, et al. 2000. A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J. Exp. Med 192: 359-366
63. Cohen, PL, R Caricchio, V Abraham, et al. 2002. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med 196: 135-140
64. Munoz, LE, C Janko, RA Chaurio, et al. 2010. IgG opsonized nuclear remnants from dead cells cause systemic inflammation in SLE. Autoimmunity 43: 232-235
65. Crotty, S. 2011. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29: 621-663
66. Vinuesa, CG, MC Cook, C Angelucci, et al. 2005. A RINGtype ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity. Nature 435: 452-458
67. Simpson, N, PA Gatenby, AWilson, et al. 2010. 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 62: 234-244
68. Zinkernagel, RM, S Cooper, J Chambers, et al. 1990. Virusinduced autoantibody response to a transgenic viral antigen. Nature 345: 68-71
69. Hou, B, P Saudan, G Ott, et al. 2011. Selective utilization of toll-like receptor and MyD88 signaling in B cells for enhancement of the antiviral germinal center response. Immunity 34: 375-384
70. Eilat, D, and M Wabl. 2012. B cell tolerance and positive selection in lupus. J. Immunol 189: 503-509