Autoreactive IgG memory antibodies in patients with systemic lupus erythematosus arise from nonreactive and polyreactive precursors

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 28, 2008, Pages 9727-9732

  Mietzner, Brun ^a   Tsuiji, Makoto ^c,f   Scheid, Johannes ^c   Velinzon, Klara ^c   Tiller, Thomas ^a   Abraham, Klaus ^d   Gonzalez, Jose B ^d   Pascual, Virginia ^e   Stichweh, Dorothee ^e   Wardemann, Hedda ^a   Nussenzweig, Michel C ^b,c  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

^f TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Autoimmunity; B cell; Repertoire; Self tolerance

Indexed keywords

AUTOANTIBODY; B LYMPHOCYTE ANTIBODY; CELL NUCLEUS ANTIGEN; IMMUNOGLOBULIN G;

ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; GERM LINE; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MEMORY CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMATIC MUTATION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANTIBODY SPECIFICITY; ANTIGENS, NUCLEAR; AUTOANTIBODIES; AUTOANTIGENS; B-LYMPHOCYTES; HUMANS; IMMUNOGLOBULIN G; IMMUNOLOGIC MEMORY; LUPUS ERYTHEMATOSUS, SYSTEMIC; RIBONUCLEOPROTEINS;

EID: 47749123498     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0803644105     Document Type: Article

References (61)

1. Amanna IJ, Carlson NE, Slifka MK (2007) Duration of humoral immunity to common viral and vaccine antigens. N Engl J Med 357:1903-1915.
2. McHeyzer-Williams LJ, McHeyzer-Williams MG (2005) Antigen-specific memory B cell development. Annu Rev Immunol 23:487-513.
3. Ahmed R, Gray D (1996) Immunological memory and protective immunity: Understanding their relation. Science 272:54-60.
4. Davidson A, Diamond B (2001) Autoimmune diseases. N Engl J Med 345:340-350.
5. Kotzin BL (1996) Systemic lupus erythematosus. Cell 85:303-306.
6. Sherer Y, Gorstein A, Fritzler MJ, Shoenfeld Y (2004) Autoantibody explosion in systemic lupus erythematosus: More than 100 different antibodies found in SLE patients. Semin Arthritis Rheum 34:501-537.
7. Yurasov S, et al. (2006) Persistent expression of autoantibodies in SLE patients in remission. J Exp Med 203:2255-2261.
8. Yurasov S, et al. (2005) Defective B cell tolerance checkpoints in systemic lupus erythematosus. J Exp Med 201:703-711.
9. MacLennan IC (1994) Germinal centers. Annu Rev Immunol 12:117-139.
10. Radbruch A, et al. (2006) Competence and competition: The challenge of becoming a long-lived plasma cell. Nat Rev Immunol 6:741-750.
11. Bernasconi NL, Traggiai E, Lanzavecchia A (2002) Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298:2199-2202.
12. Maruyama M, Lam KP, Rajewsky K (2000) Memory B-cell persistence is independent of persisting immunizing antigen. Nature 407:636-642.
13. Tangye SG, Good KL (2007) Human IgM+CD27+ B cells: memory B cells or "memory" B cells? J Immunol 179:13-19.
14. Arce E, et al. (2001) Increased frequency of pre-germinal center B cells and plasma cell precursors in the blood of children with systemic lupus erythematosus. J Immunol 167:2361-2369.
15. Odendahl M, et al. (2000) Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus. J Immunol 165:5970-5979.
16. Vallerskog T, et al. (2007) Treatment with rituximab affects both the cellular and the humoral arm of the immune system in patients with SLE. Clin Immunol 122:62-74.
17. de Wildt RM, Hoet RM, van Venrooij WJ, Tomlinson IM, Winter G (1999) Analysis of heavy and light chain pairings indicates that receptor editing shapes the human antibody repertoire. J Mol Biol 285:895-901.
18. de Wildt RM, Tomlinson IM, van Venrooij WJ, Winter G, Hoet RM (2000) Comparable heavy and light chain pairings in normal and systemic lupus erythematosus IgG(+) B cells. Eur J Immunol 30:254-261.
19. Dorner T, Lipsky PE (2005) Molecular basis of immunoglobulin variable region gene usage in systemic autoimmunity. Clin Exp Med 4:159-169.
20. Lefranc MP, et al. (2005) IMGT-Choreography for immunogenetics and immunoinformatics. In Silico Biol 5:45-60.
21. Dorner T, Lipsky PE (2001) Immunoglobulin variable-region gene usage in systemic autoimmune diseases. Arthritis Rheum 44:2715-2727.
22. Giachino C, Padovan E, Lanzavecchia A (1995) Kappa+lambda+ dual receptor B cells are present in the human peripheral repertoire. J Exp Med 181:1245-1250.
23. Dorner T, Heimbacher C, Farner NL, Lipsky PE (1999) Enhanced mutational activity of Vkappa gene rearrangements in systemic lupus erythematosus. Clin Immunol 92:188-196.
24. Tiller T, et al. (2007) Autoreactivity in human IgG(+) memory B cells. Immunity 26:205-213.
25. Koelsch K, et al. (2007) Mature B cells class switched to IgD are autoreactive in healthy individuals. J Clin Invest 117:1558-1565.
26. Wardemann H, et al. (2003) Predominant autoantibody production by early human B cell precursors. Science 301:1374-1377.
27. Tiller T, et al. (2007) Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods.
28. Herve M, et al. (2005) Unmutated and mutated chronic lymphocytic leukemia derive from self-reactive B cell precursors despite expressing different antibody reactivity. J Clin Invest 115:1636-1643.
29. Tsuiji M, et al. (2006) A checkpoint for autoreactivity in human IgM+ memory B cell development. J Exp Med 203:393-400.
30. Bensimon C, Chastagner P, Zouali M (1994) Human lupus anti-DNA autoantibodies undergo essentially primary V kappa gene rearrangements. EMBO J 13:2951-2962.
31. Manheimer-Lory AJ, Zandman-Goddard G, Davidson A, Aranow C, Diamond B (1997) Lupus-specific antibodies reveal an altered pattern of somatic mutation. J Clin Invest 100:2538-2546.
32. Pugh-Bernard AE, et al. (2001) Regulation of inherently autoreactive VH4-34 B cells in the maintenance of human B cell tolerance. J Clin Invest 108:1061-1070.
33. Suzuki N, Harada T, Mihara S, Sakane T (1996) Characterization of a germline Vk gene encoding cationic anti-DNA antibody and role of receptor editing for development of the autoantibody in patients with systemic lupus erythematosus. J Clin Invest 98:1843-1850.
34. Gay D, Saunders T, Camper S, Weigert M (1993) Receptor editing: An approach by autoreactive B cells to escape tolerance. J Exp Med 177:999-1008.
35. Retter MW, Nemazee D (1998) Receptor editing occurs frequently during normal B cell development. J Exp Med 188:1231-1238.
36. Tiegs SL, Russell DM, Nemazee D (1993) Receptor editing in self-reactive bone marrow B cells. J Exp Med 177:1009-1020.
37. Li Y, Louzoun Y, Weigert M (2004) Editing anti-DNA B cells by Vlambdax. J Exp Med 199:337-346.
38. Witsch EJ, Cao H, Fukuyama H, Weigert M (2006) Light chain editing generates polyreactive antibodies in chronic graft-versus-host reaction. J Exp Med 203:1761-1772.
39. Casellas R, et al. (2007) Igkappa allelic inclusion is a consequence of receptor editing. J Exp Med 204:153-160.
40. Li Y, Li H, Weigert M (2002) Autoreactive B cells in the marginal zone that express dual receptors. J Exp Med 195:181-188.
41. Pelanda R, Torres RM (2006) Receptor editing for better or for worse. Curr Opin Immunol 18:184-190.
42. Doyle CM, Han J, Weigert MG, Prak ET (2006) Consequences of receptor editing at the lambda locus: Multireactivity and light chain secretion. Proc Natl Acad Sci USA 103:11264-11269.
43. Gerdes T, Wabl M (2004) Autoreactivity and allelic inclusion in a B cell nuclear transfer mouse. Nat Immunol 5:1282-1287.
44. Liu S, et al. (2005) Receptor editing can lead to allelic inclusion and development of B cells that retain antibodies reacting with high avidity autoantigens. J Immunol 175:5067-5076.
45. Velez MG, et al. (2007) Ig allotypic inclusion does not prevent B cell development or response. J Immunol 179:1049-1057.
46. Herve M, et al. (2007) CD40 ligand and MHC class II expression are essential for human peripheral B cell tolerance. J Exp Med 204:1583-1593.
47. Foster SJ, Brezinschek HP, Brezinschek RI, Lipsky PE (1997) Molecular mechanisms and selective influences that shape the kappa gene repertoire of IgM+ B cells. J Clin Invest 99:1614-1627.
48. Jacobi AM, Hansen A, Burmester GR, Dorner T, Lipsky PE (2000) Enhanced mutational activity and disturbed selection of mutations in V(H) gene rearrangements in a patient with systemic lupus erythematosus. Autoimmunity 33:61-76.
49. Radic MZ, et al. (1993) Residues that mediate DNA binding of autoimmune antibodies. J Immunol 150:4966-4977.
50. Cocca BA, et al. (2001) Structural basis for autoantibody recognition of phosphatidylserine-beta 2 glycoprotein I and apoptotic cells. Proc Natl Acad Sci USA 98:13826-13831.
51. Li H, et al. (2003) Regulation of anti-phosphatidylserine antibodies. Immunity 18:185-192.
52. Radic MZ, Weigert M (1994) Genetic and structural evidence for antigen selection of anti-DNA antibodies. Annu Rev Immunol 12:487-520.
53. Wellmann U, et al. (2005) The evolution of human anti-double-stranded DNA autoantibodies. Proc Natl Acad Sci USA 102:9258-9263.
54. Leandro MJ, Cambridge G, Edwards JC, Ehrenstein MR, Isenberg DA (2005) B-cell depletion in the treatment of patients with systemic lupus erythematosus: A longitudinal analysis of 24 patients. Rheumatology 44:1542-1545.
55. NgKP, et al. (2007) B cell depletion therapy in systemic lupus erythematosus: Long-term follow-up and predictors of response. Ann Rheum Dis 66:1259-1262.
56. Arpin C, Banchereau J, Liu YJ (1997) Memory B cells are biased towards terminal differentiation: A strategy that may prevent repertoire freezing. J Exp Med 186:931-940.
57. Lanzavecchia A, et al. (2006) Understanding and making use of human memory B cells. Immunol Rev 211:303-309.
58. Anolik JH, et al. (2007) Delayed memory B cell recovery in peripheral blood and lymphoid tissue in systemic lupus erythematosus after B cell depletion therapy. Arthritis Rheum 56:3044-3056.
59. Leandro MJ, Cambridge G, Ehrenstein MR, Edwards JC (2006) Reconstitution of peripheral blood B cells after depletion with rituximab in patients with rheumatoid arthritis. Arthritis Rheum 54:613-620.
60. Edwards JC, et al. (2004) Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 350:2572-2581.
61. Meffre E, et al. (2004) Surrogate light chain expressing human peripheral B Cells produce self-reactive antibodies. J Exp Med 199:145-150.