Rheumatoid arthritis synovial tissue harbours dominant B-cell and plasma-cell clones associated with autoreactivity

Annals of the Rheumatic Diseases

Volumn 73, Issue 4, 2014, Pages 756-762

  Doorenspleet, M E ^a   Klarenbeek, P L ^a   De Hair, M J H D ^a   Van Schaik, B D C ^b   Esveldt, R E E ^a   Van Kampen, A H C ^b,c   Gerlag, D M ^a   Musters, A ^a   Baas, F ^a   Tak, P P ^a   De Vries, N ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN M; MESSENGER RNA;

ARTICLE; B LYMPHOCYTE; BLOOD SAMPLING; CELL EXPANSION; CLINICAL ARTICLE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOGLOBULIN HEAVY CHAIN GENE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CLONE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RHEUMATOID ARTHRITIS; RNA SEQUENCE; SIGNAL TRANSDUCTION; SYNOVIUM;

B CELLS; EARLY RHEUMATOID ARTHRITIS; RHEUMATOID ARTHRITIS; SYNOVITIS;

AMINO ACID SEQUENCE; ARTHRITIS, RHEUMATOID; AUTOIMMUNITY; B-LYMPHOCYTES; CLONE CELLS; COMPLEMENTARITY DETERMINING REGIONS; FEMALE; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; LYMPHOCYTE ACTIVATION; MALE; MOLECULAR SEQUENCE DATA; PLASMA CELLS; SEVERITY OF ILLNESS INDEX; SYNOVIAL MEMBRANE;

EID: 84895454215     PISSN: 00034967     EISSN: 14682060     Source Type: Journal    
DOI: 10.1136/annrheumdis-2012-202861     Document Type: Article

References (50)

1. Franciotta D, Salvetti M, Lolli F, et al. B cells and multiple sclerosis. Lancet Neurol 2008;7:852-8.
2. Fraussen J, Vrolix K, Martinez-Martinez P, et al. B cell characterization and reactivity analysis in multiple sclerosis. Autoimmun Rev 2009;8:654-8.
3. Hu CY, Rodriguez-Pinto D, Du W, et al. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J Clin Invest 2007;117:3857-67. (Pubitemid 350224095)
4. Serreze DV, Chapman HD, Varnum DS, et al. B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new "speed congenic" stock of NOD. Ig mu null mice. J Exp Med 1996;184:2049-53. (Pubitemid 26404497)
5. Cohen SB, Emery P, Greenwald MW, et al. Rituximab for rheumatoid Arthritis Refractory to anti-tumor necrosis factor therapy: results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum 2006;54:2793-806. (Pubitemid 44497758)
6. Edwards JC, Szczepanski L, Szechinski J, et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004;350:2572-81. (Pubitemid 38758544)
7. Emery P, Fleischmann R, Filipowicz-Sosnowska A, et al. The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, dose-ranging trial. Arthritis Rheum 2006;54:1390-400.
8. Hauser SL, Waubant E, Arnold DL, et al. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N Engl J Med 2008;358:676-88. (Pubitemid 351240747)
9. Tamimoto Y, Horiuchi T, Tsukamoto H, et al. A dose-escalation study of rituximab for treatment of systemic lupus erythematosus and Evans' syndrome: immunological analysis of B cells, T cells and cytokines. Rheumatology (Oxford) 2008;47:821-7. (Pubitemid 351796367)
10. Vigna-Perez M, Hernandez-Castro B, Paredes-Saharopulos O, et al. Clinical and immunological effects of Rituximab in patients with lupus nephritis refractory to conventional therapy: a pilot study. Arthritis Res Ther 2006;8:R83.
11. Leandro MJ, Cambridge G, Ehrenstein MR, et al. Reconstitution of peripheral blood B cells after depletion with rituximab in patients with rheumatoid arthritis. Arthritis Rheum 2006;54:613-20. (Pubitemid 43228639)
12. Klarenbeek PL, de Hair MJ, Doorenspleet ME, et al. Inflamed target tissue provides a specific niche for highly expanded T-cell clones in early human autoimmune disease. Ann Rheum Dis 2012;71:1088-93.
13. Cantaert T, Doorenspleet ME, Francosalinas G, et al. Increased numbers of CD5+ B lymphocytes with a regulatory phenotype in spondylarthritis. Arthritis Rheum 2012;64:1859-68.
14. Freeman JD, Warren RL, Webb JR, et al. Profiling the T-cell receptor beta-chain repertoire by massively parallel sequencing. Genome Res 2009;19:1817-24.
15. Robins HS, Campregher PV, Srivastava SK, et al. Comprehensive assessment of T-cell receptor beta-chain diversity in alphabeta T cells. Blood 2009;114:4099-107.
16. Weinstein JA, Jiang N, White RA III, et al. High-throughput sequencing of the zebrafish antibody repertoire. Science 2009;324:807-10.
17. Maillette de Buy Wenniger LJ, Doorenspleet ME, Klarenbeek PL, et al. IgG4+ clones identified by next-generation sequencing dominate the b-cell receptor repertoire in IgG4-associated cholangitis. Hepatology Published Onine First: 8 Jan 2013. doi:10.1002/hep. 26232
18. Shan H, Shlomchik MJ, Marshak-Rothstein A, et al. The mechanism of autoantibody production in an autoimmune MRL/lpr mouse. J Immunol 1994;153:5104-20. (Pubitemid 24356141)
19. Shlomchik M, Mascelli M, Shan H, et al. Anti-DNA antibodies from autoimmune mice arise by clonal expansion and somatic mutation. J Exp Med 1990;171:265-92.
20. Gause A, Gundlach K, Zdichavsky M, et al. The B lymphocyte in rheumatoid arthritis: analysis of rearranged V kappa genes from B cells infiltrating the synovial membrane. Eur J Immunol 1995;25:2775-82.
21. Marion TN, Bothwell AL, Briles DE, et al. IgG anti-DNA autoantibodies within an individual autoimmune mouse are the products of clonal selection. J Immunol 1989;142:4269-74. (Pubitemid 19162312)
22. Randen I, Thompson KM, Thorpe SJ, et al. Human monoclonal IgG rheumatoid factors from the synovial tissue of patients with rheumatoid arthritis. Scand J Immunol 1993;37:668-72. (Pubitemid 23181490)
23. Scheel T, Gursche A, Zacher J, et al. V-region gene analysis of locally defined synovial B and plasma cells reveals selected B cell expansion and accumulation of plasma cell clones in rheumatoid arthritis. Arthritis Rheum 2011;63:63-72.
24. Schroder AE, Greiner A, Seyfert C, et al. Differentiation of B cells in the nonlymphoid tissue of the synovial membrane of patients with rheumatoid arthritis. Proc Natl Acad Sci USA 1996;93:221-5. (Pubitemid 26038131)
25. Shlomchik MJ, Marshak-Rothstein A, Wolfowicz CB, et al. The role of clonal selection and somatic mutation in autoimmunity. Nature 1987;328:805-11. (Pubitemid 17118532)
26. Winkler TH, Fehr H, Kalden JR. Analysis of immunoglobulin variable region genes from human IgG anti-DNA hybridomas. Eur J Immunol 1992;22:1719-28.
27. Pugh-Bernard AE, Silverman GJ, Cappione AJ, et al. Regulation of inherently autoreactive VH4-34 B cells in the maintenance of human B cell tolerance. J Clin Invest 2001;108:1061-70. (Pubitemid 32946080)
28. Wardemann H, Yurasov S, Schaefer A, et al. Predominant autoantibody production by early human B cell precursors. Science 2003;301:1374-7. (Pubitemid 37075812)
29. Arnett FC, Edworthy SM, Bloch DA, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988;31:315-24. (Pubitemid 18091653)
30. Gerlag DM, Tak PP. How to perform and analyse synovial biopsies. Best Pract Res Clin Rheumatol 2009;23:221-32.
31. Klarenbeek PL, Tak PP, van Schaik BD, et al. Human T-cell memory consists mainly of unexpanded clones. Immunol Lett 2010;133:42-8.
32. Keats JJ, Reiman T, Maxwell CA, et al. In multiple myeloma, t (4;14) (p16;q32) is an adverse prognostic factor irrespective of FGFR3 expression. Blood 2003;101:1520-9. (Pubitemid 36182529)
33. Aarts WM, Willemze R, Bende RJ, et al. VH gene analysis of primary cutaneous B-cell lymphomas: evidence for ongoing somatic hypermutation and isotype switching. Blood 1998;92:3857-64. (Pubitemid 28525212)
34. van Dongen JJ, Langerak AW, Bruggemann M, et al. Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98-3936. Leukemia 2003;17:2257-317. (Pubitemid 38072572)
35. Giudicelli V, Chaume D, Lefranc MP. IMGT/GENE-DB: a comprehensive database for human and mouse immunoglobulin and T cell receptor genes. Nucleic Acids Res 2005;33:D256-61. (Pubitemid 40207873)
36. Aguilera I, Melero J, Nunez-Roldan A, et al. Molecular structure of eight human autoreactive monoclonal antibodies. Immunology 2001;102:273-80. (Pubitemid 32281154)
37. Crouzier R, Martin T, Pasquali JL. Heavy chain variable region, light chain variable region, and heavy chain CDR3 influences on the mono- and polyreactivity and on the affinity of human monoclonal rheumatoid factors. J Immunol 1995;154:4526-35.
38. Ichiyoshi Y, Casali P. Analysis of the structural correlates for antibody polyreactivity by multiple reassortments of chimeric human immunoglobulin heavy and light chain V segments. J Exp Med 1994;180:885-95. (Pubitemid 24256601)
39. Klonowski KD, Primiano LL, Monestier M. Atypical VH-D-JH rearrangements in newborn autoimmune MRL mice. J Immunol 1999;162:1566-72. (Pubitemid 29307030)
40. Itoh K, Patki V, Furie RA, et al. Clonal expansion is a characteristic feature of the B-cell repetoire of patients with rheumatoid arthritis. Arthritis Res 2000;2:50-8. (Pubitemid 32223700)
41. Voswinkel J, Weisgerber K, Pfreundschuh M, et al. The B lymphocyte in rheumatoid arthritis: recirculation of B lymphocytes between different joints and blood. Autoimmunity 1999;31:25-34. (Pubitemid 32457782)
42. Eckmann L, Huang GT, Smith JR, et al. Increased transcription and coordinate stabilization of mRNAs for secreted immunoglobulin alpha heavy chain and kappa light chain following stimulation of immunoglobulin A expressing B cells. J Biol Chem 1994;269:33102-8.
43. Xiang SD, Benson EM, Dunn IS. Tracking membrane and secretory immunoglobulin alpha heavy chain mRNA variation during B-cell differentiation by real-time quantitative polymerase chain reaction. Immunol Cell Biol 2001;79:472-81. (Pubitemid 34225142)
44. Mcgee B, Small RE, Singh R, et al. B lymphocytic clonal expansion in rheumatoid arthritis. J Rheumatol 1996;23:36-43. (Pubitemid 26037211)
45. Williams DG, Taylor PC. Clonal analysis of immunoglobulin mRNA in rheumatoid arthritis synovium: characterization of expanded IgG3 populations. Eur J Immunol 1997;27:476-85. (Pubitemid 27085253)
46. Monach PA, Hueber W, Kessler B, et al. A broad screen for targets of immune complexes decorating arthritic joints highlights deposition of nucleosomes in rheumatoid arthritis. Proc Natl Acad Sci USA 2009;106:15867-72.
47. Sokolove J, Bromberg R, Deane KD, et al. Autoantibody epitope spreading in the pre-clinical phase predicts progression to rheumatoid arthritis. PLoS ONE 2012;7:e35296.
48. van de Stadt LA, de Koning MH, van de Stadt RJ, et al. Development of the anti-citrullinated protein antibody repertoire prior to the onset of rheumatoid arthritis. Arthritis Rheum 2011;63:3226-33.
49. van der Woude D, Rantapaa-Dahlqvist S, Ioan-Facsinay A, et al. Epitope spreading of the anti-citrullinated protein antibody response occurs before disease onset and is associated with the disease course of early arthritis. Ann Rheum Dis 2010;69:1554-61.
50. Larman HB, Zhao Z, Laserson U, et al. Autoantigen discovery with a synthetic human peptidome. Nat Biotechnol 2011;29:535-41.