Association of Defective Regulation of Autoreactive Interleukin-6–Producing Transitional B Lymphocytes With Disease in Patients With Systemic Sclerosis

Arthritis and Rheumatology

Volumn 70, Issue 3, 2018, Pages 450-461

  Taher, Taher E ^a,b   Ong, Voon H ^c   Bystrom, Jonas ^a   Hillion, Sophie ^d   Simon, Quentin ^d   Denton, Christopher P ^c   Pers, Jacques Olivier ^d   Abraham, David J ^c   Mageed, Rizgar A ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITÉ DE BRETAGNE OCCIDENTALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADP RIBOSYL CYCLASE/CYCLIC ADP RIBOSE HYDROLASE 1; ANTINUCLEAR ANTIBODY; AUTOANTIBODY; B LYMPHOCYTE RECEPTOR; CD24 ANTIGEN; CD27 ANTIGEN; CD32 ANTIGEN; CENTROMERE ANTIBODY; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; JO 1 ANTIBODY; RIBONUCLEOPROTEIN ANTIBODY; RNA POLYMERASE; SCL 70 ANTIBODY; CYTOKINE;

ADULT; ANTIBODY PRODUCTION; APOPTOSIS; ARTICLE; B LYMPHOCYTE ACTIVATION; B LYMPHOCYTE SUBPOPULATION; CELLULAR DISTRIBUTION; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE DURATION; EX VIVO STUDY; FEMALE; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOGENESIS; IMMUNOREACTIVITY; IMMUNOREGULATION; IMMUNOSTIMULATION; INNATE IMMUNITY; INTRACELLULAR SIGNALING; LYMPHOCYTE FUNCTION; MAJOR CLINICAL STUDY; MALE; MEMORY CELL; MIDDLE AGED; PRE B LYMPHOCYTE; PRIORITY JOURNAL; SYSTEMIC SCLEROSIS; AGED; B LYMPHOCYTE; FLOW CYTOMETRY; IMMUNOLOGY; METABOLISM;

ADULT; AGED; AUTOANTIBODIES; B-LYMPHOCYTES; CYTOKINES; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; MIDDLE AGED; SCLERODERMA, SYSTEMIC;

EID: 85041598565     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.40390     Document Type: Article

References (47)

1. LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger TA Jr, et al. Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 1988;15:202–5.
2. Abraham DJ, Varga J. Scleroderma: from cell and molecular mechanisms to disease models. Trends Immunol 2005;26:587–95.
3. Feghali-Bostwick C, Medsger TA Jr, Wright TM. Analysis of systemic sclerosis in twins reveals low concordance for disease and high concordance for the presence of antinuclear antibodies. Arthritis Rheum 2003;48:1956–63.
4. Whitfield ML, Finlay DR, Murray JI, Troyanskaya OG, Chi JT, Pergamenschikov A, et al. Systemic and cell type-specific gene expression patterns in scleroderma skin. Proc Natl Acad Sci U S A 2003;100:12319–24.
5. Lafyatis R, O'Hara C, Feghali-Bostwick CA, Matteson E. B cell infiltration in systemic sclerosis–associated interstitial lung disease. Arthritis Rheum 2007;56:3167–8.
6. Fujimoto M, Sato S. B lymphocytes and systemic sclerosis. Curr Opin Rheumatol 2005;17:746–51.
7. Saito E, Fujimoto M, Hasegawa M, Komura K, Hamaguchi Y, Kaburagi Y, et al. CD19-dependent B lymphocyte signaling thresholds influence skin fibrosis and autoimmunity in the tight-skin mouse. J Clin Invest 2002;109:1453–62.
8. Hasegawa M, Hamaguchi Y, Yanaba K, Bouaziz JD, Uchida J, Fujimoto M, et al. B-lymphocyte depletion reduces skin fibrosis and autoimmunity in the tight-skin mouse model for systemic sclerosis. Am J Pathol 2006;169:954–66.
9. Yoshizaki A, Iwata Y, Komura K, Ogawa F, Hara T, Muroi E, et al. CD19 regulates skin and lung fibrosis via Toll-like receptor signaling in a model of bleomycin-induced scleroderma. Am J Pathol 2008;172:1650–63.
10. Lafyatis R, Kissin E, York M, Farina G, Viger K, Fritzler MJ, et al. B cell depletion with rituximab in patients with diffuse cutaneous systemic sclerosis. Arthritis Rheum 2009;60:578–83.
11. Smith V, van Praet JT, Vandooren B, van der Cruyssen B, Naeyaert JM, Decuman S, et al. Rituximab in diffuse cutaneous systemic sclerosis: an open-label clinical and histopathological study. Ann Rheum Dis 2010;69:193–7.
12. Asano N, Fujimoto M, Yazawa N, Shirasawa S, Hasegawa M, Okochi H, et al. B lymphocyte signaling established by the CD19/CD22 loop regulates autoimmunity in the tight-skin mouse. Am J Pathol 2004;165:641–50.
13. Daoussis D, Liossis SN, Tsamandas AC, Kalogeropoulou C, Kazantzi A, Sirinian C, et al. Experience with rituximab in scleroderma: results from a 1-year, proof-of-principle study. Rheumatology (Oxford) 2010;49:271–80.
14. Daoussis D, Liossis SN, Tsamandas AC. Efficacy and safety of rituximab in patients with diffuse scleroderma. Rheumatol Int 2011;31:841–2.
15. Jordan S, Distler JH, Maurer B, Huscher D, van Laar JM, Allanore Y, et al. Effects and safety of rituximab in systemic sclerosis: an analysis from the European Scleroderma Trial and Research (EUSTAR) group. Ann Rheum Dis 2015;74:1188–94.
16. Carsetti R, Kohler G, Lamers MC. Transitional B cells are the target of negative selection in the B cell compartment. J Exp Med 1995;181:2129–40.
17. Loder F, Mutschler B, Ray RJ, Paige CJ, Sideras P, Torres R, et al. B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J Exp Med 1999;190:75–89.
18. Simon Q, Pers JO, Cornec D, le Pottier L, Mageed RA, Hillion S. In-depth characterization of CD24CD38 transitional human B cells reveals different regulatory profiles. J Allergy Clin Immunol 2016;137:1577–84.
19. Barr TA, Shen P, Brown S, Lampropoulou V, Roch T, Lawrie S, et al. B cell depletion therapy ameliorates autoimmune disease through ablation of IL-6-producing B cells. J Exp Med 2012;209:1001–10.
20. Barr TA, Brown S, Ryan G, Zhao J, Gray D. TLR-mediated stimulation of APC: Distinct cytokine responses of B cells and dendritic cells. Eur J Immunol 2007;37:3040–53.
21. Van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A, et al. 2013 classification criteria for systemic sclerosis: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 2013;65:2737–47.
22. Lynch BM, Stern EP, Ong V, Harber M, Burns A, Denton CP. UK Scleroderma Study Group (UKSSG) guidelines on the diagnosis and management of scleroderma renal crisis. Clin Exp Rheumatol 2016;34 Suppl 100:106–9.
23. Alzabin S, Abraham SM, Taher TE, Palfreeman A, Hull D, McNamee K, et al. Incomplete response of inflammatory arthritis to TNFα blockade is associated with the Th17 pathway. Ann Rheum Dis 2012;71:1741–8.
24. Denton CP, Hughes M, Gak N, Vila J, Buch MH, Chakravarty K, et al. BSR and BHPR guideline for the treatment of systemic sclerosis. Rheumatology (Oxford) 2016;55:1906–10.
25. hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity 2010;32:129–40.
26. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat Immunol 2002;3:944–50.
27. De Valle E, Grigoriadis G, O'Reilly LA, Willis SN, Maxwell MJ, Corcoran LM, et al. NFκB1 is essential to prevent the development of multiorgan autoimmunity by limiting IL-6 production in follicular B cells. J Exp Med 2016;213:621–41.
28. Cuss AK, Avery DT, Cannons JL, Yu LJ, Nichols KE, Shaw PJ, et al. Expansion of functionally immature transitional B cells is associated with human-immunodeficient states characterized by impaired humoral immunity. J Immunol 2006;176:1506–16.
29. Suryani S, Fulcher DA, Santner-Nanan B, Nanan R, Wong M, Shaw PJ, et al. Differential expression of CD21 identifies developmentally and functionally distinct subsets of human transitional B cells. Blood 2010;115:519–29.
30. Ueda Y, Liao D, Yang K, Patel A, Kelsoe G. T-independent activation-induced cytidine deaminase expression, class-switch recombination, and antibody production by immature/transitional 1 B cells. J Immunol 2007;178:3593–601.
31. Hildebrandt S, Weiner ES, Senecal JL, Noell GS, Earnshaw WC, Rothfield NF. Autoantibodies to topoisomerase I (Scl-70): analysis by gel diffusion, immunoblot, and enzyme-linked immunosorbent assay. Clin Immunol Immunopathol 1990;57:399–410.
32. Shah HB, Koelsch KA. B-cell ELISPOT: for the identification of antigen-specific antibody-secreting cells. Methods Mol Biol 2015;1312:419–26.
33. Ohashi PS, DeFranco AL. Making and breaking tolerance. Curr Opin Immunol 2002;14:744–59.
34. Su TT, Rawlings DJ. Transitional B lymphocyte subsets operate as distinct checkpoints in murine splenic B cell development. J Immunol 2002;168:2101–10.
35. Allman D, Lindsley RC, DeMuth W, Rudd K, Shinton SA, Hardy RR. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J Immunol 2001;167:6834–40.
36. Merrell KT, Benschop RJ, Gauld SB, Aviszus K, Decote-Ricardo D, Wysocki LJ, et al. Identification of anergic B cells within a wild-type repertoire. Immunity 2006;25:953–62.
37. Neurath MF, Finotto S. IL-6 signaling in autoimmunity, chronic inflammation and inflammation-associated cancer. Cytokine Growth Factor Rev 2011;22:83–9.
38. + T cell-mediated suppression by dendritic cells. Science 2003;299:1033–6.
39. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006;441:235–8.
40. Serada S, Fujimoto M, Mihara M, Koike N, Ohsugi Y, Nomura S, et al. IL-6 blockade inhibits the induction of myelin antigen-specific Th17 cells and Th1 cells in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 2008;105:9041–6.
41. Lundy SK. Killer B lymphocytes: the evidence and the potential. Inflamm Res 2009;58:345–57.
42. Yanaba K, Bouaziz JD, Matsushita T, Tsubata T, Tedder TF. The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol 2009;182:7459–72.
43. Wardemann H, Yurasov S, Schaefer A, Young JW, Meffre E, Nussenzweig MC. Predominant autoantibody production by early human B cell precursors. Science 2003;301:1374–7.
44. Samuels J, Ng YS, Coupillaud C, Paget D, Meffre E. Impaired early B cell tolerance in patients with rheumatoid arthritis. J Exp Med 2005;201:1659–67.
45. Yurasov S, Wardemann H, Hammersen J, Tsuiji M, Meffre E, Pascual V, et al. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J Exp Med 2005;201:703–11.
46. Goodnow CC, Sprent J, de St Groth BF, Vinuesa CG. Cellular and genetic mechanisms of self tolerance and autoimmunity. Nature 2005;435:590–7.
47. Shlomchik MJ. Sites and stages of autoreactive B cell activation and regulation. Immunity 2008;28:18–28.