Increased interleukin 21 and follicular helper T-like cells and reduced interleukin 10+ B cells in patients with new-onset systemic lupus erythematosus

Journal of Rheumatology

Volumn 41, Issue 9, 2014, Pages 1781-1792

  Wang, Li ^a   Zhao, Pingwei ^a   Ma, Liang ^a   Shan, Yuxing ^a   Jiang, Zhenyu ^a   Wang, Juan ^a   Jiang, Yanfang ^a  

^a JILIN UNIVERSITY   (China)

Author keywords

B Cells; Follicular Helper T Like Cells; Interleukin 10; Interleukin 21; Regulatory B Cell; Systemic Lupus Erythematosus

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 21; INTERLEUKIN DERIVATIVE;

ADOLESCENT; ADULT; B LYMPHOCYTE; CHILD; FEMALE; HELPER CELL; HUMAN; IMMUNOLOGY; MALE; METABOLISM; MIDDLE AGED; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE SUBPOPULATION; YOUNG ADULT;

ADOLESCENT; ADULT; B-LYMPHOCYTES; CHILD; FEMALE; HUMANS; INTERLEUKIN-10; INTERLEUKINS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER; YOUNG ADULT;

EID: 84906848022     PISSN: 0315162X     EISSN: 14992752     Source Type: Journal    
DOI: 10.3899/jrheum.131025     Document Type: Article

References (43)

1. Kang I, Craft J. The immunology of systemic lupus erythematosus in the autoimmune diseases. In: Rose NR, Mackay IR, eds. The autoimmune diseases. London: Elsevier; 2006;4:357-68.
2. Terrier B, Costedoat-Chalumeau N, Garrido M, Geri G, Rosenzwajg M, Musset L, et al. Interleukin 21 correlates with T cell and B cell subset alterations in systemic lupus erythematosus. J Rheumatol 2012;39:1819-28.
3. Morimoto C, Reinherz EL, Schlossman SF, Schur PH, Mills JA, Steinberg AD. Alterations in immunoregulatory T cell subsets in active systemic lupus erythematosus. J Clin Invest 1980;66:1171-4. (Pubitemid 11233820)
4. Klinman DM, Steinberg AD. Inquiry into murine and human lupus. Immunol Rev 2006;144:157-93.
5. Chan OT, Madaio MP, Shlomchik MJ. The central and multiple roles of B cells in lupus pathogenesis. Immunol Rev 1999;169:107-21. (Pubitemid 29338727)
6. Odendahl M, Jacobi A, Hansen A, Feist E, Hiepe F, Burmester GR, et al. Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus. J Immunol 2000;165:5970-9.
7. LeBien TW, Tedder TF. Blymphocytes: how they develop and function. Blood 2008;112:1570-80.
8. Agematsu K. Memory B-cells and CD27. Histol Histopathol 2005;115:573-6.
9. Belouski SS, Wallace D, Weisman M, Ishimori M, Hendricks L, Zack D, et al. Sample stability and variability of b cell subsets in blood from healthy subjects and patients with systemic lupus erythematosus. Cytometry B Clin Cytom 2010;78:49-58.
10. Arpin C, Déchanet J, Van Kooten C, Merville P, Grouard G, Brière F, et al. Generation of memory B-cells and plasma cells in vitro. Science 1995;268:720-2.
11. Arpin C, Déchanet J, Van Kooten C, Merville P, Grouard G, Brière F, et al. Detection and characterization of plasma cells in peripheral blood: correlation of IgE+ plasma cell frequency with IgE serum titre. Clin Exp Immunol 2002;130:370-8.
12. Ding Q, Yeung M, Camirand G, Zeng Q, Akiba H, Yagita H, et al. Regulatory B cells are identified by expression of TIM-1 and can be induced through TIM-1 ligation to promote tolerance in mice. J Clin Invest 2011;121:3645-56.
13. Chang NH, Tamara M, Gabriel B, Carolina LM, Paul RF, Dafna G, et al. Expanded population of activated antigen-engaged cells within the naive B cell compartment of patients with systemic lupus erythematosus. J Immunol 2012;180:1276-84.
14. Carter NA, Vasconcellos R, Rosser EC, Tulone C, Muñoz-Suano A, Kamanaka M, et al. Mice lacking endogenous IL-10-producing regulatory b cells develop exacerbated disease and present with an increased frequency of Th1/Th17 but a decrease in regulatory T cells. J Immunol 2011;186:5569-79.
15. Carter NA, Rosser EC, Mauri C. IL-10 produced by B cells is crucial for the suppression of Th17/ Th1 responses, induction of Tr1 cells and reduction of collagen-induced arthritis. Arthritis Res Ther 2012;14:R32.
16. Allen CD, Okada T, Cyster JG. Germinal-center organization and cellular dynamics. Immunity 2007;27:190-202. (Pubitemid 47284923)
17. King C, Tangye SG, Mackay CR. T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu Rev Immunol 2008;26:741-66. (Pubitemid 351600391)
18. Fazilleau N, Mark L, McHeyzer-Williams LJ, McHeyzer-Williams MG. Follicular helper T cells: lineage and location. Immunity 2009;30:324-35.
19. McHeyzer-Williams LJ, McHeyzer-Williams M. Antigen-specific memory B cell development. Annu Rev Immunol 2005;23:487-513. (Pubitemid 40563178)
20. Tarlinton D. Germinal centers: form and function. Curr Opin Immunol 1998;10:245-51. (Pubitemid 28286949)
21. Linterman MA, Rigby RJ, Wong RK, Yu D, Brink R, Cannons JL, et al. Follicular helper T cells are required for systemic autoimmunity. J Exp Med 2009;206:561-76.
22. Morita R, Schmitt N, Bentebibel SE, Ranganathan R, Bourdery L, Zurawski G, et al. Human blood CXCR5+ CD4+ T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 2011;34:108-21.
23. Fortin PR, Abrahamowicz M, Ferland D, Lacaille D, Smith CD, Zummer M, et al. Steroid-sparing effects of methotrexate in systemic lupus erythematosus: a double-blind, randomized, placebo-controlled trial. Arthritis Rheum 2008;59:1796-804.
24. Walchner M, Meurer M, Plewig G, Messer G. Clinical and immunologic parameters during thalidomide treatment of lupus erythematosus. Int J Dermatol 2000;39:383-8. (Pubitemid 30335791)
25. Lehman TJ, Edelheit BS, Onel KB. Combined intravenous methotrexate and ecyclophosphamide for refractory childhood lupus nephritis. Ann Rheum Dis 2004;63:321-3. (Pubitemid 38250678)
26. Duramad P, McMahon CW, Hubbard A, Eskenazi B, Holland NT. Flow cytometric detection of intracellular Th1/Th2 cytokines using whole blood: validation of immunologic biomarker for use in epidemiologic studies. Cancer Epidemiol Biomarkers Prev 2004;13:1452-8. (Pubitemid 39202311)
27. Sims GP, Ettinger R, Shirota Y, Yarboro CH, Illei GG, Lipsky PE. Identification and characterization of circulating human transitional B cells. Blood 2005;105:4390-8. (Pubitemid 40720786)
28. Iwata S, Yamaoka K, Niiro H, Nakano K, Wang SP, Akashi K, et al. Amplification of Toll-like receptor-mediated signaling through spleen tyrosine kinase in human B-cell activation. J Allergy Clin Immunol 2012;129:1594-601.
29. Mills JA. Systemic lupus erythematosus. N Engl J Med 1994;330:1871-9.
30. Kotzin BL. Systemic lupus erythematosus. Cell 1996;85:303-6. (Pubitemid 26160701)
31. Johnston RJ, Poholek AC, DiToro D, Yusuf I, Eto D, Barnett B, et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 2009;325:1006-10.
32. Liu YJ, Banchereau J. Regulation of B cell commitment to plasma cells or to memory B cells. Semin Immunol 1997;9:235-40. (Pubitemid 27331992)
33. Wang J, Watanabe T. Expression and function of Fas during differentiation and activation of B cells. Int Rev Immunol 1999;18:367-79. (Pubitemid 29392082)
34. Gröndal G, Kristjansdottir H, Gunnlaugsdottir B, Arnason A, Lundberg I, Klareskog L, et al. Increased number of interleukin-10-producing cells in systemic lupus erythematosus patients and their first-degree relatives and spouses in Icelandic multicase families. Arthritis Rheum 1999;42:1649-54. (Pubitemid 30263633)
35. Simpson N, Gatenby PA, Wilson A, Malik S, Fulcher DA, Tangye SG, et al. 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;62:234-44.
36. Breitfeld D, Ohl L, Kremmer E, Ellwart J, Sallusto F, Lipp M, et al. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J Exp Med 2000;192:1545-52.
37. Schaerli P, Willimann K, Lang AB, Lipp M, Loetscher P, Moser B. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J Exp Med 2000;192:1553-62.
38. Noh J, Choi WS, Noh G, Lee JH. Presence of Foxp3-expressing CD19(+)CD5(+) B cells in human peripheral blood mononuclear cells: human CD19(+)CD5(+) Foxp3(+) regulatory B cell (Breg). Immune Netw 2010;10:247-9.
39. Ma L, Zhao P, Jiang ZY, Shan YX, Jiang YF. Imbalance of different types of CD4(+) forkhead box protein 3 (FoxP3)(+) T cells in patients with new-onset systemic lupus erythematosus. Clin Exp Immunol 2013;174:345-55.
40. Linterman MA, Vinuesa CG. T follicular helper cells during immunity and tolerance. Prog Mol Biol Transl Sci 2010;92:207-48.
41. Ettinger R, Kuchen S, Lipsky PE. The role of IL-21 in regulating B-cell function in health and disease. Immunol Rev 2008;223:60-86. (Pubitemid 351986176)
42. Konforte D, Simard N, Paige CJ. IL-21: an executor of B cell fate. J Immunol 2009;182:1781-7.
43. Feng XB, Wang DD, Chen JJ, Lu L, Hua BZ, Li X, et al. Inhibition of aberrant circulating Tfh cell proportions by corticosteroids in patients with systemic lupus erythematosus. PLoS One 2012;7:e51982.