T Follicular Helper Cells Mediate Expansion of Regulatory B Cells via IL-21 in Lupus-Prone MRL/lpr Mice

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Yang, Xue ^a,b   Yang, Ji ^b   Chu, Yiwei ^b   Wang, Jiucun ^c   Guan, Ming ^a   Zhu, Xiaoxia ^a,b   Xue, Yu ^a,b   Zou, Hejian ^a,b  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 21; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; P STAT3 PROTEIN; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; B10 CELL; CELL ACTIVITY; CELL COUNT; CELL DIFFERENTIATION; CELL EXPANSION; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; HELPER CELL; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SPLEEN; SYSTEMIC LUPUS ERYTHEMATOSUS; T FOLLICULAR HELPER CELL;

ANIMALS; ANTIBODY FORMATION; AUTOANTIBODIES; AUTOIMMUNE DISEASES; AUTOIMMUNITY; B-LYMPHOCYTES, REGULATORY; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; FEMALE; INTERLEUKIN-10; INTERLEUKINS; MICE; MICE, INBRED MRL LPR; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, HELPER-INDUCER;

MUS;

EID: 84876513517     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062855     Document Type: Article

References (52)

1. Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, et al. (2003) Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med 349: 1526-1533.
2. Yang J, Chu Y, Yang X, Gao D, Zhu L, et al. (2009) Th17 and natural Treg cell population dynamics in systemic lupus erythematosus. Arthritis Rheum 60: 1472-1483.
3. DiLillo DJ, Matsushita T, Tedder TF, (2010) B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci 1183: 38-57.
4. Herlands RA, Christensen SR, Sweet RA, Hershberg U, Shlomchik MJ, (2008) T cell-independent and toll-like receptor-dependent antigen-driven activation of autoreactive B cells. Immunity 29: 249-260.
5. Yang J, Yang X, Zou H, Chu Y, Li M, (2011) Recovery of the immune balance between Th17 and regulatory T cells as a treatment for systemic lupus erythematosus. Rheumatology (Oxford) 50: 1366-1372.
6. Johnston RJ, Poholek AC, DiToro D, Yusuf I, Eto D, et al. (2009) Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 325: 1006-1010.
7. Nurieva RI, Chung Y, Hwang D, Yang XO, Kang HS, et al. (2008) Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29: 138-149.
8. Crotty S, (2011) Follicular helper CD4 T cells (TFH). Annu Rev Immunol 29: 621-663.
9. Fazilleau N, Mark L, McHeyzer-Williams LJ, McHeyzer-Williams MG, (2009) Follicular helper T cells: lineage and location. Immunity 30: 324-335.
10. Hamel KM, Liarski VM, Clark MR (2012) Germinal Center B-cells. Autoimmunity.
11. King C, Tangye SG, Mackay CR, (2008) T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu Rev Immunol 26: 741-766.
12. Simpson N, Gatenby PA, Wilson A, Malik S, Fulcher DA, 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.
13. Linterman MA, Rigby RJ, Wong RK, Yu D, Brink R, et al. (2009) Follicular helper T cells are required for systemic autoimmunity. J Exp Med 206: 561-576.
14. Yu B, Guan M, Peng Y, Shao Y, Zhang C, et al. (2011) Copy number variations of interleukin-17F, interleukin-21, and interleukin-22 are associated with systemic lupus erythematosus. Arthritis Rheum 63: 3487-3492.
15. Spolski R, Kim HP, Zhu W, Levy DE, Leonard WJ, (2009) IL-21 mediates suppressive effects via its induction of IL-10. J Immunol 182: 2859-2867.
16. Brandt K, Bulfone-Paus S, Foster DC, Ruckert R, (2003) Interleukin-21 inhibits dendritic cell activation and maturation. Blood 102: 4090-4098.
17. Yanaba K, Bouaziz JD, Matsushita T, Tsubata T, Tedder TF, (2009) The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol 182: 7459-7472.
18. Yanaba K, Bouaziz JD, Haas KM, Poe JC, Fujimoto M, et al. (2008) A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28: 639-650.
19. Mauri C, Gray D, Mushtaq N, Londei M, (2003) Prevention of arthritis by interleukin 10-producing B cells. J Exp Med 197: 489-501.
20. Mauri C, Ehrenstein MR, (2008) The 'short' history of regulatory B cells. Trends Immunol 29: 34-40.
21. Matsushita T, Yanaba K, Bouaziz JD, Fujimoto M, Tedder TF, (2008) Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest 118: 3420-3430.
22. Matsushita T, Horikawa M, Iwata Y, Tedder TF, (2010) Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J Immunol 185: 2240-2252.
23. Watson ML, Rao JK, Gilkeson GS, Ruiz P, Eicher EM, et al. (1992) Genetic analysis of MRL-lpr mice: relationship of the Fas apoptosis gene to disease manifestations and renal disease-modifying loci. J Exp Med 176: 1645-1656.
24. Watanabe R, Ishiura N, Nakashima H, Kuwano Y, Okochi H, et al. (2010) Regulatory B cells (B10 cells) have a suppressive role in murine lupus: CD19 and B10 cell deficiency exacerbates systemic autoimmunity. J Immunol 184: 4801-4809.
25. Cohen PL, Eisenberg RA, (1991) Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu Rev Immunol 9: 243-269.
26. Nurieva RI, Chung Y, Martinez GJ, Yang XO, Tanaka S, et al. (2009) Bcl6 mediates the development of T follicular helper cells. Science 325: 1001-1005.
27. Korn T, Bettelli E, Gao W, Awasthi A, Jager A, et al. (2007) IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448: 484-487.
28. Yang L, Anderson DE, Baecher-Allan C, Hastings WD, Bettelli E, et al. (2008) IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 454: 350-352.
29. Zotos D, Coquet JM, Zhang Y, Light A, D'Costa K, et al. (2010) IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J Exp Med 207: 365-378.
30. Nguyen V, Luzina I, Rus H, Tegla C, Chen C, et al. (2012) IL-21 promotes lupus-like disease in chronic graft-versus-host disease through both CD4 T cell- and B cell-intrinsic mechanisms. J Immunol 189: 1081-1093.
31. Vogelzang A, McGuire HM, Yu D, Sprent J, Mackay CR, et al. (2008) A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 29: 127-137.
32. Zeng R, Spolski R, Casas E, Zhu W, Levy DE, et al. (2007) The molecular basis of IL-21-mediated proliferation. Blood 109: 4135-4142.
33. Good KL, Bryant VL, Tangye SG, (2006) Kinetics of human B cell behavior and amplification of proliferative responses following stimulation with IL-21. J Immunol 177: 5236-5247.
34. Tomita M, Kawakami H, Uchihara JN, Okudaira T, Masuda M, et al. (2006) Inhibition of constitutively active Jak-Stat pathway suppresses cell growth of human T-cell leukemia virus type 1-infected T-cell lines and primary adult T-cell leukemia cells. Retrovirology 3: 22.
35. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A, (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19: 683-765.
36. Dong W, Zhu P, Wang Y, Wang Z, (2011) Follicular helper T cells in systemic lupus erythematosus: a potential therapeutic target. Autoimmun Rev 10: 299-304.
37. Li J, Pan HF, Cen H, Tian J, Ma Y, et al. (2011) Interleukin-21 as a potential therapeutic target for systemic lupus erythematosus. Mol Biol Rep 38: 4077-4081.
38. Ettinger R, Kuchen S, Lipsky PE, (2008) Interleukin 21 as a target of intervention in autoimmune disease. Ann Rheum Dis 67Suppl 3: iii83-86.
39. Yanaba K, Bouaziz JD, Matsushita T, Magro CM, St Clair EW, et al. (2008) B-lymphocyte contributions to human autoimmune disease. Immunol Rev 223: 284-299.
40. Yoshizaki A, Miyagaki T, DiLillo DJ, Matsushita T, Horikawa M, et al. (2010) Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 491: 264-268.
41. Yang M, Sun L, Wang S, Ko KH, Xu H, et al. (2010) Novel function of B cell-activating factor in the induction of IL-10-producing regulatory B cells. J Immunol 184: 3321-3325.
42. Nurieva R, Yang XO, Martinez G, Zhang Y, Panopoulos AD, et al. (2007) Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448: 480-483.
43. Bauquet AT, Jin H, Paterson AM, Mitsdoerffer M, Ho IC, et al. (2009) The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and TH-17 cells. Nat Immunol 10: 167-175.
44. Blenman KR, Duan B, Xu Z, Wan S, Atkinson MA, et al. (2006) IL-10 regulation of lupus in the NZM2410 murine model. Lab Invest 86: 1136-1148.
45. Yin Z, Bahtiyar G, Zhang N, Liu L, Zhu P, et al. (2002) IL-10 regulates murine lupus. J Immunol 169: 2148-2155.
46. Blair PA, Chavez-Rueda KA, Evans JG, Shlomchik MJ, Eddaoudi A, et al. (2009) Selective targeting of B cells with agonistic anti-CD40 is an efficacious strategy for the generation of induced regulatory T2-like B cells and for the suppression of lupus in MRL/lpr mice. J Immunol 182: 3492-3502.
47. Teichmann LL, Kashgarian M, Weaver CT, Roers A, Muller W, et al. (2012) B cell-derived IL-10 does not regulate spontaneous systemic autoimmunity in MRL.Fas(lpr) mice. J Immunol 188: 678-685.
48. Gateva V, Sandling JK, Hom G, Taylor KE, Chung SA, et al. (2009) A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet 41: 1228-1233.
49. D'Alfonso S, Rampi M, Bocchio D, Colombo G, Scorza-Smeraldi R, et al. (2000) Systemic lupus erythematosus candidate genes in the Italian population: evidence for a significant association with interleukin-10. Arthritis Rheum 43: 120-128.
50. Lauwerys BR, Garot N, Renauld JC, Houssiau FA, (2000) Interleukin-10 blockade corrects impaired in vitro cellular immune responses of systemic lupus erythematosus patients. Arthritis Rheum 43: 1976-1981.
51. Iwata Y, Matsushita T, Horikawa M, Dilillo DJ, Yanaba K, et al. (2011) Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 117: 530-541.
52. Yang J, Yang X, Chu Y, Li M, (2011) Identification of Baicalin as an immunoregulatory compound by controlling T(H)17 cell differentiation. PLoS One 6: e17164.