Accumulation of peripheral autoreactive B cells in the absence of functional human regulatory T cells

Blood

Volumn 121, Issue 9, 2013, Pages 1595-1603

  Kinnunen, Tuure ^a   Chamberlain, Nicolas ^a   Morbach, Henner ^a   Choi, Jinyoung ^a   Kim, Sangtaek ^a   Craft, Joseph ^a   Mayer, Lloyd ^b   Cancrini, Caterina ^c   Passerini, Laura ^d   Bacchetta, Rosa ^a   Ochs, Hans D ^e   Torgerson, Troy R ^e   Meffre, Eric ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; INDUCIBLE T CELL COSTIMULATOR; RECOMBINANT ANTIBODY; TRANSCRIPTION FACTOR FOXP3;

ARTICLE; B LYMPHOCYTE; CELL ISOLATION; DONOR; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IPEX SYNDROME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; UPREGULATION;

EID: 84876468583     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-09-457465     Document Type: Article

References (50)

1. Bennett CL, Christie J, Ramsdell F, et al. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet. 2001;27(1): 20-21. (Pubitemid 32044513)
2. Barzaghi F, Passerini L, Bacchetta R. Immune dysregulation, polyendocrinopathy, enteropathy, X-linked (IPEX) syndrome: a paradigm of immunodeficiency with autoimmunity. Front Immunol. 2012;3:211.
3. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25-regulatory T cells. Nat Immunol. 2003;4(4):330-336. (Pubitemid 36432314)
4. Khattri R, Cox T, Yasayko SA, Ramsdell F. An essential role for Scurfin in CD4+CD25-T regulatory cells. Nat Immunol. 2003;4(4):337-342. (Pubitemid 36432315)
5. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003;299(5609):1057-1061. (Pubitemid 36222930)
6. Tsuda M, Torgerson TR, Selmi C, et al. The spectrum of autoantibodies in IPEX syndrome is broad and includes anti-mitochondrial autoantibodies. J Autoimmun. 2010;35(3):265-268.
7. Wardemann H, Yurasov S, Schaefer A, Young JW, Meffre E, Nussenzweig MC. Predominant autoantibody production by early human B cell precursors. Science. 2003;301(5638):1374-1377. (Pubitemid 37075812)
8. Ng Y-S, Wardemann H, Chelnis J, Cunningham-Rundles C, Meffre E. Bruton's tyrosine kinase (Btk) is essential for human B cell tolerance. J Exp Med. 2004;200:927-934. (Pubitemid 39362928)
9. Menard L, Saadoun D, Isnardi I, et al. The PTPN22 allele encoding an R620W variant interferes with the removal of developing autoreactive B cells in humans. J Clin Invest. 2011;121(9): 3635-3644.
10. Isnardi I, Ng YS, Srdanovic I, et al. IRAK-4-And MyD88-dependent pathways are essential for the removal of developing autoreactive B cells in humans. Immunity. 2008;29(5):746-757.
11. Sauer AV, Morbach H, Brigida I, Ng YS, Aiuti A, Meffre E. Defective B cell tolerance in adenosine deaminase deficiency is corrected by gene therapy. J Clin Invest. 2012;122(6):2141-2152.
12. Hervé M, Isnardi I, Ng YS, et al. CD40 ligand and MHC class II expression are essential for human peripheral B cell tolerance. J Exp Med. 2007; 204(7):1583-1593. (Pubitemid 47048025)
13. van Zelm MC, Szczepanski T, van der Burg M, van Dongen JJ. Replication history of B lymphocytes reveals homeostatic proliferation and extensive antigen-induced B cell expansion. J Exp Med. 2007;204(3):645-655. (Pubitemid 46457086)
14. Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, Rudensky AY. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity. 2005;22(3):329-341. (Pubitemid 40387475)
15. Gavin MA, Torgerson TR, Houston E, et al. Singlecell analysis of normal and FOXP3-mutant human T cells: FOXP3 expression without regulatory T cell development. Proc Natl Acad Sci U S A. 2006;103(17):6659-6664.
16. Tran DQ, Ramsey H, Shevach EM. Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood. 2007; 110(8):2983-2990. (Pubitemid 350006952)
17. Allan SE, Crome SQ, Crellin NK, et al. Activationinduced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int Immunol. 2007;19(4):345-354. (Pubitemid 46523383)
18. Bacchetta R, Passerini L, Gambineri E, et al. Defective regulatory and effector T cell functions in patients with FOXP3 mutations. J Clin Invest. 2006;116(6):1713-1722.
19. Passerini L, Olek S, Di Nunzio S, et al. Forkhead box protein 3 (FOXP3) mutations lead to increased TH17 cell numbers and regulatory T-cell instability. J Allergy Clin Immunol. 2011;128(6): 1376-1379.
20. Leonardo SM, Josephson JA, Hartog NL, Gauld SB. Altered B cell development and anergy in the absence of Foxp3. J Immunol. 2010;185(4):2147- 2156.
21. Meyers G, Ng YS, Bannock JM, et al. Activationinduced cytidine deaminase (AID) is required for B-cell tolerance in humans. Proc Natl Acad Sci U S A. 2011;108(28):11554-11559.
22. Mackay F, Schneider P. Cracking the BAFF code. Nat Rev Immunol. 2009;9(7):491-502.
23. Gambineri E, Perroni L, Passerini L, et al. Clinical and molecular profile of a new series of patients with immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome: inconsistent correlation between forkhead box protein 3 expression and disease severity. J Allergy Clin Immunol. 2008;122(6):1105-1112.
24. d'Hennezel E, Ben-Shoshan M, Ochs HD, et al. FOXP3 forkhead domain mutation and regulatory T cells in the IPEX syndrome. N Engl J Med. 2009;361(17):1710-1713.
25. Thornton AM, Korty PE, Tran DQ, et al. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3-T regulatory cells. J Immunol. 2010;184(7):3433-3441.
26. Williams LM, Rudensky AY. Maintenance of the Foxp3-dependent developmental program in mature regulatory T cells requires continued expression of Foxp3. Nat Immunol. 2007;8(3):277-284. (Pubitemid 46745377)
27. McMurchy AN, Gillies J, Allan SE, et al. Point mutants of forkhead box P3 that cause immune dysregulation, polyendocrinopathy, enteropathy, X-linked have diverse abilities to reprogram T cells into regulatory T cells. J Allergy Clin Immunol. 2010;126(6):1242-1251.
28. Morita R, Schmitt N, Bentebibel SE, 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(1):108-121.
29. Breitfeld D, Ohl L, Kremmer E, 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(11): 1545-1552.
30. 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(11): 1553-1562.
31. Passerini L, Di Nunzio S, Gregori S, et al. Functional type 1 regulatory T cells develop regardless of FOXP3 mutations in patients with IPEX syndrome. Eur J Immunol. 2011;41(4):1120-1131.
32. Rathmell JC, Townsend SE, Xu JC, Flavell RA, Goodnow CC. Expansion or elimination of B cells in vivo: dual roles for CD40-And Fas (CD95)-ligands modulated by the B cell antigen receptor. Cell. 1996;87(2):319-329. (Pubitemid 26359009)
33. Bystry RS, Aluvihare V, Welch KA, Kallikourdis M, Betz AG. B cells and professional APCs recruit regulatory T cells via CCL4. Nat Immunol. 2001; 2(12):1126-1132. (Pubitemid 33130146)
34. Seo SJ, Fields ML, Buckler JL, et al. The impact of T helper and T regulatory cells on the regulation of anti-double-stranded DNA B cells. Immunity. 2002;16(4):535-546. (Pubitemid 34442578)
35. Ludwig-Portugall I, Hamilton-Williams EE, Gottschalk C, Kurts C. Cutting edge: CD25-regulatory T cells prevent expansion and induce apoptosis of B cells specific for tissue autoantigens. J Immunol. 2008;181(7):4447-4451.
36. Zhao DM, Thornton AM, DiPaolo RJ, Shevach EM. Activated CD4+CD25-T cells selectively kill B lymphocytes. Blood. 2006;107(10):3925-3932. (Pubitemid 43726798)
37. Iikuni N, Lourenco EV, Hahn BH, La Cava A. Cutting edge: regulatory T cells directly suppress B cells in systemic lupus erythematosus. J Immunol. 2009;183(3):1518-1522.
38. Hondowicz BD, Fields ML, Nish SA, Larkin J, Caton AJ, Erikson J. Autoantibody production in lpr/lpr gld/gld mice reflects accumulation of CD4+ effector cells that are resistant to regulatory T cell activity. J Autoimmun. 2008;31(2):98-109.
39. Kim JM, Rasmussen JP, Rudensky AY. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol. 2007;8(2):191-197. (Pubitemid 46152650)
40. Linterman MA, Pierson W, Lee SK, et al. Foxp3-follicular regulatory T cells control the germinal center response. Nat Med. 2011;17(8):975-982.
41. Chung Y, Tanaka S, Chu F, et al. Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat Med. 2011;17(8): 983-988.
42. Lim HW, Hillsamer P, Banham AH, Kim CH. Cutting edge: direct suppression of B cells by CD4+ CD25-regulatory T cells. J Immunol. 2005; 175(7):4180-4183. (Pubitemid 41361949)
43. Marson A, Kretschmer K, Frampton GM, et al. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature. 2007; 445(7130):931-935.
44. Zheng Y, Josefowicz SZ, Kas A, Chu TT, Gavin MA, Rudensky AY. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature. 2007;445(7130):936-940.
45. Zhou X, Bailey-Bucktrout SL, Jeker LT, et al. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat Immunol. 2009;10(9):1000-1007.
46. Akimova T, Beier UH, Wang L, Levine MH, Hancock WW. Helios expression is a marker of T cell activation and proliferation. PloS One. 2011;6(8):e24226.
47. Ehrenstein MR, Evans JG, Singh A, et al. Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J Exp Med. 2004;200(3):277-285. (Pubitemid 39031247)
48. Lindley S, Dayan CM, Bishop A, Roep BO, Peakman M, Tree TI. Defective suppressor function in CD4(-)CD25(-) T-cells from patients with type 1 diabetes. Diabetes. 2005;54(1):92-99. (Pubitemid 40105099)
49. Viglietta V, Baecher-Allan C,Weiner HL, Hafler DA. Loss of functional suppression by CD4+CD25-regulatory T cells in patients with multiple sclerosis. J Exp Med. 2004;199(7):971-979. (Pubitemid 38481088)
50. Samuels J, Ng Y-S, Coupillaud C, Paget D, Meffre E. Impaired early B cell tolerance in patients with rheumatoid arthritis. J Exp Med. 2005;201(10): 1659-1667. (Pubitemid 40721009)