Germinal center B cell depletion diminishes CD4+ follicular T helper cells in autoimmune mice

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Yusuf, Isharat ^a   Stern, Jessica ^a   McCaughtry, Tom M ^a   Gallagher, Sandra ^a   Sun, Hong ^a   Gao, Changshou ^a   Tedder, Thomas ^b   Carlesso, Gianluca ^a   Carter, Laura ^a   Herbst, Ronald ^a   Wang, Yue ^a  

^a MEDIMMUNE   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD28 ANTIGEN; INDUCIBLE T CELL COSTIMULATOR; INDUCIBLE T CELL COSTIMULATOR LIGAND;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL COMMUNICATION; CONTROLLED STUDY; FOLLICULAR CD4+ T HELPER CELL; FOLLICULAR DENDRITIC CELL; GERMINAL CENTER; HELPER CELL; HUMORAL IMMUNITY; LYMPHOCYTE DEPLETION; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; IMMUNOLOGY; NEW ZEALAND BLACK MOUSE; PHYSIOLOGY;

ANIMALS; AUTOIMMUNE DISEASES; B-LYMPHOCYTES; CELL DIFFERENTIATION; GERMINAL CENTER; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED NZB; MODELS, IMMUNOLOGICAL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84905482389     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102791     Document Type: Article

References (88)

1. Vinuesa CG, Sanz I, Cook MC (2009) Dysregulation of germinal centres in autoimmune disease. Nat Rev Immunol 9: 845-857.
2. Craft JE (2012) Follicular helper T cells in immunity and systemic autoimmunity. Nat Rev Rheumatol 8: 337-347.
3. Tangye SG, Ma CS, Brink R, Deenick EK (2013) The good, the bad and the ugly - TFH cells in human health and disease. Nat Rev Immunol 13: 412-426.
4. Crotty S (2011) Follicular helper CD4 T cells (TFH). Annu Rev Immunol 29: 621-663.
5. Ramiscal RR, Vinuesa CG (2013) T-cell subsets in the germinal center. Immunol Rev 252: 146-155.
6. Tobon GJ, Izquierdo JH, Canas CA (2013) B lymphocytes: development, tolerance, and their role in autoimmunity-focus on systemic lupus erythematosus. Autoimmune Dis 2013: 827254.
7. Grammer AC, Lipsky PE (2003) B cell abnormalities in systemic lupus erythematosus. Arthritis Res Ther 5 Suppl 4: S22-27. (Pubitemid 38239913)
8. Grammer AC, Slota R, Fischer R, Gur H, Girschick H, et al. (2003) Abnormal germinal center reactions in systemic lupus erythematosus demonstrated by blockade of CD154-CD40 interactions. J Clin Invest 112: 1506-1520. (Pubitemid 38056277)
9. Cappione A III, Anolik JH, Pugh-Bernard A, Barnard J, Dutcher P, et al. (2005) Germinal center exclusion of autoreactive B cells is defective in human systemic lupus erythematosus. J Clin Invest 115: 3205-3216. (Pubitemid 41567585)
10. Luzina IG, Atamas SP, Storrer CE, daSilva LC, Kelsoe G, et al. (2001) Spontaneous formation of germinal centers in autoimmune mice. J Leukoc Biol 70: 578-584. (Pubitemid 32954768)
11. Victora GD, NussenzweigMC (2012) Germinal centers. Annu Rev Immunol 30: 429-457.
12. King C, Sprent J (2012) Emerging cellular networks for regulation of T follicular helper cells. Trends Immunol 33: 59-65.
13. Linterman MA, Liston A, Vinuesa CG (2012) T-follicular helper cell differentiation and the co-option of this pathway by non-helper cells. Immunol Rev 247: 143-159.
14. Ma CS, Deenick EK, Batten M, Tangye SG (2012) The origins, function, and regulation of T follicular helper cells. J Exp Med 209: 1241-1253.
15. Subramanian S, Tus K, Li QZ, Wang A, Tian XH, et al. (2006) A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc Natl Acad Sci U S A 103: 9970-9975. (Pubitemid 43993607)
16. Vinuesa CG, Cook MC, Angelucci C, Athanasopoulos V, Rui L, et al. (2005) A RING-type ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity. Nature 435: 452-458. (Pubitemid 40734237)
17. 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.
18. Bubier JA, Sproule TJ, Foreman O, Spolski R, Shaffer DJ, et al. (2009) A critical role for IL-21 receptor signaling in the pathogenesis of systemic lupus erythematosus in BXSB-Yaa mice. Proc Natl Acad Sci U S A 106: 1518-1523.
19. King C, Tangye SG, Mackay CR (2008) T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu Rev Immunol 26: 741-766. (Pubitemid 351600391)
20. 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.
21. Hutloff A, Buchner K, Reiter K, Baelde HJ, Odendahl M, et al. (2004) Involvement of inducible costimulator in the exaggerated memory B cell and plasma cell generation in systemic lupus erythematosus. Arthritis Rheum 50: 3211-3220. (Pubitemid 39371998)
22. Saito R, Onodera H, Tago H, Suzuki Y, Shimizu M, et al. (2005) Altered expression of chemokine receptor CXCR5 on T cells of myasthenia gravis patients. J Neuroimmunol 170: 172-178. (Pubitemid 41740917)
23. Tackenberg B, Kruth J, Bartholomaeus JE, Schlegel K, Oertel WH, et al. (2007) Clonal expansions of CD4+ B helper T cells in autoimmune myasthenia gravis. Eur J Immunol 37: 849-863. (Pubitemid 46916951)
24. Ma J, Zhu C, Ma B, Tian J, Baidoo SE, et al. (2012) Increased frequency of circulating follicular helper T cells in patients with rheumatoid arthritis. Clin Dev Immunol 2012: 827480.
25. Zhu C, Ma J, Liu Y, Tong J, Tian J, et al. (2012) Increased frequency of follicular helper T cells in patients with autoimmune thyroid disease. J Clin Endocrinol Metab 97: 943-950.
26. Liu R, Wu Q, Su D, Che N, Chen H, et al. (2012) A regulatory effect of IL-21 on T follicular helper-like cell and B cell in rheumatoid arthritis. Arthritis Res Ther 14: R255.
27. Li XY, Wu ZB, Ding J, Zheng ZH, Li XY, et al. (2012) Role of the frequency of blood CD4 (+) CXCR5(+) CCR6(+) T cells in autoimmunity in patients with Sjogren's syndrome. Biochem Biophys Res Commun 422: 238-244.
28. Wong CK, Wong PT, Tam LS, Li EK, Chen DP, et al. (2010) Elevated production of B cell chemokine CXCL13 is correlated with systemic lupus erythematosus disease activity. J Clin Immunol 30: 45-52.
29. Morita R, Schmitt N, Bentebibel SE, Ranganathan R, Bourdery L, et al. (2011) Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 34: 108-121.
30. He J, Tsai LM, Leong YA, Hu X, Ma CS, et al. (2013) Circulating precursor CCR7(lo)PD-1(hi) CXCR5(+) CD4(+) T cells indicate Tfh cell activity and promote antibody responses upon antigen reexposure. Immunity 39: 770-781.
31. Salomonsson S, Larsson P, Tengner P, Mellquist E, Hjelmstrom P, et al. (2002) Expression of the B cell-attracting chemokine CXCL13 in the target organ and autoantibody production in ectopic lymphoid tissue in the chronic inflammatory disease Sjogren's syndrome. Scand J Immunol 55: 336-342. (Pubitemid 34429788)
32. Chakera A, Bennett SC, Morteau O, Bowness P, Luqmani RA, et al. (2012) The phenotype of circulating follicular-helper T cells in patients with rheumatoid arthritis defines CD200 as a potential therapeutic target. Clin Dev Immunol 2012: 948218.
33. Vinuesa CG, Cyster JG (2011) How T cells earn the follicular rite of passage. Immunity 35: 671-680.
34. 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.
35. 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.
36. Yu D, Rao S, Tsai LM, Lee SK, He Y, et al. (2009) The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 31: 457-468.
37. Choi YS, Kageyama R, Eto D, Escobar TC, Johnston RJ, et al. (2011) ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 34: 932-946.
38. Goenka R, Barnett LG, Silver JS, O'Neill PJ, Hunter CA, et al. (2011) Cutting edge: dendritic cell-restricted antigen presentation initiates the follicular helper T cell program but cannot complete ultimate effector differentiation. J Immunol 187: 1091-1095.
39. Haynes NM, Allen CD, Lesley R, Ansel KM, Killeen N, et al. (2007) Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal center-associated subpopulation. J Immunol 179: 5099-5108.
40. Baumjohann D, Preite S, Reboldi A, Ronchi F, Ansel KM, et al. (2013) Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity 38: 596-605.
41. Fahey LM, Wilson EB, Elsaesser H, Fistonich CD, McGavern DB, et al. (2011) Viral persistence redirects CD4 T cell differentiation toward T follicular helper cells. J Exp Med 208: 987-999.
42. Rosenblum MD, Gratz IK, Paw JS, Abbas AK (2012) Treating human autoimmunity: current practice and future prospects. Sci Transl Med 4: 125sr121.
43. Murphy G, Lisnevskaia L, Isenberg D (2013) Systemic lupus erythematosus and other autoimmune rheumatic diseases: challenges to treatment. Lancet 382: 809-818.
44. Shi X, Xie C, Chang S, Zhou XJ, Tedder T, et al. (2007) CD19 hyperexpression augments Sle1-induced humoral autoimmunity but not clinical nephritis. Arthritis Rheum 56: 3057-3069. (Pubitemid 47502753)
45. Gilliland LK, Norris NA, Marquardt H, Tsu TT, Hayden MS, et al. (1996) Rapid and reliable cloning of antibody variable regions and generation of recombinant single chain antibody fragments. Tissue Antigens 47: 1-20. (Pubitemid 26048776)
46. Herbst R, Wang Y, Gallagher S, Mittereder N, Kuta E, et al. (2010) B-cell depletion in vitro and in vivo with an afucosylated anti-CD19 antibody. J Pharmacol Exp Ther 335: 213-222.
47. Oganesyan V, Gao C, Shirinian L, Wu H, Dall'Acqua WF (2008) Structural characterization of a human Fc fragment engineered for lack of effector functions. Acta Crystallogr D Biol Crystallogr 64: 700-704. (Pubitemid 351872072)
48. Hamaguchi Y, Xiu Y, Komura K, Nimmerjahn F, Tedder TF (2006) Antibody isotype-specific engagement of Fcgamma receptors regulates B lymphocyte depletion during CD20 immunotherapy. J Exp Med 203: 743-753.
49. Browning JL, Sizing ID, Lawton P, Bourdon PR, Rennert PD, et al. (1997) Characterization of lymphotoxin-alpha beta complexes on the surface of mouse lymphocytes. J Immunol 159: 3288-3298. (Pubitemid 127482087)
50. Steurer W, Nickerson PW, Steele AW, Steiger J, Zheng XX, et al. (1995) Ex vivo coating of islet cell allografts with murine CTLA4/Fc promotes graft tolerance. J Immunol 155: 1165-1174.
51. Yusuf I, Kageyama R, Monticelli L, Johnston RJ, Ditoro D, et al. (2010) Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150). J Immunol 185: 190-202.
52. Yao Y, Richman L, Morehouse C, de los Reyes M, Higgs BW, et al. (2008) Type I interferon: potential therapeutic target for psoriasis? PLoS One 3: e2737.
53. Mohan C, Alas E, Morel L, Yang P, Wakeland EK (1998) Genetic dissection of SLE pathogenesis. Sle1 on murine chromosome 1 leads to a selective loss of tolerance to H2A/H2B/DNA subnucleosomes. J Clin Invest 101: 1362-1372. (Pubitemid 28145253)
54. Morel L, Mohan C, Yu Y, Croker BP, Tian N, et al. (1997) Functional dissection of systemic lupus erythematosus using congenic mouse strains. J Immunol 158: 6019-6028. (Pubitemid 127484012)
55. Vuyyuru R, Mohan C, Manser T, Rahman ZS (2009) The lupus susceptibility locus Sle1 breaches peripheral B cell tolerance at the antibody-forming cell and germinal center checkpoints. J Immunol 183: 5716-5727.
56. Perry D, Sang A, Yin Y, Zheng YY, Morel L (2011) Murine models of systemic lupus erythematosus. J Biomed Biotechnol 2011: 271694.
57. Shinall SM, Gonzalez-Fernandez M, Noelle RJ, Waldschmidt TJ (2000) Identification of murine germinal center B cell subsets defined by the expression of surface isotypes and differentiation antigens. J Immunol 164: 5729-5738. (Pubitemid 30389815)
58. Liu X, Nurieva RI, Dong C (2013) Transcriptional regulation of follicular T-helper (Tfh) cells. Immunol Rev 252: 139-145.
59. Chung Y, Tanaka S, Chu F, Nurieva RI, Martinez GJ, et al. (2011) Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat Med 17: 983-988.
60. Linterman MA, Pierson W, Lee SK, Kallies A, Kawamoto S, et al. (2011) Foxp3+ follicular regulatory T cells control the germinal center response. Nat Med 17: 975-982.
61. Victora GD, Schwickert TA, Fooksman DR, Kamphorst AO, Meyer-Hermann M, et al. (2010) Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell 143: 592-605.
62. Yazawa N, Hamaguchi Y, Poe JC, Tedder TF (2005) Immunotherapy using unconjugated CD19 monoclonal antibodies in animal models for B lymphocyte malignancies and autoimmune disease. Proc Natl Acad Sci U S A 102: 15178-15183. (Pubitemid 41513355)
63. Bekar KW, Owen T, Dunn R, Ichikawa T, Wang W, et al. (2010) Prolonged effects of short-term anti-CD20 B cell depletion therapy in murine systemic lupus erythematosus. Arthritis Rheum 62: 2443-2457.
64. Haas KM, Watanabe R, Matsushita T, Nakashima H, Ishiura N, et al. (2010) Protective and pathogenic roles for B cells during systemic autoimmunity in NZB/W F1 mice. J Immunol 184: 4789-4800.
65. Han S, Hathcock K, Zheng B, Kepler TB, Hodes R, et al. (1995) Cellular interaction in germinal centers. Roles of CD40 ligand and B7-2 in established germinal centers. J Immunol 155: 556-567.
66. Takahashi Y, Dutta PR, Cerasoli DM, Kelsoe G (1998) In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. V. Affinity maturation develops in two stages of clonal selection. J Exp Med 187: 885-895. (Pubitemid 28141662)
67. Han S, Zheng B, Dal Porto J, Kelsoe G (1995) In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. IV. Affinity-dependent, antigen-driven B cell apoptosis in germinal centers as a mechanism for maintaining self-tolerance. J Exp Med 182: 1635-1644.
68. Mohan C, Shi Y, Laman JD, Datta SK (1995) Interaction between CD40 and its ligand gp39 in the development of murine lupus nephritis. J Immunol 154: 1470-1480.
69. Wang X, Huang W, Schiffer LE, Mihara M, Akkerman A, et al. (2003) Effects of anti-CD154 treatment on B cells in murine systemic lupus erythematosus. Arthritis Rheum 48: 495-506. (Pubitemid 36278019)
70. Schiffer L, Sinha J, Wang X, Huang W, von Gersdorff G, et al. (2003) Short term administration of costimulatory blockade and cyclophosphamide induces remission of systemic lupus erythematosus nephritis in NZB/W F1 mice by a mechanism downstream of renal immune complex deposition. J Immunol 171: 489-497. (Pubitemid 36745324)
71. Monk NJ, Hargreaves RE, Marsh JE, Farrar CA, Sacks SH, et al. (2003) Fc-dependent depletion of activated T cells occurs through CD40L-specific antibody rather than costimulation blockade. Nat Med 9: 1275-1280. (Pubitemid 37279850)
72. Coyle AJ, Lehar S, Lloyd C, Tian J, Delaney T, et al. (2000) The CD28-related molecule ICOS is required for effective T cell-dependent immune responses. Immunity 13: 95-105.
73. Hu YL, Metz DP, Chung J, Siu G, Zhang M (2009) B7RP-1 blockade ameliorates autoimmunity through regulation of follicular helper T cells. J Immunol 182: 1421-1428.
74. Walker LS, Wiggett HE, Gaspal FM, Raykundalia CR, Goodall MD, et al. (2003) Established T cell-driven germinal center B cell proliferation is independent of CD28 signaling but is tightly regulated through CTLA-4. J Immunol 170: 91-98. (Pubitemid 36026127)
75. Bluml S, McKeever K, Ettinger R, Smolen J, Herbst R (2013) B-cell targeted therapeutics in clinical development. Arthritis Res Ther 15 Suppl 1: S4.
76. Lee SK, Silva DG, Martin JL, Pratama A, Hu X, et al. (2012) Interferon-gamma excess leads to pathogenic accumulation of follicular helper T cells and germinal centers. Immunity 37: 880-892.
77. Ding Y, Li J, Wu Q, Yang P, Luo B, et al. (2013) IL-17RA is essential for optimal localization of follicular Th cells in the germinal center light zone to promote autoantibody-producing B cells. J Immunol 191: 1614-1624.
78. Ahuja A, Shupe J, Dunn R, Kashgarian M, Kehry MR, et al. (2007) Depletion of B cells in murine lupus: efficacy and resistance. J Immunol 179: 3351-3361.
79. Wang X, Cho B, Suzuki K, Xu Y, Green JA, et al. (2011) Follicular dendritic cells help establish follicle identity and promote B cell retention in germinal centers. J Exp Med 208: 2497-2510.
80. Boulianne B, Le MX, Ward LA, Meng L, Haddad D, et al. (2013) AID-expressing germinal center B cells cluster normally within lymph node follicles in the absence of FDC-M1+ CD35+ follicular dendritic cells but dissipate prematurely. J Immunol 191: 4521-4530.
81. Cannons JL, Qi H, Lu KT, Dutta M, Gomez-Rodriguez J, et al. (2010) Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 32: 253-265.
82. Good-Jacobson KL, Shlomchik MJ (2010) Plasticity and heterogeneity in the generation of memory B cells and long-lived plasma cells: the influence of germinal center interactions and dynamics. J Immunol 185: 3117-3125.
83. Qi H, Cannons JL, Klauschen F, Schwartzberg PL, Germain RN (2008) SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 455: 764-769.
84. Linton PJ, Harbertson J, Bradley LM (2000) A critical role for B cells in the development of memory CD4 cells. J Immunol 165: 5558-5565.
85. Pepper M, Pagan AJ, Igyarto BZ, Taylor JJ, Jenkins MK (2011) Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 35: 583-595.
86. Whitmire JK, Asano MS, Kaech SM, Sarkar S, Hannum LG, et al. (2009) Requirement of B cells for generating CD4+ T cell memory. J Immunol 182: 1868-1876.
87. Terrier B, Costedoat-Chalumeau N, Garrido M, Geri G, Rosenzwajg M, et al. (2012) Interleukin 21 correlates with T cell and B cell subset alterations in systemic lupus erythematosus. J Rheumatol 39: 1819-1828.
88. Xu X, Shi Y, Cai Y, Zhang Q, Yang F, et al. (2013) Inhibition of Increased Circulating Tfh Cell by Anti-CD20 Monoclonal Antibody in Patients with Type 1 Diabetes. PLoS One 8: e79858.