Human Circulating T Follicular Helper Cell Subsets in Health and Disease

Journal of Clinical Immunology

Volumn 36, Issue , 2016, Pages 34-39

  Ueno, Hideki ^a  

^a BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

Author keywords

autoimmune diseases; ctfh cells; humans; subsets; t cell differentiation; T follicular helper cells

Indexed keywords

CD40 LIGAND; CYTOKINE; INDUCIBLE T CELL COSTIMULATOR; INDUCIBLE T CELL COSTIMULATOR LIGAND; INTERLEUKIN 21; OX40 LIGAND; PROGRAMMED DEATH 1 RECEPTOR; BIOLOGICAL MARKER;

AUTOIMMUNE DISEASE; CIRCULATING T FOLLICULAR HELPER CELL; HELPER CELL; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RHEUMATOID ARTHRITIS; SJOEGREN SYNDROME; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; ANIMAL; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; DISEASE PREDISPOSITION; GENE EXPRESSION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; METABOLISM;

ANIMALS; AUTOIMMUNE DISEASES; BIOMARKERS; CELL DIFFERENTIATION; CELL MOVEMENT; CYTOKINES; DISEASE SUSCEPTIBILITY; GENE EXPRESSION; HUMANS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84961209472     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-016-0268-3     Document Type: Review

References (51)

1. Crotty S Follicular helper CD4 T cells (TFH). Annu Rev Immunol. 2011;29:621–63. doi:10.1146/annurev-immunol-031210-101400.
2. Tangye SG, Ma CS, Brink R, Deenick EK. The good, the bad and the ugly - TFH cells in human health and disease. Nat Rev Immunol. 2013;13(6):412–26. doi:10.1038/nri3447.
3. Linterman MA, Beaton L, Yu D, Ramiscal RR, Srivastava M, Hogan JJ, et al. IL-21 acts directly on B cells to regulate bcl-6 expression and germinal center responses. J Exp Med. 2010;207(2):353–63.
4. Zotos D, Coquet JM, Zhang Y, Light A, D’Costa K, Kallies A, et al. IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J Exp Med. 2010;207(2):365–78.
5. Victora GD, Schwickert TA, Fooksman DR, Kamphorst AO, Meyer-Hermann M, Dustin ML, et al. Germinal Center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell. 2010;143(4):592–605. doi:10.1016/j.cell.2010.10.032.
6. Tarlinton DM. Evolution in miniature: selection, survival and distribution of antigen reactive cells in the germinal centre. Immunol Cell Biol. 2008;86(2):133–8. doi:10.1038/sj.icb.7100148.
7. MacLennan IC. Germinal centers. Annu Rev Immunol. 1994;12:117–39.
8. 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(11):1545–52.
9. 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):1553–62.
10. Kim CH, Rott LS, Clark-Lewis I, Campbell DJ, Wu L, Butcher EC. Subspecialization of CXCR5+ T cells: B helper activity is focused in a germinal center-localized subset of CXCR5+ T cells. J Exp Med. 2001;193(12):1373–81.
11. Nurieva RI, Chung Y, Martinez GJ, Yang XO, Tanaka S, Matskevitch TD, et al. Bcl6 mediates the development of T follicular helper cells. Science. 2009;325(5943):1001–5.
12. 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(5943):1006–10.
13. Yu D, Rao S, Tsai LM, Lee SK, He Y, Sutcliffe EL, et al. The transcriptional repressor bcl-6 directs T follicular helper cell lineage commitment. Immunity. 2009;31(3):457–68. doi:10.1016/j.immuni.2009.07.002.
14. Rasheed AU, Rahn HP, Sallusto F, Lipp M, Muller G. Follicular B helper T cell activity is confined to CXCR5(hi)ICOS(hi) CD4 T cells and is independent of CD57 expression. Eur J Immunol. 2006;36(7):1892–903.
15. Akiba H, Takeda K, Kojima Y, Usui Y, Harada N, Yamazaki T, et al. The role of ICOS in the CXCR5+ follicular B helper T cell maintenance in vivo. J Immunol. 2005;175(4):2340–8.
16. Bossaller L, Burger J, Draeger R, Grimbacher B, Knoth R, Plebani A, et al. ICOS deficiency Is associated with a severe reduction of CXCR5 + CD4 Germinal Center Th cells. J Immunol. 2006;177(7):4927–32.
17. Choi YS, Kageyama R, Eto D, Escobar TC, Johnston RJ, Monticelli L, et al. ICOS receptor instructs T Follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity. 2011;34(6):932–46. doi:10.1016/j.immuni.2011.03.023.
18. Xu H, Li X, Liu D, Li J, Zhang X, Chen X, et al. Follicular T-helper cell recruitment governed by bystander B cells and ICOS-driven motility. Nature. 2013;496(7446):523–7. doi:10.1038/nature12058.
19. Hutloff A, Dittrich AM, Beier KC, Eljaschewitsch B, Kraft R, Anagnostopoulos I, et al. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature. 1999;397(6716):263–6.
20. Vogelzang A, McGuire HM, Yu D, Sprent J, Mackay CR, King C. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity. 2008;29(1):127–37.
21. Cubas RA, Mudd JC, Savoye AL, Perreau M, van Grevenynghe J, Metcalf T, et al. Inadequate T follicular cell help impairs B cell immunity during HIV infection. Nat Med. 2013;19(4):494–9. doi:10.1038/nm.3109.
22. Kashiwakuma D, Suto A, Hiramatsu Y, Ikeda K, Takatori H, Suzuki K, et al. B and T lymphocyte attenuator suppresses IL-21 production from follicular Th cells and subsequent humoral immune responses. J Immunol. 2010;185(5):2730–6. doi:10.4049/jimmunol.0903839.
23. Forster R, Emrich T, Kremmer E, Lipp M. Expression of the G-protein–coupled receptor BLR1 defines mature, recirculating B cells and a subset of T-helper memory cells. Blood. 1994;84(3):830–40.
24. Schmitt N, Bentebibel SE, Ueno H. Phenotype and functions of memory tfh cells in human blood. Trends Immunol. 2014;35(9):436–42. doi:10.1016/j.it.2014.06.002.
25. Acosta-Rodriguez EV, Rivino L, Geginat J, Jarrossay D, Gattorno M, Lanzavecchia A, et al. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol. 2007;8(6):639–46.
26. 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(1):108–21. doi:10.1016/j.immuni.2010.12.012.
27. Locci M, Havenar-Daughton C, Landais E, Wu J, Kroenke MA, Arlehamn CL, et al. Human circulating PD-1(+)CXCR3(−)CXCR5(+) memory tfh cells are highly functional and correlate with broadly neutralizing HIV Antibody responses. Immunity. 2013;39(4):758–69. doi:10.1016/j.immuni.2013.08.031.
28. Boswell KL, Paris R, Boritz E, Ambrozak D, Yamamoto T, Darko S, et al. Loss of circulating CD4 T cells with B cell helper function during chronic HIV infection. PLoS Pathog. 2014;10(1):e1003853. doi:10.1371/journal.ppat.1003853.
29. Bentebibel SE, Lopez S, Obermoser G, Schmitt N, Mueller C, Harrod C et al. Induction of ICOS + CXCR3 + CXCR5+ TH cells correlates with antibody responses to influenza vaccination. Sci Transl Med. 2013;5(176):176ra32. doi:10.1126/scitranslmed.3005191.
30. Lee SK, Silva DG, Martin JL, Pratama A, Hu X, Chang PP, et al. Interferon-gamma excess leads to pathogenic accumulation of follicular helper T cells and germinal centers. Immunity. 2012;37(5):880–92. doi:10.1016/j.immuni.2012.10.010.
31. Schmitt N, Bustamante J, Bourdery L, Bentebibel SE, Boisson-Dupuis S, Hamlin F, et al. IL-12 receptor beta1 deficiency alters in vivo T follicular helper cell response in humans. Blood. 2013;121(17):3375–85. doi:10.1182/blood-2012-08-448902.
32. Ueno H, Banchereau J, Vinuesa CG. Pathophysiology of T follicular helper cells in humans and mice. Nat Immunol. 2015;16(2):142–52. doi:10.1038/ni.3054.
33. Kitano M, Moriyama S, Ando Y, Hikida M, Mori Y, Kurosaki T, et al. Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity. 2011;34(6):961–72. doi:10.1016/j.immuni.2011.03.025.
34. Baumjohann D, Okada T, Ansel KM. Cutting Edge: distinct waves of BCL6 expression during T Follicular helper cell development. Journal of Immunology. 2011;187(5):2089–92. doi:10.4049/jimmunol.1101393.
35. Kerfoot SM, Yaari G, Patel JR, Johnson KL, Gonzalez DG, Kleinstein SH, et al. Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity. 2011;34(6):947–60. doi:10.1016/j.immuni.2011.03.024.
36. Liu X, Chen X, Zhong B, Wang A, Wang X, Chu F, et al. Transcription factor achaete-scute homologue 2 initiates follicular T-helper-cell development. Nature. 2014;507(7493):513–8. doi:10.1038/nature12910.
37. Haynes NM, Allen CD, Lesley R, Ansel KM, Killeen N, Cyster JG. 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. 2007;179(8):5099–108.
38. Odegard JM, Marks BR, DiPlacido LD, Poholek AC, Kono DH, Dong C, et al. ICOS-dependent extrafollicular helper T cells elicit IgG production via IL-21 in systemic autoimmunity. J Exp Med. 2008;205(12):2873–86.
39. Schmitt N, Liu Y, Bentebibel SE, Munagala I, Bourdery L, Venuprasad K, et al. The cytokine TGF-beta co-opts signaling via STAT3-STAT4 to promote the differentiation of human TFH cells. Nat Immunol. 2014;15(9):856–65. doi:10.1038/ni.2947.
40. Schmitt N, Morita R, Bourdery L, Bentebibel SE, Zurawski SM, Banchereau J, et al. Human dendritic cells induce the differentiation of interleukin-21-producing T follicular helper-like cells through interleukin-12. Immunity. 2009;31(1):158–69. doi:10.1016/j.immuni.2009.04.016.
41. Ma CS, Avery DT, Chan A, Batten M, Bustamante J, Boisson-Dupuis S, et al. Functional STAT3 deficiency compromises the generation of human T follicular helper cells. Blood. 2012;119(17):3997–4008. doi:10.1182/blood-2011-11-392985.
42. Nurieva RI, Chung Y, Hwang D, Yang XO, Kang HS, Ma L, et al. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity. 2008;29(1):138–49.
43. Suto A, Kashiwakuma D, Kagami S, Hirose K, Watanabe N, Yokote K, et al. Development and characterization of IL-21-producing CD4+ T cells. J Exp Med. 2008;205(6):1369–79.
44. Ferguson SE, Han S, Kelsoe G, Thompson CB. CD28 is required for germinal center formation. J Immunol. 1996;156(12):4576–81.
45. Furie R, Nicholls K, Cheng TT, Houssiau F, Burgos-Vargas R, Chen SL, et al. Efficacy and safety of abatacept in lupus nephritis: a twelve-month, randomized, double-blind study. Arthritis Rheumatol. 2014;66(2):379–89. doi:10.1002/art.38260.
46. Iwata S, Nakayamada S, Fukuyo S, Kubo S, Yunoue N, Wang SP, et al. Activation of syk in peripheral blood B cells in patients with rheumatoid arthritis: a potential target for abatacept therapy. Arthritis Rheumatol. 2015;67(1):63–73. doi:10.1002/art.38895.
47. Teichmann LL, Cullen JL, Kashgarian M, Dong C, Craft J, Shlomchik MJ. Local triggering of the ICOS coreceptor by CD11c(+) myeloid cells drives organ inflammation in lupus. Immunity. 2015;42(3):552–65. doi:10.1016/j.immuni.2015.02.015.
48. Bentebibel SE, Schmitt N, Banchereau J, Ueno H. Human tonsil B-cell lymphoma 6 (BCL6)-expressing CD4+ T-cell subset specialized for B-cell help outside germinal centers. Proc Natl Acad Sci U S A. 2011;108(33):E488–97.
49. Liarski VM, Kaverina N, Chang A, Brandt D, Yanez D, Talasnik L et al. Cell distance mapping identifies functional T follicular helper cells in inflamed human renal tissue. Sci Transl Med. 2014;6(230):230ra46. doi:10.1126/scitranslmed.3008146.
50. Iwai H, Abe M, Hirose S, Tsushima F, Tezuka K, Akiba H, et al. Involvement of inducible costimulator-B7 homologous protein costimulatory pathway in murine lupus nephritis. J Immunol. 2003;171(6):2848–54.
51. Jacquemin C, Schmitt N, Contin-Bordes C, Liu Y, Narayanan P, Seneschal J, et al. OX40 ligand contributes to human lupus pathogenesis by promoting T Follicular helper response. Immunity. 2015;42(6):1159–70. doi:10.1016/j.immuni.2015.05.012.