T follicular helper cell diversity and plasticity

Trends in Immunology

Volumn 34, Issue 5, 2013, Pages 200-207

  Cannons, Jennifer L ^a   Lu, Kristina T ^a   Schwartzberg, Pamela L ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

Bcl 6; Histone modification; T cell plasticity; T follicular helper cells

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR5; CYTOKINE; DNA BINDING PROTEIN; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 21; INTERLEUKIN 4; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN BCL 6; RETINOIC ACID RECEPTOR GAMMA; STAT3 PROTEIN; STAT5 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR C MAF; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET;

ANTIGEN SPECIFICITY; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TYPE; CHROMATIN STRUCTURE; CYTOKINE PRODUCTION; EFFECTOR CELL; EPIGENETICS; HELPER CELL; HUMAN; HUMORAL IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PHENOTYPIC PLASTICITY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; REGULATORY T LYMPHOCYTE; REVIEW; T FOLLICULAR HELPER CELL; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; TH2 CELL;

ANIMALS; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINEAGE; CYTOKINES; EPIGENESIS, GENETIC; GERMINAL CENTER; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOMODULATION; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84877140255     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2013.01.001     Document Type: Review

References (96)

1. FH). Annu. Rev. Immunol. 2011, 29:621-663.
2. Mosmann T.R., et al. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 1986, 136:2348-2357.
3. + T-cell differentiation regulated by networks of cytokines and transcription factors. Immunol. Rev. 2010, 238:247-262.
4. Breitfeld D., 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, 192:1545-1552.
5. Schaerli P., et al. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J. Exp. Med. 2000, 192:1553-1562.
6. Reinhardt R.L., et al. Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 2009, 10:385-393.
7. Baumjohann D., et al. Cutting edge: distinct waves of BCL6 expression during T follicular helper cell development. J. Immunol. 2011, 187:2089-2092.
8. Kitano M., et al. Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity 2011, 34:961-972.
9. Liu X., et al. Bcl6 expression specifies the T follicular helper cell program in vivo. J. Exp. Med. 2012, 209:1841-1852.
10. Ansel K.M., et al. In vivo-activated CD4 T cells upregulate CXC chemokine receptor 5 and reprogram their response to lymphoid chemokines. J. Exp. Med. 1999, 190:1123-1134.
11. Hardtke S., et al. Balanced expression of CXCR5 and CCR7 on follicular T helper cells determines their transient positioning to lymph node follicles and is essential for efficient B-cell help. Blood 2005, 106:1924-1931.
12. Haynes N.M., et al. 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, 179:5099-5108.
13. Okada T., et al. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 2005, 3:e150.
14. Qi H., et al. SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 2008, 455:764-769.
15. + dendritic cells and lymphotoxin-expressing B cells. Nat. Immunol. 2012, 13:681-690.
16. Choi Y.S., et al. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 2011, 34:932-946.
17. Goenka R., et al. Cutting edge: dendritic cell-restricted antigen presentation initiates the follicular helper T cell program but cannot complete ultimate effector differentiation. J. Immunol. 2011, 187:1091-1095.
18. Kerfoot S.M., et al. Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity 2011, 34:947-960.
19. Poholek A.C., et al. In vivo regulation of Bcl6 and T follicular helper cell development. J. Immunol. 2010, 185:313-326.
20. Fazilleau N., et al. The function of follicular helper T cells is regulated by the strength of T cell antigen receptor binding. Nat. Immunol. 2009, 10:375-384.
21. Lu K.T., et al. Functional and epigenetic studies reveal multistep differentiation and plasticity of in vitro-generated and in vivo-derived follicular T helper cells. Immunity 2011, 35:622-632.
22. Nurieva R.I., 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, 29:138-149.
23. + T cells. J. Exp. Med. 2008, 205:1369-1379.
24. Linterman M.A., et al. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J. Exp. Med. 2010, 207:353-363.
25. Zotos D., et al. IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J. Exp. Med. 2010, 207:365-378.
26. Batten M., et al. IL-27 supports germinal center function by enhancing IL-21 production and the function of T follicular helper cells. J. Exp. Med. 2010, 207:2895-2906.
27. Ma C.S., et al. Functional STAT3 deficiency compromises the generation of human T follicular helper cells. Blood 2012, 119:3997-4008.
28. Ballesteros-Tato A., et al. Interleukin-2 inhibits germinal center formation by limiting T follicular helper cell differentiation. Immunity 2012, 36:847-856.
29. FH cell differentiation. J. Exp. Med. 2012, 209:243-250.
30. Hotson A.N., et al. The T cell STAT signaling network is reprogrammed within hours of bacteremia via secondary signals. J. Immunol. 2009, 182:7558-7568.
31. Lee S.K., et al. Interferon-gamma excess leads to pathogenic accumulation of follicular helper T cells and germinal centers. Immunity 2012, 37:880-892.
32. FH) cell lineage is induced by IL-12. Immunol. Cell Biol. 2009, 87:590-600.
33. Schmitt N., et al. Human dendritic cells induce the differentiation of interleukin-21-producing T follicular helper-like cells through interleukin-12. Immunity 2009, 31:158-169.
34. Nakayamada S., et al. Early Th1 cell differentiation is marked by a Tfh cell-like transition. Immunity 2011, 35:919-931.
35. Hirota K., et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 2011, 12:255-263.
36. + cell subset with combined Th2 and Th1 cell functions. Immunity 2010, 32:116-128.
37. Lee S.K., et al. B cell priming for extrafollicular antibody responses requires Bcl-6 expression by T cells. J. Exp. Med. 2011, 208:1377-1388.
38. Luthje K., et al. The development and fate of follicular helper T cells defined by an IL-21 reporter mouse. Nat. Immunol. 2012, 13:491-498.
39. Vogelzang A., et al. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 2008, 29:127-137.
40. Johnston R.J., et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 2009, 325:1006-1010.
41. Nurieva R.I., et al. Bcl6 mediates the development of T follicular helper cells. Science 2009, 325:1001-1005.
42. Yu D., et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 2009, 31:457-468.
43. Toellner K.M., et al. T helper 1 (Th1) and Th2 characteristics start to develop during T cell priming and are associated with an immediate ability to induce immunoglobulin class switching. J. Exp. Med. 1998, 187:1193-1204.
44. + cell properties during viral infection. Immunity 2011, 35:633-646.
45. Hsu H.C., et al. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat. Immunol. 2008, 9:166-175.
46. H-17 cells. Nat. Immunol. 2009, 10:167-175.
47. H17 cells. Nat. Immunol. 2012, 13:991-999.
48. Cao A.T., et al. Th17 cells upregulate polymeric Ig receptor and intestinal IgA and contribute to intestinal homeostasis. J. Immunol. 2012, 189:4666-4673.
49. + T cells in reactive lymph nodes during helminth infection are T follicular helper cells. J. Exp. Med. 2009, 206:1001-1007.
50. Zaretsky A.G., et al. T follicular helper cells differentiate from Th2 cells in response to helminth antigens. J. Exp. Med. 2009, 206:991-999.
51. Liang H.E., et al. Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat. Immunol. 2012, 13:58-66.
52. Yusuf I., et al. Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150). J. Immunol. 2010, 185:190-202.
53. Kusam S., et al. Inhibition of Th2 differentiation and GATA-3 expression by BCL-6. J. Immunol. 2003, 170:2435-2441.
54. Oestreich K.J., et al. The lineage-defining factors T-bet and Bcl-6 collaborate to regulate Th1 gene expression patterns. J. Exp. Med. 2011, 208:1001-1013.
55. Gong D., Malek T.R. Cytokine-dependent Blimp-1 expression in activated T cells inhibits IL-2 production. J. Immunol. 2007, 178:242-252.
56. FH-like gene profile. Nat. Immunol. 2012, 13:405-411.
57. Martins G., Calame K. Regulation and functions of Blimp-1 in T and B lymphocytes. Annu. Rev. Immunol. 2008, 26:133-169.
58. Mathew R., et al. BTB-ZF factors recruit the E3 ligase cullin 3 to regulate lymphoid effector programs. Nature 2012, 491:618-621.
59. Mandal M., et al. Epigenetic repression of the Igk locus by STAT5-mediated recruitment of the histone methyltransferase Ezh2. Nat. Immunol. 2011, 12:1212-1220.
60. Yang X.P., et al. Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat. Immunol. 2011, 12:247-254.
61. Pepper M., et al. Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 2011, 35:583-595.
62. H17 differentiation. Nature 2009, 460:405-409.
63. hi CD4 T cells and is independent of CD57 expression. Eur. J. Immunol. 2006, 36:1892-1903.
64. Betz B.C., et al. Batf coordinates multiple aspects of B and T cell function required for normal antibody responses. J. Exp. Med. 2010, 207:933-942.
65. Ise W., et al. The transcription factor BATF controls the global regulators of class-switch recombination in both B cells and T cells. Nat. Immunol. 2011, 12:536-543.
66. Ho I.C., et al. The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 1996, 85:973-983.
67. Kroenke M.A., et al. Bcl6 and Maf cooperate to instruct human follicular helper CD4 T cell differentiation. J. Immunol. 2012, 188:3734-3744.
68. Kwon H., et al. Analysis of interleukin-21-induced Prdm1 gene regulation reveals functional cooperation of STAT3 and IRF4 transcription factors. Immunity 2009, 31:941-952.
69. H-17 cells requires interferon-regulatory factor 4. Nat. Immunol. 2007, 8:958-966.
70. Ma C.S., et al. Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J. Exp. Med. 2008, 205:1551-1557.
71. H17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 2008, 452:773-776.
72. Glasmacher E., et al. A genomic regulatory element that directs assembly and function of immune-specific AP-1-IRF complexes. Science 2012, 338:975-980.
73. Li P., et al. BATF-JUN is critical for IRF4-mediated transcription in T cells. Nature 2012, 490:543-547.
74. + T cells. Immunity 2009, 30:155-167.
75. Miller S.A., et al. Jmjd3 and UTX play a demethylase-independent role in chromatin remodeling to regulate T-box family member-dependent gene expression. Mol. Cell 2010, 40:594-605.
76. + T cell subsets. Semin. Immunol. 2009, 21:62-68.
77. Agarwal S., Rao A. Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 1998, 9:765-775.
78. Ansel K.M., et al. Regulation of Th2 differentiation and Il4 locus accessibility. Annu. Rev. Immunol. 2006, 24:607-656.
79. Vijayanand P., et al. Interleukin-4 production by follicular helper T cells requires the conserved Il4 enhancer hypersensitivity site V. Immunity 2012, 36:175-187.
80. Harada Y., et al. The 3' enhancer CNS2 is a critical regulator of interleukin-4-mediated humoral immunity in follicular helper T cells. Immunity 2012, 36:188-200.
81. Josefowicz S.Z., et al. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 2012, 30:531-564.
82. Takahashi H., et al. TGF-beta and retinoic acid induce the microRNA miR-10a, which targets Bcl-6 and constrains the plasticity of helper T cells. Nat. Immunol. 2012, 13:587-595.
83. + regulatory T cells inhibit the maturation but not the initiation of an autoantibody response. J. Immunol. 2005, 175:4255-4264.
84. + T cells in gut Peyer's patches. Science 2009, 323:1488-1492.
85. Chung Y., et al. Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat. Med. 2011, 17:983-988.
86. + follicular regulatory T cells control the germinal center response. Nat. Med. 2011, 17:975-982.
87. + follicular regulatory T cells. J. Immunol. 2011, 187:4553-4560.
88. Sage P.T., et al. The receptor PD-1 controls follicular regulatory T cells in the lymph nodes and blood. Nat. Immunol. 2013, 14:152-161.
89. Barral P., et al. The location of splenic NKT cells favours their rapid activation by blood-borne antigen. EMBO J. 2012, 31:2378-2390.
90. Chang P.P., et al. Identification of Bcl-6-dependent follicular helper NKT cells that provide cognate help for B cell responses. Nat. Immunol. 2012, 13:35-43.
91. King I.L., et al. Invariant natural killer T cells direct B cell responses to cognate lipid antigen in an IL-21-dependent manner. Nat. Immunol. 2012, 13:44-50.
92. Heintzman N.D., et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009, 459:108-112.
93. Visel A., et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
94. Kanno Y., et al. Transcriptional and epigenetic control of T helper cell specification: molecular mechanisms underlying commitment and plasticity. Annu. Rev. Immunol. 2012, 30:707-731.
95. Wilson C.B., et al. Epigenetic control of T-helper-cell differentiation. Nat. Rev. Immunol. 2009, 9:91-105.
96. Wilson C.B., et al. DNA methylation and the expanding epigenetics of T cell lineage commitment. Semin. Immunol. 2005, 17:105-119.