T cell help to B cells in germinal centers: Putting the jigsaw together

International Reviews of Immunology

Volumn 29, Issue 4, 2010, Pages 403-420

  Gowthaman, Uthaman ^a   Chodisetti, Sathi Babu ^a   Agrewala, Javed N ^a  

^a INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

Author keywords

B cells; Follicular T helper cells; Germinal centers; T cell subsets

Indexed keywords

B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL LINEAGE; GERMINAL CENTER; HUMAN; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; HELPER CELL; HUMORAL IMMUNITY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MOUSE;

ANIMALS; B-LYMPHOCYTES; CELL DIFFERENTIATION; GERMINAL CENTER; HUMANS; IMMUNITY, HUMORAL; LYMPHOCYTE ACTIVATION; MICE; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 77954784906     PISSN: 08830185     EISSN: 15635244     Source Type: Journal    
DOI: 10.3109/08830185.2010.496503     Document Type: Review

References (75)

1. Rajewsky K, Schirrmacher V, Nase S, Jerne NK. The requirement of more than one antigenic determinant for immunogenicity. J Exp Med 1969; 129: 1131-1143
2. Miller JF. Immunological function of the thymus. Lancet 1961; 2: 748-749
3. Claman HN, Chaperon EA, Triplett RF. Thymus-marrow cell combinations. Synergism in antibody production. Proc Soc Exp Biol Med 1966; 122: 1167-1171
4. Parker DC. T cell-dependent B cell activation. Annu Rev Immunol 1993; 11: 331-360
5. Lanzavecchia A. Antigen-specific interaction between T and B cells. Nature 1985; 314: 537-539
6. McHeyzer-Williams LJ, McHeyzer-Williams MG. Antigen-specific memory B cell development. Annu Rev Immunol 2005; 23 487-513
7. Vinuesa CG, Tangye SG, Moser B, Mackay CR. Follicular B helper T cells in antibody responses and autoimmunity. Nat Rev Immunol 2005; 5: 853-865.
8. Ettinger R, Kuchen S, Lipsky PE. The role of IL-21 in regulating B-cell function in health and disease. Immunol Rev 2008; 223: 60-86.
9. Suvas S, Singh V, Sahdev S, et al. Distinct role of CD80 and CD86 in the regulation of the activation of B cell and B cell lymphoma. J Biol Chem 2002; 277: 77667775.
10. Quezada SA, Jarvinen LZ, Lind EF, Noelle RJ. CD40/CD154 interactions at the interface of tolerance and immunity. Annu Rev Immunol 2004; 22: 307-328.
11. Allen CD, Okada T, Cyster JG. Germinal-center organization and cellular dynamics. Immunity 2007; 27: 190-202.
12. MacLennan IC. Germinal centers. Annu Rev Immunol 1994; 12: 117-139.
13. Klein U, Dalla-Favera R. Germinal centres: Role in B-cell physiology and malignancy. Nat Rev Immunol 2008; 8: 22-33.
14. Mosmann TR, Cherwinski H, Bond MW, 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.
15. MosmannTR, CoffmanRL. TH1 andTH2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 1989; 7: 145-173.
16. Snapper CM, Paul WE. Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 1987; 236: 944-947.
17. Stevens TL, Bossie A, Sanders VM, et al. Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature 1988; 334: 255-258.
18. Boom WH, Liano D, Abbas AK. Heterogeneity of helper/inducer T lymphocytes. II. Effects of interleukin 4- and interleukin 2-producing T cell clones on resting B lymphocytes. J Exp Med 1988; 167: 1350-1363.
19. Finkelman FD, Holmes J, Katona IM, et al. Lymphokine control of in vivo immunoglobulin isotype selection. Annu Rev Immunol 1990; 8: 303-333.
20. Zhu J, Yamane H, Paul WE. Differentiation of effector CD4 T cell populations. Annu Rev Immunol 2010; 28: 445-489.
21. Zhou L, Chong MM, Littman DR. Plasticity of CD4+ T cell lineage differentiation. Immunity 2009; 30: 646-655.
22. Locksley RM. Nine lives: Plasticity among T helper cell subsets. J Exp Med 2009; 206: 1643-1646.
23. Reinhardt RL, Liang HE, Locksley RM. Cytokine-secreting follicular T cells shape the antibody repertoire. Nat Immunol 2009; 10: 385-393.
24. Schaerli P, Willimann K, Lang AB, et al. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J Exp Med 2000; 192: 1553-1562.
25. 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: 1545-1552.
26. Chtanova T, Tangye SG, Newton R, et al. T follicular helper cells express a distinctive transcriptional profile, reflecting their role as non-Th1/Th2 effector cells that provide help for B cells. J Immunol 2004; 173: 68-78.
27. King C, Tangye SG, Mackay CR. T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu Rev Immunol 2008; 26: 741-766.
28. Fazilleau N, Mark L, McHeyzer-Williams LJ, McHeyzer-Williams MG. Follicular helper T cells: Lineage and location. Immunity 2009; 30: 324-335.
29. Catron DM, Itano AA, Pape KA, et al. Visualizing the first 50 hr of the primary immune response to a soluble antigen. Immunity 2004; 21: 341-347.
30. Bromley SK, Mempel TR, Luster AD. Orchestrating the orchestrators: Chemokines in control of T cell traffic. Nat Immunol 2008; 9: 970-980.
31. Reif K, Ekland EH, Ohl L, et al. Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature 2002; 416: 94-99.
32. Haynes NM, Allen CD, Lesley R, et al. Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1 high germinal center-associated subpopulation. J Immunol 2007; 179: 5099-5108.
33. Hardtke S, Ohl L, Forster R. 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.
34. MacLennan IC, Toellner KM, Cunningham AF, et al. Extrafollicular antibody responses. Immunol Rev 2003; 194: 8-18.
35. Allen CD, Cyster JG. Follicular dendritic cell networks of primary follicles and germinal centers: Phenotype and function. Semin Immunol 2008; 20: 14-25.
36. Suzuki K, Grigorova I, Phan TG, et al. Visualizing B cell capture of cognate antigen from follicular dendritic cells. J Exp Med 2009; 206: 1485-1493.
37. Allen CD, Okada T, Tang HL, Cyster JG. Imaging of germinal center selection events during affinity maturation. Science 2007; 315: 528-531.
38. Allen CD, Ansel KM, Low C, et al. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat Immunol 2004; 5: 943-952.
39. Muramatsu M, Kinoshita K, Fagarasan S, et al. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000; 102: 553-563.
40. Harriman W, Volk H, Defranoux N, Wabl M. Immunoglobulin class switch recombination. Annu Rev Immunol 1993; 11: 361-384.
41. Ozaki K, Spolski R, Feng CG, et al. A critical role for IL-21 in regulating immunoglobulin production. Science 2002; 298: 1630-1634.
42. Nurieva RI, Chung Y, Hwang D, 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.
43. Coffey F, Alabyev B, Manser T. Initial clonal expansion of germinal center B cells takes place at the perimeter of follicles. Immunity 2009; 30: 599-609.
44. McHeyzer-Williams MG, McLean MJ, Lalor PA, Nossal GJ. Antigen-driven B cell differentiation in vivo. J Exp Med 1993; 178: 295-307.
45. Zaheen A, Boulianne B, Parsa JY, et al. AID constrains germinal center size by rendering B cells susceptible to apoptosis. Blood 2009; 114: 547-554.
46. Vogelzang A, McGuire HM, Yu D, et al. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 2008; 29: 127-137.
47. Nurieva RI, Chung Y, Martinez GJ, et al. Bcl6 mediates the development of T follicular helper cells. Science 2009; 325: 1001-1005.
48. Johnston RJ, Poholek AC, DiToro D, et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators ofT follicular helper cell differentiation. Science 2009; 325: 1006-1010.
49. Yu D, Rao S, Tsai LM, et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 2009; 31: 457-468.
50. King IL, Mohrs M. IL-4-producing CD4+ T cells in reactive lymph nodes during helminth infection are T follicular helper cells. J Exp Med 2009; 206: 10011007.
51. Zaretsky AG, Taylor JJ, King IL, et al. T follicular helper cells differentiate from Th2 cells in response to helminth antigens. J Exp Med 2009; 206: 991999.
52. Tsuji M, Komatsu N, Kawamoto S, et al. Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science 2009; 323: 1488-1492.
53. Fazilleau N, McHeyzer-Williams LJ, Rosen H, McHeyzer-Williams MG. The function of follicular helper T cells is regulated by the strength of T cell antigen receptor binding. Nat Immunol 2009; 10: 375-384.
54. Hsu HC, Yang P, Wang J, 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.
55. Crotty S, Johnston RJ, Schoenberger SP. Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat Immunol 2010; 11: 114-120.
56. Schaerli P, Loetscher P, Moser B. Cutting edge: Induction of follicular homing precedes effector Th cell development. J Immunol 2001; 167: 6082-6086.
57. Linterman MA, Rigby RJ, Wong RK, et al. Follicular helper T cells are required for systemic autoimmunity. J Exp Med 2009; 206: 561-576.
58. Mak TW, Shahinian A, Yoshinaga SK, et al. Costimulation through the inducible costimulator ligand is essential for both T helper and B cell functions in T cell- dependent B cell responses. Nat Immunol 2003; 4: 765-772.
59. Tafuri A, Shahinian A, Bladt F, et al. ICOS is essential for effective T-helper-cell responses. Nature 2001; 409: 105-109.
60. McAdam AJ, Greenwald RJ, Levin MA, et al. ICOS is critical for CD40-mediated antibody class switching. Nature 2001; 409: 102-105.
61. Crotty S, Kersh EN, Cannons J, et al. SAP is required for generating long-term humoral immunity. Nature 2003; 421: 282-287.
62. Qi H, Cannons JL, Klauschen F, et al. SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 2008; 455: 764-769.
63. Cannons JL, Qi H, Lu KT, et al. Optimal germinal center responses require a multistage T cell: B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 2010; 32: 253-265.
64. Baccam M, Woo SY, Vinson C, Bishop GA. CD40-mediated transcriptional regulation of the IL-6 gene in B lymphocytes: Involvement of NF-kappa B, AP-1, and C/EBP. J Immunol 2003; 170: 3099-3108.
65. Urashima M, Chauhan D, Hatziyanni M, et al. CD40 ligand triggers interleukin-6 mediated B cell differentiation. Leuk Res 1996; 20: 507-515.
66. Odegard JM, Marks BR, DiPlacido LD, et al. ICOS-dependent extrafollicular helper T cells elicit IgG production via IL-21 in systemic autoimmunity. J Exp Med 2008; 205: 2873-2886.
67. Han S, Hathcock K, Zheng B, et al. Cellular interaction in germinal centers. Roles of CD40 ligand and B7-2 in established germinal centers. J Immunol 1995; 155: 556-567.
68. Good-Jacobson KL, Szumilas CG, Chen L, et al. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat Immunol 2010; 11: 535-542.
69. Spolski R, Leonard WJ. Interleukin-21: Basic biology and implications for cancer and autoimmunity. Annu Rev Immunol 2008; 26: 57-79.
70. Jin H, Carrio R, Yu A, Malek TR. Distinct activation signals determine whether IL-21 induces B cell costimulation, growth arrest, or Bim-dependent apoptosis. J Immunol 2004; 173: 657-665.
71. Zotos D, Coquet JM, Zhang Y, 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.
72. Linterman MA, Beaton L, Yu D, 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.
73. Meyer-Hermann M, Figge MT, Toellner KM. Germinal centres seen through the mathematical eye: B-cell models on the catwalk. Trends Immunol 2009; 30: 157-164.
74. Phan TG, Paus D, Chan TD, et al. High affinity germinal center B cells are actively selected into the plasma cell compartment. J Exp Med 2006; 203: 2419-2424.
75. Wei G, Wei L, Zhu J, et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 2009; 30: 155-167.