Priming of T follicular helper cells by dendritic cells

Immunology and Cell Biology

Volumn 92, Issue 1, 2014, Pages 22-27

  Ballesteros Tato, André ^a   Randall, Troy D ^a  

^a The University of Alabama at Birmingham   (United States)

Author keywords

CD4+ T cells; Dendritic cells; T follicular helper

Indexed keywords

INTERLEUKIN 2; INTERLEUKIN 6;

ANTIBODY RESPONSE; CD4+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL MATURATION; CROSS PRESENTATION; DENDRITIC CELL; EFFECTOR CELL; HELPER CELL; HUMAN; NONHUMAN; REVIEW; T LYMPHOCYTE ACTIVATION;

ANIMALS; CELL DIFFERENTIATION; DENDRITIC CELLS; HUMANS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84891799353     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2013.62     Document Type: Review

References (93)

1. Crotty S. Follicular helper CD4 T cells (TFH). Ann Rev Immunol 2011; 29: 621-663.
2. Yu D, Vinuesa CG. The elusive identity of T follicular helper cells. Trends Immunol 2010; 31: 377-383.
3. Goodnow CC, Vinuesa CG, Randall KL, Mackay F, Brink R. Control systems and decision making for antibody production. Nat Immunol 2010; 11: 681-688.
4. Ballesteros-Tato A, Leon B, Graf BA, Moquin A, Adams PS, Lund FE et al. Interleukin-2 inhibits germinal center formation by limiting T follicular helper cell differentiation. Immunity 2012; 36: 847-856.
5. 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: 1006-1010.
6. 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: 1001-1005.
7. 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: 457-468.
8. 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: 932-946.
9. Goenka R, Barnett LG, Silver JS, O'Neill PJ, Hunter CA, Cancro MP 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.
10. Deenick EK, Chan A, Ma CS, Gatto D, Schwartzberg PL, Brink R et al. Follicular helper T cell differentiation requires continuous antigen presentation that is independent of unique B cell signaling. Immunity 2010; 33: 241-253.
11. Poholek AC, Hansen K, Hernandez SG, Eto D, Chandele A, Weinstein JS et al. In vivo regulation of Bcl6 and T follicular helper cell development. J Immunol 2010; 185: 313-326.
12. 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: 5099-5108.
13. Glatman Zaretsky A, Taylor JJ, King IL, Marshall FA, Mohrs M, Pearce EJ. T follicular helper cells differentiate from Th2 cells in response to helminth antigens. J Exp Med 2009; 206: 991-999.
14. Baumjohann D, Okada T, Ansel KM. Cutting edge: distinct waves of BCL6 expression during T follicular helper cell development. J Immunol 2011; 187: 2089-2092.
15. 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: 947-960.
16. Qi H, Cannons JL, Klauschen F, Schwartzberg PL, Germain RN. SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 2008; 455: 764-769.
17. Zaretsky AG, Taylor JJ, King IL, Marshall FA, Mohrs M, Pearce EJ. T follicular helper cells differentiate from Th2 cells in response to helminth antigens. J Exp Med 2009; 206: 991-999.
18. Germain RN, Robey EA, Cahalan MD. A decade of imaging cellular motility and interaction dynamics in the immune system. Science 2012; 336: 1676-1681.
19. Baumjohann D, Preite S, Reboldi A, Ronchi F, Ansel KM, Lanzavecchia A et al. Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity 2013; 38: 596-605.
20. Good-Jacobson KL, Szumilas CG, Chen L, Sharpe AH, Tomayko MM, Shlomchik MJ. PD-1 regulates germinal center B cell survival and the formation and affinity of longlived plasma cells. Nat Immunol 2010; 11: 535-542.
21. Choi YS, Yang JA, Yusuf I, Johnston RJ, Greenbaum J, Peters B et al. Bcl6 expressing follicular helper CD4 T cells are fate committed early and have the capacity to form memory. J Immunol 2013; 190: 4014-4026.
22. Crawford A, Macleod M, Schumacher T, Corlett L, Gray D. Primary T cell expansion and differentiation in vivo requires antigen presentation by B cells. J Immunol 2006; 176: 3498-3506.
23. Forster R, Davalos-Misslitz AC, Rot A. CCR7 and its ligands: balancing immunity and tolerance. Nature reviews. Immunology 2008; 8: 362-371.
24. Weaver CT, Hatton RD, Mangan PR, Harrington LE. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Ann Rev Immunol 2007; 25: 821-852.
25. Pulendran B, Tang H, Manicassamy S. Programming dendritic cells to induce T(H)2 and tolerogenic responses. Nat Immunol 2010; 11: 647-655.
26. Matloubian M, Cyster JG. Th1 cell induction in lymph nodes according to a red-blue chemokine map. Immunity 2012; 37: 954-956.
27. Groom JR, Richmond J, Murooka TT, Sorensen EW, Sung JH, Bankert K et al. CXCR3 chemokine receptor-ligand interactions in the lymph node optimize CD4+ T helper 1 cell differentiation. Immunity 2012; 37: 1091-1103.
28. Leon B, Ballesteros-Tato A, Browning JL, Dunn R, Randall TD, Lund FE. Regulation of T(H)2 development by CXCR5+ dendritic cells and lymphotoxin-expressing B cells. Nat Immunol 2012; 13: 681-690.
29. Randolph DA, Huang G, Carruthers CJ, Bromley LE, Chaplin DD. The role of CCR7 in TH1 and TH2 cell localization and delivery of B cell help in vivo. Science 1999; 286: 2159-2162.
30. 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.
31. Ansel KM, Ngo VN, Hyman PL, Luther SA, Forster R, Sedgwick JD et al. A chemokinedriven positive feedback loop organizes lymphoid follicles. Nature 2000; 406: 309-314.
32. Liu X, Yan X, Zhong B, Nurieva RI, Wang A, Wang X et al. Bcl6 expression specifies the T follicular helper cell program in vivo. J Exp Med 2012; 209: 1841-1852. S1-24.
33. Fillatreau S, Gray D. T cell accumulation in B cell follicles is regulated by dendritic cells and is independent of B cell activation. J Exp Med 2003; 197: 195-206.
34. Saeki H, Wu MT, Olasz E, Hwang ST. A migratory population of skin-derived dendritic cells expresses CXCR5, responds to B lymphocyte chemoattractant in vitro, and colocalizes to B cell zones in lymph nodes in vivo. Eur J Immunol 2000; 30: 2808-2814.
35. Yu P, Wang Y, Chin RK, Martinez-Pomares L, Gordon S, Kosco-Vibois MH et al. B cells control the migration of a subset of dendritic cells into B cell follicles via CXC chemokine ligand 13 in a lymphotoxin-dependent fashion. J Immunol 2002; 168: 5117-5123.
36. Berney C, Herren S, Power CA, Gordon S, Martinez-Pomares L, Kosco-Vilbois MH. A member of the dendritic cell family that enters B cell follicles and stimulates primary antibody responses identified by a mannose receptor fusion protein. J Exp Med 1999; 190: 851-860.
37. Lambrecht BN, Hammad H. Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Ann Rev Immunol 2012; 30: 243-270.
38. Leon B, Lopez-Bravo M, Ardavin C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 2007; 26: 519-531.
39. Nakano H, Lin KL, Yanagita M, Charbonneau C, Cook DN, Kakiuchi T et al. Bloodderived inflammatory dendritic cells in lymph nodes stimulate acute T helper type 1 immune responses. Nat Immunol 2009; 10: 394-402.
40. Ballesteros-Tato A, Leon B, Lund FE, Randall TD. Temporal changes in dendritic cell subsets, cross-priming and costimulation via CD70 control CD8(+) T cell responses to influenza. Nat Immunol 11: 216-224.
41. Randolph GJ, Ochando J, Partida-Sanchez S. Migration of dendritic cell subsets and their precursors. Ann Rev Immunol 2008; 26: 293-316.
42. Plantinga M, Guilliams M, Vanheerswynghels M, Deswarte K, Branco-Madeira F, Toussaint W et al. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 2013; 38: 322-335.
43. Kim TS, Braciale TJ. Respiratory dendritic cell subsets differ in their capacity to support the induction of virus-specific cytotoxic CD8+ T cell responses. PLoS One 2009; 4: e4204.
44. Saeki H, Moore AM, Brown MJ, Hwang ST. Cutting edge: secondary lymphoid-tissue chemokine (SLC) and CC chemokine receptor 7 (CCR7) participate in the emigration pathway of mature dendritic cells from the skin to regional lymph nodes. J Immunol 1999; 162: 2472-2475.
45. Braun A, Worbs T, Moschovakis GL, Halle S, Hoffmann K, Bolter J et al. Afferent lymph-derived T cells and DCs use different chemokine receptor CCR7-dependent routes for entry into the lymph node and intranodal migration. Nat Immunol 2011; 12: 879-887.
46. Forster R, Schubel A, Breitfeld D, Kremmer E, Renner-Muller I, Wolf E et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 1999; 99: 23-33.
47. Ohl L, Mohaupt M, Czeloth N, Hintzen G, Kiafard Z, Zwirner J et al. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 2004; 21: 279-288.
48. Belz GT, Smith CM, Kleinert L, Reading P, Brooks A, Shortman K et al. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc Natl Acad Sci USA 2004; 101: 8670-8675.
49. den Haan JM, Lehar SM, Bevan MJ. CD8(+) but not CD8(-) dendritic cells crossprime cytotoxic T cells in vivo. J Exp Med 2000; 192: 1685-1696.
50. Allan RS, Waithman J, Bedoui S, Jones CM, Villadangos JA, Zhan Y et al. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006; 25: 153-162.
51. Carbone FR, Belz GT, Heath WR. Transfer of antigen between migrating and lymph node-resident DCs in peripheral T-cell tolerance and immunity. Trends Immunol 2004; 25: 655-658.
52. Yoo JK, Fish EN, Braciale TJ. LAPCs promote follicular helper T cell differentiation of Ag-primed CD4+ T cells during respiratory virus infection. J Exp Med 2012; 209: 1853-1867.
53. Bachmann MF, Kopf M, Marsland BJ. Chemokines: more than just road signs. Nat Rev. Immunol 2006; 6: 159-164.
54. Marsland BJ, Battig P, Bauer M, Ruedl C, Lassing U, Beerli RR et al. CCL19 and CCL21 induce a potent proinflammatory differentiation program in licensed dendritic cells. Immunity 2005; 22: 493-505.
55. Yanagawa Y, Onoe K. CCR7 ligands induce rapid endocytosis in mature dendritic cells with concomitant up-regulation of Cdc42 and Rac activities. Blood 2003; 101: 4923-4929.
56. Choi YS, Yang JA, Crotty S. Dynamic regulation of Bcl6 in follicular helper CD4 T (Tfh) cells. Curr Opin Immunol 2013; 25: 366-372.
57. Cannons JL, Lu KT, Schwartzberg PL. T follicular helper cell diversity and plasticity. Trends Immunol 2013; 34: 200-207.
58. Choi YS, Eto D, Yang JA, Lao C, Crotty S. Cutting edge: STAT1 is required for IL-6-mediated Bcl6 induction for early follicular helper cell differentiation. J Immunol 2013; 190: 3049-3053.
59. Eto D, Lao C, DiToro D, Barnett B, Escobar TC, Kageyama R et al. IL-21 and IL-6 are critical for different aspects of B cell immunity and redundantly induce optimal follicular helper CD4 T cell (Tfh) differentiation. PLoS One 2011; 6: e17739.
60. 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: 138-149.
61. 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: 127-137.
62. Nurieva RI, Podd A, Chen Y, Alekseev AM, Yu M, Qi X et al. STAT5 protein negatively regulates T follicular helper (Tfh) cell generation and function. J Biol Chem 2012; 287: 11234-11239.
63. Johnston RJ, Choi YS, Diamond JA, Yang JA, Crotty S. STAT5 is a potent negative regulator of TFH cell differentiation. J Exp Med 2012; 209: 243-250.
64. Harker JA, Lewis GM, Mack L, Zuniga EI. Late interleukin-6 escalates T follicular helper cell responses and controls a chronic viral infection. Science 2011; 334: 825-829.
65. Ferrer IR, Liu D, Pinelli DF, Koehn BH, Stempora LL, Ford ML. CD40/CD154 blockade inhibits dendritic cell expression of inflammatory cytokines but not costimulatory molecules. J Immunol 2012; 189: 4387-4395.
66. Cucak H, Yrlid U, Reizis B, Kalinke U, Johansson-Lindbom B. Type I interferon signaling in dendritic cells stimulates the development of lymph-node-resident T follicular helper cells. Immunity 2009; 31: 491-501.
67. Naranjo-Gomez M, Oliva H, Climent N, Fernandez MA, Ruiz-Riol M, Bofill M et al. Expression and function of the IL-2 receptor in activated human plasmacytoid dendritic cells. Eur J Immunol 2007; 37: 1764-1772.
68. Bonnefoy F, Couturier M, Clauzon A, Remy-Martin JP, Gaugler B, Tiberghien P et al. TGF-beta-exposed plasmacytoid dendritic cells participate in Th17 commitment. J Immunol 2011; 186: 6157-6164.
69. Jego G, Palucka AK, Blanck JP, Chalouni C, Pascual V, Banchereau J. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 2003; 19: 225-234.
70. Ogata M, Ito T, Shimamoto K, Nakanishi T, Satsutani N, Miyamoto R et al. Plasmacytoid dendritic cells have a cytokine-producing capacity to enhance ICOS ligand-mediated IL-10 production during T-cell priming. Int Immunol 2013; 25: 171-182.
71. Ito T, Yang M, Wang YH, Lande R, Gregorio J, Perng OA et al. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med 2007; 204: 105-115.
72. Conrad C, Gregorio J, Wang YH, Ito T, Meller S, Hanabuchi S et al. Plasmacytoid dendritic cells promote immunosuppression in ovarian cancer via ICOS costimulation of Foxp3(+) T-regulatory cells. Cancer Res 2012; 72: 5240-5249.
73. Faget J, Bendriss-Vermare N, Gobert M, Durand I, Olive D, Biota C et al. ICOS-ligand expression on plasmacytoid dendritic cells supports breast cancer progression by promoting the accumulation of immunosuppressive CD4+ T cells. Cancer Res 2012; 72: 6130-6141.
74. GeurtsvanKessel CH, Willart MA, van Rijt LS, Muskens F, Kool M, Baas C et al. Clearance of influenza virus from the lung depends on migratory langerin+CD11b-but not plasmacytoid dendritic cells. J Exp Med 2008; 205: 1621-1634.
75. Kim SJ, Zou YR, Goldstein J, Reizis B, Diamond B. Tolerogenic function of Blimp-1 in dendritic cells. J Exp Med 2011; 208: 2193-2199.
76. Chan YH, Chiang MF, Tsai YC, Su ST, Chen MH, Hou MS et al. Absence of the transcriptional repressor Blimp-1 in hematopoietic lineages reveals its role in dendritic cell homeostatic development and function. J Immunol 2009; 183: 7039-7046.
77. Oestreich KJ, Mohn SE, Weinmann AS. Molecular mechanisms that control the expression and activity of Bcl-6 in TH1 cells to regulate flexibility with a TFH-like gene profile. Nature immunology 2012; 13: 405-411.
78. Granucci F, Vizzardelli C, Pavelka N, Feau S, Persico M, Virzi E et al. Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat Immunol 2001; 2: 882-888.
79. Granucci F, Feau S, Angeli V, Trottein F, Ricciardi-Castagnoli P. Early IL-2 production by mouse dendritic cells is the result of microbial-induced priming. J Immunol 2003; 170: 5075-5081.
80. Andrews DM, Andoniou CE, Granucci F, Ricciardi-Castagnoli P, Degli-Esposti MA. Infection of dendritic cells by murine cytomegalovirus induces functional paralysis. Nat Immunol 2001; 2: 1077-1084.
81. Liao W, Schones DE, Oh J, Cui Y, Cui K, Roh TY et al. Priming for T helper type 2 differentiation by interleukin 2-mediated induction of interleukin 4 receptor alphachain expression. Nat Immunol 2008; 9: 1288-1296.
82. Liao W, Lin JX, Wang L, Li P, Leonard WJ. Modulation of cytokine receptors by IL-2 broadly regulates differentiation into helper T cell lineages. Nat Immunol 2011; 12: 551-559.
83. Wuest SC, Edwan JH, Martin JF, Han S, Perry JS, Cartagena CM et al. A role for interleukin-2 trans-presentation in dendritic cell-mediated T cell activation in humans, as revealed by daclizumab therapy. Nat Med 2011; 17: 604-609.
84. Velten FW, Rambow F, Metharom P, Goerdt S. Enhanced T-cell activation and T-celldependent IL-2 production by CD83+, CD25high, CD43high human monocytederived dendritic cells. Mol Immunol 2007; 44: 1544-1550.
85. Fukao T, Koyasu S. Expression of functional IL-2 receptors on mature splenic dendritic cells. Eur J Immunol 2000; 30: 1453-1457.
86. Nakayamada S, Kanno Y, Takahashi H, Jankovic D, Lu KT, Johnson TA et al. Early Th1 cell differentiation is marked by a Tfh cell-like transition. Immunity 2011; 35: 919-931.
87. Ma CS, Suryani S, Avery DT, Chan A, Nanan R, Santner-Nanan B et al. Early commitment of naive human CD4(+) T cells to the T follicular helper (T(FH)) cell lineage is induced by IL-12. Immunol Cell Biol 2009; 87: 590-600.
88. 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: 158-169.
89. Yang Y, Ochando JC, Bromberg JS, Ding Y. Identification of a distant T-bet enhancer responsive to IL-12/Stat4 and IFNgamma/Stat1 signals. Blood 2007; 110: 2494-2500.
90. Schulz EG, Mariani L, Radbruch A, Hofer T. Sequential polarization and imprinting of type 1T helper lymphocytes by interferon-gamma and interleukin-12. Immunity 2009; 30: 673-683.
91. Huang LY, Reis e Sousa C, Itoh Y, Inman J, Scott DE. IL-12 induction by a TH1-inducing adjuvant in vivo: dendritic cell subsets and regulation by IL-10. J Immunol 2001; 167: 1423-1430.
92. De Smedt T, Butz E, Smith J, Maldonado-Lopez R, Pajak B, Moser M et al. CD8alpha(-) and CD8alpha(+) subclasses of dendritic cells undergo phenotypic and functional maturation in vitro and in vivo. J Leukocyte Biol 2001; 69: 951-958.
93. Hochrein H, Shortman K, Vremec D, Scott B, Hertzog P, O'Keeffe M. Differential production of IL-12, IFN-alpha, and IFN-gamma by mouse dendritic cell subsets. J Immunol 2001; 166: 5448-5455.