Modulation of SAP dependent T:B cell interactions as a strategy to improve vaccination

Current Opinion in Virology

Volumn 3, Issue 3, 2013, Pages 363-370

  Hu, Joyce ^a   Havenar Daughton, Colin ^a   Crotty, Shane ^a,b,c  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c Center for HIV/AIDS Vaccine Immunology and Immunogen Discovery   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 4; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN;

ANTIBODY RESPONSE; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL SURVIVAL; CYTOKINE RELEASE; GERMINAL CENTER; HELPER CELL; HUMAN; MODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SOMATIC HYPERMUTATION; T LYMPHOCYTE; VACCINATION;

EID: 84880321279     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2013.05.015     Document Type: Review

References (75)

1. S. Crotty Follicular helper CD4 T cells (TFH) Annu Rev Immunol 29 2011 621 663
2. R.J. Johnston, A.C. Poholek, D. DiToro, I. Yusuf, D. Eto, B. Barnett, A.L. Dent, J. Craft, and S. Crotty Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation Science 325 2009 1006 1010
3. R.I. Nurieva, Y. Chung, G.J. Martinez, X.O. Yang, S. Tanaka, T.D. Matskevitch, Y.-H. Wang, and C. Dong Bcl6 mediates the development of T follicular helper cells Science 325 2009 1001 1005
4. D. Yu, S. Rao, L.M. Tsai, S.K. Lee, Y. He, E.L. Sutcliffe, M. Srivastava, M. Linterman, L. Zheng, and N. Simpson The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment Immunity 31 2009 457 468
5. G.D. Victora, and M.C. Nussenzweig Germinal centers Annu Rev Immunol 30 2012 429 457
6. C.G. Vinuesa, and J.G. Cyster How T cells earn the follicular rite of passage Immunity 35 2011 671 680
7. G.D. Victora, T.A. Schwickert, D.R. Fooksman, A.O. Kamphorst, M. Meyer-Hermann, M.L. Dustin, and M.C. Nussenzweig Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter Cell 143 2010 592 605
8. J. Rolf, K. Fairfax, and M. Turner Signaling pathways in T follicular helper cells J Immunol 184 2010 6563 6568
9. A.E. Ballesteros-Tato, B. León, B.A. Graf, A. Moquin, P.S. Adams, F.E. Lund, and T.D. Randall Interleukin-2 inhibits germinal center formation by limiting T follicular helper cell differentiation Immunity 36 2012 847 856
10. C. Petrovas, T. Yamamoto, M.Y. Gerner, K.L. Boswell, K. Wloka, E.C. Smith, D.R. Ambrozak, N.G. Sandler, K.J. Timmer, and X. Sun CD4 T follicular helper cell dynamics during SIV infection The Journal of clinical investigation 122 2012 3281 3294
11. H. Streeck, M.P. D'Souza, D.R. Littman, and S. Crotty Harnessing CD4(+) T cell responses in HIV vaccine development Nat Med 19 2013 143 149
12. M. Lindqvist, J. van Lunzen, D.Z. Soghoian, B.D. Kuhl, S. Ranasinghe, G. Kranias, M.D. Flanders, S. Cutler, N. Yudanin, and M.I. Muller Expansion of HIV-specific T follicular helper cells in chronic HIV infection J Clin Invest 122 2012 3271 3280
13. R.A. Cubas, J.C. Mudd, A.-L. Savoye, M. Perreau, J. van Grevenynghe, T. Metcalf, E. Connick, A. Meditz, G.J. Freeman, and G. Abesada-Terk Inadequate T follicular cell help impairs B cell immunity during HIV infection Nat Med 19 2013 494 499
14. N. Mehta, C.K. Cunningham, P. Flynn, J. Pepe, S. Obaro, B.G. Kapogiannis, J. Bethel, and K. Luzuriaga Adolescent Trials Network for HIV/AIDS Interventions: impaired generation of hepatitis B virus-specific memory B cells in HIV infected individuals following vaccination Vaccine 28 2010 3672 3678
15. K. Titanji, A. De Milito, A. Cagigi, R. Thorstensson, S. Grutzmeier, A. Atlas, B. Hejdeman, F.P. Kroon, L. Lopalco, and A. Nilsson Loss of memory B cells impairs maintenance of long-term serologic memory during HIV-1 infection Blood 108 2006 1580 1587
16. S. Pallikkuth, S. Pilakka Kanthikeel, S.Y. Silva, M. Fischl, R. Pahwa, and S. Pahwa Upregulation of IL-21 receptor on B cells and IL-21 secretion distinguishes novel 2009 H1N1 vaccine responders from nonresponders among HIV-infected persons on combination antiretroviral therapy J Immunol 186 2011 6173 6181
17. S. Pallikkuth, S. Pilakka Kanthikeel, S.Y. Silva, M. Fischl, R. Pahwa, and S. Pahwa Upregulation of IL-21 receptor on B cells and IL-21 secretion distinguishes novel 2009 H1N1 vaccine responders from nonresponders among HIV-infected persons on combination antiretroviral therapy J Immunol 186 2011 6173 6181
18. M.A. Kroenke, D. Eto, M. Locci, M. Cho, T. Davidson, E.K. Haddad, and S. Crotty Bcl6 and Maf cooperate to instruct human follicular helper CD4 T cell differentiation J Immunol 188 2012 3734 3744
19. R.J. Armitage, W.C. Fanslow, L. Strockbine, T.A. Sato, K.N. Clifford, B.M. Macduff, D.M. Anderson, S.D. Gimpel, T. Davis-Smith, and C.R. Maliszewski Molecular and biological characterization of a murine ligand for CD40 Nature 357 1992 80 82
20. S. Lederman, M.J. Yellin, G. Inghirami, J.J. Lee, D.M. Knowles, and L. Chess Molecular interactions mediating T-B lymphocyte collaboration in human lymphoid follicles. Roles of T cell-B-cell-activating molecule (5c8 antigen) and CD40 in contact-dependent help J Immunol 149 1992 3817 3826
21. R.J. Noelle, M. Roy, D.M. Shepherd, I. Stamenkovic, J.A. Ledbetter, and A. Aruffo A 39-kDa protein on activated helper T cells binds CD40 and transduces the signal for cognate activation of B cells Proc Natl Acad Sci USA 89 1992 6550 6554
22. R. Ettinger, G.P. Sims, A.-M. Fairhurst, R. Robbins, Y.S. da Silva, R. Spolski, W.J. Leonard, and P.E. Lipsky IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells J Immunol 175 2005 7867 7879
23. V.L. Bryant, C.S. Ma, D.T. Avery, Y. Li, K.L. Good, L.M. Corcoran, R. de Waal Malefyt, and S.G. Tangye Cytokine-mediated regulation of human B cell differentiation into Ig-secreting cells: predominant role of IL-21 produced by CXCR5+ T follicular helper cells J Immunol 179 2007 8180 8190
24. D.T. Avery, E.K. Deenick, C.S. Ma, S. Suryani, N. Simpson, G.Y. Chew, T.D. Chan, U. Palendira, J. Bustamante, and S. Boisson-Dupuis B cell-intrinsic signaling through IL-21 receptor and STAT3 is required for establishing long-lived antibody responses in humans J Exp Med 207 2010 155 171
25. D. Zotos, J.M. Coquet, Y. Zhang, A. Light, K. D'Costa, A. Kallies, L.M. Corcoran, D.I. Godfrey, K.-M. Toellner, and M.J. Smyth IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism J Exp Med 207 2010 365 378
26. M.A. Linterman, L. Beaton, D. Yu, R.R. Ramiscal, M. Srivastava, J.J. Hogan, N.K. Verma, M.J. Smyth, R.J. Rigby, and C.G. Vinuesa IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses J Exp Med 207 2010 353 363
27. E. Arguni JunD/AP-1 and STAT3 are the major enhancer molecules for high Bcl6 expression in germinal center B cells Int Immunol 18 2006 1079 1089
28. R.L. Reinhardt, H.-E. Liang, and R.M. Locksley Cytokine-secreting follicular T cells shape the antibody repertoire Nat Immunol 10 2009 385 393
29. I. Yusuf, R. Kageyama, L. Monticelli, R.J. Johnston, D. DiToro, K. Hansen, B. Barnett, and S. Crotty Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150) J Immunol 185 2010 190 202
30. H.-E. Liang, R.L. Reinhardt, J.K. Bando, B.M. Sullivan, I.-C. Ho, and R.M. Locksley Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity Nat Immunol 2011 10.1038/ni.2182
31. P. Vijayanand, G.E.G. Seumois, L.J. Simpson, S. Abdul-Wajid, D. Baumjohann, M. Panduro, X. Huang, J. Interlandi, I.M. Djuretic, and D.R. Brown Interleukin-4 production by follicular helper T cells requires the conserved Il4 enhancer hypersensitivity site V Immunity 36 2012 175 187
32. Y. Harada, S. Tanaka, Y. Motomura, Y. Harada, S.-I. Ohno, S. Ohno, Y. Yanagi, H. Inoue, and M. Kubo The 3′ enhancer CNS2 is a critical regulator of interleukin-4-mediated humoral immunity in follicular helper T cells Immunity 36 2012 188 200
33. S. Tanaka, Y. Motomura, Y. Suzuki, R. Yagi, H. Inoue, S. Miyatake, and M. Kubo The enhancer HS2 critically regulates GATA-3-mediated Il4 transcription in T(H)2 cells Nat Immunol 12 2011 77 85
34. J.I. Kim, I.C. Ho, M.J. Grusby, and L.H. Glimcher The transcription factor c-Maf controls the production of interleukin-4 but not other Th2 cytokines Immunity 10 1999 745 751
35. Y. Hiramatsu, A. Suto, D. Kashiwakuma, H. Kanari, S.-I. Kagami, K. Ikeda, K. Hirose, N. Watanabe, M.J. Grusby, and I. Iwamoto c-Maf activates the promoter and enhancer of the IL-21 gene, and TGF-beta inhibits c-Maf-induced IL-21 production in CD4+ T cells J Leukoc Biol 87 2010 703 712
36. A.T. Bauquet, H. Jin, A.M. Paterson, M. Mitsdoerffer, I.-C. Ho, A.H. Sharpe, and V.K. Kuchroo The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and TH-17 cells Nat Immunol 10 2009 167 175
37. A. Rani, B. Afzali, A. Kelly, L. Tewolde-Berhan, M. Hackett, A.S. Kanhere, I. Pedroza-Pacheco, H. Bowen, S. Jurcevic, and R.G. Jenner IL-2 regulates expression of C-MAF in human CD4 T cells J Immunol 187 2011 3721 3729
38. K. Basso, C. Schneider, Q. Shen, A.B. Holmes, M. Setty, C. Leslie, and R. Dalla-Favera BCL6 positively regulates AID and germinal center gene expression via repression of miR-155 J Exp Med 209 2012 2455 2465
39. L.M. Walker, M. Huber, K.J. Doores, E. Falkowska, R. Pejchal, J.-P. Julien, S.-K. Wang, A. Ramos, P.-Y. Chan-Hui, and M. Moyle Broad neutralization coverage of HIV by multiple highly potent antibodies Nature 477 2011 466 470
40. D.R. Burton, R. Ahmed, D.H. Barouch, S.T. Butera, S. Crotty, A. Godzik, D.E. Kaufmann, M.J. McElrath, M.C. Nussenzweig, and B. Pulendran A blueprint for HIV vaccine discovery Cell Host and Microbe 12 2012 396 407
41. S. Crotty, E.N. Kersh, J. Cannons, P.L. Schwartzberg, and R. Ahmed SAP is required for generating long-term humoral immunity Nature 421 2003 282 287
42. J.L. Cannons, S.G. Tangye, and P.L. Schwartzberg SLAM family receptors and SAP adaptors in immunity Annu Rev Immunol 29 2011 665 705
43. C.S. Ma, S. Suryani, D.T. Avery, A. Chan, R. Nanan, B. Santner-Nanan, E.K. Deenick, and S.G. Tangye Early commitment of naïve human CD4(+) T cells to the T follicular helper (T(FH)) cell lineage is induced by IL-12 Immunol Cell Biol 87 2009 590 600
44. J.L. Cannons, H. Qi, K.T. Lu, M. Dutta, J. Gomez-Rodriguez, J. Cheng, E.K. Wakeland, R.N. Germain, and P.L. Schwartzberg Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84 Immunity 32 2010 253 265
45. R. Kageyama, J.L. Cannons, F. Zhao, I. Yusuf, C. Lao, M. Locci, P.L. Schwartzberg, and S. Crotty The Receptor Ly108 Functions as a SAP Adaptor-Dependent On-Off Switch for T Cell Help to B Cells and NKT Cell Development Immunity 2012 10.1016/j.immuni.2012.05.016
46. M.A. la Fuente de, V. Tovar, N. Villamor, N. Zapater, P. Pizcueta, E. Campo, J. Bosch, and P. Engel Molecular characterization and expression of a novel human leukocyte cell-surface marker homologous to mouse Ly-9 Blood 97 2001 3513 3520
47. J. Sintes, M. Vidal-Laliena, X. Romero, V. Tovar, and P. Engel Characterization of mouse CD229 (Ly9), a leukocyte cell surface molecule of the CD150 (SLAM) family Tissue Antigens 70 2007 355 362
48. C.G. Vinuesa, S.G. Tangye, B. Moser, and C.R. Mackay Follicular B helper T cells in antibody responses and autoimmunity Nat Rev Immunol 5 2005 853 865
49. C.S. Ma, N.J. Hare, K.E. Nichols, L. Dupré, G. Andolfi, M.-G. Roncarolo, S. Adelstein, P.D. Hodgkin, and S.G. Tangye Impaired humoral immunity in X-linked lymphoproliferative disease is associated with defective IL-10 production by CD4+ T cells J Clin Invest 115 2005 1049 1059
50. J.L. Cannons, L.J. Yu, B. Hill, L.A. Mijares, and Dombroski D SAP regulates TH2 differentiation and PKC-θ-mediated activation of NF-κB1 Immunity 21 2004 693 706
51. H. Qi, J.L. Cannons, F. Klauschen, P.L. Schwartzberg, and R.N. Germain SAP-controlled T-B cell interactions underlie germinal centre formation Nature 455 2008 764 769
52. Y.S. Choi, R. Kageyama, D. Eto, T.C. Escobar, R.J. Johnston, L. Monticelli, C. Lao, and S. Crotty ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6 Immunity 34 2011 932 946
53. F. Zhao, J.L. Cannons, M. Dutta, G.M. Griffiths, and P.L. Schwartzberg Positive and Negative Signaling through SLAM Receptors Regulate Synapse Organization and Thresholds of Cytolysis Immunity 36 2012 1003 1016
54. Z. Dong, D. Davidson, L.A. Pérez-Quintero, T. Kurosaki, W. Swat, and A.E. Veillette The adaptor SAP controls NK cell activation by regulating the enzymes Vav-1 and SHIP-1 and by enhancing conjugates with target cells Immunity 36 2012 974 985
55. S. Latour, R. Roncagalli, R. Chen, M. Bakinowski, X. Shi, P.L. Schwartzberg, D. Davidson, and A.E. Veillette Binding of SAP SH2 domain to FynT SH3 domain reveals a novel mechanism of receptor signalling in immune regulation Nature Publishing Group 5 2003 149 154
56. J.L. Cannons, J.Z. Wu, J. Gomez-Rodriguez, J. Zhang, B. Dong, Y. Liu, S. Shaw, K.A. Siminovitch, and P.L. Schwartzberg Biochemical and genetic evidence for a SAP-PKC-interaction contributing to IL-4 regulation J Immunol 185 2010 2819 2827
57. D.B. Graham, M.P. Bell, M.M. McCausland, C.J. Huntoon, J. van Deursen, W.A. Faubion, S. Crotty, and D.J. McKean Ly9 (CD229)-deficient mice exhibit T cell defects yet do not share several phenotypic characteristics associated with SLAM- and SAP-deficient mice J Immunol 176 2006 291 300
58. M.M. McCausland, I. Yusuf, H. Tran, N. Ono, Y. Yanagi, and S. Crotty SAP regulation of follicular helper CD4 T Cell development and humoral immunity is independent of SLAM and Fyn kinase J Immunol 178 2007 817 828
59. M. Kitano, S. Moriyama, Y. Ando, M. Hikida, Y. Mori, T. Kurosaki, and T. Okada Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity Immunity 34 2011 961 972
60. S.M. Kerfoot, G. Yaari, J.R. Patel, K.L. Johnson, D.G. Gonzalez, S.H. Kleinstein, and A.M. Haberman Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone Immunity 34 2011 947 960
61. S.K. Lee, R.J. Rigby, D. Zotos, L.M. Tsai, S. Kawamoto, J.L. Marshall, R.R. Ramiscal, T.D. Chan, D. Gatto, and R. Brink B cell priming for extrafollicular antibody responses requires Bcl-6 expression by T cells J Exp Med 208 2011 1377 1388
62. T. Okada, M.J. Miller, I. Parker, M.F. Krummel, M. Neighbors, S.B. Hartley, A. O'Garra, M.D. Cahalan, and J.G. Cyster Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells PLoS Biol 3 2005 e150
63. A.J. Pollard, and A.V.S. Hill Antibody repertoire: embracing diversity Sci Transl Med 3 2011 ps32
64. W.E. Purtha, T.F. Tedder, S. Johnson, D. Bhattacharya, and M.S. Diamond Memory B cells, but not long-lived plasma cells, possess antigen specificities for viral escape mutants J Exp Med 208 2011 2599 2606
65. M.J. Czar, E.N. Kersh, L.A. Mijares, G. Lanier, J. Lewis, G. Yap, A. Chen, A. Sher, C.S. Duckett, and R. Ahmed Altered lymphocyte responses and cytokine production in mice deficient in the X-linked lymphoproliferative disease gene SH2D1A/DSHP/SAP Proc Natl Acad Sci USA 98 2001 7449 7454
66. S. Latour, G. Gish, C.D. Helgason, R.K. Humphries, T. Pawson, and A. Veillette Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product Nat Immunol 2 2001 681 690
67. C. Wu, K.B. Nguyen, G.C. Pien, N. Wang, C. Gullo, D. Howie, M.R. Sosa, M.J. Edwards, P. Borrow, and A.R. Satoskar SAP controls T cell responses to virus and terminal differentiation of TH2 cells Nat Immunol 2 2001 410 414
68. G.D. Victora, D. Dominguez-Sola, A.B. Holmes, S. Deroubaix, R. Dalla-Favera, and Nussenzweig MC Identification of human germinal center light and dark zone cells and their relationship to human B-cell lymphomas Blood 120 2012 2240 2248
69. C.D.C. Allen, T. Okada, and J.G. Cyster Germinal-center organization and cellular dynamics Immunity 27 2007 190 202
70. S. Martin, and M.J. Bevan Transient alteration of T cell fine specificity by a strong primary stimulus correlates with T cell receptor down-regulation Eur J Immunol 28 1998 2991 3002
71. E. San José, A. Borroto, F. Niedergang, A. Alcover, and B. Alarcón Triggering the TCR complex causes the downregulation of nonengaged receptors by a signal transduction-dependent mechanism Immunity 12 2000 161 170
72. I. Stefanová, B. Hemmer, M. Vergelli, R. Martin, W.E. Biddison, and R.N. Germain TCR ligand discrimination is enforced by competing ERK positive and SHP-1 negative feedback pathways Nat Immunol 4 2003 248 254
73. Y.A. Aldhamen, D.M. Appledorn, S.S. Seregin, Liu C-JJ, N.J. Schuldt, S. Godbehere, and A. Amalfitano Expression of the SLAM family of receptors adapter EAT-2 as a novel strategy for enhancing beneficial immune responses to vaccine antigens J Immunol 186 2011 722 732
74. R.A. Cubas, J.C. Mudd, A.-L. Savoye, M. Perreau, J. van Grevenynghe, T. Metcalf, E. Connick, A. Meditz, G.J. Freeman, and G. Abesada-Terk Inadequate T follicular cell help impairs B cell immunity during HIV infection Nat Med 19 2013 494 499
75. L.M. Shlapatska, S.V. Mikhalap, A.G. Berdova, O.M. Zelensky, T.J. Yun, and K.E. Nichols CD150 association with either the SH2-containing inositol phosphatase or the SH2-containing protein tyrosine phosphatase is regulated by the adaptor protein SH2D1A Journal of Immunology 166 9 2001 5480 5487