B and T lymphocyte attenuator suppresses IL-21 production from follicular Th cells and subsequent humoral immune responses

Journal of Immunology

Volumn 185, Issue 5, 2010, Pages 2730-2736

  Kashiwakuma, Daisuke ^a,b   Suto, Akira ^a,b   Hiramatsu, Yukiko ^a,b   Ikeda, Kei ^b   Takatori, Hiroaki ^a   Suzuki, Kotaro ^a   Kagami, Shin Ichiro ^a,b   Hirose, Koichi ^b   Watanabe, Norihiko ^b   Iwamoto, Itsuo ^c   Nakajima, Hiroshi ^a,b  

^a CHIBA UNIVERSITY   (Japan)

^b CHIBA UNIVERSITY HOSPITAL   (Japan)

^c ASAHI GENERAL HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

B AND T LYMPHOCYTE ATTENUATOR PROTEIN; CHEMOKINE RECEPTOR CXCR5; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; INTERLEUKIN 21; INTERLEUKIN 21 RECEPTOR; LYMPHOCYTE RECEPTOR; MONOCLONAL ANTIBODY; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; BLR1 PROTEIN, MOUSE; BTLA PROTEIN, HUMAN; BTLA PROTEIN, MOUSE; CXCR5 PROTEIN, HUMAN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN RECEPTOR; INTERLEUKIN DERIVATIVE;

ADOPTIVE TRANSFER; ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLUORESCENCE ACTIVATED CELL SORTING; FOLLICULAR TH CELL; HUMORAL IMMUNITY; IMMUNOGLOBULIN PRODUCTION; IMMUNOREGULATION; LYMPHOCYTE TRANSFER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPLEEN CELL; T LYMPHOCYTE; TH17 CELL; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL DIFFERENTIATION; COMPARATIVE STUDY; CYTOLOGY; DOWN REGULATION; DRUG ANTAGONISM; GENETICS; HELPER CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPH NODE; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; TRANSGENIC MOUSE; TRANSPLANTATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; DOWN-REGULATION; IMMUNE TOLERANCE; IMMUNOGLOBULIN G; INTERLEUKINS; LYMPH NODES; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, CXCR5; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 78049354525     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903839     Document Type: Article

References (43)

1. Vinuesa, C. G., S. G. Tangye, B. Moser, and C. R. Mackay. 2005. Follicular B helper T cells in antibody responses and autoimmunity. Nat. Rev. Immunol. 5: 853-865.
2. King, C., S. G. Tangye, and C. R. Mackay. 2008. T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu. Rev. Immunol. 26: 741-766.
3. Fazilleau, N., L. Mark, L. J. McHeyzer-Williams, and M. G. McHeyzer-Williams. 2009. Follicular helper T cells: lineage and location. Immunity 30: 324-335.
4. Dong, C., U. A. Temann, and R. A. Flavell. 2001. Cutting edge: critical role of inducible costimulator in germinal center reactions. J. Immunol. 166: 3659-3662.
5. Mak, T. W., A. Shahinian, S. K. Yoshinaga, A. Wakeham, L. M. Boucher, M. Pintilie, G. Duncan, B. U. Gajewska, M. Gronski, U. Eriksson, et al. 2003. 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. 4: 765-772.
6. Parrish-Novak, J., S. R. Dillon, A. Nelson, A. Hammond, C. Sprecher, J. A. Gross, J. Johnston, K. Madden, W. Xu, J. West, et al. 2000. Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 408: 57-63.
7. Spolski, R., and W. J. Leonard. 2008. Interleukin-21: basic biology and implications for cancer and autoimmunity. Annu. Rev. Immunol. 26: 57-79.
8. Monteleone, G., F. Pallone, and T. T. Macdonald. 2009. Interleukin-21 (IL-21)-mediated pathways in T cell-mediated disease. Cytokine Growth Factor Rev. 20: 185-191.
9. Nurieva, R. I., Y. Chung, D. Hwang, X. O. Yang, H. S. Kang, L. Ma, Y. H. Wang, S. S. Watowich, A. M. Jetten, Q. Tian, and C. Dong. 2008. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29: 138-149.
10. Vogelzang, A., H. M. McGuire, D. Yu, J. Sprent, C. R. Mackay, and C. King. 2008. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 29: 127-137.
11. Suto, A., H. Nakajima, K. Hirose, K. Suzuki, S. Kagami, Y. Seto, A. Hoshimoto, Y. Saito, D. C. Foster, and I. Iwamoto. 2002. Interleukin 21 prevents antigen-induced IgE production by inhibiting germ line C(ε) transcription of IL-4-stimulated B cells. Blood 100: 4565-4573.
12. Ozaki, K., R. Spolski, C. G. Feng, C. F. Qi, J. Cheng, A. Sher, H. C. Morse, III, C. Liu, P. L. Schwartzberg, and W. J. Leonard. 2002. A critical role for IL-21 in regulating immunoglobulin production. Science 298: 1630-1634.
13. Harada, M., K. Magara-Koyanagi, H. Watarai, Y. Nagata, Y. Ishii, S. Kojo, S. Horiguchi, Y. Okamoto, T. Nakayama, N. Suzuki, et al. 2006. IL-21-induced Bepsilon cell apoptosis mediated by natural killer T cells suppresses IgE responses. J. Exp. Med. 203: 2929-2937.
14. Croft, M. 2005. The evolving crosstalk between co-stimulatory and co-inhibitory receptors: HVEM-BTLA. Trends Immunol. 26: 292-294.
15. Murphy, K. M., C. A. Nelson, and J. R. Sedý. 2006. Balancing co-stimulation and inhibition with BTLA and HVEM. Nat. Rev. Immunol. 6: 671-681.
16. Cai, G., and G. J. Freeman. 2009. The CD160, BTLA, LIGHT/HVEM pathway: a bidirectional switch regulating T-cell activation. Immunol. Rev. 229: 244-258.
17. Montgomery, R. I., M. S. Warner, B. J. Lum, and P. G. Spear. 1996. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87: 427-436.
18. Sedy, J. R., M. Gavrieli, K. G. Potter, M. A. Hurchla, R. C. Lindsley, K. Hildner, S. Scheu, K. Pfeffer, C. F. Ware, T. L. Murphy, and K. M. Murphy. 2005. B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator. Nat. Immunol. 6: 90-98.
19. Gonzalez, L. C., K. M. Loyet, J. Calemine-Fenaux, V. Chauhan, B. Wranik, W. Ouyang, and D. L. Eaton. 2005. A coreceptor interaction between the CD28 and TNF receptor family members B and T lymphocyte attenuator and herpesvirus entry mediator. Proc. Natl. Acad. Sci. USA 102: 1116-1121.
20. Watanabe, N., M. Gavrieli, J. R. Sedy, J. Yang, F. Fallarino, S. K. Loftin, M. A. Hurchla, N. Zimmerman, J. Sim, X. Zang, et al. 2003. BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1. Nat. Immunol. 4: 670-679.
21. Oya, Y., N. Watanabe, T. Owada, M. Oki, K. Hirose, A. Suto, S. Kagami, H. Nakajima, T. Kishimoto, I. Iwamoto, et al. 2008. Development of autoimmune hepatitis-like disease and production of autoantibodies to nuclear antigens in mice lacking B and T lymphocyte attenuator. Arthritis Rheum. 58: 2498-2510.
22. Chtanova, T., R. Newton, S. M. Liu, L. Weininger, T. R. Young, D. G. Silva, F. Bertoni, A. Rinaldi, S. Chappaz, F. Sallusto, et al. 2005. Identification of T cell-restricted genes, and signatures for different T cell responses, using a comprehensive collection of microarray datasets. J. Immunol. 175: 7837-7847.
23. Kasaian, M. T., M. J. Whitters, L. L. Carter, L. D. Lowe, J. M. Jussif, B. Deng, K. A. Johnson, J. S. Witek, M. Senices, R. F. Konz, et al. 2002. IL-21 limits NK cell responses and promotes antigen-specific T cell activation: a mediator of the transition from innate to adaptive immunity. Immunity 16: 559-569.
24. lo thymocytes in vivo. Science 250: 1720-1723.
25. + T cells. J. Exp. Med. 205: 1369-1379.
26. Kagami, S., H. Nakajima, K. Kumano, K. Suzuki, A. Suto, K. Imada, H. W. Davey, Y. Saito, K. Takatsu, W. J. Leonard, and I. Iwamoto. 2000. Both stat5a and stat5b are required for antigen-induced eosinophil and T-cell recruitment into the tissue. Blood 95: 1370-1377.
27. Cheung, T. C., L. M. Oborne, M. W. Steinberg, M. G. Macauley, S. Fukuyama, H. Sanjo, C. D'Souza, P. S. Norris, K. Pfeffer, K. M. Murphy, et al. 2009. T cell intrinsic heterodimeric complexes between HVEM and BTLA determine receptivity to the surrounding microenvironment. J. Immunol. 183: 7286-7296.
28. McHeyzer-Williams, L. J., N. Pelletier, L. Mark, N. Fazilleau, and M. G. McHeyzer-Williams. 2009. Follicular helper T cells as cognate regulators of B cell immunity. Curr. Opin. Immunol. 21: 266-273.
29. Han, P., O. D. Goularte, K. Rufner, B. Wilkinson, and J. Kaye. 2004. An inhibitory Ig superfamily protein expressed by lymphocytes and APCs is also an early marker of thymocyte positive selection. J. Immunol. 172: 5931-5939.
30. Vendel, A. C., J. Calemine-Fenaux, A. Izrael-Tomasevic, V. Chauhan, D. Arnott, and D. L. Eaton. 2009. B and T lymphocyte attenuator regulates B cell receptor signaling by targeting Syk and BLNK. J. Immunol. 182: 1509-1517.
31. Mehta, D. S., A. L. Wurster, A. S. Weinmann, and M. J. Grusby. 2005. NFATc2 and T-bet contribute to T-helper-cell-subset-specific regulation of IL-21 expression. Proc. Natl. Acad. Sci. USA 102: 2016-2021.
32. Kim, J. I., I.-C. Ho, M. J. Grusby, and L. H. Glimcher. 1999. The transcription factor c-Maf controls the production of interleukin-4 but not other Th2 cytokines. Immunity 10: 745-751.
33. Bauquet, A. T., H. Jin, A. M. Paterson, M. Mitsdoerffer, I. C. Ho, A. H. Sharpe, and V. K. Kuchroo. 2009. 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: 167-175.
34. + T cells. J. Leukoc. Biol. 87: 703-712.
35. Nurieva, R. I., Y. Chung, G. J. Martinez, X. O. Yang, S. Tanaka, T. D. Matskevitch, Y. H. Wang, and C. Dong. 2009. Bcl6 mediates the development of T follicular helper cells. Science 325: 1001-1005.
36. Johnston, R. J., A. C. Poholek, D. DiToro, I. Yusuf, D. Eto, B. Barnett, A. L. Dent, J. Craft, and S. Crotty. 2009. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 325: 1006-1010.
37. Yu, D., S. Rao, L. M. Tsai, S. K. Lee, Y. He, E. L. Sutcliffe, M. Srivastava, M. Linterman, L. Zheng, N. Simpson, et al. 2009. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 31: 457-468.
38. Linterman, M. A., 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. 2010. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J. Exp. Med. 207: 353-363.
39. Zotos, D., J. M. Coquet, Y. Zhang, A. Light, K. D'Costa, A. Kallies, L. M. Corcoran, D. I. Godfrey, K. M. Toellner, M. J. Smyth, et al. 2010. IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J. Exp. Med. 207: 365-378.
40. King, C., A. Ilic, K. Koelsch, and N. Sarvetnick. 2004. Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell 117: 265-277.
41. Spolski, R., M. Kashyap, C. Robinson, Z. Yu, and W. J. Leonard. 2008. IL-21 signaling is critical for the development of type I diabetes in the NOD mouse. Proc. Natl. Acad. Sci. USA 105: 14028-14033.
42. Sutherland, A. P., T. Van Belle, A. L. Wurster, A. Suto, M. Michaud, D. Zhang, M. J. Grusby, and M. von Herrath. 2009. Interleukin-21 is required for the development of type 1 diabetes in NOD mice. Diabetes 58: 1144-1155.
43. Vinuesa, C. G., M. C. Cook, C. Angelucci, V. Athanasopoulos, L. Rui, K. M. Hill, D. Yu, H. Domaschenz, B. Whittle, T. Lambe, et al. 2005. A RING-type ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity. Nature 435: 452-458.