Sustained signaling by canonical helper T cell cytokines throughout the reactive lymph node

Nature Immunology

Volumn 11, Issue 6, 2010, Pages 520-526

  Perona Wright, Georgia ^a   Mohrs, Katja ^a   Mohrs, Markus ^a  

^a TRUDEAU INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; STAT6 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HELIGMOSOMOIDES POLYGYRUS; HELPER CELL; IMMUNE RESPONSE; IN VIVO STUDY; LYMPHATIC DRAINAGE; LYMPHOCYTE; MESENTERY LYMPH NODE; NEMATODIASIS; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TH1 CELL; TH2 CELL; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ANIMALS; CELL DIFFERENTIATION; CYTOKINES; IMMUNOBLOTTING; INTERLEUKIN-4; LYMPH NODES; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NEMATOSPIROIDES DUBIUS; SIGNAL TRANSDUCTION; STAT6 TRANSCRIPTION FACTOR; STRONGYLIDA INFECTIONS; TH2 CELLS;

EID: 77952585347     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1866     Document Type: Article

References (50)

1. O'Garra, A. & Murphy, K. Role of cytokines in determining T-lymphocyte function. Curr. Opin. Immunol. 6, 458-466 (1994).
2. Anthony, R.M., Rutitzky, L.I., Urban, J.F. Jr., Stadecker, M.J. & Gause, W.C. Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 7, 975-987 (2007).
3. Zhu, J. & Paul, W.E. CD4 T cells: fates, functions, and faults. Blood 112, 1557-1569 (2008).
4. Shimoda, K. et al. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 380, 630-633 (1996).
5. Kaplan, M.H., Schindler, U., Smiley, S.T. & Grusby, M.J. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4, 313-319 (1996).
6. Finkelman, F.D. et al. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 15, 505-533 (1997).
7. Reinhardt, R.L., Liang, H.E. & Locksley, R.M. Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 10, 385-393 (2009).
8. + T cells in reactive lymph nodes during helminth infection are T follicular helper cells. J. Exp. Med. 206, 1001-1007 (2009).
9. Zaretsky, A.G. et al. T follicular helper cells differentiate from Th2 cells in response to helminth antigens. J. Exp. Med. 206, 991-999 (2009).
10. Poo, W.J., Conrad, L. & Janeway, C.A. Jr. Receptor-directed focusing of lymphokine release by helper T cells. Nature 332, 378-380 (1988).
11. Kupfer, A., Mosmann, T.R. & Kupfer, H. Polarized expression of cytokines in cell conjugates of helper T cells and splenic B cells. Proc. Natl. Acad. Sci. USA 88, 775-779 (1991).
12. Paul, W.E. & Seder, R.A. Lymphocyte responses and cytokines. Cell 76, 241-251 (1994).
13. O'Shea, J.J. Jaks, STATs, cytokine signal transduction, and immunoregulation: are we there yet? Immunity 7, 1-11 (1997).
14. Takeda, K. et al. Essential role of Stat6 in IL-4 signalling. Nature 380, 627-630 (1996).
15. Nelms, K., Keegan, A.D., Zamorano, J., Ryan, J.J. & Paul, W.E. The IL-4 receptor: signaling mechanisms and biologic functions. Annu. Rev. Immunol. 17, 701-738 (1999).
16. Mohrs, K., Wakil, A.E., Killeen, N., Locksley, R.M. & Mohrs, M.A. Two-step process for cytokine production revealed by IL-4 dual-reporter mice. Immunity 23, 419-429 (2005).
17. Mohrs, M., Shinkai, K., Mohrs, K. & Locksley, R.M. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 15, 303-311 (2001).
18. Perona-Wright, G., Mohrs, K., Mayer, K.D. & Mohrs, M. Differential regulation of IL-4Ra expression by antigen versus cytokine stimulation characterizes Th2 progression in vivo. J. Immunol. 184, 615-623 (2010).
19. Ohara, J. & Paul, W.E. Up-regulation of interleukin 4/B-cell stimulatory factor 1 receptor expression. Proc. Natl. Acad. Sci. USA 85, 8221-8225 (1988).
20. Schindler, C, Shuai, K., Prezioso, V.R. & Darnell, J.E. Jr. Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257, 809-813 (1992).
21. Maldonado, R.A. et al. Control of T helper cell differentiation through cytokine receptor inclusion in the immunological synapse. J. Exp. Med. 206, 877-892 (2009).
22. Bach, E.A. et al. Ligand-induced autoregulation of IFN-y receptor p chain expression in T helper cell subsets. Science 270, 1215-1218 (1995).
23. Zhou, F. Molecular mechanisms of IFN-y to up-regulate MHC class I antigen processing and presentation. Int. Rev. Immunol. 28, 239-260 (2009).
24. Manetti, R. et al. Natural killer cell stimulatory factor (interleukin 12 [IL-12]) induces T helper type 1 (Th1)-specifc immune responses and inhibits the development of IL-4-producing Th cells. J. Exp. Med. 177, 1199-1204 (1993).
25. Trinchieri, G. Interleukin-12: a proinfammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specifc adaptive immunity. Annu. Rev. Immunol. 13, 251-276 (1995).
26. Szabo, S.J., Dighe, A.S., Gubler, U. & Murphy, K.M. Regulation of the interleukin (IL)-12R |32 subunit expression in developing T helper 1 (Th1) and Th2 cells. J. Exp. Med. 185, 817-824 (1997).
27. Perona-Wright, G. et al. Systemic but not local infections elicit immunosuppressive IL-10 production by natural killer cells. Cell Host Microbe 6, 503-512 (2009).
28. Ekkens, M.J. et al. The role of OX40 ligand interactions in the development of the Th2 response to the gastrointestinal nematode parasite Heligmosomoides polygyrus. J. Immunol. 170, 384-393 (2003).
29. Hotson, A.N., Hardy, J.W., Hale, M.B., Contag, C.H. & Nolan, G.P. The T cell STAT signaling network is reprogrammed within hours of bacteremia via secondary signals. J. Immunol. 182, 7558-7568 (2009).
30. Andrews, R.P., Ericksen, M.B., Cunningham, CM., Daines, M.O. & Hershey, G.K. Analysis of the life cycle of stat6. Continuous cycling of STAT6 is required for IL-4 signaling. J. Biol. Chem. 277, 36563-36569 (2002).
31. Galizzi, J.P., Zuber, C.E., Cabrillat, H., Djossou, O. & Banchereau, J. Internalization of human interleukin 4 and transient down-regulation of its receptor in the CD23-inducible Jijoye cells. J. Biol. Chem. 264, 6984-6989 (1989).
32. Abbas, A.K., Murphy, K.M. & Sher, A. Functional diversity of helper T lymphocytes. Nature 383, 787-793 (1996).
33. Robinson, R.T. et al. Yersinia pestis evades TLR4-dependent induction of IL-12(p40)2 by dendritic cells and subsequent cell migration. J. Immunol. 181, 5560-5567 (2008).
34. Maldonado, R.A., Irvine, D.J., Schreiber, R. & Glimcher, L.H. A role for the immunological synapse in lineage commitment of CD4 lymphocytes. Nature 431, 527-532 (2004).
35. Miller, M.J., Wei, S.H., Parker, I. & Cahalan, M.D. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296, 1869-1873 (2002).
36. + T cells activated in cutaneous or mucosal lymphoid tissues. J. Exp. Med. 195, 135-141 (2002).
37. + T cells. J. Exp. Med. 194, 953-966 (2001).
38. Huse, M., Lillemeier, B.F., Kuhns, M.S., Chen, D.S. & Davis, M.M. T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 7, 247-255 (2006).
39. Haque, S.J. et al. Receptor-associated constitutive protein tyrosine phosphatase activity controls the kinase function of JAK1. Proc. Natl. Acad. Sci. USA 94, 8563-8568 (1997).
40. Haque, S.J., Harbor, P., Tabrizi, M., Yi, T. & Williams, B.R. Protein-tyrosine phosphatase Shp-1 is a negative regulator of IL-4-and IL-13-dependent signal transduction. J. Biol. Chem. 273, 33893-33896 (1998).
41. Hanson, E.M., Dickensheets, H., Qu, C.K., Donnelly, R.P. & Keegan, A.D. Regulation of the dephosphorylation of Stat6. Participation of Tyr-713 in the interleukin-4 receptor α, the tyrosine phosphatase SHP-1, and the proteasome. J. Biol. Chem. 278, 3903-3911 (2003).
42. Tanaka, Y. et al. T helper type 2 differentiation and intracellular traffcking of the interleukin 4 receptor-α subunit controlled by the Rac activator Dock2. Nat. Immunol. 8, 1067-1075 (2007).
43. Skrenta, H., Yang, Y., Pestka, S. & Fathman, C.G. Ligand-independent down-regulation of IFN-γ receptor 1 following TCR engagement. J. Immunol. 164, 3506-3511 (2000).
44. 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. 187, 1193-1204 (1998).
45. Sutton, T.L. et al. Anti-infammatory mechanisms of enteric Heligmosomoides polygyrus infection against trinitrobenzene sulfonic acid-induced colitis in a murine model. Infect. Immun. 76, 4772-4782 (2008).
46. Elliott, D.E. et al. Colonization with Heligmosomoides polygyrus suppresses mucosal IL-17 production. J. Immunol. 181, 2414-2419 (2008).
47. Bethony, J. et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367, 1521-1532 (2006).
48. Mohrs, M. et al. Differences between IL-4-and IL-4 receptor α-defcient mice in chronic leishmaniasis reveal a protective role for IL-13 receptor signaling. J. Immunol. 162, 7302-7308 (1999).
49. Mayer, K.D. et al. The functional heterogeneity of type 1 effector T cells in response to infection is related to the potential for IFN-γ production. J. Immunol. 174, 7732-7739 (2005).
50. - dendritic cell activation status plays an integral role in infuencing Th2 response development. J. Immunol. 167, 1982-1988 (2001).