IL-2-inducible T cell kinase tunes T regulatory cell development and is required for suppressive function

Journal of Immunology

Volumn 193, Issue 5, 2014, Pages 2267-2272

  Huang, Weishan ^a   Jeong, Ah Reum ^a,b   Kannan, Arun K ^a   Huang, Lu ^a   August, Avery ^a  

^a Animal Health Diagnostic Center   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2 INDUCIBLE T CELL KINASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NEUROPILIN 1; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; EMT PROTEIN-TYROSINE KINASE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; HLA ANTIGEN CLASS 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL EXPANSION; COLITIS; CONTROLLED STUDY; EFFECTOR CELL; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY; THYMUS;

ANIMALS; COLITIS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; IMMUNE TOLERANCE; MICE; MICE, KNOCKOUT; NEUROPILIN-1; PROTEIN-TYROSINE KINASES; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND;

EID: 84907033007     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400968     Document Type: Article

References (38)

1. Andreotti, A. H., P. L. Schwartzberg, R. E. Joseph, and L. J. Berg. 2010. T-cell signaling regulated by the Tec family kinase, Itk. Cold Spring Harb. Perspect. Biol. 2: a002287.
2. Hu, J., and A. August. 2008. Naive and innate memory phenotype CD4+ T cells have different requirements for active Itk for their development. J. Immunol. 180: 6544-6552.
3. Hu, J., N. Sahu, E. Walsh, and A. August. 2007. Memory phenotype CD8+ T cells with innate function selectively develop in the absence of active Itk. Eur. J. Immunol. 37: 2892-2899.
4. Broussard, C., C. Fleischacker, R. Horai, M. Chetana, A. M. Venegas, L. L. Sharp, S. M. Hedrick, B. J. Fowlkes, and P. L. Schwartzberg. 2006. Altered development of CD8+ T cell lineages in mice deficient for the Tec kinases Itk and Rlk. Immunity 25: 93-104.
5. Atherly, L. O., J. A. Lucas, M. Felices, C. C. Yin, S. L. Reiner, and L. J. Berg. 2006. The Tec family tyrosine kinases Itk and Rlk regulate the development of conventional CD8+ T cells. Immunity 25: 79-91.
6. Felices, M., and L. J. Berg. 2008. The Tec kinases Itk and Rlk regulate NKT cell maturation, cytokine production, and survival. J. Immunol. 180: 3007-3018.
7. Qi, Q., W. Huang, Y. Bai, G. Balmus, R. S. Weiss, and A. August. 2012. A unique role for ITK in survival of invariant NKT cells associated with the p53- dependent pathway in mice. J. Immunol. 188: 3611-3619.
8. Xia, M., Q. Qi, Y. Jin, D. L. Wiest, A. August, and N. Xiong. 2010. Differential roles of IL-2-inducible T cell kinase-mediated TCR signals in tissue-specific localization and maintenance of skin intraepithelial T cells. J. Immunol. 184: 6807-6814.
9. Qi, Q., M. Xia, J. Hu, E. Hicks, A. Iyer, N. Xiong, and A. August. 2009. Enhanced development of CD4+ gammadelta T cells in the absence of Itk results in elevated IgE production. Blood 114: 564-571.
10. Felices, M., C. C. Yin, Y. Kosaka, J. Kang, and L. J. Berg. 2009. Tec kinase Itk in gammadeltaT cells is pivotal for controlling IgE production in vivo. Proc. Natl. Acad. Sci. USA 106: 8308-8313.
11. Yin, C. C., O. H. Cho, K. E. Sylvia, K. Narayan, A. L. Prince, J. W. Evans, J. Kang, and L. J. Berg. 2013. The Tec kinase ITK regulates thymic expansion, emigration, and maturation of gd NKT cells. J. Immunol. 190: 2659-2669.
12. Mueller, C., and A. August. 2003. Attenuation of immunological symptoms of allergic asthma in mice lacking the tyrosine kinase ITK. J. Immunol. 170: 5056-5063.
13. Kannan, A. K., N. Sahu, S. Mohanan, S. Mohinta, and A. August. 2013. IL-2- inducible T-cell kinase modulates TH2-mediated allergic airway inflammation by suppressing IFN-gamma in naive CD4+ T cells. J. Allergy Clin. Immunol. 132: 811-820 e1-5.
14. Gomez-Rodriguez, J., N. Sahu, R. Handon, T. S. Davidson, S. M. Anderson, M. R. Kirby, A. August, and P. L. Schwartzberg. 2009. Differential expression of interleukin-17A and -17F is coupled to T cell receptor signaling via inducible T cell kinase. Immunity 31: 587-597.
15. Sakaguchi, S., N. Sakaguchi, M. Asano, M. Itoh, and M. Toda. 1995. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155: 1151-1164.
16. Baecher-Allan, C., and D. A. Hafler. 2006. Human regulatory T cells and their role in autoimmune disease. Immunol. Rev. 212: 203-216.
17. Fu, S., N. Zhang, A. C. Yopp, D. Chen, M. Mao, D. Chen, H. Zhang, Y. Ding, and J. S. Bromberg. 2004. TGF-beta induces Foxp3 + T-regulatory cells from CD4 + CD25 - precursors. Am. J. Transplant. 4: 1614-1627.
18. Marson, A., K. Kretschmer, G. M. Frampton, E. S. Jacobsen, J. K. Polansky, K. D. MacIsaac, S. S. Levine, E. Fraenkel, H. von Boehmer, and R. A. Young. 2007. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 445: 931-935.
19. Gomez-Rodriguez, J., E. A. Wohlfert, R. Handon, F. Meylan, J. Z. Wu, S. M. Anderson, M. R. Kirby, Y. Belkaid, and P. L. Schwartzberg. 2014. Itkmediated integration of T cell receptor and cytokine signaling regulates the balance between Th17 and regulatory T cells. J. Exp. Med. 211: 529-543.
20. Huang, W., F. Huang, A. K. Kannan, J. Hu, and A. August. 2014. ITK tunes IL- 4-induced development of innate memory CD8+ T cells in a gd T and invariant NKT cell-independent manner. J. Leukoc. Biol. 96: 55-63.
21. Sakaguchi, S., T. Yamaguchi, T. Nomura, and M. Ono. 2008. Regulatory T cells and immune tolerance. Cell 133: 775-787.
22. Luo, C. T., and M. O. Li. 2013. Transcriptional control of regulatory T cell development and function. Trends Immunol. 34: 531-539.
23. Tai, X., B. Erman, A. Alag, J. Mu, M. Kimura, G. Katz, T. Guinter, T. McCaughtry, R. Etzensperger, L. Feigenbaum, et al. 2013. Foxp3 transcription factor is proapoptotic and lethal to developing regulatory T cells unless counterbalanced by cytokine survival signals. Immunity 38: 1116-1128.
24. Smigiel, K. S., E. Richards, S. Srivastava, K. R. Thomas, J. C. Dudda, K. D. Klonowski, and D. J. Campbell. 2014. CCR7 provides localized access to IL-2 and defines homeostatically distinct regulatory T cell subsets. J. Exp. Med. 211: 121-136.
25. Sim, G. C., N. Martin-Orozco, L. Jin, Y. Yang, S. Wu, E. Washington, D. Sanders, C. Lacey, Y. Wang, L. Vence, et al. 2014. IL-2 therapy promotes suppressive ICOS+ Treg expansion in melanoma patients. J. Clin. Invest. 124: 99-110.
26. Josefowicz, S. Z., L. F. Lu, and A. Y. Rudensky. 2012. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30: 531-564.
27. Gottschalk, R. A., E. Corse, and J. P. Allison. 2010. TCR ligand density and affinity determine peripheral induction of Foxp3 in vivo. J. Exp. Med. 207: 1701-1711.
28. Hinterberger, M., M. Aichinger, O. Prazeres da Costa, D. Voehringer, R. Hoffmann, and L. Klein. 2010. Autonomous role of medullary thymic epithelial cells in central CD4(+) T cell tolerance. Nat. Immunol. 11: 512-519.
29. Shimoda, M., F. Mmanywa, S. K. Joshi, T. Li, K. Miyake, J. Pihkala, J. A. Abbas, and P. A. Koni. 2006. Conditional ablation of MHC-II suggests an indirect role for MHC-II in regulatory CD4 T cell maintenance. J. Immunol. 176: 6503-6511.
30. Huang, W., Q. Qi, J. Hu, F. Huang, T. M. Laufer, and A. August. 2014. Dendritic cell-MHC class II and Itk regulate functional development of regulatory innate memory CD4+ T cells in bone marrow transplantation. J. Immunol. 192: 3435-3441.
31. Powrie, F., M. W. Leach, S. Mauze, S. Menon, L. B. Caddle, and R. L. Coffman. 1994. Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells. Immunity 1: 553-562.
32. Mottet, C., H. H. Uhlig, and F. Powrie. 2003. Cutting edge: cure of colitis by CD4+CD25+ regulatory T cells. J. Immunol. 170: 3939-3943.
33. Yadav, M., C. Louvet, D. Davini, J. M. Gardner, M. Martinez-Llordella, S. Bailey-Bucktrout, B. A. Anthony, F. M. Sverdrup, R. Head, D. J. Kuster, et al. 2012. Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J. Exp. Med. 209: 1713-1722.
34. Liu, K. Q., S. C. Bunnell, C. B. Gurniak, and L. J. Berg. 1998. T cell receptorinitiated calcium release is uncoupled from capacitative calcium entry in Itkdeficient T cells. J. Exp. Med. 187: 1721-1727.
35. Caton, A. J., E. Kropf, D. M. Simons, M. Aitken, K. A. Weissler, and M. S. Jordan. 2013. Strength of TCR signal from self-peptide modulates autoreactive thymocyte deletion and Foxp3 Treg-cell formation. Eur. J. Immunol. 44: 785-793.
36. Hwang, S., K. D. Song, R. Lesourne, J. Lee, J. Pinkhasov, L. Li, D. El-Khoury, and P. E. Love. 2012. Reduced TCR signaling potential impairs negative selection but does not result in autoimmune disease. J. Exp. Med. 209: 1781-1795.
37. Berg, L. J. 2009. Strength of T cell receptor signaling strikes again. Immunity 31: 529-531.
38. Sauer, S., L. Bruno, A. Hertweck, D. Finlay, M. Leleu, M. Spivakov, Z. A. Knight, B. S. Cobb, D. Cantrell, E. O'Connor, et al. 2008. T cell receptor signaling controls Foxp3 expression via PI3K, Akt, and mTOR. Proc. Natl. Acad. Sci. USA 105: 7797-7802.