CD28 and ITK signals regulate autoreactive T cell trafficking

Nature Medicine

Volumn 19, Issue 12, 2013, Pages 1632-1637

  Jain, Nitya ^a   Miu, Bing ^a   Jiang, Jian Kang ^b   McKinstry, Kai K ^a   Prince, Amanda ^a   Swain, Susan L ^a   Greiner, Dale L ^a   Thomas, Craig J ^b   Sanderson, Michael J ^a   Berg, Leslie J ^a   Kang, Joonsoo ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INTERLEUKIN 2 INDUCIBLE T CELL KINASE; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; CELL INFILTRATION; CELL MIGRATION; CELL PROLIFERATION; IMMUNE RESPONSE; INSULIN DEPENDENT DIABETES MELLITUS; LIFESPAN; LYMPHOID ORGAN; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

MUS;

EID: 84889880803     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3393     Document Type: Article

References (60)

1. Bour-Jordan, H. et al. Intrinsic and extrinsic control of peripheral T-cell tolerance by costimulatory molecules of the CD28/B7 family. Immunol. Rev. 241, 180-205 (2011).
2. Harding, F.A., McArthur, J.G., Gross, J.A., Raulet, D.H. & Allison, J.P. CD28 mediated signalling costimulates murine T cells and prevents the induction of anergy in T cell clones. Nature 356, 607-609 (1992).
3. Boise, L.H. et al. CD28 costimulation can promote T cell survival by enhancing the expression of bcl-xl. Immunity 3, 87-98 (1995).
4. Frauwirth, K.A. et al. The CD28 signaling pathway regulates glucose metabolism. Immunity 16, 769-777 (2002). (Pubitemid 34786476)
5. Marelli-Berg, F.M., Okkenhaug, K. & Mirenda, V. A two-signal model for T cell trafficking. Trends Immunol. 28, 267-273 (2007). (Pubitemid 46810354)
6. Shimizu, Y. et al. Crosslinking of the T cell-specific accessory molecules CD7 and CD28 modulates T cell adhesion. J. Exp. Med. 175, 577-582 (1992).
7. Michel, F. et al. CD28 utilizes Vav-1 to enhance TCR-proximal signaling and NF-AT activation. J. Immunol. 165, 3820-3829 (2000). (Pubitemid 32057289)
8. Salazar-Fontana, L.I., Barr, V., Samelson, L.E. & Bierer, B.E. CD28 engagement promotes actin polymerization through the activation of the small Rho GTPase Cdc42 in human T cells. J. Immunol. 171, 2225-2232 (2003). (Pubitemid 37025527)
9. Kondo, S., Kooshesh, F., Wang, B., Fujisawa, H. & Sauder, D.N. Contribution of the CD28 molecule to allergic and irritant-induced skin reactions in CD28 mice. J. Immunol. 157, 4822-4829 (1996). (Pubitemid 126449556)
10. Girvin, A.M. et al. A critical role for B7/CD28 costimulation in experimental autoimmune encephalomyelitis: a comparative study using costimulatory molecule-deficient mice and monoclonal antibody blockade. J. Immunol. 164, 136-143 (2000). (Pubitemid 30012983)
11. Chang, T.T., Jabs, C., Sobel, R.A., Kuchroo, V.K. & Sharpe, A.H. Studies in B7-deficient mice reveal a critical role for B7 costimulation in both induction and effector phases of experimental autoimmune encephalomyelitis. J. Exp. Med. 190, 733-740 (1999). (Pubitemid 29428655)
12. Lenschow, D.J. et al. CD28/B7 regulation of TH1 and TH2 subsets in the development of autoimmune diabetes. Immunity 5, 285-293 (1996). (Pubitemid 26341371)
13. Salomon, B. et al. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 12, 431-440 (2000).
14. Lenschow, D.J. et al. Differential effects of anti-B7-1 and anti-B7-2 monoclonal antibody treatment on the development of diabetes in the nonobese diabetic mouse. J. Exp. Med. 181, 1145-1155 (1995).
15. Chambers, C.A., Kuhns, M.S., Egen, J.G. & Allison, J.P. CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy. Annu. Rev. Immunol. 19, 565-594 (2001). (Pubitemid 32368046)
16. Greenwald, R.J., Freeman, G.J. & Sharpe, A.H. The B7 family revisited. Annu. Rev. Immunol. 23, 515-548 (2005). (Pubitemid 40563179)
17. Gough, S.C., Walker, L.S. & Sansom, D.M. CTLA4 gene polymorphism and autoimmunity. Immunol. Rev. 204, 102-115 (2005). (Pubitemid 40460496)
18. Chambers, C.A., Sullivan, T.J. & Allison, J.P. Lymphoproliferation in CTLA-4-deficient mice is mediated by costimulation-dependent activation of CD4+ T cells. Immunity 7, 885-895 (1997). (Pubitemid 28064901)
19. Ise, W. et al. CTLA-4 suppresses the pathogenicity of self antigen-specific T cells by cell-intrinsic and cell-extrinsic mechanisms. Nat. Immunol. 11, 129-135 (2010).
20. Wing, K. et al. CTLA-4 control over Foxp3+ regulatory T cell function. Science 322, 271-275 (2008).
21. Friedline, R.H. et al. CD4+ regulatory T cells require CTLA-4 for the maintenance of systemic tolerance. J. Exp. Med. 206, 421-434 (2009).
22. Jain, N., Nguyen, H., Chambers, C. & Kang, J. Dual function of CTLA-4 in regulatory T cells and conventional T cells to prevent multiorgan autoimmunity. Proc. Natl. Acad. Sci. USA 107, 1524-1528 (2010).
23. Masteller, E.L., Chuang, E.A.C.M., Reiner, S.L. & Thompson, C.B. Structural analysis of CTLA-4 function in vivo. J. Immunol. 164, 5319-5327 (2000). (Pubitemid 30305211)
24. Okkenhaug, K. et al. A point mutation in CD28 distinguishes proliferative signals from survival signals. Nat. Immunol. 2, 325-332 (2001). (Pubitemid 33706343)
25. Mirenda, V. et al. Physiologic and aberrant regulation of memory T-cell trafficking by the costimulatory molecule CD28. Blood 109, 2968-2977 (2007). (Pubitemid 46482095)
26. Michel, F., Attal-Bonnefoy, G., Mangino, G., Mise-Omata, S. & Acuto, O. CD28 as a molecular amplifier extending TCR ligation and signaling capabilities. Immunity 15, 935-945 (2001). (Pubitemid 34075374)
27. Berg, L.J., Finkelstein, L.D., Lucas, J.A. & Schwartzberg, P.L. Tec family kinases in T lymphocyte development and function. Annu. Rev. Immunol. 23, 549-600 (2005). (Pubitemid 40563180)
28. Woods, M.L. et al. A novel function for the Tec family tyrosine kinase Itk in activation of 1 integrins by the T-cell receptor. EMBO J. 20, 1232-1244 (2001). (Pubitemid 32233964)
29. Takesono, A., Horai, R., Mandai, M., Dombroski, D. & Schwartzberg, P.L. Requirement for Tec kinases in chemokine-induced migration and activation of Cdc42 and Rac. Curr. Biol. 14, 917-922 (2004). (Pubitemid 38800915)
30. Fowell, D.J. et al. Impaired NFATc translocation and failure of Th2 development in Itk-deficient CD4+ T cells. Immunity 11, 399-409 (1999). (Pubitemid 29504195)
31. Mandelbrot, D.A. et al. B7-dependent T-cell costimulation in mice lacking CD28 and CTLA4. J. Clin. Invest. 107, 881-887 (2001). (Pubitemid 32274041)
32. Fletcher, A.L. et al. Lymph node fibroblastic reticular cells directly present peripheral tissue antigen under steady-state and inflammatory conditions. J. Exp. Med. 207, 689-697 (2010).
33. Lozanoska-Ochser, B., Klein, N.J., Huang, G.C., Alvarez, R.A. & Peakman, M. Expression of CD86 on human islet endothelial cells facilitates T cell adhesion and migration. J. Immunol. 181, 6109-6116 (2008).
34. Perez, V.L., Henault, L. & Lichtman, A.H. Endothelial antigen presentation: stimulation of previously activated but not naive TCR-transgenic mouse T cells. Cell. Immunol. 189, 31-40 (1998). (Pubitemid 28489598)
35. Kreisel, D. et al. Mouse vascular endothelium activates CD8+ T lymphocytes in a B7-dependent fashion. J. Immunol. 169, 6154-6161 (2002). (Pubitemid 36903460)
36. Thornton, E.E. et al. Spatiotemporally separated antigen uptake by alveolar dendritic cells and airway presentation to T cells in the lung. J. Exp. Med. 209, 1183-1199 (2012).
37. Ledgerwood, L.G. et al. The sphingosine 1-phosphate receptor 1 causes tissue retention by inhibiting the entry of peripheral tissue T lymphocytes into afferent lymphatics. Nat. Immunol. 9, 42-53 (2008). (Pubitemid 350286203)
38. Cahalan, M.D. & Parker, I. Choreography of cell motility and interaction dynamics imaged by two-photon microscopy in lymphoid organs. Annu. Rev. Immunol. 26, 585-626 (2008). (Pubitemid 351600386)
39. Sanderson, M.J. Exploring lung physiology in health and disease with lung slices. Pulm. Pharmacol. Ther. 24, 452-465 (2011).
40. Dennehy, K.M. et al. Cutting edge: monovalency of CD28 maintains the antigen dependence of T cell costimulatory responses. J. Immunol. 176, 5725-5729 (2006).
41. Goverman, J., Brabb, T., Paez, A., Harrington, C. & von Dassow, P. Initiation and regulation of CNS autoimmunity. Crit. Rev. Immunol. 17, 469-480 (1997). (Pubitemid 27527396)
42. Liu, L., Callahan, M.K., Huang, D. & Ransohoff, R.M. Chemokine receptor CXCR3: an unexpected enigma. Curr. Top. Dev. Biol. 68, 149-181 (2005). (Pubitemid 43588858)
43. Burkhardt, J.K., Carrizosa, E. & Shaffer, M.H. The actin cytoskeleton in T cell activation. Annu. Rev. Immunol. 26, 233-259 (2008). (Pubitemid 351600376)
44. Readinger, J.A. et al. Selective targeting of ITK blocks multiple steps of HIV replication. Proc. Natl. Acad. Sci. USA 105, 6684-6689 (2008). (Pubitemid 351754567)
45. Lin, T.A. et al. Selective Itk inhibitors block T-cell activation and murine lung inflammation. Biochemistry 43, 11056-11062 (2004).
46. Riether, D. et al. 5-Aminomethylbenzimidazoles as potent ITK antagonists. Bioorg. Med. Chem. Lett. 19, 1588-1591 (2009).
47. Peterson, J.D. & Haskins, K. Transfer of diabetes in the NOD-scid mouse by CD4 T-cell clones. Differential requirement for CD8 T-cells. Diabetes 45, 328-336 (1996). (Pubitemid 26069047)
48. Bachmann, M.F. et al. Normal responsiveness of CTLA-4-deficient anti-viral cytotoxic T cells. J. Immunol. 160, 95-100 (1998). (Pubitemid 28116719)
49. Shahinian, A. et al. Differential T cell costimulatory requirements in CD28-deficient mice. Science 261, 609-612 (1993). (Pubitemid 23278372)
50. Collins, A.V. et al. The interaction properties of costimulatory molecules revisited. Immunity 17, 201-210 (2002). (Pubitemid 35245962)
51. Yokosuka, T. et al. Spatiotemporal basis of CTLA-4 costimulatory molecule-mediated negative regulation of T cell activation. Immunity 33, 326-339 (2010).
52. Puccetti, P. & Grohmann, U. IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-B activation. Nat. Rev. Immunol. 7, 817-823 (2007). (Pubitemid 47480306)
53. Qureshi, O.S. et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 332, 600-603 (2011).
54. Bachmann, M.F., Littman, D.R. & Liao, X.C. Antiviral immune responses in Itk-deficient mice. J. Virol. 71, 7253-7257 (1997). (Pubitemid 27391660)
55. Orban, T. et al. Co-stimulation modulation with abatacept in patients with recent-onset type 1 diabetes: a randomised, double-blind, placebo-controlled trial. Lancet 378, 412-419 (2011).
56. Bauer, M. et al. 1 integrins differentially control extravasation of inflammatory cell subsets into the CNS during autoimmunity. Proc. Natl. Acad. Sci. USA 106, 1920-1925 (2009).
57. Dombroski, D. et al. Kinase-independent functions for Itk in TCR-induced regulation of Vav and the actin cytoskeleton. J. Immunol. 174, 1385-1392 (2005).
58. Guo, W. et al. Molecular characteristics of CTA056, a novel interleukin-2-inducible T-cell kinase inhibitor that selectively targets malignant T cells and modulates oncomirs. Mol. Pharmacol. 82, 938-947 (2012).
59. McCausland, M.M. & Crotty, S. Quantitative PCR technique for detecting lymphocytic choriomeningitis virus in vivo. J. Virol. Methods 147, 167-176 (2008). (Pubitemid 350250859)
60. McKinstry, K.K. et al. IL-10 deficiency unleashes an influenza-specific TH17 response and enhances survival against high-dose challenge. J. Immunol. 182, 7353-7363 (2009).