Differential targeting of IL-2 and T cell receptor signaling pathways selectively expands regulatory T cells while inhibiting conventional Tcells

Journal of Autoimmunity

Volumn 44, Issue , 2013, Pages 13-20

  Satake, Atsushi ^a   Schmidt, Amanda M ^a   Archambault, Angela ^b   Leichner, Theresa M ^a   Wu, Gregory F ^b   Kambayashi, Taku ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autoimmunity; Conventional T cells; IL 2; Proliferation; Regulatory T cells; T cell receptor

Indexed keywords

CYCLOSPORIN A; INTERLEUKIN 2; INTERLEUKIN 2 IMMUNE COMPLEX; PHOSPHOLIPASE C GAMMA; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN ANTIBODY COMPLEX; ARTICLE; CELL EXPANSION; CONTROLLED STUDY; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION;

EID: 84881367948     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2013.06.009     Document Type: Article

References (45)

1. Sakaguchi S., Yamaguchi T., Nomura T., Ono M. Regulatory T cells and immune tolerance. Cell 2008, 133(5):775-787.
2. Josefowicz S.Z., Rudensky A. Control of regulatory T cell lineage commitment and maintenance. Immunity 2009, 30(5):616-625.
3. Buckner J.H. Mechanisms of impaired regulation by CD4(+)CD25(+)FOXP3(+) regulatory T cells in human autoimmune diseases. Nat Rev Immunol 2010, 10(12):849-859.
4. Wood K.J., Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Rev Immunol 2003, 3(3):199-210.
5. Webster K.E., Walters S., Kohler R.E., Mrkvan T., Boyman O., Surh C.D., et al. Invivo expansion of T reg cells with IL-2-mAb complexes: induction of resistance to EAE and long-term acceptance of isletallografts without immunosuppression. JExp Med 2009, 206(4):751-760.
6. Steiner D., Brunicki N., Bachar-Lustig E., Taylor P.A., Blazar B.R., Reisner Y. Overcoming T cell-mediated rejection of bone marrow allografts by T-regulatory cells: synergism with veto cells and rapamycin. Exp Hematol 2006, 34(6):802-808.
7. Zeiser R., Leveson-Gower D.B., Zambricki E.A., Kambham N., Beilhack A., Loh J., et al. Differential impact of mammalian target of rapamycin inhibition on CD4+CD25+Foxp3+ regulatory T cells compared with conventional CD4+ T cells. Blood 2008, 111(1):453-462.
8. Gao W., Lu Y., El Essawy B., Oukka M., Kuchroo V.K., Strom T.B. Contrasting effects of cyclosporine and rapamycin in de novo generation of alloantigen-specific regulatory T cells. Am J Transplant 2007, 7(7):1722-1732.
9. Ruggenenti P., Perico N., Gotti E., Cravedi P., D'Agati V., Gagliardini E., et al. Sirolimus versus cyclosporine therapy increases circulating regulatory T cells, but does not protect renal transplant patients given alemtuzumab induction from chronic allograft injury. Transplantation 2007, 84(8):956-964.
10. Kim J.K., Klinger M., Benjamin J., Xiao Y., Erle D.J., Littman D.R., et al. Impact of the TCR signal on regulatory T cell homeostasis, function, and trafficking. PLoS One 2009, 4(8):e6580.
11. Shen S., Chuck M.I., Zhu M., Fuller D.M., Yang C.W., Zhang W. The importance of LAT in the activation, homeostasis, and regulatory function of T cells. JBiol Chem 2010, 285(46):35393-35405.
12. Burchill M.A., Yang J., Vang K.B., Moon J.J., Chu H.H., Lio C.W., et al. Linked T cell receptor and cytokine signaling govern the development of the regulatory T cell repertoire. Immunity 2008, 28(1):112-121.
13. Tang Q., Henriksen K.J., Boden E.K., Tooley A.J., Ye J., Subudhi S.K., et al. Cutting edge: CD28 controls peripheral homeostasis of CD4+CD25+ regulatory T cells. JImmunol 2003, 171(7):3348-3352.
14. Setoguchi R., Hori S., Takahashi T., Sakaguchi S. Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. JExp Med 2005, 201(5):723-735.
15. Bhandoola A., Tai X., Eckhaus M., Auchincloss H., Mason K., Rubin S.A., et al. Peripheral expression of self-MHC-II influences the reactivity and self-tolerance of mature CD4(+) T cells: evidence from a lymphopenic T cell model. Immunity 2002, 17(4):425-436.
16. Gavin M.A., Clarke S.R., Negrou E., Gallegos A., Rudensky A. Homeostasis and anergy of CD4(+)CD25(+) suppressor T cells invivo. Nat Immunol 2002, 3(1):33-41.
17. Zou T., Satake A., Corbo-Rodgers E., Schmidt A.M., Farrar M.A., Maltzman J.S., et al. Cutting edge: IL-2 signals determine the degree of TCR signaling necessary to support regulatory T cell proliferation invivo. JImmunol 2012, 189(1):28-32.
18. Wu G.F., Corbo E., Schmidt M., Smith-Garvin J.E., Riese M.J., Jordan M.S., et al. Conditional deletion of SLP-76 in mature T cells abrogates peripheral immune responses. Eur J Immunol 2011, 41(7):2064-2073.
19. Jordan M.S., Smith J.E., Burns J.C., Austin J.E., Nichols K.E., Aschenbrenner A.C., et al. Complementation in trans of altered thymocyte development in mice expressing mutant forms of the adaptor molecule SLP76. Immunity 2008, 28(3):359-369.
20. Zou T., Caton A.J., Koretzky G.A., Kambayashi T. Dendritic cells induce regulatory T cell proliferation through antigen-dependent and -independent interactions. JImmunol 2010, 185(5):2790-2799.
21. Racke M.K. Experimental autoimmune encephalomyelitis (EAE). Curr Protoc Neurosci 2001, Chapter 9:Unit9 7.
22. Wu G.F., Shindler K.S., Allenspach E.J., Stephen T.L., Thomas H.L., Mikesell R.J., et al. Limited sufficiency of antigen presentation by dendritic cells in models of central nervous system autoimmunity. JAutoimmun 2011, 36(1):56-64.
23. Smith-Garvin J.E., Koretzky G.A., Jordan M.S. Tcell activation. Annu Rev Immunol 2009, 27:591-619.
24. Jordan M.S., Sadler J., Austin J.E., Finkelstein L.D., Singer A.L., Schwartzberg P.L., et al. Functional hierarchy of the N-terminal tyrosines of SLP-76. JImmunol 2006, 176(4):2430-2438.
25. Coenen J.J., Koenen H.J., van Rijssen E., Kasran A., Boon L., Hilbrands L.B., et al. Rapamycin, not cyclosporine, permits thymic generation and peripheral preservation of CD4+ CD25+ FoxP3+ T cells. Bone Marrow Transplant 2007, 39(9):537-545.
26. Zeiser R., Nguyen V.H., Beilhack A., Buess M., Schulz S., Baker J., et al. Inhibition of CD4+CD25+ regulatory T-cell function by calcineurin-dependent interleukin-2 production. Blood 2006, 108(1):390-399.
27. Mantel P.Y., Ouaked N., Ruckert B., Karagiannidis C., Welz R., Blaser K., et al. Molecular mechanisms underlying FOXP3 induction in human T cells. JImmunol 2006, 176(6):3593-3602.
28. Kohm A.P., Carpentier P.A., Anger H.A., Miller S.D. Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. JImmunol 2002, 169(9):4712-4716.
29. O'Connor R.A., Anderton S.M. Foxp3+ regulatory T cells in the control of experimental CNS autoimmune disease. JNeuroimmunol 2008, 193(1-2):1-11.
30. Schreiner B., Heppner F.L., Becher B. Modeling multiple sclerosis in laboratory animals. Semin Immunopathol 2009, 31(4):479-495.
31. Swee L.K., Bosco N., Malissen B., Ceredig R., Rolink A. Expansion of peripheral naturally occurring T regulatory cells by Fms-like tyrosine kinase 3 ligand treatment. Blood 2009, 113(25):6277-6287.
32. Wu Y., Borde M., Heissmeyer V., Feuerer M., Lapan A.D., Stroud J.C., et al. FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 2006, 126(2):375-387.
33. Segundo D.S., Ruiz J.C., Izquierdo M., Fernandez-Fresnedo G., Gomez-Alamillo C., Merino R., et al. Calcineurin inhibitors, but not rapamycin, reduce percentages of CD4+CD25+FOXP3+ regulatory T cells in renal transplant recipients. Transplantation 2006, 82(4):550-557.
34. Zorn E., Nelson E.A., Mohseni M., Porcheray F., Kim H., Litsa D., et al. IL-2 regulates FOXP3 expression in human CD4+CD25+ regulatory T cells through a STAT-dependent mechanism and induces the expansion of these cells invivo. Blood 2006, 108(5):1571-1579.
35. Yao Z., Kanno Y., Kerenyi M., Stephens G., Durant L., Watford W.T., et al. Nonredundant roles for Stat5a/b in directly regulating Foxp3. Blood 2007, 109(10):4368-4375.
36. Szymczak-Workman A.L., Workman C.J., Vignali D.A. Cutting edge: regulatory T cells do not require stimulation through their TCR to suppress. JImmunol 2009, 182(9):5188-5192.
37. Bensinger S.J., Walsh P.T., Zhang J., Carroll M., Parsons R., Rathmell J.C., et al. Distinct IL-2 receptor signaling pattern in CD4+CD25+ regulatory T cells. JImmunol 2004, 172(9):5287-5296.
38. Walsh P.T., Buckler J.L., Zhang J., Gelman A.E., Dalton N.M., Taylor D.K., et al. PTEN inhibits IL-2 receptor-mediated expansion of CD4+ CD25+ Tregs. JClin Invest 2006, 116(9):2521-2531.
39. McGeachy M.J., Stephens L.A., Anderton S.M. Natural recovery and protection from autoimmune encephalomyelitis: contribution of CD4+CD25+ regulatory cells within the central nervous system. JImmunol 2005, 175(5):3025-3032.
40. Zhang X., Koldzic D.N., Izikson L., Reddy J., Nazareno R.F., Sakaguchi S., et al. IL-10 is involved in the suppression of experimental autoimmune encephalomyelitis by CD25+CD4+ regulatory T cells. Int Immunol 2004, 16(2):249-256.
41. Zammit D.J., Cauley L.S., Pham Q.M., Lefrancois L. Dendritic cells maximize the memory CD8 T cell response to infection. Immunity 2005, 22(5):561-570.
42. Isaksson M., Lundgren B.A., Ahlgren K.M., Kampe O., Lobell A. Conditional DC depletion does not affect priming of encephalitogenic Th cells in EAE. Eur J Immunol 2012, 42(10):2555-2563.
43. Subramanian S., Yates M., Vandenbark A.A., Offner H. Oestrogen-mediated protection of experimental autoimmune encephalomyelitis in the absence of Foxp3+ regulatory T cells implicates compensatory pathways including regulatory B cells. Immunology 2011, 132(3):340-347.
44. Kohm A.P., McMahon J.S., Podojil J.R., Begolka W.S., DeGutes M., Kasprowicz D.J., et al. Cutting edge: anti-CD25 monoclonal antibody injection results in the functional inactivation, not depletion, of CD4+CD25+ T regulatory cells. JImmunol 2006, 176(6):3301-3305.
45. Korn T., Reddy J., Gao W., Bettelli E., Awasthi A., Petersen T.R., et al. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat Med 2007, 13(4):423-431.