IL-2 signaling prevents T cell anergy by inhibiting the expression of anergy-inducing genes

Molecular Immunology

Volumn 46, Issue 5, 2009, Pages 999-1006

  Duré, Myrianne ^a   Macian, Fernando ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Anergy; Interleukin 2; mTOR; NFAT; T cell

Indexed keywords

CYTOKINE; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; JANUS KINASE 3; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; TRANSCRIPTION FACTOR AP 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE PROGRESSION; CELL SHAPE; CELLULAR IMMUNITY; CLONAL ANERGY; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; INHIBITION KINETICS; MICROENVIRONMENT; MOUSE; NONHUMAN; PREVENTION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANIMALS; CELL CYCLE; CLONAL ANERGY; GENE EXPRESSION REGULATION; INTERLEUKIN-2; JANUS KINASE 3; MICE; MICE, INBRED BALB C; PROTEIN KINASES; RECEPTORS, INTERLEUKIN-2; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSCRIPTION FACTOR AP-1;

EID: 59249103441     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2008.09.029     Document Type: Article

References (44)

1. Allen A., Zheng Y., Gardner L., Safford M., Horton M.R., and Powell J.D. The novel cyclophilin binding compound, sanglifehrin A, disassociates G1 cell cycle arrest from tolerance induction. J. Immunol. 172 (2004) 4797-4803
2. Anandasabapathy N., Ford G.S., Bloom D., Holness C., Paragas V., Seroogy C., Skrenta H., Hollenhorst M., Fathman C.G., and Soares L. GRAIL: an E3 ubiquitin ligase that inhibits cytokine gene transcription is expressed in anergic CD4+ T cells. Immunity 18 (2003) 535-547
3. Appleman L.J., Berezovskaya A., Grass I., and Boussiotis V.A. CD28 costimulation mediates T cell expansion via IL-2-independent and IL-2-dependent regulation of cell cycle progression. J. Immunol. 164 (2000) 144-151
4. Bandyopadhyay S., Dure M., Paroder M., Soto-Nieves N., Puga I., and Macian F. Interleukin 2 gene transcription is regulated by Ikaros-induced changes in histone acetylation in anergic T cells. Blood 109 (2007) 2878-2886
5. Bandyopadhyay S., Soto-Nieves N., and Macian F. Transcriptional regulation of T cell tolerance. Semin. Immunol. 19 (2007) 180-187
6. Barlic J., McDermott D.H., Merrell M.N., Gonzales J., Via L.E., and Murphy P.M. Interleukin (IL)-15 and IL-2 reciprocally regulate expression of the chemokine receptor CX3CR1 through selective NFAT1- and NFAT2-dependent mechanisms. J. Biol. Chem. 279 (2004) 48520-48534
7. Bendiksen S., and Rekvig O.P. Interleukin-2, but not interleukin-15, is required to terminate experimentally induced clonal T-cell anergy. Scand. J. Immunol. 60 (2004) 64-73
8. Boussiotis V.A., Barber D.L., Nakarai T., Freeman G.J., Gribben J.G., Bernstein G.M., D'Andrea A.D., Ritz J., and Nadler L.M. Prevention of T cell anergy by signaling through the gamma c chain of the IL-2 receptor. Science 266 (1994) 1039-1042
9. Choi S., and Schwartz R.H. Molecular mechanisms for adaptive tolerance and other T cell anergy models. Semin. Immunol. 19 (2007) 140-152
10. Collins S., Lutz M.A., Zarek P.E., Anders R.A., Kersh G.J., and Powell J.D. Opposing regulation of T cell function by Egr-1/NAB2 and Egr-2/Egr-3. Eur. J. Immunol. 38 (2008) 528-536
11. Colombetti S., Basso V., Mueller D.L., and Mondino A. Prolonged TCR/CD28 engagement drives IL-2-independent T cell clonal expansion through signaling mediated by the mammalian target of rapamycin. J. Immunol. 176 (2006) 2730-2738
12. Colombetti S., Benigni F., Basso V., and Mondino A. Clonal anergy is maintained independently of T cell proliferation. J. Immunol. 169 (2002) 6178-6186
13. Eicher D.M. IL- 2 and IL-15 manifest opposing effects on activation of nuclear factor of activated T cells. Cell. Immunol. 223 (2003) 133-142
14. Ellery J.M., and Nicholls P.J. Alternate signalling pathways from the interleukin-2 receptor. Cytokine Growth Factor Rev. 13 (2002) 27-40
15. Fathman C.G., and Lineberry N.B. Molecular mechanisms of CD4(+) T-cell anergy. Nat. Rev. Immunol. 7 (2007) 599-609
16. Gaffen S.L. Signaling domains of the interleukin 2 receptor. Cytokine 14 (2001) 63-77
17. Gollob J.A., Schnipper C.P., Murphy E.A., Ritz J., and Frank D.A. The functional synergy between IL-12 and IL-2 involves p38 mitogen-activated protein kinase and is associated with the augmentation of STAT serine phosphorylation. J. Immunol. 162 (1999) 4472-4481
18. Harris J.E., Bishop K.D., Phillips N.E., Mordes J.P., Greiner D.L., Rossini A.A., and Czech M.P. Early growth response gene-2, a zinc-finger transcription factor, is required for full induction of clonal anergy in CD4+ T cells. J. Immunol. 173 (2004) 7331-7338
19. Heissmeyer V., Macian F., Im S.H., Varma R., Feske S., Venuprasad K., Gu H., Liu Y.C., Dustin M.L., and Rao A. Calcineurin imposes T cell unresponsiveness through targeted proteolysis of signaling proteins. Nat. Immunol. 5 (2004) 255-265
20. Heissmeyer V., Macian F., Varma R., Im S.H., Garcia-Cozar F., Horton H.F., Byrne M.C., Feske S., Venuprasad K., Gu H., Liu Y.C., Dustin M.L., and Rao A. A molecular dissection of lymphocyte unresponsiveness induced by sustained calcium signalling. Novartis Found. Symp. 267 (2005) 165-174
21. Inoki K., Li Y., Xu T., and Guan K.L. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev. 17 (2003) 1829-1834
22. Inoki K., Li Y., Zhu T., Wu J., and Guan K.L. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 4 (2002) 648-657
23. Jenkins M.K., Chen C.A., Jung G., Mueller D.L., and Schwartz R.H. Inhibition of antigen-specific proliferation of type 1 murine T cell clones after stimulation with immobilized anti-CD3 monoclonal antibody. J. Immunol. 144 (1990) 16-22
24. Jeon M.S., Atfield A., Venuprasad K., Krawczyk C., Sarao R., Elly C., Yang C., Arya S., Bachmaier K., Su L., Bouchard D., Jones R., Gronski M., Ohashi P., Wada T., Bloom D., Fathman C.G., Liu Y.C., and Penninger J.M. Essential role of the E3 ubiquitin ligase Cbl-b in T cell anergy induction. Immunity 21 (2004) 167-177
25. Li L., Iwamoto Y., Berezovskaya A., and Boussiotis V.A. A pathway regulated by cell cycle inhibitor p27(Kip1) and checkpoint inhibitor Smad3 is involved in the induction of T cell tolerance. Nat. Immunol. 7 (2006) 1157-1165
26. Macian F. NFAT proteins: key regulators of T-cell development and function. Nat. Rev. Immunol. 5 (2005) 472-484
27. Macian F., Garcia-Cozar F., Im S.H., Horton H.F., Byrne M.C., and Rao A. Transcriptional mechanisms underlying lymphocyte tolerance. Cell 109 (2002) 719-731
28. Macian F., Garcia-Rodriguez C., and Rao A. Gene expression elicited by NFAT in the presence or absence of cooperative recruitment of Fos and Jun. EMBO J. 19 (2000) 4783-4795
29. Macian F., Im S.H., Garcia-Cozar F.J., and Rao A. T-cell anergy. Curr. Opin. Immunol. 16 (2004) 209-216
30. Mondino A., and Mueller D.L. mTOR at the crossroads of T cell proliferation and tolerance. Semin. Immunol. 19 (2007) 162-172
31. Olenchock B.A., Guo R., Carpenter J.H., Jordan M., Topham M.K., Koretzky G.A., and Zhong X.P. Disruption of diacylglycerol metabolism impairs the induction of T cell anergy. Nat. Immunol. 7 (2006) 1174-1181
32. Powell J.D. The induction and maintenance of T cell anergy. Clin. Immunol. 120 (2006) 239-246
33. Powell J.D., Bruniquel D., and Schwartz R.H. TCR engagement in the absence of cell cycle progression leads to T cell anergy independent of p27 (Kip1). Eur. J. Immunol. 31 (2001) 3737-3746
34. Powell J.D., Lerner C.G., and Schwartz R.H. Inhibition of cell cycle progression by rapamycin induces T cell clonal anergy even in the presence of costimulation. J. Immunol. 162 (1999) 2775-2784
35. Quill H., and Schwartz R.H. Stimulation of normal inducer T cell clones with antigen presented by purified Ia molecules in planar lipid membranes: specific induction of a long-lived state of proliferative nonresponsiveness. J. Immunol. 138 (1987) 3704-3712
36. Safford M., Collins S., Lutz M.A., Allen A., Huang C.T., Kowalski J., Blackford A., Horton M.R., Drake C., Schwartz R.H., and Powell J.D. Egr-2 and Egr-3 are negative regulators of T cell activation. Nat. Immunol. 6 (2005) 472-480
37. Schwartz R.H. T cell anergy. Annu. Rev. Immunol. 21 (2003) 305-334
38. Seroogy C.M., Soares L., Ranheim E.A., Su L., Holness C., Bloom D., and Fathman C.G. The gene related to anergy in lymphocytes, an E3 ubiquitin ligase, is necessary for anergy induction in CD4 T cells. J. Immunol. 173 (2004) 79-85
39. Soares L., Seroogy C., Skrenta H., Anandasabapathy N., Lovelace P., Chung C.D., Engleman E., and Fathman C.G. Two isoforms of otubain 1 regulate T cell anergy via GRAIL. Nat. Immunol. 5 (2004) 45-54
40. Su L., Lineberry N., Huh Y., Soares L., and Fathman C.G. A novel E3 ubiquitin ligase substrate screen identifies Rho guanine dissociation inhibitor as a substrate of gene related to anergy in lymphocytes. J. Immunol. 177 (2006) 7559-7566
41. Tee A.R., Fingar D.C., Manning B.D., Kwiatkowski D.J., Cantley L.C., and Blenis J. Tuberous sclerosis complex-1 and -2 gene products function together to inhibit mammalian target of rapamycin (mTOR)-mediated downstream signalling. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 13571-13576
42. Thomas R.M., Chunder N., Chen C., Umetsu S.E., Winandy S., and Wells A.D. Ikaros enforces the costimulatory requirement for IL2 gene expression and is required for anergy induction in CD4+ T lymphocytes. J. Immunol. 179 (2007) 7305-7315
43. Zha Y., Marks R., Ho A.W., Peterson A.C., Janardhan S., Brown I., Praveen K., Stang S., Stone J.C., and Gajewski T.F. T cell anergy is reversed by active Ras and is regulated by diacylglycerol kinase-alpha. Nat. Immunol. 7 (2006) 1166-1173
44. Zheng Y., Collins S.L., Lutz M.A., Allen A.N., Kole T.P., Zarek P.E., and Powell J.D. A role for mammalian target of rapamycin in regulating T cell activation versus anergy. J. Immunol. 178 (2007) 2163-2170