The TGF-β-Smad3 pathway inhibits CD28-dependent cell growth and proliferation of CD4 T cells

Genes and Immunity

Volumn 14, Issue 2, 2013, Pages 115-126

  Delisle, J S ^a,b   Giroux, M ^a   Boucher, G ^c   Landry, J R ^c   Hardy, M P ^c   Lemieux, S ^c   Jones, R G ^d   Wilhelm, B T ^c   Perreault, C ^a,b,c  

^a MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; MAMMALIAN TARGET OF RAPAMYCIN; RAPAMYCIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL GROWTH; CELL METABOLISM; CONTROLLED STUDY; GENE EXPRESSION REGULATION; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE PROLIFERATION; MICROARRAY ANALYSIS; MITOSIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION REGULATION;

ANIMALS; ANTIGENS, CD28; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; IMMUNOSUPPRESSIVE AGENTS; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; SIROLIMUS; SMAD3 PROTEIN; TOR SERINE-THREONINE KINASES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84874769606     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2012.63     Document Type: Article

References (82)

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37. Rathmell JC, Elstrom RL, Cinalli RM, Thompson CB. Activated Akt promotes increased resting T cell size, CD28-independent T cell growth, and development of autoimmunity and lymphoma. Eur J Immunol 2003; 33: 2223-2232.
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39. Caron E, Vincent K, Fortier MH, Laverdure JP, Bramoulle A, Hardy MP et al. The MHC I immunopeptidome conveys to the cell surface an integrative view of cellular regulation. Mol Syst Biol 2011; 7: 533.
40. Choo AY, Yoon SO, Kim SG, Roux PP, Blenis J. Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc Natl Acad Sci USA 2008; 105: 17414-17419.
41. Baron C, Somogyi R, Greller LD, Rineau V, Wilkinson P, Cho CR et al. Prediction of graft-versus-host disease in humans by donor gene-expression profiling. PLoS Med 2007; 4: 69-83.
42. Newfeld SJ, Wisotzkey RG, Kumar S. Molecular evolution of a developmental pathway: phylogenetic analyses of transforming growth factor-beta family ligands, receptors and Smad signal transducers. Genetics 1999; 152: 783-795.
43. Schmierer B, Hill CS. TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 2007; 8: 970-982.
44. Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RA. Transforming growth factorbeta regulation of immune responses. Annu Rev Immunol 2006; 24: 99-146.
45. Li MO, Flavell RA. TGF-beta: a master of all T cell trades. Cell 2008; 134: 392-404.
46. Gorelik L, Flavell RA. Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 2000; 12: 171-181.
47. Letterio JJ, Geiser AG, Kulkarni AB, Dang H, Kong L, Nakabayashi T et al. Autoimmunity associated with TGF-beta1-deficiency in mice is dependent on MHC class II antigen expression. J Clin Invest 1996; 98: 2109-2119.
48. Marie JC, Liggitt D, Rudensky AY. Cellular mechanisms of fatal early-onset autoimmunity in mice with the T cell-specific targeting of transforming growth factorbeta receptor. Immunity 2006; 25: 441-454.
49. Zhang N, Bevan MJ. TGF-beta signaling to T cells inhibits autoimmunity during lymphopenia-driven proliferation. Nat Immunol 2012; 13: 667-673.
50. Classen S, Zander T, Eggle D, Chemnitz JM, Brors B, Buchmann I et al. Human resting CD4 T cells are constitutively inhibited by TGF beta under steady-state conditions. J Immunol 2007; 178: 6931-6940.
51. Feng XH, Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol 2005; 21: 659-693.
52. Letterio JJ. TGF-beta signaling in T cells: roles in lymphoid and epithelial neoplasia. Oncogene 2005; 24: 5701-5712.
53. Li L, Iwamoto Y, Berezovskaya A, Boussiotis VA. A pathway regulated by cell cycle inhibitor p27Kip1 and checkpoint inhibitor Smad3 is involved in the induction of T cell tolerance. Nat Immunol 2006; 7: 1157-1165.
54. Maggio-Price L, Treuting P, Zeng W, Tsang M, Bielefeldt-Ohmann H, Iritani BM. Helicobacter infection is required for inflammation and colon cancer in SMAD3- deficient mice. Cancer Res 2006; 66: 828-838.
55. Giroux M, Delisle JS, Gauthier SD, Heinonen KM, Hinsinger J, Houde B et al. SMAD3 prevents graft-versus-host disease by restraining Th1 differentiation and granulocyte- mediated tissue damage. Blood 2011; 117: 1734-1744.
56. Giroux M, Delisle JS, O'Brien A, Hebert MJ, Perreault C. T cell activation leads to protein kinase C theta-dependent inhibition of TGF-beta signaling. J Immunol 2010; 185: 1568-1576.
57. Tone Y, Furuuchi K, Kojima Y, Tykocinski ML, Greene MI, Tone M. Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nat Immunol 2008; 9: 194-202.
58. Iwashima M. Kinetic perspectives of T cell antigen receptor signaling. A two-tier model for T cell full activation. Immunol Rev 2003; 191: 196-210.
59. Rutz S, Noubade R, Eidenschenk C, Ota N, Zeng W, Zheng Y et al. Transcription factor c-Maf mediates the TGF-beta-dependent suppression of IL-22 production in T(H)17 cells. Nat Immunol 2011; 12: 1238-1245.
60. Zou L, Barnett B, Safah H, Larussa VF, Evdemon-Hogan M, Mottram P et al. Bone marrow is a reservoir for CD4CD25 regulatory T cells that traffic through CXCL12/CXCR4 signals. Cancer Res 2004; 64: 8451-8455.
61. Sugita S, Horie S, Nakamura O, Maruyama K, Takase H, Usui Y et al. Acquisition of T regulatory function in cathepsin L-inhibited T cells by eye-derived CTLA-2alpha during inflammatory conditions. J Immunol 2009; 183: 5013-5022.
62. Solomon BD, Mueller C, Chae WJ, Alabanza LM, Bynoe MS. Neuropilin-1 attenuates autoreactivity in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 2011; 108: 2040-2045.
63. Ondr JK, Pham CT. Characterization of murine cathepsin W and its role in cellmediated cytotoxicity. J Biol Chem 2004; 279: 27525-27533.
64. Harada Y, Elly C, Ying G, Paik JH, Depinho RA, Liu YC. Transcription factors Foxo3a and Foxo1 couple the E3 ligase Cbl-b to the induction of Foxp3 expression in induced regulatory T cells. J Exp Med 2010; 207: 1381-1391.
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66. Jones RG, Thompson CB. Revving the engine: signal transduction fuels T cell activation. Immunity 2007; 27: 173-178.
67. Araki K, Turner AP, Shaffer VO, Gangappa S, Keller SA, Bachmann MF et al. mTOR regulates memory CD8 T-cell differentiation. Nature 2009; 460: 108-112.
68. Chi H. Regulation and function of mTOR signalling in T cell fate decisions. Nat Rev Immunol 2012; 12: 325-338.
69. Powell JD, Pollizzi KN, Heikamp EB, Horton MR. Regulation of immune responses by mTOR. Annu Rev Immunol 2012; 30: 39-68.
70. Pearce EL, Walsh MC, Cejas PJ, Harms GM, Shen H, Wang LS et al. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 2009; 460: 103-107.
71. Fox CJ. Hammerman PS & Thompson CB. Fuel feeds function: energy metabolism and the T-cell response. Nat Rev Immunol 2005; 5: 844-852.
72. Zheng Y, Delgoffe GM, Meyer CF, Chan W, Powell JD. Anergic T cells are metabolically anergic. J Immunol 2009; 183: 6095-6101.
73. Gerriets VA, Rathmell JC. Metabolic pathways in T cell fate and function. Trends Immunol 2012; 33: 168-173.
74. Mondino A, Mueller DL. mTOR at the crossroads of T cell proliferation and tolerance. Semin Immunol 2007; 19: 162-172.
75. Song J, Salek-Ardakani S, So T, Croft M. The kinases aurora B and mTOR regulate the G1-S cell cycle progression of T lymphocytes. Nat Immunol 2007; 8: 64-73.
76. Gudmundsdottir H, Wells AD, Turka LA. Dynamics and requirements of T cell clonal expansion in vivo at the single-cell level: effector function is linked to proliferative capacity. J Immunol 1999; 162: 5212-5223.
77. McKarns SC, Schwartz RH. Distinct effects of TGF-beta 1 on CD4 and CD8 T cell survival, division, and IL-2 production: a role for T cell intrinsic Smad3. J Immunol 2005; 174: 2071-2083.
78. Rathmell JC, Elstrom RL, Cinalli RM, Thompson CB. Activated Akt promotes increased resting T cell size, CD28-independent T cell growth, and development of autoimmunity and lymphoma. Eur J Immunol 2003; 33: 2223-2232.
79. Dowling RJ, Topisirovic I, Alain T, Bidinosti M, Fonseca BD, Petroulakis E et al. mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 2010; 328: 1172-1176.
80. Caron E, Vincent K, Fortier MH, Laverdure JP, Bramoulle A, Hardy MP et al. The MHC I immunopeptidome conveys to the cell surface an integrative view of cellular regulation. Mol Syst Biol 2011; 7: 533.
81. Choo AY, Yoon SO, Kim SG, Roux PP, Blenis J. Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc Natl Acad Sci USA 2008; 105: 17414-17419.
82. Baron C, Somogyi R, Greller LD, Rineau V, Wilkinson P, Cho CR et al. Prediction of graft-versus-host disease in humans by donor gene-expression profiling. PLoS Med 2007; 4: 69-83.