Resistance of Foxp3+ regulatory T cells to Nur77-induced apoptosis promotes allograft survival

PLoS ONE

Volumn 3, Issue 5, 2008, Pages

  Tao, Ran ^a   Hancock, Wayne W ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASILIXIMAB; CD4 ANTIGEN; CD8 ANTIGEN; HISTONE DEACETYLASE; HISTONE DEACETYLASE 7; HISTONE DEACETYLASE 9; INTERLEUKIN 2 RECEPTOR ALPHA; NUCLEAR RECEPTOR NUR77; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP1; TRANSCRIPTION FACTOR FOXP3; DNA BINDING PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; STEROID RECEPTOR;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CARDIAC GRAFT REJECTION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL LINEAGE; CONTROLLED STUDY; DONOR; GENE EXPRESSION; GENE OVEREXPRESSION; GRAFT RECIPIENT; GRAFT SURVIVAL; HEART GRAFT; HEART TRANSPLANTATION; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE TRANSFER; LYMPHOID ORGAN; MOUSE; NONHUMAN; POSTOPERATIVE PERIOD; PROTEIN FAMILY; RECEPTOR UPREGULATION; REGULATORY T LYMPHOCYTE; SPLEEN CELL; SURVIVAL RATE; T LYMPHOCYTE; THYMOCYTE; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; IMMUNOLOGY; PHYSIOLOGY;

MURINAE; MUS; MUS MUSCULUS;

ANIMALS; APOPTOSIS; DNA-BINDING PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; GRAFT SURVIVAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, STEROID; T-LYMPHOCYTES, REGULATORY;

EID: 48449099740     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002321     Document Type: Article

References (36)

1. Woronicz JD, Calnan B, Ngo V, Winoto A (1994) Requirement for the orphan steroid receptor Nur77 in apoptosis of T-cell hybridomas. Nature 367: 277-281.
2. Liu ZG, Smith SW, McLaughlin KA, Schwartz LM, Osborne BA (1994) Apoptotic signals delivered through the T-cell receptor of a T-cell hybrid require the immediate-early gene nur77. Nature 367: 281-284.
3. Calnan BJ, Szychowski S, Chan FK, Cado D, Winoto A (1995) A role for the orphan steroid receptor Nur77 in apoptosis accompanying antigen-induced negative selection. Immunity 3: 273-282.
4. Weih F, Ryseck RP, Chen L, Bravo R (1996) Apoptosis of nur77/ N10-transgenic thymocytes involves the Fas/Fas ligand pathway. Proc Natl Acad Sci U S A 93: 5533-5538.
5. Zhou T, Cheng J, Yang P, Wang Z, Liu C, et al. (1996) Inhibition of Nur77/Nurr1 leads to inefficient clonal deletion of self-reactive T cells. J Exp Med 183: 1879-1892.
6. Lee SL, Wesselschmidt RL, Linette GP, Kanagawa O, Russell JH, et al. (1995) Unimpaired thymic and peripheral T cell death in mice lacking the nuclear receptor NGFI-B (Nur77). Science 269: 532-535.
7. Dequiedt F, Kasler H, Fischle W, Kiermer V, Weinstein M, et al. (2003) HDAC7, a thymus-specific class II histone deacetylase, regulates Nur77 transcription and TCR-mediated apoptosis. Immunity 18: 687-698.
8. Kao HY, Verdel A, Tsai CC, Simon C, Juguilon H, et al. (2001) Mechanism for nucleocytoplasmic shuttling of histone deacetylase 7. J Biol Chem 276: 47496-47507.
9. Dequiedt F, Van Lint J, Lecomte E, Van Duppen V, Seufferlein T, et al. (2005) Phosphorylation of histone deacetylase 7 by protein kinase D mediates T cell receptor-induced Nur77 expression and apoptosis. J Exp Med 201: 793-804.
10. Parra M, Kasler H, McKinsey TA, Olson EN, Verdin E (2005) Protein kinase D1 phosphorylates HDAC7 and induces its nuclear export after T-cell receptor activation. J Biol Chem 280: 13762-13770.
11. Zhang J, DeYoung A, Kasler HG, Kabra NH, Kuang AA, et al. (1999) Receptor-mediated apoptosis in T lymphocytes. Cold Spring Harb Symp Quant Biol 64: 363-371.
12. Singer GG, Abbas AK (1994) The fas antigen is involved in peripheral but not thymic deletion of T lymphocytes in T cell receptor transgrnic mice. Immunity 1: 365-371.
13. DeYoung AL, Duramad O, Winoto A (2000) The TNF receptor family member CD30 is not essential for negative selection. J Immunol 165: 6170-6173.
14. Li H, Kolluri SK, Gu J, Dawson MI, Cao X, et al. (2000) Cytochrome c release and apoptosis induced by mitochondrial targeting of nuclear orphan receptor TR3. Science 289: 1159-1164.
15. Dawson MI, Hobbs PD, Peterson VJ, Leid M, Lange CW, et al. (2001) Apopitosis induction in cancer cells by a novel analogue of 6-[3-(1-adamantyl)-4-hydroxyphenyl]-2-naphthalenecarboxytic acid lacking retinoid receptor transcriptional activation activity. Cancer Res 61: 4723-4730.
16. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, et al. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489.
17. Rajpal A, Cho YA, Yelent B, Koza-Taylor PH, Li D, et al. (2003) Transcriptional activation of known and novel apoptotic pathways by Nur77 orphan steroid receptor. EMBO J 22: 6526-6536.
18. Kim H, Kim BY, Soh JW, Cho EJ, Liu JO, et al. (2006) A novel function of Nur77: physical and functional association with protein kinase C. Biochem Biophys Res Commun 348: 950-956.
19. Li B, Samanta A, Song X, Iacono KT, Bembas K, et al. (2007) FOXP3 interactions with historic acetyltransferase and class II historic deacetylases we required for repression. Proc Natl Acad Sci U S A 104: 4571-4576.
20. Lce I, Wang L, Wells AD, Dorf ME, Ozkaynak E, et al. (2005) Recruitment of Foxp3+ T regulatory cells mediating allograft tolerance depends on the CCR4 chemokine receptor. J Exp Med 201: 1037-1044.
21. Tao R, de Zoeten EF, Ozkaynak E, Chen C, Wang L, et al. (2007) Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat Med 13: 1299-1307.
22. Gennari A, Bleumink R, Viviani B, Galli CL, Marinovich M, et al. (2002) Identification by DNA macroarray of nur77 as a gene induced by di-n-butyltin dichloride: its role in organotin-induced apoptosis. Toxicol Appl Pharmacol 181: 27-31.
23. De Silva S, Han S, Zhang X, Huston DP, Winoto A, et al. (2005) Reduction of the incidence and severity of collagen-induced arthritis by constitutive Nur77 expression in the T cell lineage. Arthritis Rheum 52: 333-338.
24. Hancock WW, Wang L, Ye Q, Han R, Lee I (2003) Chemokines and their receptors as markers of allograft rejection and targets for immunosuppression. Curr Opin Immunol 15: 479-486.
25. Kasprowic DJ, Droin N, Soper DM, Ramsdell F, Green DR, et al. (2005) Dynamic regulation of FoxP3 expression controls the balance between CD4+ T cell activation and cell death. Eur J Immunol 35: 3424-3432.
26. Mohamood AS, Trujillo CJ, Zheng D, Jie C, Murillo FM, et al. (2006) Gld mutation of Fas ligand increases the frequency and up-regulates cell survival genes in CD25+CD4+ TR cells. Int Immunol 18: 1265-1277.
27. Fritzsching B, Oberle N, Pauly E, Geffers R, Buer J, et al. (2006) Naive regulatory T cells: a novel subpopulation defined by resistance toward GD95L-mediated cell death. Blood 108: 3371-3378.
28. Fritzsching B, Oberle N, Eberhardt N, Quick S, Haas J, et al. (2005) In contrast to effector T cells, CD4+CD25+FoxP3+ regulatory T cells are highly susceptible to CD95 ligand- but not to TCR-mediated cell death. J Immunol 175: 32-36.
29. Kang HJ, Song MR, Lee SK, Shin EC, Choi YH, et al. (2000) Retinoic acid and its receptors repress the expression and transactivation functions of Nur77: a possible mechanism for the inhibition of apoptosis by retinoic acid. Exp Cell Res 256: 545-554.
30. Toth R, Szegezdi E, Reichert U, Bernardon JM, Michel S, et al. (2001) Activation-induced apoptosis and cell surface expression of Fas (CD95) ligand are reciprocally regulated by retinoic acid receptor alpha and gamma and involve nur77 in T cells. Eur J Immunol 31: 1382-1391.
31. Li Y, Lin B, Agadir A, Liu R, Dawson MI, et al. (1998) Molecular determinants of AHPN (CD437)-induced growth arrest and apoptosis in human lung cancer cell lines. Mol Cell Biol 18: 4719-4731.
32. Liu W, Youn HD, Liu JO (2001) Thapsigargin-induced apoptosis involves Cabin1-MEF2-mediated induction of Nur77. Eur J Immunol 31: 1757-1764.
33. Yazdanbakhsh K, Choi JW, Li Y, Lau LF, Choi Y (1995) Cyclosporin A blocks apoptosis by initibiting the DNA binding activity of the transcription factor Nur77. Proc Natl Acad Sci U S A 92: 437-441.
34. Suchin EJ, Langmuir PB, Palmer E, Sayegh MH, Wells AD, et al. (2001) Quantifying the frequency of alloreactive T cells in vivo: new answers to an old question. J Immunol 166: 973-981.
35. Tao R, Wang L, Han R, Wang T, Ye Q et al. (2005) Differential effects of B and T lymphocyte attenuator and programmed death-1 on acceptance of partially versus filly MHC-mismatched cardiac allografts. J Immunol 175: 5774-5782.
36. Corry RJ, Winn HJ, Russell PS (1973) Primarily vascularized allografts of hearts in mice. The role of H-2D, H-2K, and non-H-2 antigens in rejection. Transplantation 16: 343-350.