Prevention of allogeneic cardiac graft rejection by transfer of ex vivo expanded antigen-specific regulatory T-cells

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Takasato, Fumika ^a,d   Morita, Rimpei ^a,d   Schichita, Takashi ^a,d   Sekiya, Takashi ^a,d   Morikawa, Yasuhide ^b   Kuroda, Tatsuo ^a   Niimi, Masanori ^c   Yoshimura, Akihiko ^a,d  

^a KEIO UNIVERSITY   (Japan)

^b INTERNATIONAL UNIVERSITY OF JAPAN   (Japan)

^c TEIKYO UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CARDIAC GRAFT REJECTION; CELL EXPANSION; CHRONIC GRAFT REJECTION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; ENGRAFTMENT; EX VIVO STUDY; GRAFT RECIPIENT; GRAFT SURVIVAL; HEART TRANSPLANTATION; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; VASCULITIS;

ADOPTIVE TRANSFER; ANIMALS; ANTIGEN PRESENTATION; DENDRITIC CELLS; GRAFT REJECTION; GRAFT SURVIVAL; GRAFT VS HOST DISEASE; HEART TRANSPLANTATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED CBA; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION, HOMOLOGOUS;

EID: 84894630932     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087722     Document Type: Article

References (47)

1. Cervera C, Fernandez-Ruiz M, Valledor A, Linares L, Anton A, et al. (2011) Epidemiology and risk factors for late infection in solid organ transplant recipients. Transpl Infect Dis 13: 598-607.
2. Sampaio MS, Cho YW, Qazi Y, Bunnapradist S, Hutchinson IV, et al. (2012) Posttransplant malignancies in solid organ adult recipients: an analysis of the u.s. National transplant database. Transplantation 94: 990-998.
3. Zuppan CW, Wells LM, Kerstetter JC, Johnston JK, Bailey LL, et al. (2009) Cause of death in pediatric and infant heart transplant recipients: review of a 20-year, single-institution cohort. J Heart Lung Transplant 28: 579-584.
4. Akiyama Y, Shirasugi N, Aramaki O, Matsumoto K, Shimazu M, et al. (2002) Intratracheal delivery of a single major histocompatibility complex class I peptide induced prolonged survival of fully allogeneic cardiac grafts and generated regulatory cells. Hum Immunol 63: 888-892. (Pubitemid 35246769)
5. Aramaki O, Shirasugi N, Akiyama Y, Takayama T, Shimazu M, et al. (2003) Induction of operational tolerance and generation of regulatory cells after intratracheal delivery of alloantigen combined with nondepleting anti-CD4 monoclonal antibody. Transplantation 76: 1305-1314. (Pubitemid 37430716)
6. Koenecke C, Czeloth N, Bubke A, Schmitz S, Kissenpfennig A, et al. (2009) Alloantigen-specific de novo-induced Foxp3+ Treg revert in vivo and do not protect from experimental GVHD. Eur J Immunol 39: 3091-3096.
7. Floess S, Freyer J, Siewert C, Baron U, Olek S, et al. (2007) Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol 5: e38.
8. Sakaguchi S, Yamaguchi T, Nomura T, Ono M (2008) Regulatory T cells and immune tolerance. Cell 133: 775-787. (Pubitemid 351707693)
9. Zhou X, Kong N, Wang J, Fan H, Zou H, et al. (2010) Cutting edge: all-trans retinoic acid sustains the stability and function of natural regulatory T cells in an inflammatory milieu. J Immunol 185: 2675-2679.
10. Lu L, Ma J, Li Z, Lan Q, Chen M, et al. (2011) All-trans retinoic acid promotes TGF-beta-induced Tregs via histone modification but not DNA demethylation on Foxp3 gene locus. PLoS One 6: e24590.
11. van Kooten C, Lombardi G, Gelderman KA, Sagoo P, Buckland M, et al. (2011) Dendritic cells as a tool to induce transplantation tolerance: obstacles and opportunities. Transplantation 91: 2-7.
12. Morelli AE, Thomson AW (2007) Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 7: 610-621. (Pubitemid 47123548)
13. Woltman AM, van der Kooij SW, de Fijter JW, van Kooten C (2006) Maturation-resistant dendritic cells induce hyporesponsiveness in alloreactive CD45RA+ and CD45RO+ T-cell populations. Am J Transplant 6: 2580-2591. (Pubitemid 44571678)
14. Taner T, Hackstein H, Wang Z, Morelli AE, Thomson AW (2005) Rapamycin-treated, alloantigen-pulsed host dendritic cells induce ag-specific T cell regulation and prolong graft survival. Am J Transplant 5: 228-236. (Pubitemid 40179509)
15. Latek R, Fleener C, Lamian V, Kulbokas E, 3rd, Davis PM, et al. (2009) Assessment of belatacept-mediated costimulation blockade through evaluation of CD80/86-receptor saturation. Transplantation 87: 926-933.
16. Zhang X, Li M, Lian D, Zheng X, Zhang ZX, et al. (2008) Generation of therapeutic dendritic cells and regulatory T cells for preventing allogeneic cardiac graft rejection. Clin Immunol 127: 313-321.
17. Joffre O, Santolaria T, Calise D, Al Saati T, Hudrisier D, et al. (2008) Prevention of acute and chronic allograft rejection with CD4+CD25+Foxp3+ regulatory T lymphocytes. Nat Med 14: 88-92.
18. Ichiyama K, Sekiya T, Inoue N, Tamiya T, Kashiwagi I, et al. (2011) Transcription factor Smad-independent T helper 17 cell induction by transforming-growth factor-beta is mediated by suppression of eomesodermin. Immunity 34: 741-754.
19. Niimi M (2001) The technique for heterotopic cardiac transplantation in mice: experience of 3000 operations by one surgeon. J Heart Lung Transplant 20: 1123-1128.
20. Sekiya T, Kashiwagi I, Yoshida R, Fukaya T, Morita R, et al. (2013) Nr4a receptors are essential for thymic regulatory T cell development and immune homeostasis. Nature immunology 14: 230-237.
21. Tamiya T, Ichiyama K, Kotani H, Fukaya T, Sekiya T, et al. (2013) Smad2/3 and IRF4 play a cooperative role in IL-9-producing T cell induction. Journal of immunology 191: 2360-2371.
22. Takahashi R, Nishimoto S, Muto G, Sekiya T, Tamiya T, et al. (2011) SOCS1 is essential for regulatory T cell functions by preventing loss of Foxp3 expression as well as IFN-{gamma} and IL-17A production. J Exp Med 208: 2055-2067.
23. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, et al. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223: 77-92. (Pubitemid 29096240)
24. Koga K, Takaesu G, Yoshida R, Nakaya M, Kobayashi T, et al. (2009) Cyclic adenosine monophosphate suppresses the transcription of proinflammatory cytokines via the phosphorylated c-Fos protein. Immunity 30: 372-383.
25. Takimoto T, Wakabayashi Y, Sekiya T, Inoue N, Morita R, et al. (2010) Smad2 and Smad3 are redundantly essential for the TGF-beta-mediated regulation of regulatory T plasticity and Th1 development. Journal of immunology 185: 842-855.
26. Shichita T, Hasegawa E, Kimura A, Morita R, Sakaguchi R, et al. (2012) Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nature medicine 18: 911-917.
27. Hasegawa E, Sonoda KH, Shichita T, Morita R, Sekiya T, et al. (2013) IL-23-independent induction of IL-17 from gammadeltaT cells and innate lymphoid cells promotes experimental intraocular neovascularization. Journal of immunology 190: 1778-1787.
28. Zheng SG, Wang J, Wang P, Gray JD, Horwitz DA (2007) IL-2 is essential for TGF-beta to convert naive CD4+CD25- cells to CD25+Foxp3+ regulatory T cells and for expansion of these cells. J Immunol 178: 2018-2027. (Pubitemid 46233398)
29. Shevach EM, Davidson TS, Huter EN, Dipaolo RA, Andersson J (2008) Role of TGF-Beta in the induction of Foxp3 expression and T regulatory cell function. J Clin Immunol 28: 640-646.
30. Chai JG, Coe D, Chen D, Simpson E, Dyson J, et al. (2008) In vitro expansion improves in vivo regulation by CD4+CD25+ regulatory T cells. J Immunol 180: 858-869.
31. Sela U, Olds P, Park A, Schlesinger SJ, Steinman RM (2011) Dendritic cells induce antigen-specific regulatory T cells that prevent graft versus host disease and persist in mice. J Exp Med 208: 2489-2496.
32. Brennan TV, Jaigirdar A, Hoang V, Hayden T, Liu FC, et al. (2009) Preferential priming of alloreactive T cells with indirect reactivity. Am J Transplant 9: 709-718.
33. Tarbell KV, Petit L, Zuo X, Toy P, Luo X, et al. (2007) Dendritic cellexpanded, islet-specific CD4+ CD25+ CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice. J Exp Med 204: 191-201. (Pubitemid 46148769)
34. Gupta S, Balasubramanian S, Thornley TB, Strom TB, Kenny JJ (2011) Direct pathway T-cell alloactivation is more rapid than indirect pathway alloactivation. Transplantation 91: e65-67.
35. Burrell BE, Nakayama Y, Xu J, Brinkman CC, Bromberg JS (2012) Regulatory T cell induction, migration, and function in transplantation. J Immunol 189: 4705-4711.
36. Wood KJ (2011) Regulatory T cells in transplantation. Transplant Proc 43: 2135-2136.
37. Tang Q, Bluestone JA (2008) The Foxp3+ regulatory T cell: a jack of all trades, master of regulation. Nat Immunol 9: 239-244. (Pubitemid 351267321)
38. Kang SM, Tang Q, Bluestone JA (2007) CD4+CD25+ regulatory T cells in transplantation: progress, challenges and prospects. Am J Transplant 7: 1457-1463. (Pubitemid 46776267)
39. Wood KJ, Sakaguchi S (2003) Regulatory T cells in transplantation tolerance. Nat Rev Immunol 3: 199-210. (Pubitemid 37323205)
40. Waldmann H (2008) Tolerance can be infectious. Nat Immunol 9: 1001-1003.
41. Jonuleit H, Schmitt E, Kakirman H, Stassen M, Knop J, et al. (2002) Infectious tolerance: human CD25(+) regulatory T cells convey suppressor activity to conventional CD4(+) T helper cells. J Exp Med 196: 255-260. (Pubitemid 34787515)
42. Li M, Zhang X, Zheng X, Lian D, Zhang ZX, et al. (2008) Tolerogenic dendritic cells transferring hyporesponsiveness and synergizing T regulatory cells in transplant tolerance. Int Immunol 20: 285-293. (Pubitemid 351234396)
43. van Maurik A, Herber M, Wood KJ, Jones ND (2002) Cutting edge: CD4+CD25+ alloantigen-specific immunoregulatory cells that can prevent CD8+ T cell-mediated graft rejection: implications for anti-CD154 immunotherapy. J Immunol 169: 5401-5404. (Pubitemid 35291635)
44. Jones ND, Brook MO, Carvalho-Gaspar M, Luo S, Wood KJ (2010) Regulatory T cells can prevent memory CD8+ T-cell-mediated rejection following polymorphonuclear cell depletion. Eur J Immunol 40: 3107-3116.
45. Sutmuller RP, van Duivenvoorde LM, van Elsas A, Schumacher TN, Wildenberg ME, et al. (2001) Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. The Journal of experimental medicine 194: 823-832. (Pubitemid 32983017)
46. Kinter A, McNally J, Riggin L, Jackson R, Roby G, et al. (2007) Suppression of HIV-specific T cell activity by lymph node CD25+ regulatory T cells from HIV-infected individuals. Proceedings of the National Academy of Sciences of the United States of America 104: 3390-3395. (Pubitemid 46364169)
47. Fernandez MA, Puttur FK, Wang YM, Howden W, Alexander SI, et al. (2008) T regulatory cells contribute to the attenuated primary CD8+ and CD4+ T cell responses to herpes simplex virus type 2 in neonatal mice. Journal of immunology 180: 1556-1564.