Common gamma chain cytokines promote rapid in vitro expansion of allo-specific human CD8 + suppressor T cells

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Yu, Yuming ^a,b   Zitzner, Jennifer R ^a   Houlihan, Josetta ^a   Herrera, Nancy ^a   Xu, Luting ^a   Miller, Joshua ^a   Mathew, James M ^a   Tambur, Anat R ^a   Luo, Xunrong ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD56 ANTIGEN; CD57 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 2 RECEPTOR GAMMA; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; PERFORIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; CYTOKINE; EPITOPE;

ALLOGENEIC RESTRICTION; ANTIGEN PRESENTING CELL; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL SPECIFICITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; HLA MATCHING; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; SUPPRESSOR CELL; CELL ADHESION; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; CYTOTOXICITY; DONOR; DRUG EFFECT; HISTOCOMPATIBILITY TEST; IMMUNOLOGY; METABOLISM; PHENOTYPE; SPECIES DIFFERENCE;

ANTIGEN-PRESENTING CELLS; ANTIGENS, CD28; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HISTOCOMPATIBILITY TESTING; HUMANS; INTERFERON-GAMMA; INTERLEUKIN RECEPTOR COMMON GAMMA SUBUNIT; PHENOTYPE; SPECIES SPECIFICITY; TISSUE DONORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 83355168683     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028948     Document Type: Article

References (49)

1. Sakaguchi S, (2005) Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 6: 345-352.
2. Tsang JY, Tanriver Y, Jiang S, Leung E, Ratnasothy K, et al. (2009) Indefinite mouse heart allograft survival in recipient treated with CD4(+)CD25(+) regulatory T cells with indirect allospecificity and short term immunosuppression. Transpl Immunol 21: 203-209.
3. 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.
4. Trzonkowski P, Bieniaszewska M, Juscinska J, Dobyszuk A, Krzystyniak A, et al. (2009) First-in-man clinical results of the treatment of patients with graft versus host disease with human ex vivo expanded CD4+CD25+CD127- T regulatory cells. Clin Immunol 133: 22-26.
5. Liu Z, Tugulea S, Cortesini R, Suciu-Foca N, (1998) Specific suppression of T helper alloreactivity by allo-MHC class I-restricted CD8+CD28- T cells. Int Immunol 10: 775-783.
6. Dijke IE, Caliskan K, Klepper M, de Kuiper R, Balk AH, et al. (2009) Donor-specific immune regulation by CD8 lymphocytes expanded from rejecting human cardiac allografts. Am J Transplant 9: 397-403.
7. Li XL, Menoret S, Bezie S, Caron L, Chabannes D, et al. (2010) Mechanism and localization of CD8 regulatory T cells in a heart transplant model of tolerance. J Immunol 185: 823-833.
8. Guillonneau C, Hill M, Hubert FX, Chiffoleau E, Herve C, et al. (2007) CD40Ig treatment results in allograft acceptance mediated by CD8CD45RC T cells, IFN-gamma, and indoleamine 2,3-dioxygenase. J Clin Invest 117: 1096-1106.
9. Konya C, Goronzy JJ, Weyand CM, (2009) Treating autoimmune disease by targeting CD8(+) T suppressor cells. Expert Opin Biol Ther 9: 951-965.
10. Tsai S, Shameli A, Yamanouchi J, Clemente-Casares X, Wang J, et al. (2010) Reversal of autoimmunity by boosting memory-like autoregulatory T cells. Immunity 32: 568-580.
11. Jarnicki AG, Lysaght J, Todryk S, Mills KH, (2006) Suppression of antitumor immunity by IL-10 and TGF-beta-producing T cells infiltrating the growing tumor: influence of tumor environment on the induction of CD4+ and CD8+ regulatory T cells. J Immunol 177: 896-904.
12. Godlove J, Chiu WK, Weng NP, (2007) Gene expression and generation of CD28-CD8 T cells mediated by interleukin 15. Exp Gerontol 42: 412-415.
13. Cosmi L, Liotta F, Lazzeri E, Francalanci M, Angeli R, et al. (2003) Human CD8+CD25+ thymocytes share phenotypic and functional features with CD4+CD25+ regulatory thymocytes. Blood 102: 4107-4114.
14. Rifa'i M, Kawamoto Y, Nakashima I, Suzuki H, (2004) Essential roles of CD8+CD122+ regulatory T cells in the maintenance of T cell homeostasis. J Exp Med 200: 1123-1134.
15. Shi Z, Okuno Y, Rifa'i M, Endharti AT, Akane K, et al. (2009) Human CD8+CXCR3+ T cells have the same function as murine CD8+CD122+ Treg. Eur J Immunol 39: 2106-2119.
16. Uss E, Rowshani AT, Hooibrink B, Lardy NM, van Lier RA, et al. (2006) CD103 is a marker for alloantigen-induced regulatory CD8+ T cells. J Immunol 177: 2775-2783.
17. Joosten SA, van Meijgaarden KE, Savage ND, de Boer T, Triebel F, et al. (2007) Identification of a human CD8+ regulatory T cell subset that mediates suppression through the chemokine CC chemokine ligand 4. Proc Natl Acad Sci U S A 104: 8029-8034.
18. Mahic M, Henjum K, Yaqub S, Bjornbeth BA, Torgersen KM, et al. (2008) Generation of highly suppressive adaptive CD8(+)CD25(+)FOXP3(+) regulatory T cells by continuous antigen stimulation. Eur J Immunol 38: 640-646.
19. Davila E, Kang YM, Park YW, Sawai H, He X, et al. (2005) Cell-based immunotherapy with suppressor CD8+ T cells in rheumatoid arthritis. J Immunol 174: 7292-7301.
20. Chang CC, Ciubotariu R, Manavalan JS, Yuan J, Colovai AI, et al. (2002) Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol 3: 237-243.
21. Zhang L, Bertucci AM, Ramsey-Goldman R, Burt RK, Datta SK, (2009) Regulatory T cell (Treg) subsets return in patients with refractory lupus following stem cell transplantation, and TGF-beta-producing CD8+ Treg cells are associated with immunological remission of lupus. J Immunol 183: 6346-6358.
22. Luo X, Tarbell KV, Yang H, Pothoven K, Bailey SL, et al. (2007) Dendritic cells with TGF-beta1 differentiate naive CD4+CD25- T cells into islet-protective Foxp3+ regulatory T cells. Proc Natl Acad Sci U S A 104: 2821-2826.
23. Saito M, Nagasawa M, Takada H, Hara T, Tsuchiya S, et al. (2011) Defective IL-10 signaling in hyper-IgE syndrome results in impaired generation of tolerogenic dendritic cells and induced regulatory T cells. J Exp Med 208: 235-249.
24. Bedke T, Pretsch L, Karakhanova S, Enk AH, Mahnke K, (2010) Endothelial cells augment the suppressive function of CD4+ CD25+ Foxp3+ regulatory T cells: involvement of programmed death-1 and IL-10. J Immunol 184: 5562-5570.
25. Hippen KL, Merkel SC, Schirm DK, Nelson C, Tennis NC, et al. (2011) Generation and Large-Scale Expansion of Human Inducible Regulatory T Cells That Suppress Graft-Versus-Host Disease. Am J Transplant.
26. Chiu WK, Fann M, Weng NP, (2006) Generation and growth of CD28nullCD8+ memory T cells mediated by IL-15 and its induced cytokines. J Immunol 177: 7802-7810.
27. Borthwick NJ, Lowdell M, Salmon M, Akbar AN, (2000) Loss of CD28 expression on CD8(+) T cells is induced by IL-2 receptor gamma chain signalling cytokines and type I IFN, and increases susceptibility to activation-induced apoptosis. Int Immunol 12: 1005-1013.
28. Kapp JA, Honjo K, Kapp LM, Xu X, Cozier A, et al. (2006) TCR transgenic CD8+ T cells activated in the presence of TGFbeta express FoxP3 and mediate linked suppression of primary immune responses and cardiac allograft rejection. Int Immunol 18: 1549-1562.
29. He H, Yang P, Jiang L, Zhang J, Zhao C, et al. (2008) Upregulation of CD94 on CD8+T cells in anterior chamber-associated immune deviation. BMC Immunol 9: 53.
30. Hahn BH, Singh RP, La Cava A, Ebling FM, (2005) Tolerogenic treatment of lupus mice with consensus peptide induces Foxp3-expressing, apoptosis-resistant, TGFbeta-secreting CD8+ T cell suppressors. J Immunol 175: 7728-7737.
31. Myers L, Croft M, Kwon BS, Mittler RS, Vella AT, (2005) Peptide-specific CD8 T regulatory cells use IFN-gamma to elaborate TGF-beta-based suppression. J Immunol 174: 7625-7632.
32. Seo SK, Choi JH, Kim YH, Kang WJ, Park HY, et al. (2004) 4-1BB-mediated immunotherapy of rheumatoid arthritis. Nat Med 10: 1088-1094.
33. Martin AJ, McCarthy D, Waltenbaugh C, Goings G, Luo X, et al. (2010) Ethylenecarbodiimide-treated splenocytes carrying male CD4 epitopes confer histocompatibility Y chromosome antigen transplant protection by inhibiting CD154 upregulation. J Immunol 185: 3326-3336.
34. Koide J, Engleman EG, (1990) Differences in surface phenotype and mechanism of action between alloantigen-specific CD8+ cytotoxic and suppressor T cell clones. J Immunol 144: 32-40.
35. Damle NK, Engleman EG, (1989) Antigen-specific suppressor T lymphocytes in man. Clin Immunol Immunopathol 53: S17-24.
36. Surh CD, Sprent J, (2008) Homeostasis of naive and memory T cells. Immunity 29: 848-862.
37. Zheng J, Liu Y, Qin G, Chan PL, Mao H, et al. (2009) Efficient induction and expansion of human alloantigen-specific CD8 regulatory T cells from naive precursors by CD40-activated B cells. J Immunol 183: 3742-3750.
38. Gilliet M, Liu YJ, (2002) Generation of human CD8 T regulatory cells by CD40 ligand-activated plasmacytoid dendritic cells. J Exp Med 195: 695-704.
39. Cobbold SP, Adams E, Nolan KF, Regateiro FS, Waldmann H, (2010) Connecting the mechanisms of T-cell regulation: dendritic cells as the missing link. Immunol Rev 236: 203-218.
40. Bisikirska B, Colgan J, Luban J, Bluestone JA, Herold KC, (2005) TCR stimulation with modified anti-CD3 mAb expands CD8+ T cell population and induces CD8+CD25+ Tregs. J Clin Invest 115: 2904-2913.
41. Herold KC, Gitelman SE, Masharani U, Hagopian W, Bisikirska B, et al. (2005) A single course of anti-CD3 monoclonal antibody hOKT3gamma1(Ala-Ala) results in improvement in C-peptide responses and clinical parameters for at least 2 years after onset of type 1 diabetes. Diabetes 54: 1763-1769.
42. Allan SE, Crome SQ, Crellin NK, Passerini L, Steiner TS, et al. (2007) Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int Immunol 19: 345-354.
43. Morgan ME, van Bilsen JH, Bakker AM, Heemskerk B, Schilham MW, et al. (2005) Expression of FOXP3 mRNA is not confined to CD4+CD25+ T regulatory cells in humans. Hum Immunol 66: 13-20.
44. Sansom DM, Walker LS, (2006) The role of CD28 and cytotoxic T-lymphocyte antigen-4 (CTLA-4) in regulatory T-cell biology. Immunol Rev 212: 131-148.
45. Fife BT, Griffin MD, Abbas AK, Locksley RM, Bluestone JA, (2006) Inhibition of T cell activation and autoimmune diabetes using a B cell surface-linked CTLA-4 agonist. J Clin Invest 116: 2252-2261.
46. Qureshi OS, Zheng Y, Nakamura K, Attridge K, Manzotti C, et al. (2011) Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 332: 600-603.
47. Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T, Miyara M, et al. (2008) CTLA-4 control over Foxp3+ regulatory T cell function. Science 322: 271-275.
48. Onishi Y, Fehervari Z, Yamaguchi T, Sakaguchi S, (2008) Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc Natl Acad Sci U S A 105: 10113-10118.
49. Huang L, Baban B, Johnson BA 3rd, Mellor AL, (2010) Dendritic cells, indoleamine 2,3 dioxygenase and acquired immune privilege. Int Rev Immunol 29: 133-155.