Transplant tolerance is associated with reduced expression of cystathionine-γ-lyase that controls IL-12 production by dendritic cells and TH-1 immune responses

Blood

Volumn 119, Issue 11, 2012, Pages 2633-2643

  De Silly, Romain Vuillefroy ^a,b   Coulon, Flora ^a,b   Poirier, Nicolas ^a,b   Jovanovic, Vojislav ^a   Brouard, Sophie ^a   Ferchaud Roucher, Véronique ^a,b   Blancho, Gilles ^a,b   Vanhove, Bernard ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE NANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTATHIONINE GAMMA LYASE; CYSTEINE; GAMMA INTERFERON; HYDROGEN SULFIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12; PROPARGYLGLYCINE; TRANSCRIPTION FACTOR T BET;

ALLOTRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CARDIAC GRAFT REJECTION; CONTROLLED STUDY; DENDRITIC CELL; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; HYPERSENSITIVITY; IMMUNE RESPONSE; MONOCYTE; NONHUMAN; ORGAN TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SULFATION; TH1 CELL; TRANSPLANTATION TOLERANCE;

EID: 84858668806     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-04-350546     Document Type: Article

References (53)

1. Szabo C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov. 2007;6(11):917-935. (Pubitemid 350042399)
2. Angelini G, Gardella S, Ardy M, et al. Antigen-presenting dendritic cells provide the reducing extracellular microenvironment required for T lymphocyte activation. Proc Natl Acad Sci U S A. 2002;99(3):1491-1496. (Pubitemid 34136520)
3. Sen CK. Redox signaling and the emerging therapeutic potential of thiol antioxidants. Biochem Pharmacol. 1998;55(11):1747-1758. (Pubitemid 28305256)
4. Suthanthiran M, Anderson ME, Sharma VK, Meister A. Glutathione regulates activation-dependent DNA synthesis in highly purified normal human T lymphocytes stimulated via the CD2 and CD3 antigens. Proc Natl Acad Sci U S A. 1990;87(9):3343-3347.
5. Yan Z, Garg SK, Banerjee R. Regulatory T cells interfere with glutathione metabolism in dendritic cells and T cells. J Biol Chem. 2010;285(53):41525- 41532.
6. Yan Z, Garg SK, Kipnis J, Banerjee R. Extracellular redox modulation by regulatory T cells. Nat Chem Biol. 2009;5(10):721-723.
7. Srivastava MK, Sinha P, Clements VK, Rodriguez P, Ostrand-Rosenberg S. Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Cancer Res. 2010;70(1):68-77.
8. Alam K, Ghousunnissa S, Nair S, Valluri VL, Mukhopadhyay S. Glutathione-redox balance regulates c-rel-driven IL-12 production in macrophages: possible implications in antituberculosis immunotherapy. J Immunol. 2010;184(6):2918-2929.
9. Kuppner MC, Scharner A, Milani V, et al. Ifosfamide impairs the allostimulatory capacity of human dendritic cells by intracellular glutathione depletion. Blood. 2003;102(10):3668-3674. (Pubitemid 37409387)
10. Kim HJ, Barajas B, Chan RC, Nel AE. Glutathione depletion inhibits dendritic cell maturation and delayed-type hypersensitivity: implications for systemic disease and immunosenescence. J Allergy Clin Immunol. 2007;119(5):1225-1233. (Pubitemid 46654168)
11. Mustafa AK, Gadalla MM, Sen N, et al. H2S signals through protein S-sulfhydration. Sci Signal. 2009;2(96):ra72.
12. Collin M, Anuar FB, Murch O, Bhatia M, Moore PK, Thiemermann C. Inhibition of endogenous hydrogen sulfide formation reduces the organ injury caused by endotoxemia. Br J Pharmacol. 2005;146(4):498-505. (Pubitemid 41487065)
13. Bhatia M, Wong FL, Fu D, Lau HY, Moochhala SM, Moore PK. Role of hydrogen sulfide in acute pancreatitis and associated lung injury. FASEB J. 2005;19(6):623-625. (Pubitemid 40471265)
14. Zhang H, Zhi L, Moochhala S, Moore PK, Bhatia M. Hydrogen sulfide acts as an inflammatory mediator in cecal ligation and puncture-induced sepsis in mice by upregulating the production of cytokines and chemokines via NF-kappaB. Am J Physiol Lung Cell Mol Physiol. 2007;292(4):L960-L971. (Pubitemid 46608243)
15. Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL. Hydrogen sulfide is an endogenous modulator of leukocytemediated inflammation. FASEB J. 2006;20(12):2118-2120.
16. Bhatia M, Sidhapuriwala J, Moochhala SM, Moore PK. Hydrogen sulphide is a mediator of carrageenan-induced hindpaw oedema in the rat. Br J Pharmacol. 2005;145(2):141-144. (Pubitemid 40756518)
17. Lechler RI, Sykes M, Thomson AW, Turka LA. Organ transplantation: how much of the promise has been realized? Nat Med. 2005;11(6):605-613. (Pubitemid 40868300)
18. Dugast AS, Vanhove B. Immune regulation by non-lymphoid cells in transplantation. Clin Exp Immunol. 2009;156(1):25-34.
19. Ono K, Lindsey ES. Improved technique of heart transplantation in rats. J Thorac Cardiovasc Surg. 1969;57(2):225-229.
20. Soulillou JP, Carpenter CB, d'Apice AJ, Strom TB. The role of nonclassical Fc receptor-associated, Ag-B antigens (Ia) in rat allograft enhancement. J Exp Med. 1976;143(2):405-421.
21. Degauque N, Lair D, Dupont A, et al. Dominant tolerance to kidney allografts induced by anti-donor MHC class II antibodies: cooperation between T and non-T CD103+ cells. J Immunol. 2006;176(7):3915-3922. (Pubitemid 44264368)
22. Haspot F, Seveno C, Dugast AS, et al. Anti-CD28 antibody-induced kidney allograft tolerance related to tryptophan degradation and TCR class II B7 regulatory cells. Am J Transplant. 2005;5(10):2339-2348.
23. Josien R, Pannetier C, Douillard P, et al. Graft-infiltrating T helper cells, CD45RC phenotype, and Th1/Th2-related cytokines in donor-specific transfusion-induced tolerance in adult rats. Transplantation. 1995;60(10):1131-1139.
24. Guillonneau C, Hill M, Hubert FX, et al. CD40Ig treatment results in allograft acceptance mediated by CD8CD45RC T cells, IFN-gamma, and indoleamine 2,3-dioxygenase. J Clin Invest. 2007;117(4):1096-1106. (Pubitemid 46556766)
25. Chiffoleau E, Beriou G, Dutartre P, Usal C, Soulillou JP, Cuturi MC. Role for thymic and splenic regulatory CD4(+) T cells induced by donor dendritic cells in allograft tolerance by LF15-0195 treatment. J Immunol. 2002;168(10):5058-5069. (Pubitemid 34495969)
26. Haspot F, Villemain F, Laflamme G, et al. Differential effect of CD28 versus B7 blockade on direct pathway of allorecognition and self-restricted responses. Blood. 2002;99(6):2228-2234. (Pubitemid 34525511)
27. Stipanuk MH, Beck PW. Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem J. 1982;206(2):267-277.
28. Kuster A, Tea I, Sweeten S, Roze JC, Robins RJ, Darmaun D. Simultaneous determination of glutathione and cysteine concentrations and 2H enrichments in microvolumes of neonatal blood using gas chromatography-mass spectrometry. Anal Bioanal Chem. 2008;390(5):1403-1412.
29. Chiffoleau E, Beriou G, Dutartre P, Usal C, Soulillou JP, Cuturi MC. Induction of donor-specific allograft tolerance by short-term treatment with LF15-0195 after transplantation: evidence for a direct effect on T-cell differentiation. Am J Transplant. 2002;2(8):745-757. (Pubitemid 36342617)
30. Ishii I, Akahoshi N, Yamada H, Nakano S, Izumi T, Suematsu M. Cystathionine gamma-Lyase-deficient mice require dietary cysteine to protect against acute lethal myopathy and oxidative injury. J Biol Chem. 2010;285(34):26358-26368.
31. Bode KA, Schmitz F, Vargas L, Heeg K, Dalpke AH. Kinetic of RelA activation controls magnitude of TLR-mediated IL-12p40 induction. J Immunol. 2009;182(4):2176-2184.
32. Finkelman FD, Madden KB, Cheever AW, et al. Effects of interleukin 12 on immune responses and host protection in mice infected with intestinal nematode parasites. J Exp Med. 1994;179(5):1563-1572. (Pubitemid 24129573)
33. Black CA. Delayed type hypersensitivity: current theories with an historic perspective. Dermatol Online J. 1999;5(1):7.
34. van Kooten C, Lombardi G, Gelderman KA, et al. Dendritic cells as a tool to induce transplantation tolerance: obstacles and opportunities. Transplantation. 2011;91(1):2-7.
35. Muthukumar T, Dadhania D, Ding R, et al. Messenger RNA for FOXP3 in the urine of renal-allograft recipients. N Engl J Med. 2005;353(22):2342-2351. (Pubitemid 41713746)
36. Kendal AR, Chen Y, Regateiro FS, et al. Sustained suppression by Foxp3+ regulatory T cells is vital for infectious transplantation tolerance. J Exp Med. 2011;208(10):2043-2053.
37. Zhi L, Ang AD, Zhang H, Moore PK, Bhatia M. Hydrogen sulfide induces the synthesis of proinflammatory cytokines in human monocyte cell line U937 via the ERK-NF-kappaB pathway. J Leukoc Biol. 2007;81(5):1322-1332. (Pubitemid 46702052)
38. Oh GS, Pae HO, Lee BS, et al. Hydrogen sulfide inhibits nitric oxide production and nuclear factorkappaB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic Biol Med. 2006;41(1):106-119.
39. Yang G, Wu L, Jiang B, et al. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science. 2008;322(5901):587-590.
40. Yang G, Cao K, Wu L, Wang R. Cystathionine gamma-lyase overexpression inhibits cell proliferation via a H2S-dependent modulation of ERK1/2 phosphorylation and p21Cip/WAK-1. J Biol Chem. 2004;279(47):49199-49205. (Pubitemid 39625803)
41. McKenna GJ, Kim PT, Mui AL, et al. Glutathione depletion of stimulator cells inhibits responder T-cell immunogenicity in vitro and prolongs allograft survival in vivo. Am J Surg. 2006;191(5):588-592.
42. Yin H, Li XY, Jin XB, et al. IL-33 prolongs murine cardiac allograft survival through induction of TH2-type immune deviation. Transplantation. 2010;89(10):1189-1197.
43. Li XC, Zand MS, Li Y, Zheng XX, Strom TB. On histocompatibility barriers, Th1 to Th2 immune deviation, and the nature of the allograft responses. J Immunol. 1998;161(5):2241-2247. (Pubitemid 28397035)
44. Piccotti JR, Chan SY, Li K, Eichwald EJ, Bishop DK. Differential effects of IL-12 receptor blockade with IL-12 p40 homodimer on the induction of CD4+ and CD8+ IFN-gamma-producing cells. J Immunol. 1997;158(2):643-648. (Pubitemid 127492641)
45. Williamson E, Garside P, Bradley JA, More IA, Mowat AM. Neutralizing IL-12 during induction of murine acute graft-versus-host disease polarizes the cytokine profile toward a Th2-type alloimmune response and confers long term protection from disease. J Immunol. 1997;159(3):1208-1215. (Pubitemid 127484097)
46. Xie A, Wang S, Zhang K, et al. Treatment with interleukin-12/23p40 antibody attenuates acute cardiac allograft rejection. Transplantation. 2011;91(1):27-34.
47. Renga B, Mencarelli A, Migliorati M, Distrutti E, Fiorucci S. Bile-acid-activated farnesoid X receptor regulates hydrogen sulfide production and hepatic microcirculation. World J Gastroenterol. 2009;15(17):2097-2108.
48. Link D, Drebing C, Glode LM. Cystathionase: a potential cytoplasmic marker of hematopoietic differentiation. Blut. 1983;47(1):31-39. (Pubitemid 13063802)
49. Beriou G, Peche H, Guillonneau C, Merieau E, Cuturi MC. Donor-specific allograft tolerance by administration of recipient-derived immature dendritic cells and suboptimal immunosuppression. Transplantation. 2005;79(8):969-972. (Pubitemid 40586872)
50. Ma X, Montaner LJ. Proinflammatory response and IL-12 expression in HIV-1 infection. J Leukoc Biol. 2000;68(3):383-390.
51. Toohey JI. Sulfur metabolism in AIDS: cystamine as an anti-HIV agent. AIDS Res Hum Retroviruses. 2009;25(11):1057-1060.
52. Fraternale A, Paoletti MF, Dominici S, et al. Modulation of Th1/Th2 immune responses to HIV-1 Tat by new pro-GSH molecules. Vaccine. 2011;29(40):6823-6829.
53. Breitkreutz R, Holm S, Pittack N, et al. Massive loss of sulfur in HIV infection. AIDS Res Hum Retroviruses. 2000;16(3):203-209.