Administration of low doses of IL-2 combined to rapamycin promotes allogeneic skin graft survival in mice

American Journal of Transplantation

Volumn 14, Issue 12, 2014, Pages 2874-2882

  Pilon, C B ^a,b,c   Petillon, S ^a,b   Naserian, S ^a,b   Martin, G H ^a,b   Badoual, C ^d   Lang, P ^a,b,c   Azoulay, D ^a,b,c   Piaggio, E ^e,f,g   Grimbert, P ^a,b,c   Cohen, J L ^a,b,c  

^a FACULTÉ DE MÉDECINE   (France)

^b INSERM U955   (France)

^c HENRI MONDOR HOSPITAL   (France)

^d HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^e PSL RESEARCH UNIVERSITY   (France)

^f INSTITUT CURIE   (France)

^g INSERM   (France)

Author keywords

alloantigen; Basic (laboratory) research; graft survival; immune modulation; immune regulation; immunobiology; immunosuppression; murine; tissue (nonvascularized); tolerance; translational research; transplantation

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; RAPAMYCIN; RECOMBINANT INTERLEUKIN 2; ANTINEOPLASTIC AGENT; DRUG COMBINATION; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL EXPANSION; CLINICAL EVALUATION; CONTROLLED STUDY; FEMALE; GRAFT REJECTION; GRAFT SURVIVAL; LOW DRUG DOSE; MALE; MOUSE; NONHUMAN; SKIN GRAFT; ALLOTRANSPLANTATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; DBA MOUSE; DOSE RESPONSE; DRUG COMBINATION; DRUG EFFECTS; ENZYME IMMUNOASSAY; FLOW CYTOMETRY; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; POSTOPERATIVE COMPLICATION; REGULATORY T LYMPHOCYTE; SKIN TRANSPLANTATION; TRANSPLANTATION TOLERANCE;

ANIMALS; ANTINEOPLASTIC AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG COMBINATIONS; FLOW CYTOMETRY; GRAFT REJECTION; GRAFT SURVIVAL; HUMANS; IMMUNOENZYME TECHNIQUES; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED DBA; POSTOPERATIVE COMPLICATIONS; SIROLIMUS; SKIN TRANSPLANTATION; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION TOLERANCE; TRANSPLANTATION, HOMOLOGOUS;

EID: 84910637672     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12944     Document Type: Article

References (31)

1. Li XC, Turka LA., An update on regulatory T cells in transplant tolerance and rejection. Nat Rev Nephrol 2010; 6: 577-583.
2. Darrasse-Jeze G, Klatzmann D, Charlotte F, Salomon BL, Cohen JL., CD4+CD25+ regulatory/suppressor T cells prevent allogeneic fetus rejection in mice. Immunol Lett 2006; 102: 106-109.
3. Taylor PA, Lees CJ, Blazar BR., The infusion of ex vivo activated and expanded CD4(+)CD25(+) immune regulatory cells inhibits graft-versus-host disease lethality. Blood 2002; 99: 3493-3499.
4. Cohen JL, Trenado A, Vasey D, Klatzmann D, Salomon BL., CD4(+)CD25(+) immunoregulatory T cells: New therapeutics for graft-versus-host disease. J Exp Med 2002; 196: 401-406.
5. Hoffmann P, Ermann J, Edinger M, Fathman CG, Strober S., Donor-type CD4(+)CD25(+) regulatory T cells suppress lethal acute graft-versus-host disease after allogeneic bone marrow transplantation. J Exp Med 2002; 196: 389-399.
6. Nadig SN, Wieckiewicz J, Wu DC, et al. In vivo prevention of transplant arteriosclerosis by ex vivo-expanded human regulatory T cells. Nat Med 2010; 16: 809-813.
7. Landwehr-Kenzel S, Issa F, Luu SH, et al. Novel GMP-compatible protocol employing an allogeneic B cell bank for clonal expansion of allospecific natural regulatory T cells. Am J Transplant 2014; 14: 594-606.
8. Putnam AL, Safinia N, Medvec A, et al. Clinical grade manufacturing of human alloantigen-reactive regulatory T cells for use in transplantation. Am J Transplant 2013; 13: 3010-3020.
9. Sagoo P, Ali N, Garg G, Nestle FO, Lechler RI, Lombardi G., Human regulatory T cells with alloantigen specificity are more potent inhibitors of alloimmune skin graft damage than polyclonal regulatory T cells. Sci Transl Med 2011; 3: 83ra42.
10. Brunstein CG, Miller JS, Cao Q, et al. Infusion of ex vivo expanded T regulatory cells in adults transplanted with umbilical cord blood: Safety profile and detection kinetics. Blood 2011; 117: 1061-1070.
11. Di Ianni M, Falzetti F, Carotti A, et al. Tregs prevent GVHD and promote immune reconstitution in HLA-haploidentical transplantation. Blood 2011; 117: 3921-3928.
12. Zhang H, Chua KS, Guimond M, et al. Lymphopenia and interleukin-2 therapy alter homeostasis of CD4+CD25+ regulatory T cells. Nat Med 2005; 11: 1238-1243.
13. Weiss L, Letimier FA, Carriere M, et al. In vivo expansion of naive and activated CD4+CD25+FOXP3+ regulatory T cell populations in interleukin-2-treated HIV patients. Proc Natl Acad Sci USA 2010; 107: 10632-10637.
14. Scheffold A, Huhn J, Hofer T., Regulation of CD4+CD25+ regulatory T cell activity: It takes (IL-)two to tango. Eur J Immunol 2005; 35: 1336-1341.
15. Grinberg-Bleyer Y, Baeyens A, You S, et al. IL-2 reverses established type 1 diabetes in NOD mice by a local effect on pancreatic regulatory T cells. J Exp Med 2010; 207: 1871-1878.
16. Saadoun D, Rosenzwajg M, Joly F, et al. Regulatory T-cell responses to low-dose interleukin-2 in HCV-induced vasculitis. N Engl J Med 2011; 365: 2067-2077.
17. Koreth J, Matsuoka K, Kim HT, et al. Interleukin-2 and regulatory T cells in graft-versus-host disease. N Engl J Med 2011; 365: 2055-2066.
18. Martin GH, Gregoire S, Landau DA, et al. In vivo activation of transferred regulatory T cells specific for third-party exogenous antigen controls GVH disease in mice. Eur J Immunol 2013; 43: 2263-2272.
19. Zeiser R, Nguyen VH, Beilhack A, et al. Inhibition of CD4+CD25+ regulatory T-cell function by calcineurin-dependent interleukin-2 production. Blood 2006; 108: 390-399.
20. Kornete M, Sgouroudis E, Piccirillo CA., ICOS-dependent homeostasis and function of Foxp3+ regulatory T cells in islets of nonobese diabetic mice. J Immunol 2012; 188: 1064-1074.
21. El Essawy B, Putheti P, Gao W, Strom TB., Rapamycin generates graft-homing murine suppressor CD8(+) T cells that confer donor-specific graft protection. Cell Transplant 2011; 20: 1759-1769.
22. Cohen JL, Boyer O., The role of CD4+CD25hi regulatory T cells in the physiopathogeny of graft-versus-host disease. Curr Opin Immunol 2006; 18: 580-585.
23. Tsang JY, Tanriver Y, Jiang S, et al. Conferring indirect allospecificity on CD4+CD25+Tregs by TCR gene transfer favors transplantation tolerance in mice. J Clin Invest 2008; 118: 3619-3628.
24. Shin HJ, Baker J, Leveson-Gower DB, Smith AT, Sega EI, Negrin RS., Rapamycin and IL-2 reduce lethal acute graft-versus-host disease associated with increased expansion of donor type CD4+CD25+Foxp3+ regulatory T cells. Blood 2011; 118: 2342-2350.
25. Battaglia M, Stabilini A, Roncarolo MG., Rapamycin selectively expands CD4+CD25+FoxP3+ regulatory T cells. Blood 2005; 105: 4743-4748.
26. Wang Y, Kissenpfennig A, Mingueneau M, et al. Th2 lymphoproliferative disorder of LatY136F mutant mice unfolds independently of TCR-MHC engagement and is insensitive to the action of Foxp3+ regulatory T cells. J Immunol 2008; 180: 1565-1575.
27. Gaidot A, Landau DA, Martin GH, et al. Immune reconstitution is preserved in hematopoietic stem cell transplant co-administered with regulatory T cells for GVHD prevention. Blood 2011; 117: 2975-2983.
28. Ito S, Bollard CM, Carlsten M, et al. Ultra-low dose interleukin-2 promotes immune-modulating function of regulatory T cells and natural killer cells in healthy volunteers. Mol Ther 2014; 22: 1388-1395.
29. Charbonnier LM, Vokaer B, Lemaitre PH, Field KA, Leo O, Le Moine A., CTLA4-Ig restores rejection of MHC class-II mismatched allografts by disabling IL-2-expanded regulatory T cells. Am J Transplant 2012; 12: 2313-2321.
30. Vokaer B, Charbonnier LM, Lemaitre PH, Le Moine A., Impact of interleukin-2-expanded regulatory T cells in various allogeneic combinations on mouse skin graft survival. Transplant Proc 2012; 44: 2840-2844.
31. Boyman O, Kovar M, Rubinstein MP, Surh CD, Sprent J., Selective stimulation of T cell subsets with antibody-cytokine immune complexes. Science 2006; 311: 1924-1927.