Induction of suppressive allogeneic regulatory T cells via rabbit antithymocyte polyclonal globulin during homeostatic proliferation in rat kidney transplantation

Transplant International

Volumn 28, Issue 1, 2015, Pages 108-119

  Valdez Ortiz, Rafael ^a,b,c   Bestard, Oriol ^a,c   Llaudó, Inés ^a   Franquesa, Marcella ^a   Cerezo, Gema ^a   Torras, Joan ^a,c   Herrero Fresneda, Inmaculada ^a   Correa Rotter, Ricardo ^d   Grinyó, Josep M ^a,c  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b HOSPITAL GENERAL DE MÉXICO   (Mexico)

^c HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^d INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

Author keywords

homeostatic proliferation; kidney transplantation; rabbit antithymocyte polyclonal globulin; Tregs

Indexed keywords

THYMOCYTE ANTIBODY; FORKHEAD TRANSCRIPTION FACTOR; INTERLEUKIN 2 RECEPTOR ALPHA; LYMPHOCYTE ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOLOGICAL ACTIVITY; BLOOD; CELL PROLIFERATION; CONTROLLED STUDY; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY GRAFT; KIDNEY TRANSPLANTATION; LYMPHOCYTE; MALE; MEMORY T LYMPHOCYTE; NONHUMAN; RABBIT; RAT; REGULATORY T LYMPHOCYTE; SINGLE DRUG DOSE; T CELL DEPLETION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; ALLOTRANSPLANTATION; ANIMAL; CD4+ T LYMPHOCYTE; CELL SEPARATION; CHEMISTRY; COCULTURE; CYTOLOGY; HOMEOSTASIS; IMMUNOLOGY; METABOLISM; MONONUCLEAR CELL; PHENOTYPE; RENAL INSUFFICIENCY; SPLEEN; THYMOCYTE;

ANIMALS; ANTILYMPHOCYTE SERUM; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELL SEPARATION; COCULTURE TECHNIQUES; FORKHEAD TRANSCRIPTION FACTORS; HOMEOSTASIS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; KIDNEY TRANSPLANTATION; LEUKOCYTES, MONONUCLEAR; MALE; PHENOTYPE; RABBITS; RATS; RENAL INSUFFICIENCY; SPLEEN; T-LYMPHOCYTES, REGULATORY; THYMOCYTES; TRANSPLANTATION, HOMOLOGOUS;

EID: 84916228570     PISSN: 09340874     EISSN: 14322277     Source Type: Journal    
DOI: 10.1111/tri.12448     Document Type: Article

References (50)

1. Freitas AA, Rocha BB,. Lymphocyte lifespans: homeostasis, selection and competition. Immunol Today 1993; 14: 25.
2. Tchao NK, Turka LA,. Lymphodepletion and homeostatic proliferation: implications for transplantation. Am J Transplant 2012; 12: 1079.
3. Freitas AA, Rocha B,. Population biology of lymphocytes: the flight for survival. Annu Rev Immunol 2000; 18: 83.
4. Gurkan S, Luan Y, Dhillon N, et al,. Immune reconstitution following rabbit antithymocyte globulin. Am J Transplant 2010; 10: 2132.
5. Mohty M,. Mechanisms of action of antithymocyte globulin: T-cell depletion and beyond. Leukemia 2007; 21: 1387.
6. Gaber AO, Monaco AP, Russell JA, Lebranchu Y, Mohty M,. Rabbit antithymocyte globulin (thymoglobulin): 25 years and new frontiers in solid organ transplantation and haematology. Drugs 2010; 70: 691.
7. Goldrath AW, Bevan MJ,. Selecting and maintaining a diverse T-cell repertoire. Nature 1999; 402: 255.
8. Chung DT, Korn T, Richard J, et al,. Anti-thymocyte globulin (ATG) prevents autoimmune encephalomyelitis by expanding myelin antigen-specific Foxp3+ regulatory T-cells. Int Immunol 2007A; 19: 1003.
9. Schmitt WH, Hagen EC, Neumann I, et al,. Treatment of refractory Wegener's granulomatosis with antithymocyte globulin (ATG): an open study in 15 patients. Kidney Int 2004; 65: 1440.
10. Hardinger KL, Brennan DC, Klein CL,. Selection of induction therapy in kidney transplantation. Transpl Int 2013; 26: 662.
11. Gennarini A, Cravedi P, Marasà M, et al,. Perioperative minimal induction therapy: a further step toward more effective immunosuppression in transplantation. J Transplant 2012; 2012: 426042.
12. Mourad G, Morelon E, Noël C, Glotz D, Lebranchu Y,. The role of Thymoglobulin induction in kidney transplantation: an update. Clin Transplant 2012; 26: E450.
13. LaCorcia G, Swistak M, Lawendowski C, et al,. Polyclonal rabbit antithymocyte globulin exhibits consistent immunosuppressive capabilities beyond cell depletion. Transplantation 2009; 87: 966.
14. Lopez M, Clarkson MR, Albin M, Sayegh MH, Najafian N,. A novel 441 mechanism of action for anti-thymocyte globulin: induction of CD4+CD25+Foxp3+ regulatory T-cells. J Am Soc Nephrol 2006; 17: 2844.
15. Broady R, Yu J, Levings MK,. ATG-induced expression of FOXP3 in human CD4(+) T-cells in vitro is associated with T-cell activation and not the induction of Foxp3(+) T regulatory cells. Blood 2009; 114: 5003.
16. Moxham VF, Karegli J, Phillips RE, et al,. Homeostatic proliferation of lymphocytes results in augmented memory-like function and accelerated allograft rejection. J Immunol 2008; 180: 3910.
17. Neujahr DC, Chen C, Huang X, et al,. Accelerated memory cell homeostasis during T cell depletion and approaches to overcome it. J Immunol 2006; 176: 4632.
18. Jennings VM, Dillehay DL,. Immunology. In:, Suckow MA, Weisbroth SH, Franklin CL, eds. The Laboratory Rat, 2nd edn. American College of Laboratory Animal Medicine, 2006: 847-864.
19. Beck JA, Lloyd S, Hafezparast M, Lennon-Pierce M, Eppig JT, Festing MF, Fisher EM,. Genealogies of mouse inbred strains. Nat Genet 2000; 24: 23-25.
20. Greenhouse DD, Festing MFW, Hasan S, Cohen AL,. Catalogue of inbreed strains of rats. In:, Hedrich H, ed. Genetic Monitorings of Inbred Strains of Rats. Stuttgart, New York: Gustav Fischer Verlag, 1999: 1410-1480.
21. Herrero-Fresneda I, Torras J, Cruzado JM, et al,. Do alloreactivity and prolonged cold ischaemia cause different elementary lesions in chronic allograft nephropathy? Am J Pathol 2003; 162: 127.
22. Puklavec MJ, Barclay AN., Monoclonal antibodies to rat leukocyte surface antigens, MHC antigens, and immunoglobulins. Curr Protoc Immunol 2001 May: Appendix.
23. Hargreaves M, Bell EB,. Identical expression of CD45R isoforms by CD45RC+ 'revertant' memory and CD45RC+ naive CD4 T-cells. Immunology 1997; 91: 323-330.
24. Subra JF, Cautain B, Xystrakis E, et al,. The balance between CD45RChigh and CD45RClow CD4 T cells in rats is intrinsic to bone marrow-derived cells and is genetically controlled. J Immunol 2001; 166: 2944.
25. Hargreaves M, Bell EB,. Identical expression of CD45R isoforms by CD45RC+ 'revertant' memory and CD45RC+ naive CD4 T-cells. Immunology 1997; 91: 323.
26. Maghni K, Nicolescu OM, Martin JG,. Suitability of cell metabolic colorimetric assays for assessment of CD4+ T cell proliferation: comparison to 5-bromo-2-deoxyuridine (BrdU) ELISA. J Immunol Methods 1999; 223: 185.
27. Venken K, Thewissen M, Hellings N, et al,. A CFSE based assay for measuring CD4+CD25+ regulatory T cell mediated suppression of auto-antigen specific and polyclonal T cell responses. J Immunol Methods 2007; 322: 1.
28. Collison LW, Vignali DA,. In vitro Treg suppression assays. Methods Mol Biol 2011; 707: 21.
29. Préville X, Flacher M, LeMauff B, et al,. Mechanisms involved in antithymocyte globulin immunosuppressive activity in a nonhuman primate model. Transplantation 2001; 71: 460.
30. Ruzek MC, Neff KS, Luong M, et al,. In vivo characterization of rabbit anti-mouse thymocyte globulin: a surrogate for rabbit anti-human thymocyte globulin. Transplantation 2009; 88: 170.
31. Feng X, Kajigaya S, Solomou EE, et al,. Rabbit ATG but not horse ATG promotes expansion of functional CD4+CD25highFOXP3+ regulatory T-cells in vitro. Blood 2008; 111: 3675.
32. Sewgobind VD, van der Laan LJ, Kho MM, et al,. Characterization of rabbit antithymocyte globulins-induced CD25+ regulatory T-cells from cells of patients with end-stage renal disease. Transplantation 2010; 89: 655.
33. Shen S, Ding Y, Tadokoro CE, et al,. Control of homeostatic proliferation by regulatory T-cells. J Clin Invest 2005; 115: 3517.
34. Winstead CJ, Fraser JM, Khoruts A,. Regulatory CD4+CD25+Foxp3+ T-cells selectively inhibit the spontaneous form of lymphopenia-induced proliferation of naive T-cells. J Immunol 2008; 180: 7305.
35. Winstead CJ, Reilly CS, Moon JJ, et al,. CD4+CD25+Foxp3+ regulatory T cells optimize diversity of the conventional T cell repertoire during reconstitution from lymphopenia. J Immunol 2010; 184: 4749.
36. Sener A, Tang AL, Farber DL,. Memory T-cell predominance following T-cell depletional therapy derives from homeostatic expansion of naive T-cells. Am J Transplant 2009; 9: 2615.
37. Wu Z, Bensinger SJ, Zhang J, et al,. Homeostatic proliferation is a barrier to transplantation tolerance. Nat Med 2004; 10: 87.
38. Yang J, Brook MO, Carvalho-Gaspar M, et al,. Allograft rejection mediated by memory T cells is resistant to regulation. Proc Natl Acad Sci USA 2007; 104: 19954.
39. McNally A, McNally M, Galea R, Thomas R, Steptoe RJ,. Immunogenic, but not steady-state, antigen presentation permits regulatory T-cells to control CD8+ T-cell effector differentiation by IL-2 modulation. PLoS One 2014; 9: e85455.
40. Singh K, Kozyr N, Stempora L, et al,. Regulatory T cells exhibit decreased proliferation but enhanced suppression after pulsing with sirolimus. Am J Transplant 2012; 12: 1441.
41. Dai Z, Li Q, Wang Y, et al,. CD4+CD25+ regulatory T cells suppress allograft rejection mediated by memory CD8+ T cells via a CD30-dependent mechanism. J Clin Invest 2004; 113: 310.
42. Bestard O, Cruzado JM, Mestre M, et al,. Achieving donor-specific hyporesponsiveness is associated with FOXP3+ regulatory T cell recruitment in human renal allograft infiltrates. J Immunol 2007; 179: 4901.
43. Noris M, Casiraghi F, Todeschini M, et al,. Regulatory T cells and T cell depletion: role of immunosuppressive drugs. J Am Soc Nephrol 2007; 18: 1007.
44. Valujskikh A,. Memory T cells in allograft rejection. Adv Exp Med Biol 2007; 601: 247.
45. Pearl JP, Parris J, Hale DA, et al,. Immunocompetent T-cells with a memory-like phenotype are the dominant cell type following antibody-mediated T-cell depletion. Am J Transplant 2005; 5: 465.
46. Popow I, Leitner J, Grabmeier-Pfistershammer K, et al,. A comprehensive and quantitative analysis of the major specificities in rabbit antithymocyte globulin preparations. Am J Transplant 2013; 13: 3103.
47. Popow I, Leitner J, Majdic O, et al,. Assessment of batch to batch variation in polyclonal antithymocyte globulin preparations. Transplantation 2012; 93: 32.
48. Cicora F, Mos F, Paz M, Roberti J,. Clinical experience with thymoglobulin and antithymocyte globulin-Fresenius as induction therapy in renal transplant patients: a retrospective study. Exp Clin Transplant 2013; 11: 418.
49. Schnetzler B, Leger P, Völp A, Dorent R, Pavie A, Gandjbakhch I,. A prospective randomized controlled study on the efficacy and tolerance of two antilymphocytic globulins in the prevention of rejection in first-heart transplant recipients. Transpl Int 2002; 15: 317.
50. Terasako K, Sato K, Sato M, et al,. The effect of different ATG preparations on immune recovery after allogeneic hematopoietic stem cell transplantation for severe aplastic anemia. Hematology 2010; 15: 165.