Potential of T-regulatory cells to protect xenografts

Current Opinion in Organ Transplantation

Volumn 17, Issue 2, 2012, Pages 155-161

  Muller, Yannick D ^a,b,c   Ehirchiou, Driss ^a   Golshayan, Déla ^c   Buhler, Leo H ^b   Seebach, Jörg D ^a  

^a University Hospital and Medical Faculty Geneva ^*  (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

rejection; T regulatory cells; tolerance; xenotransplantation

Indexed keywords

CD40 LIGAND MONOCLONAL ANTIBODY; CHEMOKINE RECEPTOR CXCR3; INTERLEUKIN 10; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; RAPAMYCIN; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; CD4+ CD25+ T LYMPHOCYTE; CELL PROLIFERATION; ENDOTHELIUM; ENDOTHELIUM CELL; GRAFT REJECTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; NONHUMAN; REGULATORY T LYMPHOCYTE; REVIEW; XENOTRANSPLANTATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ENDOTHELIUM, VASCULAR; HUMANS; IMMUNITY, CELLULAR; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-10; SIROLIMUS; SWINE; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION, HETEROLOGOUS;

EID: 84858797650     PISSN: 10872418     EISSN: 15317013     Source Type: Journal    
DOI: 10.1097/MOT.0b013e3283508e17     Document Type: Review

References (66)

1. Miyagawa S, Yamamoto A, Matsunami K, et al. Complement regulation in the GalT KO era. Xenotransplantation 2010; 17:11-25.
2. Phelps CJ, Koike C, Vaught TD, et al. Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 2003; 299:411-414.
3. Ekser B, Ezzelarab M, Hara H, et al. Clinical xenotransplantation: the next medical revolution? Lancet 2011. [Epub ahead of print]
4. Schneider MK, Seebach JD. Current cellular innate immune hurdles in pig-toprimate xenotransplantation. Curr Opin Organ Transplant 2008; 13:171-177. (Pubitemid 351374256)
5. Le Bas-Bernardet S, Blancho G. Current cellular immunological hurdles in pig-to-primate xenotransplantation. Transpl Immunol 2009; 21:60-64.
6. Plege A, Schwinzer R. Stimulatory and inhibitory receptor interactions in xenotransplantation. Curr Opin Organ Transplant 2010; 15:219-223.
7. Muller YD, Seebach JD, Buhler LH, et al. Transplantation tolerance: clinical potential of regulatory T cells. Self Nonself 2011; 2:26-34.
8. Muller YD, Golshayan D, Ehirchiou D, et al. T regulatory cells in xenotransplantation. Xenotransplantation 2009; 16:121-128.
9. Porter CM, Bloom ET. Human CD4+CD25+ regulatory T cells suppress antiporcine xenogeneic responses. Am J Transplant 2005; 5:2052-2057. (Pubitemid 41039885)
10. + regulatory T cell-mediated suppression of xenogeneic proliferation. Immunol Cell Biol 2010; 88:477-485.
11. Sun L, Yi S, O'Connell PJ. Foxp3 regulates human natural CD4+CD25+ regulatory T-cell-mediated suppression of xenogeneic response. Xenotransplantation 2010; 17:121-130.
12. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003; 4:330-336. (Pubitemid 36432314)
13. Cao T, Soto A, Zhou W, et al. Ex vivo expanded human CD4+CD25+Foxp3+ regulatory T cells prevent lethal xenogenic graft versus host disease (GVHD). Cell Immunol 2009; 258:65-71.
14. Qian X, Wang K, Wang X, et al. Generation of human regulatory T cells de novo with suppressive function prevent xenogeneic graft versus host disease. Int Immunopharmacol 2011; 11:630-637.
15. Golshayan D, Buhler L, Lechler RI, Pascual M. From current immunosuppressive strategies to clinical tolerance of allografts. Transpl Int 2007; 20:12-24
16. Rayat GR, Johnson ZA, Beilke JN, et al. The degree of phylogenetic disparity of islet grafts dictates the reliance on indirect CD4 T-cell antigen recognition for rejection. Diabetes 2003; 52:1433-1440. (Pubitemid 36666198)
17. Rogers NJ, Mirenda V, Jackson I, et al. Costimulatory blockade by the induction of an endogenous xenospecific antibody response. Nat Immunol 2000; 1:163-168.
18. Mirenda V, Golshayan D, Read J, et al. Achieving permanent survival of islet xenografts by independent manipulation of direct and indirect T-cell responses. Diabetes 2005; 54:1048-1055. (Pubitemid 40446318)
19. Friedman T, Shimizu A, Smith RN, et al. Human CD4+ T cells mediate rejection of porcine xenografts. J Immunol 1999; 162:5256-5262. (Pubitemid 29307131)
20. Dorling A, Lechler RI. T cell-mediated xenograft rejection: specific tolerance is probably required for long term xenograft survival. Xenotransplantation 1998; 5:234-245. (Pubitemid 29015964)
21. Choo JK, Seebach JD, Nickeleit V, et al. Species differences in the expression of major histocompatibility complex class II antigens on coronary artery endothelium: implications for cell-mediated xenoreactivity. Transplantation 1997; 64:1315-1322. (Pubitemid 27495966)
22. Yun S, Rose ML, Fabre JW. The induction of major histocompatibility complex class II expression is sufficient for the direct activation of human CD4+ T cells by porcine vascular endothelial cells. Transplantation 2000; 69:940-944. (Pubitemid 30174125)
23. Murray AG, Khodadoust MM, Pober JS, Bothwell AL. Porcine aortic endothelial cells activate human T cells: direct presentation of MHC antigens and costimulation by ligands for human CD2 and CD28. Immunity 1994; 1:57-63
24. Ding Q, Lu L, Zhou X, et al. Human PD-L1-overexpressing porcine vascular endothelial cells induce functionally suppressive human CD4+CD25hiFoxp3+ Treg cells. J Leukoc Biol 2011; 90:77-86.
25. Plege A, Borns K, Baars W, Schwinzer R. Suppression of human T-cell activation and expansion of regulatory T cells by pig cells overexpressing PDligands. Transplantation 2009; 87:975-982.
26. Hodgson R, Christiansen D, Ziolkowski A, et al. Prolonged xenograft survival induced by inducible costimulator-Ig is associated with increased forkhead box P3+ cells. Transplantation 2011; 91:1090-1097.
27. Singh NP, Guo L, Que X, Shirwan H. Blockade of indirect recognition mediated by CD4+ T cells leads to prolonged cardiac xenograft survival. Xenotransplantation 2004; 11:33-42. (Pubitemid 38160264)
28. Chitilian HV, Laufer TM, Stenger K, et al. The strength of cell-mediated xenograft rejection in the mouse is due to the CD4+ indirect response. Xenotransplantation 1998; 5:93-98. (Pubitemid 28137834)
29. Koulmanda M, Laufer TM, Auchincloss HJ, Smith RN. Prolonged survival of fetal pig islet xenografts in mice lacking the capacity for an indirect response. Xenotransplantation 2004; 11:525-530. (Pubitemid 39423075)
30. Gokmen MR, Lombardi G, Lechler RI. The importance of the indirect pathway of allorecognition in clinical transplantation. Curr Opin Immunol 2008; 20:568-574.
31. Nishimura T, Onda M, Takao S. CD4+ CD25+ regulatory T cells suppressed the indirect xenogeneic immune response mediated by porcine epithelial cell pulsed dendritic cells. Xenotransplantation 2010; 17:313-323.
32. Golshayan D, Jiang S, Tsang J, et al. In vitro-expanded donor alloantigenspecific CD4+CD25+ regulatory T cells promote experimental transplantation tolerance. Blood 2007; 109:827-835. (Pubitemid 46105988)
33. Peters JH, Preijers FW, Woestenenk R, et al. Clinical grade Treg: GMP isolation, improvement of purity by CD127 depletion, Treg expansion, and Treg cryopreservation. PLoS One 2008; 3:e3161.
34. Tang Q, Henriksen KJ, Bi M, et al. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J Exp Med 2004; 199:1455-1465. (Pubitemid 38780401)
35. 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.
36. Joffre O, Santolaria T, Calise D, et al. Prevention of acute and chronic allograft rejection with CD4+CD25+Foxp3+ regulatory T lymphocytes. Nat Med 2008; 14:88-92.
37. Lee I, Wang L, Wells AD, et al. Recruitment of Foxp3+ T regulatory cells mediating allograft tolerance depends on the CCR4 chemokine receptor. J Exp Med 2005; 201:1037-1044. (Pubitemid 40524671)
38. Jacobs JF, Idema AJ, Bol KF, et al. Prognostic significance and mechanism of Treg infiltration in human brain tumors. J Neuroimmunol 2010; 225:195-199.
39. Ishida T, Ueda R. Immunopathogenesis of lymphoma: focus on CCR4. Cancer Sci 2011; 102:44-50.
40. Montane J, Bischoff L, Soukhatcheva G, et al. Prevention of murine autoimmune diabetes by CCL22-mediated Treg recruitment to the pancreatic islets. J Clin Invest 2011; 121:3024-3028.
41. Hoerning A, Koss K, Datta D, et al. Subsets of human CD4+ T regulatory cells express the peripheral homing receptor CXCR3. Eur J Immunol 2011; 41:2291-2302.
42. Lacotte S, Brun S, Muller S, Dumortier H. CXCR3, inflammation, and autoimmune diseases. Ann N Y Acad Sci 2009; 1173:310-317.
43. Wells AD, Li XC, Li Y, et al. Requirement for T-cell apoptosis in the induction of peripheral transplantation tolerance. Nat Med 1999; 5:1303-1307. (Pubitemid 29535609)
44. Li Y, Li XC, Zheng XX, et al. Blocking both signal 1 and signal 2 of T-cell activation prevents apoptosis of alloreactive T cells and induction of peripheral allograft tolerance. Nat Med 1999; 5:1298-1302. (Pubitemid 29535608)
45. Muller YD, Mai G, Morel P, et al. Anti-CD154 mAb and rapamycin induce T regulatory cell mediated tolerance in rat-to-mouse islet transplantation. PLoS One 2010; 5:e10352.
46. Arefanian H, Tredget EB, Rajotte RV, et al. Short-term administrations of a combination of anti-LFA-1 and anti-CD154 monoclonal antibodies induces tolerance to neonatal porcine islet xenografts in mice. Diabetes 2010; 59:958-966.
47. Wang F, Xia J, Chen J, et al. Combination of antibodies inhibits accelerated rejection mediated by memory T cells in xenoantigen-primed mice. Xenotransplantation 2010; 17:460-468.
48. Muller YD, Golshayan D, Ehirchiou D, et al. Immunosuppressive effects of streptozotocin-induced diabetes result in absolute lymphopenia and a relative increase of T regulatory cells. Diabetes 2011; 60:2331-2340.
49. Lim DG, Koo SK, Park YH, et al. Impact of immunosuppressants on the therapeutic efficacy of in vitro-expanded CD4+CD25+Foxp3+ regulatory T cells in allotransplantation. Transplantation 2010; 89:928-936.
50. Battaglia M, Stabilini A, Draghici E, et al. Induction of tolerance in type 1 diabetes via both CD4+CD25+ T regulatory cells and T regulatory type 1 cells. Diabetes 2006; 55:1571-1580. (Pubitemid 44324109)
51. Monti P, Scirpoli M, Maffi P, et al. Rapamycin monotherapy in patients with type 1 diabetes modifies CD4+CD25+FOXP3+ regulatory T cells. Diabetes 2008; 57:2341-2347.
52. Zeiser R, Negrin RS. Interleukin-2 receptor downstream events in regulatory T cells: implications for the choice of immunosuppressive drug therapy. Cell Cycle 2008; 7:458-462. (Pubitemid 351366473)
53. Reisman NM, Floyd TL, Wagener ME, et al. LFA-1 blockade induces effector and regulatory T-cell enrichment in lymph nodes and synergizes with CTLA-4Ig to inhibit effector function. Blood 2011 [Epub ahead of print].
54. Dijke IE, Velthuis JH, Caliskan K, et al. Intragraft FOXP3 mRNA expression reflects antidonor immune reactivity in cardiac allograft patients. Transplantation 2007; 83:1477-1484. (Pubitemid 46934071)
55. Fan Z, Spencer JA, Lu Y, et al. In vivo tracking of 'color-coded' effector, natural and induced regulatory T cells in the allograft response. Nat Med 2010; 16:718-722.
56. Wang S, Jiang J, Guan Q, et al. Reduction of Foxp3-expressing regulatory T cell infiltrates during the progression of renal allograft rejection in a mouse model. Transpl Immunol 2008; 19:93-102.
57. Haanstra KG, Wubben JA, Korevaar SS, et al. Expression patterns of regulatory T-cell markers in accepted and rejected nonhuman primate kidney allografts. Am J Transplant 2007; 7:2236-2246. (Pubitemid 47347844)
58. Pons JA, Revilla-Nuin B, Baroja-Mazo A, et al. FoxP3 in peripheral blood is associated with operational tolerance in liver transplant patients during immunosuppression withdrawal. Transplantation 2008; 86:1370-1378.
59. Berney T, Ferrari-Lacraz S, Buhler L, et al. Long-term insulin-independence after allogeneic islet transplantation for type 1 diabetes: over the 10-year mark. Am J Transplant 2009; 9:419-423.
60. Stenard F, Nguyen C, Cox K, et al. Decreases in circulating CD4+CD25hiFOXP3+ cells and increases in intragraft FOXP3+ cells accompany allograft rejection in pediatric liver allograft recipients. Pediatr Transplant 2009; 13:70-80.
61. Shan J, Guo Y, Luo L, et al. Do CD4(+)Foxp3(+) Treg cells correlate with transplant outcomes: a systematic review on recipients of solid organ transplantation. Cell Immunol 2011; 270:5-12.
62. Muthukumar T, Dadhania D, Ding R, et al. Messenger RNA for FOXP3 in the urine of renal-allograft recipients. N Engl J Med 2005; 353:2342-2351. (Pubitemid 41713746)
63. Badell IR, Thompson PW, Turner AP, et al. Nondepleting anti-CD40-based therapy prolongs allograft survival in nonhuman primates. Am J Transplant 2011 [Epub ahead of print].
64. Thompson P, Cardona K, Russell M, et al. CD40-specific costimulation blockade enhances neonatal porcine islet survival in nonhuman primates. Am J Transplant 2011; 11:947-957.
65. Zhu H, Qiu W, Lei P, et al. IL-10 gene modified dendritic cells inhibit T helper type 1-mediated alloimmune responses and promote immunological tolerance in diabetes. Cell Mol Immunol 2008; 5:41-46.
66. Parker DG, Coster DJ, Brereton HM, et al. Lentivirus-mediated gene transfer of interleukin 10 to the ovine and human cornea. Clin Exp Ophthalmol 2010; 38:405-413.