Adoptive transfer with in vitro expanded human regulatory T cells protects against porcine islet xenograft rejection via interleukin-10 in humanized mice

Diabetes

Volumn 61, Issue 5, 2012, Pages 1180-1191

  Yi, Shounan ^a,b   Ji, Ming ^a,c   Wu, Jingjing ^a   Ma, Xiaoqian ^a,d   Phillips, Peta ^a   Hawthorne, Wayne J ^a   O'Connell, Philip J ^a  

^a WESTMEAD HOSPITAL   (Australia)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c The First People s Hospital of Changde City)   (China)

^d THE THIRD XIANGYA HOSPITAL OF CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; RECOMBINANT INTERLEUKIN 10;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOGRAFT; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CELL INFILTRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; EFFECTOR CELL; GRAFT RECIPIENT; GRAFT REJECTION; GRAFT SURVIVAL; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE FUNCTION; MOUSE; NEWBORN; NONHUMAN; NORMAL HUMAN; PANCREAS ISLET; PANCREAS ISLET TRANSPLANTATION; PANCREAS ISLET XENOGRAFT REJECTION; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SWINE; XENOGRAFT; XENOTRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIBODIES; CELLS, CULTURED; GENE EXPRESSION REGULATION; GRAFT REJECTION; HUMANS; INTERLEUKIN RECEPTOR COMMON GAMMA SUBUNIT; INTERLEUKIN-10; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; ISLETS OF LANGERHANS TRANSPLANTATION; LEUKOCYTES, MONONUCLEAR; MICE; MICE, KNOCKOUT; SWINE; T-LYMPHOCYTES, REGULATORY;

EID: 84860580137     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-1306     Document Type: Article

References (49)

1. Ryan EA, Paty BW, Senior PA, et al. Five-year follow-up after clinical islet transplantation. Diabetes 2005;54:2060-2069 (Pubitemid 40911269)
2. Berney T, Ferrari-Lacraz S, Bühler 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
3. Fiorina P, Shapiro AM, Ricordi C, Secchi A. The clinical impact of islet transplantation. Am J Transplant 2008;8:1990-1997
4. Hering BJ, Kandaswamy R, Ansite JD, et al. Single-donor, marginal-dose islet transplantation in patients with type 1 diabetes. JAMA 2005;293:830-835 (Pubitemid 40250366)
5. Rayat GR, Rajotte RV, Korbutt GS. Potential application of neonatal porcine islets as treatment for type 1 diabetes: a review. Ann N Y Acad Sci 1999;875:175-188 (Pubitemid 29349070)
6. MacKenzie DA, Hullett DA, Sollinger HW. Xenogeneic transplantation of porcine islets: an overview. Transplantation 2003;76:887-891 (Pubitemid 37186014)
7. Cardona K, Korbutt GS, Milas Z, et al. Long-term survival of neonatal porcine islets in nonhuman primates by targeting costimulation pathways. Nat Med 2006;12:304-306 (Pubitemid 43355077)
8. Hering BJ, Wijkstrom M, Graham ML, et al. Prolonged diabetes reversal after intraportal xenotransplantation of wild-type porcine islets in immunosuppressed nonhuman primates. Nat Med 2006;12:301-303 (Pubitemid 43355076)
9. Friedman T, Smith RN, Colvin RB, Iacomini J. A critical role for human CD4+ T-cells in rejection of porcine islet cell xenografts. Diabetes 1999;48:2340-2348 (Pubitemid 30395425)
10. 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)
11. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003;299:1057-1061 (Pubitemid 36222930)
12. Adeegbe D, Bayer AL, Levy RB, Malek TR. Cutting edge: allogeneic CD4+CD25+Foxp3+ T regulatory cells suppress autoimmunity while establishing transplantation tolerance. J Immunol 2006;176:7149-7153 (Pubitemid 43849014)
13. 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
14. Issa F, Hester J, Goto R, Nadig SN, Goodacre TE, Wood K. Ex vivo-expanded human regulatory T cells prevent the rejection of skin allografts in a humanized mouse model. Transplantation 2010;90:1321-1327
15. Porter CM, Bloom ET. Human CD4+CD25+ regulatory T cells suppress anti-porcine xenogeneic responses. Am J Transplant 2005;5:2052-2057 (Pubitemid 41039885)
16. Lin YJ, Hara H, Tai HC, et al. Suppressive efficacy and proliferative capacity of human regulatory T cells in allogeneic and xenogeneic responses. Transplantation 2008;86:1452-1462
17. Sakaguchi S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005;6:345-352 (Pubitemid 41716771)
18. Hoffmann P, Eder R, Kunz-Schughart LA, Andreesen R, Edinger M. Largescale in vitro expansion of polyclonal human CD4(+)CD25high regulatory T cells. Blood 2004;104:895-903 (Pubitemid 38970590)
19. Wu J, Yi S, Ouyang L, et al. In vitro expanded human CD4+CD25+ regulatory T cells are potent suppressors of T-cell-mediated xenogeneic responses. Transplantation 2008;85:1841-1848
20. 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
21. Sun L, Yi S, O'Connell PJ. IL-10 is required for human CD4(+)CD25(+) regulatory T cell-mediated suppression of xenogeneic proliferation. Immunol Cell Biol 2010;88:477-485
22. Korbutt GS, Elliott JF, Ao Z, Smith DK, Warnock GL, Rajotte RV. Large scale isolation, growth, and function of porcine neonatal islet cells. J Clin Invest 1996;97:2119-2129 (Pubitemid 26143967)
23. O'Connell PJ, Hawthorne WJ, Simond D, et al. Genetic and functional evaluation of the level of inbreeding of the Westran pig: a herd with potential for use in xenotransplantation. Xenotransplantation 2005;12:308-315 (Pubitemid 40868333)
24. Yi S, Hawthorne WJ, Lehnert AM, et al. T cell-activated macrophages are capable of both recognition and rejection of pancreatic islet xenografts. J Immunol 2003;170:2750-2758 (Pubitemid 36245670)
25. Fu Y, Lu X, Yi S, et al. Selective rejection of porcine islet xenografts by macrophages. Xenotransplantation 2008;15:307-312
26. Shultz LD, Pearson T, King M, et al. Humanized NOD/LtSz-scid IL2 receptor common gamma chain knockout mice in diabetes research. Ann N Y Acad Sci 2007;1103:77-89 (Pubitemid 46791104)
27. Nagahama K, Nishimura E, Sakaguchi S. Induction of tolerance by adoptive transfer of Treg cells. Methods Mol Biol 2007;380:431-442 (Pubitemid 350183345)
28. Pierson RN 3rd, Winn HJ, Russell PS, Auchincloss H Jr. Xenogeneic skin graft rejection is especially dependent on CD4+ T cells. J Exp Med 1989;170:991-996 (Pubitemid 19226679)
29. Loudovaris T, Mandel TE, Charlton B. CD4+ T cell mediated destruction of xenografts within cell-impermeable membranes in the absence of CD8+ T cells and B cells. Transplantation 1996;61:1678-1684 (Pubitemid 26242004)
30. Wood KJ, Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Rev Immunol 2003;3:199-210 (Pubitemid 37323205)
31. Warnecke G, Bushell A, Nadig SN, Wood KJ. Regulation of transplant arteriosclerosis by CD25+CD4+ T cells generated to alloantigen in vivo. Transplantation 2007;83:1459-1465 (Pubitemid 46934069)
32. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995;155:1151-1164
33. + regulatory T cells in the human immune system. Nat Rev Immunol 2010;10:490-500
34. Asseman C, Mauze S, Leach MW, Coffman RL, Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 1999;190:995-1004
35. + regulatory T cells confer infectious tolerance in a TGF-β-dependent manner. J Exp Med 2008;205:1975-1981
36. Read S, Malmström V, Powrie F. Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J Exp Med 2000;192:295-302 (Pubitemid 30470312)
37. Suri-Payer E, Cantor H. Differential cytokine requirements for regulation of autoimmune gastritis and colitis by CD4(+)CD25(+) T cells. J Autoimmun 2001;16:115-123 (Pubitemid 32552986)
38. Bacchetta R, Bigler M, Touraine JL, et al. High levels of interleukin 10 production in vivo are associated with tolerance in SCID patients transplanted with HLA mismatched hematopoietic stem cells. J Exp Med 1994;179:493-502 (Pubitemid 24058737)
39. Curiel TJ, Coukos G, Zou L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10:942-949 (Pubitemid 39273735)
40. Seo N, Hayakawa S, Takigawa M, Tokura Y. Interleukin-10 expressed at early tumour sites induces subsequent generation of CD4(+) T-regulatory cells and systemic collapse of antitumour immunity. Immunology 2001; 103:449-457 (Pubitemid 32744391)
41. Viguier M, Lemaître F, Verola O, et al. Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J Immunol 2004;173:1444-1453 (Pubitemid 38924326)
42. Woo EY, Chu CS, Goletz TJ, et al. Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res 2001;61:4766-4772 (Pubitemid 32691889)
43. Gagliani N, Jofra T, Stabilini A, et al. Antigen-specific dependence of Tr1-cell therapy in preclinical models of islet transplant. Diabetes 2010;59:433-439
44. Roncarolo MG, Gregori S, Battaglia M, Bacchetta R, Fleischhauer K, Levings MK. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006;212:28-50 (Pubitemid 44116698)
45. 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)
46. Vieira PL, Christensen JR, Minaee S, et al. IL-10-secreting regulatory T cells do not express Foxp3 but have comparable regulatory function to naturally occurring CD4+CD25+ regulatory T cells. J Immunol 2004;172:5986-5993 (Pubitemid 38621199)
47. Brun V, Bastian H, Neveu V, Foussat A. Clinical grade production of IL-10 producing regulatory Tr1 lymphocytes for cell therapy of chronic inflammatory diseases. Int Immunopharmacol 2009;9:609-613
48. Ahangarani RR, Janssens W, VanderElst L, et al. In vivo induction of type 1-like regulatory T cells using genetically modified B cells confers longterm IL-10-dependent antigen-specific unresponsiveness. J Immunol 2009;183:8232-8243
49. Schmidt P, Krook H, Maeda A, Korsgren O, Benda B. A new murine model of islet xenograft rejection: graft destruction is dependent on a major histocompatibility-specific interaction between T-cells and macrophages. Diabetes 2003;52:1111-1118 (Pubitemid 36523344)