Mesenchymal stem cells differentially mediate regulatory T cells and conventional effector T cells to protect fully allogeneic islet grafts in mice

Diabetologia

Volumn 55, Issue 4, 2012, Pages 1091-1102

  Xu, D M ^a   Yu, X F ^a   Zhang, D ^a   Zhang, M X ^a   Zhou, J F ^a   Tan, P H ^b   Ding, Y C ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Immunosuppression; Islet transplantation; Mesenchymal stem cells

Indexed keywords

5' NUCLEOTIDASE; CD28 ANTIGEN; CD4 ANTIGEN; ENDOGLIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ADOPTIVE TRANSFER; ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; BONE MARROW CELL; CD4+ CD25+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CELL PROLIFERATION; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; FLOW CYTOMETRY; GRAFT REJECTION; GRAFT SURVIVAL; IMMUNOFLUORESCENCE; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPLEEN CELL; STREPTOZOCIN DIABETES;

ANIMALS; CELL PROLIFERATION; DIABETES MELLITUS, EXPERIMENTAL; GRAFT SURVIVAL; ISLETS OF LANGERHANS TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICE; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 84862538838     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-011-2433-9     Document Type: Article

References (34)

1. Prockop DJ (1997) Marrow stromal cells as stem cells for non-hematopoietic tissues. Science (New York) 276:71-74
2. Pittenger MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science (New York) 284:143-147
3. Ding Y, Bushell A, Wood KJ (2010) Mesenchymal stem-cell immunosuppressive capabilities: therapeutic implications in islet transplantation. Transplantation 89:270-273
4. Nauta AJ, Fibbe WE (2007) Immunomodulatory properties of mesenchymal stromal cells. Blood 110:3499-3506
5. Oh JY, Kim MK, Shin MS et al (2008) The anti-inflammatory and anti-angiogenic role of mesenchymal stem cells in corneal wound healing following chemical injury. Stem Cells 26:1047-1055
6. Rasmusson I, Ringden O, Sundberg B, Le Blanc K (2005) Mes-enchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanisms. Exp Cell Res 305:33-41
7. Glennie S, Soeiro I, Dyson PJ, Lam EW, Dazzi F (2005) Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 105:2821-2827
8. Ding Y, Xu D, Feng G, Bushell A, Muschel RJ, Wood KJ (2009) Mesenchymal stem cells prevent the rejection of fully allogenic islet grafts by the immunosuppressive activity of matrix metalloproteinase-2 and-9. Diabetes 58:1797-1806
9. Bartholomew A, Sturgeon C, Siatskas M et al (2002) Mesenchy-mal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 30:42-48
10. Chabannes D, Hill M, Merieau E et al (2007) A role for heme oxygenase-1 in the immunosuppressive effect of adult rat and human mesenchymal stem cells. Blood 110:3691-3694
11. Ge W, Jiang J, Baroja ML et al (2009) Infusion of mesenchymal stem cells and rapamycin synergize to attenuate alloimmune responses and promote cardiac allograft tolerance. Am J Transplant 9:1760-1772
12. Sakaguchi S (2005) Naturally arising Foxp3-expressing CD25 +CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 6:345-352
13. Sakaguchi S (2004) Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 22:531-562
14. Prevosto C, Zancolli M, Canevali P, Zocchi MR, Poggi A (2007) Generation of CD4+ or CD8+ regulatory T cells upon mesenchy-mal stem cell-lymphocyte interaction. Haematologica 92:881-888
15. Carrion F, Nova E, Ruiz C, et al. (2010) Autologous mesenchymal stem cell treatment increased T regulatory cells with no effect on disease activity in two systemic lupus erythematosus patients. Lupus 19:317-322
16. Crop MJ, Baan CC, Korevaar SS, Ijzermans JN, Weimar W, Hoogduijn MJ (2010) Human adipose tissue-derived mesenchy-mal stem cells induce explosive T cell proliferation. Stem Cells and Development 19:1843-1853
17. Shapiro AM, Lakey JR, Ryan EA et al (2000) Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N Engl J Med 343:230-238
18. Shapiro AM, Ricordi C, Hering BJ et al (2006) International trial of the Edmonton protocol for islet transplantation. N Engl J Med 355:1318-1330
19. Ryan EA, Lakey JR, Rajotte RVet al (2001) Clinical outcomes and insulin secretion after islet transplantation with the Edmonton protocol. Diabetes 50:710-719
20. Levitsky J, Gallon L, Miller J et al (2011) Allospecific regulatory effects of sirolimus and tacrolimus in the human mixed lymphocyte reaction. Transplantation 91:199-206
21. Berman DM, Willman MA, Han D et al (2010) Mesenchymal stem cells enhance allogeneic islet engraftment in nonhuman primates. Diabetes 59:2558-2568
22. Essery G, Feldmann M, Lamb JR (1988) Interleukin-2 can prevent and reverse antigen-induced unresponsiveness in cloned human T lymphocytes. Immunology 64:413-417
23. Le Blanc K, Rasmusson I, Gotherstrom C et al (2004) Mesenchy-mal stem cells inhibit the expression of CD25 (interleukin-2 receptor) and CD38 on phytohaemagglutinin-activated lymphocytes. Scand J Immunol 60:307-315
24. Groh ME, Maitra B, Szekely E, Koc ON (2005) Human mesen-chymal stem cells require monocyte-mediated activation to suppress alloreactive T cells. Exp Hematol 33:928-934
25. Setoguchi R, Hori S, Takahashi T, Sakaguchi S (2005) Homeo-static maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 201:723-735
26. Sakaguchi S, Yamaguchi T, Nomura T, Ono M (2008) Regulatory T cells and immune tolerance. Cell 133:775-787
27. Maloy KJ, Powrie F (2005) Fueling regulation: IL-2 keeps CD4+ Treg cells fit. Nat Immunol 6:1071-1072
28. Di Nicola M, Carlo-Stella C, Magni M et al (2002) Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99:3838-3843
29. Ghannam S, Pene J, Torcy-Moquet G, Jorgensen C, Yssel H (2010) Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. J Immunol 185:302-312
30. Casiraghi F, Azzollini N, Cassis P et al (2008) Pretransplant infusion of mesenchymal stem cells prolongs the survival of a semiallogeneic heart transplant through the generation of regulatory T cells. J Immunol 181:3933-3946
31. Di Ianni M, del Papa B, de Ioanni M et al (2008) Mesenchymal cells recruit and regulate Tregulatory cells. Exp Hematol 36:309-318
32. Rochman Y, Spolski R, Leonard WJ (2009) New insights into the regulation of T cells by gamma(c) family cytokines. Nat Rev 9:480-490
33. Fontenot JD, Rasmussen JP, Gavin MA, Rudensky AY (2005) A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat Immunol 6:1142-1151
34. English K, French A, Wood KJ (2010) Mesenchymal stromal cells: facilitators of successful transplantation? Cell Stem Cell 7:431-442