Human mesenchymal stem cells suppress donor CD4+ T cell proliferation and reduce pathology in a humanized mouse model of acute graft-versus-host disease

Clinical and Experimental Immunology

Volumn 172, Issue 2, 2013, Pages 333-348

  Tobin, L M ^a   Healy, M E ^a   English, K ^a   Mahon, B P ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Acute graft versus host disease; Humanized mouse model; Mesenchymal stem cell; Xenogeneic

Indexed keywords

INTERLEUKIN 2 RECEPTOR GAMMA; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA;

ACUTE GRAFT VERSUS HOST DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CLONAL ANERGY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SCID MOUSE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; INTERFERON-GAMMA; LEUKOCYTES, MONONUCLEAR; LIVER; LYMPHOCYTE ACTIVATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; RECEPTORS, INTERLEUKIN-2; STOMACH; TISSUE THERAPY; TRANSPLANTATION, HETEROLOGOUS; TRANSPLANTATION, HOMOLOGOUS;

EID: 84876086426     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12056     Document Type: Article

References (62)

1. Reddy P, Ferrara JL. Immunobiology of acute graft-versus-host disease. Blood Rev 2003; 17:187-194.
2. Ferrara JL, Levine JE, Reddy P, Holler E. Graft-versus-host disease. Lancet 2009; 373:1550-1561.
3. Billingham RE. The biology of graft-versus-host reactions. Harvey Lect 1966; 62:21-78.
4. Messina C, Faraci M, de Fazio V, Dini G, Calo MP, Calore E. Prevention and treatment of acute GvHD. Bone Marrow Transplant 2008; 41 (Suppl. 2):S65-70.
5. Van Lint MT, Uderzo C, Locasciulli A etal. Early treatment of acute graft-versus-host disease with high- or low-dose 6-methylprednisolone: a multicenter randomized trial from the Italian Group for Bone Marrow Transplantation. Blood 1998; 92:2288-2293.
6. Van Lint MT, Milone G, Leotta S etal. Treatment of acute graft-versus-host disease with prednisolone: significant survival advantage for day +5 responders and no advantage for nonresponders receiving anti-thymocyte globulin. Blood 2006; 107:4177-4181.
7. MacMillan ML, Weisdorf DJ, Wagner JE etal. Response of 443 patients to steroids as primary therapy for acute graft-versus-host disease: comparison of grading systems. Biol Blood Marrow Transplant 2002; 8:387-394.
8. Deeg HJ. How I treat refractory acute GVHD. Blood 2007; 109:4119-4126.
9. da Silva Meirelles L, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 2006; 119 (Pt 11):2204-2213.
10. Crisan M, Yap S, Casteilla L etal. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008; 3:301-313.
11. Friedenstein AJ, Piatetzky S, II, Petrakova KV. Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 1966; 16:381-390.
12. Friedenstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF, Keiliss-Borok IV. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 1974; 17:331-340.
13. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991; 9:641-650.
14. Prockop DJ. Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther 2009; 17:939-946.
15. English K, Barry FP, Mahon BP. Murine mesenchymal stem cells suppress dendritic cell migration, maturation and antigen presentation. Immunol Lett 2008; 115:50-58.
16. + regulatory T cells. Clin Exp Immunol 2009; 156:149-160.
17. Di Nicola M, Carlo-Stella C, Magni M etal. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002; 99:3838-3843.
18. Corcione A, Benvenuto F, Ferretti E etal. Human mesenchymal stem cells modulate B-cell functions. Blood 2006; 107:367-372.
19. Spaggiari GM, Capobianco A, Becchetti S, Mingari MC, Moretta L. Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 2006; 107:1484-1490.
20. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005; 105:1815-1822.
21. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008; 8:726-736.
22. Ciccocioppo R, Bernardo ME, Sgarella A etal. Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 2011; 60:788-798.
23. Connick P, Kolappan M, Crawley C etal. Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: an open-label Phase IIa proof-of-concept study. Lancet Neurol 2012; 11:150-156.
24. Kebriaei P, Isola L, Bahceci E etal. Adult human mesenchymal stem cells added to corticosteroid therapy for the treatment of acute graft-versus-host disease. Biol Blood Marrow Transplant 2009; 15:804-811.
25. Le Blanc K, Frassoni F, Ball L etal. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a Phase II study. Lancet 2008; 371:1579-1586.
26. Le Blanc K, Rasmusson I, Sundberg B etal. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004; 363:1439-1441.
27. Martin PJ, Uberti JP, Soiffer RJ etal. Prochymal (R) improves response rates in patients with steroid-refractory acute graft-versus-host disease involving the liver and gut: results of a randomized, placebo-controlled, multicentre phase III trial in GvHD. Bone Marrow Transplant 2010; 45:S17-S17.
28. Allison M. Genzyme backs Osiris, despite Prochymal flop. Nat Biotechnol 2009; 27:966-967.
29. Pearson T, Greiner DL, Shultz LD. Creation of 'humanized' mice to study human immunity. Curr Protoc Immunol 2008; Chapter 15:Unit 15 21.
30. Hill GR, Crawford JM, Cooke KR, Brinson YS, Pan L, Ferrara JL. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood 1997; 90:3204-3213.
31. Grass JA, Wafa T, Reames A etal. Prevention of transfusion-associated graft-versus-host disease by photochemical treatment. Blood 1999; 93:3140-3147.
32. Polchert D, Sobinsky J, Douglas G etal. IFN-gamma activation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Eur J Immunol 2008; 38:1745-1755.
33. Barry FP, Murphy JM. Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 2004; 36:568-584.
34. Horwitz EM, Le Blanc K, Dominici M etal. Clarification of the nomenclature for MSC: the International Society for cellular therapy position statement. Cytotherapy 2005; 7:393-395.
35. Tsujimoto H, Efron PA, Matsumoto T etal. Maturation of murine bone marrow-derived dendritic cells with poly(I:C) produces altered TLR-9 expression and response to CpG DNA. Immunol Lett 2006; 107:155-162.
36. Ryan JM, Barry F, Murphy JM, Mahon BP. Interferon-gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin Exp Immunol 2007; 149:353-363.
37. Kavanagh H, Mahon B. Allogeneic mesenchymal stem cells prevent allergic airway inflammation by inducing murine regulatory T cells. Allergy 2011; 66:523-531.
38. Ryan JM, Barry FP, Murphy JM, Mahon BP. Mesenchymal stem cells avoid allogeneic rejection. J Inflamm (Lond) 2005; 2:8-18.
39. Reddy P. Pathophysiology of acute graft-versus-host disease. Hematol Oncol 2003; 21:149-161.
40. Sudres M, Norol F, Trenado A etal. Bone marrow mesenchymal stem cells suppress lymphocyte proliferation in vitro but fail to prevent graft-versus-host disease in mice. J Immunol 2006; 176:7761-7767.
41. Jeon MS, Lim HJ, Yi TG etal. Xenoreactivity of human clonal mesenchymal stem cells in a major histocompatibility complex-matched allogeneic graft-versus-host disease mouse model. Cell Immunol 2010; 261:57-63.
42. Christensen ME, Turner BE, Sinfield LJ etal. Mesenchymal stromal cells transiently alter the inflammatory milieu post-transplant to delay graft-versus-host disease. Haematologica 2010; 95:2102-2110.
43. Joo SY, Cho KA, Jung YJ etal. Mesenchymal stromal cells inhibit graft-versus-host disease of mice in a dose-dependent manner. Cytotherapy 2010; 12:361-370.
44. Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2, 3-dioxygenase-mediated tryptophan degradation. Blood 2004; 103:4619-4621.
45. English K, Barry FP, Field-Corbett CP, Mahon BP. IFN-gamma and TNF-alpha differentially regulate immunomodulation by murine mesenchymal stem cells. Immunol Lett 2007; 110:91-100.
46. Plumas J, Chaperot L, Richard MJ, Molens JP, Bensa JC, Favrot MC. Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia 2005; 19:1597-1604.
47. Zappia E, Casazza S, Pedemonte E etal. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005; 106:1755-1761.
48. Krampera M, Cosmi L, Angeli R etal. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 2006; 24:386-398.
49. Glennie S, Soeiro I, Dyson PJ, Lam EW, Dazzi F. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 2005; 105:2821-2827.
50. Krampera M, Glennie S, Dyson J etal. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 2003; 101:3722-3729.
51. Roncarolo MG, Battaglia M. Regulatory T-cell immunotherapy for tolerance to self antigens and alloantigens in humans. Nat Rev Immunol 2007; 7:585-598.
52. 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.
53. Edinger M, Hoffmann P, Ermann J etal. CD4+CD25+ regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med 2003; 9:1144-1150.
54. Cao T, Soto A, Zhou W etal. Ex vivo expanded human CD4+CD25+Foxp3+ regulatory T cells prevent lethal xenogenic graft versus host disease (GVHD). Cell Immunol 2009; 258:65-71.
55. Selmani Z, Naji A, Zidi I etal. Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+CD25highFOXP3+ regulatory T cells. Stem Cells 2008; 26:212-222.
56. Prevosto C, Zancolli M, Canevali P, Zocchi MR, Poggi A. Generation of CD4+ or CD8+ regulatory T cells upon mesenchymal stem cell-lymphocyte interaction. Haematologica 2007; 92:881-888.
57. 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.
58. 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.
59. 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.
60. Trenado A, Charlotte F, Fisson S etal. Recipient-type specific CD4+CD25+ regulatory T cells favor immune reconstitution and control graft-versus-host disease while maintaining graft-versus-leukemia. J Clin Invest 2003; 112:1688-1696.
61. Li Q, Zhai Z, Xu X etal. Decrease of CD4(+)CD25(+) regulatory T cells and TGF-beta at early immune reconstitution is associated to the onset and severity of graft-versus-host disease following allogeneic haematogenesis stem cell transplantation. Leuk Res 2010; 34:1158-1168.
62. Hao L, Gao L, Chen XH etal. Human umbilical cord blood-derived stromal cells prevent graft-versus-host disease in mice following haplo-identical stem cell transplantation. Cytotherapy 2011; 13:83-91.