Treatment of experimental arthritis by inducing immune tolerance with human adipose-derived mesenchymal stem cells

Arthritis and Rheumatism

Volumn 60, Issue 4, 2009, Pages 1006-1019

  González, Manuel A ^a,d   González Rey, Elena ^b   Rico, Laura ^a   Büscher, Dirk ^a   Delgado, Mario ^c  

^a Cellerix SA   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

^d CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; COLLAGEN; INTERLEUKIN 10;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EFFECTOR CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; TH1 CELL; TH17 CELL; TREATMENT RESPONSE;

ADIPOSE TISSUE; ANIMALS; ANTIGENS, CD4; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPHOCYTE COUNT; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TRANSPLANTATION, HETEROLOGOUS;

EID: 65249161683     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.24405     Document Type: Article

References (44)

1. Firestein GS. Evolving concepts of rheumatoid arthritis. Nature 2003;423:356-61.
2. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 2008;133:775-87.
3. Morgan ME, Flierman R, van Duivenvoorde LM, Witteven HJ, van Ewijk W, van Laar JM, et al. Effective treatment of collageninduced arthritis by adoptive transfer of CD25 + regulatory T cells. Arthritis Rheum 2005;52:2212-21.
4. Amelsfort JM, Jacobs KM, Bijlsma JW, Lafeber FP, Taams LS. CD4+CD25+ regulatory T cells in rheumatoid arthritis: differences in the presence, phenotype, and function between peripheral blood and synovial fluid. Arthritis Rheum 2004;50:2775-85.
5. Yudoh K, Matsuno H, Nakazawa F, Yonezawa T, Kimura T. Reduced expression of the regulatory CD4+ T cell subset is related to Th1/Th2 balance and disease severity in rheumatoid arthritis. Arthritis Rheum 2000;43:617-27.
6. Morgan ME, Sutmuller RP, Witteveen HJ, van Duivenvoorde LM, Zanelli E, Melief CJ, et al. CD25+ depletion hastens the onset of severe disease in collagen-induced arthritis. Arthritis Rheum 2003;48:1452-60.
7. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-7.
8. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AT, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001;7:211-28.
9. Rasmusson I. Immune modulation by mesenchymal stem cells. Exp Cell Res 2006;312:2169-79.
10. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007;110:3499-506.
11. Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, Mclntosh K, Patil S, et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 2002;30:42-8.
12. Glennie S, Soeiro I, Dyson PJ, Lam W, Dazzi F. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 2005;105:2821-7.
13. Beyth S, Borovsky Z, Mevorach D, Liebergall M, Gazit Z, Asian H, et al. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 2005; 105:2214-9.
14. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, et al, for the Developmental Committee of the European Group for Blood and Marrow Transplantation. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008;371:1579-86.
15. Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005;106:1755-61.
16. Ohnishi S, Yanagawa B, Tanaka K, Miyahara Y, Obata H, Kataoka M, et al. Transplantation of mesenchymal stem cells attenuates myocardial injury and dysfunction in a rat model of acute myocarditis. J Mol Cell Cardiol 2007;42:88-97.
17. Augello A, Tasso R, Negrini SM, Cancedda R, Pennesi G. Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis Rheum 2007;56:1175-86.
18. Yanez R, Lamana ML, Garcia-Castro J, Comenero I, Ramirez M, Bueren JA. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 2006;24:2582-91.
19. Liechty KW, MacKenzie TC, Shaaban AF, Radu A, Moseley AM, Deans R, et al. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 2000;6:1282-6.
20. Grinnemo KH, Mansson A, Dellgren G, Klingberg D, Wardell E, Drvota V, et al. Xenoreactivity and engraftment of human mesenchymal stem cells transplanted into infarcted rat myocardium. J Thorac Cardiovasc Surg 2004;127:1293-300.
21. Zheng ZH, Li XY, Ding J, Jia JF, Zhu P. Allogeneic mesenchymal stem cell and mesenchymal stem cell-differentiated chondrocyte suppress the responses of type II collagen-reactive T cells in rheumatoid arthritis. Rheumatology (Oxford) 2008;47:22-30.
22. Puissant B, Barreau C, Bourin P, Clavel C, Corre J, Bousquet C, et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 2005;129:118-29.
23. Cui L, Yin S, Liu W, Li N, Zhang W, Cao Y. Expanded adipose-derived stem cells suppress mixed lymphocyte reaction by secretion of prostaglandin E2. Tissue Eng 2007;13:1185-95.
24. González-Rey E, Gonzalez MA, Varela N, O'Valle F, Hernandez- Cortes P, Rico L, et al. Human adipose mesenchymal cells reduce inflammatory and T cell responses and induce regulatory T cells in vitro in rheumatoid arthritis. Ann Rheum Dis 2009. E-pub ahead of print.
25. Delgado M, Abad C, Martinez C, Leceta J, Gomariz RP. Vasoactive intestinal peptide prevents experimental arthritis by downregulating both autoimmune and inflammatory components of the disease. Nat Med 2001;7:563-8.
26. Kasama T, Strieter RM, Lukacs NW, Lincoln PM, Burdick MD, Kunkel SL. Interleukin-10 and chemokine regulation during the evolution of murine type-II collagen-induced arthritis. J Clin Invest 1995;95:2868-76.
27. Haniffa MA, Wang XN, Holtick U, Rae M, Isaacs JD, Dickinson AM, et al. Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells. J Immunol 2007;179:1595-604.
28. Seki N, Sudo Y, Yoshioka T, Sugihara S, Fujitsu T, Sakuma S, et al. Type II collagen-induced murine arthritis induction and perpetuation of arthritis require synergy between humoral and cellmediated immunity. J Immunol 1988;140:1477-87.
29. Wraith DC, Nicolson KS, Whitlet, NT. Regulatory CD4+ T cells and the control of autoimmune disease. Curr Opin Immunol 2004;16:695-701.
30. Walmsley M, Katsikis PD, Abney E, Parry S, Williams RO, Maini RN, et al. Interleukin-10 inhibition of the progression of established collagen-induced arthritis. Arthritis Rheum 1996;39: 495-503.
31. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997;389:737-42.
32. + regulatory T cell subsets. J Leukocyte Biol 2003;74:471-8.
33. + regulatory T-cell lines from human cord blood have functional and molecular properties of T-cell anergy. Blood 2005; 106:3068-73.
34. - T cells. Blood 2007;109:244-52.
35. + regulatory T cells upon mesenchymal stem cell-lymphocyte interaction. Haematologica 2007;92: 881-8.
36. + T-cell subsets expressing a regulatory /suppressive phenotype. Haematologica 2005;90:516-25.
37. + hemopoietic progenitor cells to differentiate into regulatory dendritic cells through activation of the Notch pathway. J Immunol 2008; 180:1598-608.
38. Jiang XX, Zhang Y, Liu B, Zhang SW, Wu Y, Yu XD, et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 2005;105:4120-6.
39. Gonzalez MA, Gonzalez-Rey E, Rico L, Buscher D, Delgado M. Adipose-derived mesenchymal stem cells alleviate experimental colitis by inhibiting inflammatory and autoimmune responses. Gastroenterology. 2008. E-pub ahead of print.
40. Barry FP, Murphy JM, English K, Mahon BP. Immunogenicity of adult mesenchymal stem cells: lessons from the fet al. allograft. Stem Cells Dev 2005;14:252-65.
41. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-22.
42. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, et al. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 2007;109:228-34.
43. Cho HH, Bae YC, Jung JS. Role of Toll-like receptors on human adipose-derived stromal cells. Stem Cells 2006;24:2744-52.
44. Feldmann M, Brennan FM, Maini RN. Role of cytokines in rheumatoid arthritis. Annu Rev Immunol 1996;14:397-440.