Interaction between adipose tissue-derived mesenchymal stem cells and regulatory T-cells

Cell Transplantation

Volumn 22, Issue 1, 2013, Pages 41-54

  Engela, Anja U ^a   Baan, Carla C ^a   Peeters, Annemiek M A ^a   Weimar, Willem ^a   Hoogduijn, Martin J ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Immunosuppression; Mesenchymal stem cells (MSCs); Regulatory T cells (Tregs); Transplantation

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; TUMOR NECROSIS FACTOR ALPHA;

ADIPOSE TISSUE; ADULT; ARTICLE; BLOOD BANK; CELL INTERACTION; CYTOKINE RELEASE; EFFECTOR CELL; FEMALE; GRAFT RECIPIENT; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; KIDNEY DONOR; KIDNEY TRANSPLANTATION; MALE; MESENCHYMAL STEM CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

ADIPOSE TISSUE; ADULT; CELL COMMUNICATION; FEMALE; HUMANS; KIDNEY TRANSPLANTATION; LYMPHOCYTE SUBSETS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION IMMUNOLOGY;

EID: 84873022590     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X636984     Document Type: Article

References (59)

1. Ando, W.; Tateishi, K.; Hart, D. A.; Katakai, D.; Tanaka, Y.; Nakata, K.; Hashimoto, J.; Fujie, H.; Shino, K.; Yoshikawa, H.; Nakamura, N. Cartilage repair using an in vitro generated scaffold-free tissue-engineered construct derived from porcine synovial mesenchymal stem cells. Biomaterials 28(36):5462-5470; 2007.
2. Antonucci, I.; Stuppia, L.; Kaneko, Y.; Yu, S.; Tajiri, N.; Bae, E. C.; Chheda, S. H.; Weinbren, N. L.; Borlongan, C. V. Amniotic fluid as a rich source of mesenchymal stromal cells for transplantation therapy. Cell Transplant. 20(6):789-795; 2011.
3. Augello, A.; Tasso, R.; Negrini, S. M.; Amateis, A.; Indiveri, F.; Cancedda, R.; Pennesi, G. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur. J. Immunol. 35(5):1482-1490; 2005.
4. Bacchetta, R.; Passerini, L.; Gambineri, E.; Dai, M.; Allan, S. E.; Perroni, L.; Dagna-Bricarelli, F.; Sartirana, C.; Matthes-Martin, S.; Lawitschka, A.; Azzari, C.; Ziegler, S. F.; Levings, M. K.; Roncarolo, M. G. Defective regulatory and effector T-cell functions in patients with FOXP3 mutations. J. Clin. Invest. 116(6):1713-1722; 2006.
5. Bartholomew, A.; Sturgeon, C.; Siatskas, M.; Ferrer, K.; McIntosh, K.; Patil, S.; Hardy, W.; Devine, S.; Ucker, D.; Deans, R.; Moseley, A.; Hoffman, R. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 30(1):42-48; 2002.
6. Batten, P.; Sarathchandra, P.; Antoniw, J. W.; Tay, S. S.; Lowdell, M. W.; Taylor, P. M.; Yacoub, M. H. Human mesenchymal stem cells induce T-cell anergy and downregulate T-cell allo-responses via the TH2 pathway: Relevance to tissue engineering human heart valves. Tissue Eng. 12(8):2263-2273; 2006.
7. Bennett, C. L.; Christie, J.; Ramsdell, F.; Brunkow, M. E.; Ferguson, P. J.; Whitesell, L.; Kelly, T. E.; Saulsbury, F. T.; Chance, P. F.; Ochs, H. D. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat. Genet. 27(1):20-21; 2001.
8. + regulatory T-cell recruitment in human renal allograft infiltrates. J. Immunol. 179(7):4901-4909; 2007.
9. Brunstein, C. G.; Miller, J. S.; Cao, Q.; McKenna, D. H.; Hippen, K. L.; Curtsinger, J.; Defor, T.; Levine, B. L.; June, C. H.; Rubinstein, P.; McGlave, P. B.; Blazar, B. R.; Wagner, J. E. Infusion of ex vivo expanded T regulatory cells in adults transplanted with umbilical cord blood: Safety profile and detection kinetics. Blood 117(3):1061-1070; 2011.
10. Carter, L.; Fouser, L. A.; Jussif, J.; Fitz, L.; Deng, B.; Wood, C. R.; Collins, M.; Honjo, T.; Freeman, G. J.; Carreno, B. M. PD-1:PD-L inhibitory pathway affects both CD4(+) and CD8(+) T-cells and is overcome by IL-2. Eur. J. Immunol. 32(3):634-643; 2002.
11. Chen, S. L.; Fang, W. W.; Ye, F.; Liu, Y. H.; Qian, J.; Shan, S. J.; Zhang, J. J.; Chunhua, R. Z.; Liao, L. M.; Lin, S.; Sun, J. P. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am. J. Cardiol. 94(1):92-95; 2004.
12. Crop, M. J.; Baan, C. C.; Korevaar, S. S.; Ijzermans, J. N.; Pescatori, M.; Stubbs, A. P.; van Ijcken, W. F.; Dahlke, M. H.; Eggenhofer, E.; Weimar, W.; Hoogduijn, M. J. Inflammatory conditions affect gene expression and function of human adipose tissue-derived mesenchymal stem cells. Clin. Exp. Immunol. 162(3):474-486; 2010.
13. Crop, M. J.; Baan, C. C.; Korevaar, S. S.; Ijzermans, J. N.; Weimar, W.; Hoogduijn, M. J. Human adipose tissue-derived mesenchymal stem cells induce explosive T-cell proliferation. Stem Cells Dev. 19(12):1843-1853; 2010.
14. de la Garza-Rodea, A. S.; van der Velde-van Dijke, L.; Boersma, H.; Goncalves, M. A.; van Bekkum, D. W.; de Vries, A. A.; Knaan-Shanzer, S. Myogenic properties of human mesenchymal stem cells derived from three different sources. Cell Transplant. 21(1):153-173; 2012.
15. + regulatory T-cells: Does in vitro evidence translate to the clinical setting? Transplantation 85(6):783-789; 2008.
16. Deuse, T.; Stubbendorff, M.; Tang-Quan, K.; Phillips, N.; Kay, M. A.; Eiermann, T.; Phan, T. T.; Volk, H. D.; Reichenspurner, H.; Robbins, R. C.; Schrepfer, S. Immunogenicity and immunomodulatory properties of umbilical cord lining mesenchymal stem cells. Cell Transplant. 20(5):655-667; 2011.
17. Di Nicola, M.; Carlo-Stella, C.; Magni, M.; Milanesi, M.; Longoni, P. D.; Matteucci, P.; Grisanti, S.; Gianni, A. M. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99(10):3838-3843; 2002.
18. Eggenhofer, E.; Renner, P.; Soeder, Y.; Popp, F. C.; Hoogduijn, M. J.; Geissler, E. K.; Schlitt, H. J.; Dahlke, M. H. Features of synergism between mesenchymal stem cells and immunosuppressive drugs in a murine heart transplantation model. Transpl. Immunol. 25(2-3):141-147; 2011.
19. Fallarino, F.; Grohmann, U. Using an ancient tool for igniting and propagating immune tolerance: IDO as an inducer and amplifier of regulatory T-cell functions. Curr. Med. Chem. 18(15):2215-2221; 2011.
20. + T-cells through TGF-beta-TGF-beta receptor interactions in type 1 diabetes. Proc. Natl. Acad. Sci. USA 100(19):10878-10883; 2003.
21. Groh, M. E.; Maitra, B.; Szekely, E.; Koc, O. N. Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T-cells. Exp. Hematol. 33(8):928-934; 2005.
22. Hara, M.; Kingsley, C. I.; Niimi, M.; Read, S.; Turvey, S. E.; Bushell, A. R.; Morris, P. J.; Powrie, F.; Wood, K. J. IL-10 is required for regulatory T-cells to mediate tolerance to alloantigens in vivo. J. Immunol. 166(6):3789-3796; 2001.
23. Hendrikx, T. K.; van Gurp, E. A.; Sewgobind, V. D.; Mol, W. M.; Schoordijk, W.; Klepper, M.; Velthuis, J. H.; Geel, A.; Ijzermans, J. N.; Weimar, W.; Baan, C. C. Generation of donor-specific regulatory T-cell function in kidney transplant patients. Transplantation 87(3):376-383; 2009.
24. Hoogduijn, M. J.; Crop, M. J.; Korevaar, S. S.; Peeters, A. M.; Eijken, M.; Maat, L. P.; Balk, A. H.; Weimar, W.; Baan, C. C. Susceptibility of human mesenchymal stem cells to tacrolimus, mycophenolic acid, and rapamycin. Transplantation 86(9):1283-1291; 2008.
25. Hoogduijn, M. J.; Crop, M. J.; Peeters, A. M.; Van Osch, G. J.; Balk, A. H.; Ijzermans, J. N.; Weimar, W.; Baan, C. C. Human heart, spleen, and perirenal fat-derived mesenchymal stem cells have immunomodulatory capacities. Stem Cells Dev. 16(4):597-604; 2007.
26. Hoogduijn, M. J.; Popp, F.; Verbeek, R.; Masoodi, M.; Nicolaou, A.; Baan, C.; Dahlke, M. H. The immunomodulatory properties of mesenchymal stem cells and their use for immunotherapy. Int. Immunopharmacol. 10(12):1496-1500; 2010.
27. Hoogduijn, M. J.; Popp, F. C.; Grohnert, A.; Crop, M. J.; van Rhijn, M.; Rowshani, A. T.; Eggenhofer, E.; Renner, P.; Reinders, M. E.; Rabelink, T. J.; van der Laan, L. J.; Dor, F. J.; Ijzermans, J. N.; Genever, P. G.; Lange, C.; Durrbach, A.; Houtgraaf, J. H.; Christ, B.; Seifert, M.; Shagidulin, M.; Donckier, V.; Deans, R.; Ringden, O.; Perico, N.; Remuzzi, G.; Bartholomew, A.; Schlitt, H. J.; Weimar, W.; Baan, C. C.; Dahlke, M. H.; Misot Study Group. Advancement of mesenchymal stem cell therapy in solid organ transplantation (MISOT). Transplantation 90(2):124-126; 2010.
28. Horwitz, E. M.; Prockop, D. J.; Fitzpatrick, L. A.; Koo, W. W.; Gordon, P. L.; Neel, M.; Sussman, M.; Orchard, P.; Marx, J. C.; Pyeritz, R. E.; Brenner, M. K. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat. Med. 5(3):309-313; 1999.
29. Jiang, W.; Ma, A.; Wang, T.; Han, K.; Liu, Y.; Zhang, Y.; Zhao, X.; Dong, A.; Du, Y.; Huang, X.; Wang, J.; Lei, X.; Zheng, X. Intravenous transplantation of mesenchymal stem cells improves cardiac performance after acute myocardial ischemia in female rats. Transpl. Int. 19(7):570-580; 2006.
30. Jungebluth, P.; Luedde, M.; Ferrer, E.; Luedde, T.; Vucur, M.; Peinado, V. I.; Go, T.; Schreiber, C.; Richthofen, M. V.; Bader, A. Haag, J.; Darsow, K. H.; Bartel, S. J.; Lange, H. A.; Furlani, D.; Steinhoff, G.; Macchiarini, P. Mesenchymal stem cells restore lung function by recruiting resident and nonresident proteins. Cell Transplant. 20(10):1561-1574; 2011.
31. Kinsey, G. R.; Huang, L.; Vergis, A. L.; Li, L.; Okusa, M. D. Regulatory T-cells contribute to the protective effect of ischemic preconditioning in the kidney. Kidney Int. 77(9):771-780; 2010.
32. Kobayashi, I.; Shiari, R.; Yamada, M.; Kawamura, N.; Okano, M.; Yara, A.; Iguchi, A.; Ishikawa, N.; Ariga, T.; Sakiyama, Y.; Ochs, H. D.; Kobayashi, K. Novel mutations of FOXP3 in two Japanese patients with immune dysregulation, polyendocrinopathy, enteropathy, X linked syndrome (IPEX). J. Med. Genet. 38(12):874-876; 2001.
33. Kocher, A. A.; Schlechta, B.; Gasparovicova, A.; Wolner, E.; Bonaros, N.; Laufer, G. Stem cells and cardiac regeneration. Transpl. Int. 20(9):731-746; 2007.
34. Krampera, M.; Glennie, S.; Dyson, J.; Scott, D.; Laylor, R.; Simpson, E.; Dazzi, F. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigenspecific T-cells to their cognate peptide. Blood 101(9):3722-3729; 2003.
35. Kunter, U.; Rong, S.; Djuric, Z.; Boor, P.; Muller-Newen, G.; Yu, D.; Floege, J. Transplanted mesenchymal stem cells accelerate glomerular healing in experimental glomerulonephritis. J. Am. Soc. Nephrol. 17(8):2202-2212; 2006.
36. Le Blanc, K.; Frassoni, F.; Ball, L.; Locatelli, F.; Roelofs, H.; Lewis, I.; Lanino, E.; Sundberg, B.; Bernardo, M. E.; Remberger, M.; Dini, G.; Egeler, R. M.; Bacigalupo, A.; Fibbe, W.; Ringden, O.; 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 371(9624):1579-1586; 2008.
37. Le Blanc, K.; Rasmusson, I.; Sundberg, B.; Gotherstrom, C.; Hassan, M.; Uzunel, M.; Ringden, O. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363(9419):1439-1441; 2004.
38. Livak, K. J.; Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) Method. Methods 25(4):402-408; 2001.
39. McMurchy, A. N.; Bushell, A.; Levings, M. K.; Wood, K. J. Moving to tolerance: Clinical application of T regulatory cells. Semin. Immunol. in press; 2011.
40. 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 103(12):4619-4621; 2004.
41. Muthukumar, T.; Dadhania, D.; Ding, R.; Snopkowski, C.; Naqvi, R.; Lee, J. B.; Hartono, C.; Li, B.; Sharma, V. K.; Seshan, S. V.; Kapur, S.; Hancock, W. W.; Schwartz, J. E.; Suthanthiran, M. Messenger RNA for FOXP3 in the urine of renal-allograft recipients. N. Engl. J. Med. 353(22):2342-2351; 2005.
42. Nasef, A.; Mathieu, N.; Chapel, A.; Frick, J.; Francois, S.; Mazurier, C.; Boutarfa, A.; Bouchet, S.; Gorin, N. C.; Thierry, D.; Fouillard, L. Immunosuppressive effects of mesenchymal stem cells: Involvement of HLA-G. Transplantation 84(2):231-237; 2007.
43. Page, A. J.; Ford, M. L.; Kirk, A. D. Memory T-cell-specific therapeutics in organ transplantation. Curr. Opin. Organ Transplant. 14(6):643-649; 2009.
44. Park, Y.; Oh, S. J.; Chung, D. H. CD4(+)CD25(+) regulatory T-cells attenuate Hypersensitivity Pneumonitis by suppressing IFN-IIproduction by CD4(+) and CD8(+) T-cells. J. Leukoc. Biol. 86(6):1427-1437; 2009.
45. Perico, N.; Casiraghi, F.; Introna, M.; Gotti, E.; Todeschini, M.; Cavinato, R. A.; Capelli, C.; Rambaldi, A.; Cassis, P.; Rizzo, P.; Cortinovis, M.; Marasa, M.; Golay, J.; Noris, M.; Remuzzi, G. Autologous mesenchymal stromal cells and kidney transplantation: A pilot study of safety and clinical feasibility. Clin. J. Am. Soc. Nephrol. 6(2):412-422; 2011.
46. Pittenger, M. F.; Mackay, A. M.; Beck, S. C.; Jaiswal, R. K.; Douglas, R.; Mosca, J. D.; Moorman, M. A.; Simonetti, D. W.; Craig, S.; Marshak, D. R. Multilineage potential of adult human mesenchymal stem cells. Science 284(5411):143-147; 1999.
47. Polchert, D.; Sobinsky, J.; Douglas, G.; Kidd, M.; Moadsiri, A.; Reina, E.; Genrich, K.; Mehrotra, S.; Setty, S.; Smith, B.; Bartholomew, A. IFN-BBactivation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Eur. J. Immunol. 38(6):1745-1755; 2008.
48. Popp, F. C.; Eggenhofer, E.; Renner, P.; Slowik, P.; Lang, S. A.; Kaspar, H.; Geissler, E. K.; Piso, P.; Schlitt, H. J.; Dahlke, M. H. Mesenchymal stem cells can induce long-term acceptance of solid organ allografts in synergy with low-dose mycophenolate. Transpl. Immunol. 20(1-2):55-60; 2008.
49. Quarto, R.; Mastrogiacomo, M.; Cancedda, R.; Kutepov, S. M.; Mukhachev, V.; Lavroukov, A.; Kon, E.; Marcacci, M. Repair of large bone defects with the use of autologous bone marrow stromal cells. N. Engl. J. Med. 344(5):385-386; 2001.
50. Ren, G.; Zhao, X.; Zhang, L.; Zhang, J.; L'Huillier, A.; Ling, W.; Roberts, A. I.; Le, A. D.; Shi, S.; Shao, C.; Shi, Y. Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. J. Immunol. 184(5):2321-2328; 2010.
51. Sato, K.; Ozaki, K.; Oh, I.; Meguro, A.; Hatanaka, K.; Nagai, T.; Muroi, K.; Ozawa, K. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109(1):228-234; 2007.
52. + CD25bright T-cells in kidney transplant patients: Improving suppression of donordirected responses after transplantation. Clin. Transplant. 22(5):579-586; 2008.
53. Spaggiari, G. M.; Capobianco, A.; Abdelrazik, H.; Becchetti, F.; Mingari, M. C.; Moretta, L. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: Role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood 111(3):1327-1333; 2008.
54. + T-cells secreting interleukin-10 and transforming growth factor-beta1 mediates suppression in the tumor microenvironment. Clin. Cancer Res. 13(15 Pt 1):4345-4354; 2007.
55. + regulatory T-cell: A jack of all trades, master of regulation. Nat. Immunol. 9(3):239-244; 2008.
56. - T regulatory cells. Clin. Immunol. 133(1):22-26; 2009.
57. + regulatory T-cells can mediate donor nonreactivity in long-term immunosuppressed kidney allograft patients. Am. J. Transplant. 6(12):2955-2964; 2006.
58. Wakitani, S.; Mitsuoka, T.; Nakamura, N.; Toritsuka, Y.; Nakamura, Y.; Horibe, S. Autologous bone marrow stromal cell transplantation for repair of full-thickness articular cartilage defects in human patellae: Two case reports. Cell Transplant. 13(5):595-600; 2004.
59. Zuk, P. A.; Zhu, M.; Ashjian, P.; De Ugarte, D. A.; Huang, J. I.; Mizuno, H.; Alfonso, Z. C.; Fraser, J. K.; Benhaim, P.; Hedrick, M. H. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 13(12):4279-4295; 2002.