Multipotent mesenchymal stromal cells and immune tolerance

Leukemia and Lymphoma

Volumn 48, Issue 7, 2007, Pages 1283-1289

  Noël, Danièle ^a,b,c   Djouad, Farida ^a,b,d   Bouffi, Carine ^a,b   Mrugala, Dominique ^a,b   Jorgensen, Christian ^a,b,e  

^a INSERM   (France)

^b UNIV MONTPELLIER   (France)

^c HÔPITAL SAINT ELOI   (France)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e LAPEYRONIE HOSPITAL   (France)

Author keywords

Characterization; Immunosuppression; Mesenchymal stem cell

Indexed keywords

CYTOKINE; IMMUNOSUPPRESSIVE AGENT; INDOLEAMINE 2,3 DIOXYGENASE; NITRIC OXIDE;

ALLERGIC ENCEPHALOMYELITIS; ALLOGENEIC STEM CELL TRANSPLANTATION; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; APOPTOSIS; AUTOIMMUNE DISEASE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CELL ACTIVATION; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELLULAR IMMUNITY; CLINICAL TRIAL; CYTOKINE PRODUCTION; CYTOTOXICITY; DEMYELINATING DISEASE; DISEASE CONTROL; ENZYME ACTIVITY; ENZYME ANALYSIS; GRAFT VERSUS HOST REACTION; HEMATOLOGIC MALIGNANCY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNE DEFICIENCY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL TRANSPLANTATION; MULTIPLE SCLEROSIS; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE ACTIVATION;

ANIMALS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNE SYSTEM; IMMUNE TOLERANCE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MULTIPOTENT STEM CELLS; STROMAL CELLS;

EID: 34447576602     PISSN: 10428194     EISSN: 10292403     Source Type: Journal    
DOI: 10.1080/10428190701361869     Document Type: Review

References (56)

1. Friedenstein, A. J., Piatetzky II, S. and Petrakova, K. V. (1966) Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol, 16, pp. 381-390.
2. Barry, F. P. and Murphy, J. M. (2004) Mesenchymal stem cells: Clinical applications and biological characterization. Int J Biochem Cell Biol, 36, pp. 568-584.
3. D'Ippolito, G., Diabira, S., Howard, G. A., Menei, P., Roos, B. A. and Schiller, P. C. (2004) Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci, 117, pp. 2971-2981.
4. Reyes, M., Lund, T., Lenvik, T., Aguiar, D., Koodie, L. and Verfaillie, C. M. (2001) Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood, 98, pp. 2615-2625.
5. Dominici, M., Blanc, K Le, Mueller, I., Slaper-Cortenbach, I., Marini, F. and Krause, D. (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8, pp. 315-317.
6. Friedenstein, A. J., Chailakhjan, R. K. and Lalykina, K. S. (1970) The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet, 3, pp. 393-403.
7. Gronthos, S. and Simmons, P. J. (1996) The biology and application of human bone marrow stromal cell precursors. J Hematother, 5, pp. 15-23.
8. Stolzing, A. and Scutt, A. (2006) Age-related impairment of mesenchymal progenitor cell function. Aging Cell, 5, pp. 213-224.
9. Ringden, O. and Blanc, K Le (2005) Allogeneic hematopoietic stem cell transplantation: State of the art and new perspectives. APMIS, 113, pp. 813-830.
10. Kashiwakura, I. and Takahashi, T. A. (2005) Fibroblast growth factor and ex vivo expansion of hematopoietic progenitor cells. Leuk Lymphoma, 46, pp. 329-333.
11. Pittenger, M., Vanguri, P., Simonetti, D. and Young, R. (2002) Adult mesenchymal stem cells: Potential for muscle and tendon regeneration and use in gene therapy. J Musculoskelet Neuronal Interact, 2, pp. 309-320.
12. Makino, S., Fukuda, K., Miyoshi, S., Konishi, F., Kodama, H. and Pan, J. (1999) Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest, 103, pp. 697-705.
13. Phinney, D. G. and Isakova, I. (2005) Plasticity and therapeutic potential of mesenchymal stem cells in the nervous system. Curr Pharm Des, 11, pp. 1255-1265.
14. Tropel, P., Platet, N., Platel, J. C., Noel, D., Albrieux, M. and Benabid, A. L. (2006) Functional neuronal differentiation of bone marrow-derived mesenchymal stem cells. Stem Cells, 24, pp. 2868-2876.
15. Bhatia, R. and Hare, J. M. (2005) Mesenchymal stem cells: Future source for reparative medicine. Congest Heart Fail, 11, pp. 87-91.
16. Muraglia, A., Cancedda, R. and Quarto, R. (2000) Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci, 113, pp. 1161-1166.
17. Blanc, K Le, Tammik, C., Rosendahl, K., Zetterberg, E. and Ringden, O. (2003) HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol, 31, pp. 890-896.
18. Tse, W. T., Pendleton, J. D., Beyer, W. M., Egalka, M. C. and Guinan, E. C. (2003) Suppression of allogeneic T-cell proliferation by human marrow stromal cells: Implications in transplantation. Transplantation, 75, pp. 389-397.
19. Djouad, F., Bony, C., Haupl, T., Uze, G., Lahlou, N. and Louis-Plence, P. (2005) Transcriptional profiles discriminate bone marrow-derived and synovium-derived mesenchymal stem cells. Arthritis Res Ther, 7, pp. R1304-R1315.
20. Potian, J. A., Aviv, H., Ponzio, N. M., Harrison, J. S. and Rameshwar, P. (2003) Veto-like activity of mesenchymal stem cells: Functional discrimination between cellular responses to alloantigens and recall antigens. J Immunol, 171, pp. 3426-3434.
21. Chan, J. L., Tang, K. C., Patel, A. P., Bonilla, L. M., Pierobon, N. and Ponzio, N. M. (2006) Antigen presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-{gamma}. Blood, 107, pp. 4817-4824.
22. Stagg, J., Pommey, S., Eliopoulos, N. and Galipeau, J. (2006) Interferon-gamma-stimulated marrow stromal cells: A new type of nonhematopoietic antigen-presenting cell. Blood, 107, pp. 2570-2577.
23. Krampera, M., Glennie, S., Dyson, J., Scott, D., Laylor, R. and Simpson, E. (2002) Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood, 27, p. 27.
24. Bartholomew, A., Sturgeon, C., Siatskas, M., Ferrer, K., McIntosh, K. and Patil, S. (2002) Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol, 30, pp. 42-48.
25. Djouad, F., Plence, P., Bony, C., Tropel, P., Apparailly, F. and Sany, J. (2003) Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood, 102, pp. 3837-3844.
26. Glennie, S., Soeiro, I., Dyson, P. J., Lam, E. W. and Dazzi, F. (2005) Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood, 105, pp. 2821-2827.
27. Corcione, A., Benvenuto, F., Ferretti, E., Giunti, D., Cappiello, V. and Cazzanti, F. (2006) Human mesenchymal stem cells modulate B-cell functions. Blood, 107, pp. 367-372.
28. Angoulvant, D., Clerc, A., Benchalal, S., Galambrun, C., Farre, A. and Bertrand, Y. (2004) Human mesenchymal stem cells suppress induction of cytotoxic response to alloantigens. Biorheology, 41, pp. 469-476.
29. Rasmusson, I., Ringden, O., Sundberg, B. and Blanc, K Le (2003) Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation, 76, pp. 1208-1213.
30. Aggarwal, S. and Pittenger, M. F. (2005) Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood, 105, pp. 1815-1822.
31. Poggi, A., Prevosto, C., Massaro, A. M., Negrini, S., Urbani, S. and Pierri, I. (2005) Interaction between human NK cells and bone marrow stromal cells induces NK cell triggering: Role of NKp30 and NKG2D receptors. J Immunol, 175, pp. 6352-6360.
32. Spaggiari, G. M., Capobianco, A., Becchetti, S., Mingari, M. C. and Moretta, L. (2006) 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, 107, pp. 1484-1490.
33. Maitra, B., Szekely, E., Gjini, K., Laughlin, M. J., Dennis, J. and Haynesworth, S. E. (2004) Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation. Bone Marrow Transplant, 33, pp. 597-604.
34. Groh, M. E., Maitra, B., Szekely, E. and Koc, O. N. (2005) Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T cells. Exp Hematol, 33, pp. 928-934.
35. Blanc, K Le, Tammik, L., Sundberg, B., Haynesworth, S. E. and Ringden, O. (2003) Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol, 57, pp. 11-20.
36. Rasmusson, I. (2006) Immune modulation by mesenchymal stem cells. Exp Cell Res, 312, pp. 2169-2179.
37. Jiang, X. X., Zhang, Y., Liu, B., Zhang, S. X. and Yu, X. D. (2005) Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood, 105, pp. 4120-4126.
38. Nauta, A. J., Kruisselbrink, A. B., Lurvink, E., Willemze, R. and Fibbe, W. E. (2006) Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol, 177, pp. 2080-2087.
39. Meisel, R., Zibert, A., Laryea, M., Gobel, U., Daubener, W. and Dilloo, D. (2004) Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood, 103, pp. 4619-4621.
40. Krampera, M., Cosmi, L., Angeli, R., Pasini, A., Liotta, F. and Andreini, A. (2005) Role for IFN-{gamma} in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells, 24, pp. 386-398.
41. Sato, K., Ozaki, K., Meguro, A., Hatanaka, K. and Nagai, T. (2006) Nitric oxide plays a critical role in suppression of T cell proliferation by mesenchymal stem cells. Blood, 109, pp. 228-234.
42. Nicola, M Di, Carlo-Stella, C., Magni, M., Milanesi, M., Longoni, P. D. and Matteucci, P. (2002) Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood, 99, pp. 3838-3843.
43. Zappia, E., Casazza, S., Pedemonte, E., Benvenuto, F., Bonanni, I. and Gerdoni, E. (2005) Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood, 106, pp. 1755-1761.
44. Plumas, J., Chaperot, L., Richard, M. J., Molens, J. P., Bensa, J. C. and Favrot, M. C. (2005) Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia, 19, pp. 1597-1604.
45. Maccario, R., Podesta, M., Moretta, A., Cometa, A., Comoli, P. and Montagna, D. (2005) Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favors the differentiation of CD4+ T-cell subsets expressing a regulatory/ suppressive phenotype. Haematologica, 90, pp. 516-525.
46. Beyth, S., Borovsky, Z., Mevorach, D., Liebergall, M., Gazit, Z. and Aslan, H. (2005) Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood, 105, pp. 2214-2219.
47. Albina, J. E., Abate, J. A. and Henry Jr, W. L. (1991) Nitric oxide production is required for murine resident peritoneal macrophages to suppress mitogen-stimulated T cell proliferation. Role of IFN-gamma in the induction of the nitric oxide-synthesizing pathway. J Immunol, 147, pp. 144-148.
48. Sato, K., Ozaki, K., Meguro, A., Hatanaka, K. and Nagai, T. (2007) Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood, 109, pp. 228-234.
49. Devine, S. M., Bartholomew, A. M., Mahmud, N., Nelson, M., Patil, S. and Hardy, W. (2001) Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp Hematol, 29, pp. 244-255.
50. Nauta, A. J., Westerhuis, G., Kruisselbrink, A. B., Lurvink, E. G., Willemze, R. and Fibbe, W. E. (2006) Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood, 108, pp. 2114-2120.
51. Sudres, M., Norol, F., Trenado, A., Gregoire, S., Charlotte, F. and Levacher, B. (2006) Bone marrow mesenchymal stem cells suppress lymphocyte proliferation in vitro but fail to prevent graft-versus-host disease in mice. J Immunol, 176, pp. 7761-7767.
52. Koc, O. N., Gerson, S. L., Cooper, B. W., Dyhouse, S. M., Haynesworth, S. E. and Caplan, A. I. (2000) Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy. J Clin Oncol, 18, pp. 307-316.
53. Lazarus, H. M., Haynesworth, S. E., Gerson, S. L., Rosenthal, N. S. and Caplan, A. I. (1995) Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): Implications for therapeutic use. Bone Marrow Transplant, 16, pp. 557-564.
54. Lazarus, H. M., Koc, O. N., Devine, S. M., Curtin, P., Maziarz, R. T. and Holland, H. K. (2005) Cotransplantation of HLA-identical sibling culture-expanded mesenchymal stem cells and hematopoietic stem cells in hematologic malignancy patients. Biol Blood Marrow Transplant, 11, pp. 389-398.
55. Blanc, K Le, Rasmusson, I., Sundberg, B., Gotherstrom, C., Hassan, M. and Uzunel, M. (2004) Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet, 363, pp. 1439-1441.
56. Horwitz, E. M., Prockop, D. J., Fitzpatrick, L. A., Koo, W. W., Gordon, P. L. and Neel, M. (1999) Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med, 5, pp. 309-313.