Safety and efficacy of mesenchymal stromal cell therapy in autoimmune disorders

Annals of the New York Academy of Sciences

Volumn 1266, Issue 1, 2012, Pages 107-117

  Bernardo, Maria Ester ^a   Fibbe, Willem E ^b  

^a BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Autoimmune disorders; Biosafety; Inflammatory bowel diseases; Mesenchymal stromal cells; Paracrine mechanism; Tissue repair

Indexed keywords

ADIPOSE TISSUE; ARTICLE; AUTOIMMUNE DISEASE; BONE MARROW; ENTERITIS; GRAFT FAILURE; GRAFT VERSUS HOST REACTION; HUMAN; IMMUNOGENICITY; LIVER DISEASE; MESENCHYMAL STROMA CELL; NONHUMAN; PATIENT SAFETY; RADIATION INJURY; REGENERATIVE MEDICINE; SEPSIS; THERAPY EFFECT; TISSUE REPAIR;

EID: 84865355509     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2012.06667.x     Document Type: Article

References (80)

1. Friedenstein, A.J., K.V. Petrakova, A.I. Kurolesova & G.P. Frolova 1968. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 6: 230-247.
2. Pittenger, M.F., A.M. Mackay, S.C. Beck, et al 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
3. Zhang, J., C. Niu, L. Ye, et al 2003. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425: 836-841.
4. Nauta, A.J. & W.E. Fibbe 2007. Immunomodulatory properties of mesenchymal stromal cells. Blood 110: 3499-3506.
5. Locatelli, F., R. Maccario & F. Frassoni 2007. Mesenchymal stromal cells, from indifferent spectators to principal actors. Are we going to witness a revolution in the scenario of allograft and immune-mediated disorders? Haematologica 92: 872-877.
6. Almeida-Porada, G., A.W. Flake, H.A. Glimp & E.D. Zanjani 1999. Cotransplantation of stroma results in enhancement of engraftment and early expression of donor hematopoietic stem cells in utero. Exp. Hematol. 27: 1569-1575.
7. Bartholomew, A., C. Sturgeon, M. Siatskas, et al 2002. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 30: 42-48.
8. Parekkadan, B., D. van Poll, K. Suganuma, et al 2007. Mesenchymal stem cell-derived molecules reverse fulminant hepatic failure. PLoS One 2: e941.
9. Ball, L.M., M.E. Bernardo, H. Roelofs, et al 2007. Co-transplantation of ex-vivo expanded mesenchymal stem cells accelerates lymphocyte recovery and may reduce the risk of graft failure in haploidentical hematopoietic stem cell transplantation. Blood 110: 2764-2767.
10. Le Blanc, K., F. Frassoni, L.M. Ball, et al 2008. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371: 1579-1586.
11. Duijvenstein, M., A.C. Vos, H. Roelofs, et al 2010. Autologous bone marrow-derived mesenchymal stromal cell treatment for refractory luminal Crohn's disease: results of a phase I study. Gut 59: 1662-1669.
12. Ciccocioppo, R., M.E. Bernardo, A. Sgarella, et al 2011. Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 60: 788-798.
13. Nauta, A.J., G. Westerhuis, A.B. Kruisselbrink, et al 2006. Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a non-myeloablative setting. Blood 108: 2114-2120.
14. Spaggiari, G.M., A. Capobianco, S. Becchetti, et al 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: 1484-1490.
15. Horwitz, E.M., P.L. Gordon, W.K. Koo, et al 2002. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc. Natl. Acad. Sci. U. S. A. 99: 8932-8937.
16. Spees, J.L., C.A. Gregory, H. Singh, et al 2004. Internalized antigens must be removed to prepare hypoimmunogenic mesenchymal stem cells for cell and gene therapy. Mol. Ther. 9: 747-756.
17. Horwitz, E.M., D.J. Prockop, L.A. Fitzpatrick, et al 1999. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat. Med. 5: 309-313.
18. Shahdadfar, A., K. Fronsdal, T. Haug, et al 2005. In vitro expansion of human mesenchymal stem cells: choice of serum is a determinant of cell proliferation, differentiation, gene expression, and transcriptosome stability. Stem Cells 23: 1357-1366.
19. Jung, S., A. Sen, L. Rosenberg & L.A. Behie 2010. Identification of growth and attachment factors for the serum-free isolation and expansion of human mesenchymal stromal cells. Cytotherapy 12: 637-657.
20. Doucet, C., I. Ernou, Y. Zhang, et al 2005. Platelet lysates promote mesenchymal stem cell expansion: a safety substitute for animal serum in cell-based therapy applications. J. Cell Physiol. 205: 228-236.
21. Bernardo, M.E., M.A. Avanzini, C. Perotti, et al 2007. Optimization of in vitro expansion of human multipotent mesenchymal stromal cells for cell-therapy approaches: further insights in the search for a fetal calf serum substitute. J. Cell Physiol. 211: 121-130.
22. Schallmoser, K., C. Bartmann, E. Rohde, et al 2007. Human platelet lysate can replace fetal bovine serum for clinical-scale expansion of functional mesenchymal stromal cells. Transfusion 47: 1436-1446.
23. Breitbach, M., T. Bostani, W. Roell, et al 2007. Potential risks of bone marrow cell transplantation into infarcted hearts. Blood 110: 1362-1369.
24. Kunter, U., S. Rong, P. Boor, et al 2007. Mesenchymal stem cells prevent progressive experimental renal failure but maldifferentiate into glomerular adipocytes. J. Am. Soc. Nephrol. 18: 1754-1764.
25. Prigozhina, T.B., S. Khitrin, G. Elkin, et al 2008. Mesenchymal stromal cells lose their immunosuppressive potential after allotransplantation. Exp. Hematol. 36: 1370-1376.
26. Rubio, D., J. Garcia-Castro, M.C. Martin, et al 2005. Spontaneous human adult stem cell transformation. Cancer Res. 65: 3035-3039.
27. Wang, Y., D.L. Huso, J. Harrington, et al 2005. Outgrowth of a transformed cell population derived from normal human BM mesenchymal stem cell culture. Cytotherapy 7: 509-519.
28. Røsland, G.V., A. Svendsen, A. Torsvik, et al 2009. Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. Cancer Res. 69: 5331-5339.
29. Bernardo, M.E., N. Zaffaroni, F. Novara, et al 2007. Human bone marrow-derived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms. Cancer Res. 67: 9142-9149.
30. Avanzini, M.A., M.E. Bernardo, A.M. Cometa, et al 2009. Generation of mesenchymal stromal cells in the presence of platelet lysate: a phenotypical and functional comparison between umbilical cord blood- and bone marrow-derived progenitors. Haematologica. 94: 1649-1660.
31. Tarte, K., J. Gaillard, J. Lataillade, et al 2010. Clinical-grade production of human mesenchymal stromal cells: occurrence of aneuploidy without transformation. Blood 115: 1549-1553.
32. Vogel, G. 2010. To scientists's dismay, mixed-up cell lines strike again. Science 329: 1004.
33. Torsvik, A., G.V. Røsland, A. Svendsen, et al 2010. Spontaneous malignant transformation of human mesenchymal stem cells reflects cross-contamination: putting the research field on track - letter. Cancer Res. 70: 6393-6396.
34. Prockop, D.J., M. Brenner, W.E. Fibbe, et al 2010. Defining the risks of mesenchymal stromal cell therapy. Cytotherapy 2: 576-578.
35. Tisato, V., K. Naresh, J. Girdlestone, et al 2007. Mesenchymal stem cells of cord blood origin are effective at preventing but not treating graft-versus-host disease. Leukemia 21: 1992-1999.
36. Hayashi, Y., S. Tsuji, M. Tsujii, et al 2008. Topical implantation of mesenchymal stem cells has beneficial effects on healing of experimental colitis in rats. J. Pharmacol. Exp. Ther. 326: 523-531.
37. Yabana, T., Y. Arimura, H. Tanaka, et al 2009. Enhancing epithelial engrafment of rat mesenchymal stem cells restores epithelial barrier integrity. J. Pathol. 218: 350-359.
38. González, M.A., E. Gonzalez-Rey, L. Rico, et al 2009. Adipose-derived mesenchymal stem cells alleviate experimental colitis by inhibiting inflammatory and autoimmune responses. Gastroenterology 136: 978-989.
39. Tanaka, F., K. Tominaga, M. Ochi, et al 2008. Exogenous administration of mesenchymal stem cells ameliorates dextran sulphate-sodium-induced colitis via anti-inflammatory action in damaged tissue in rats. Life Science 83: 771-779.
40. Zhang, Q., S. Shi, Y. Liu, et al 2009. Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J. Immunol. 183: 7787-7798.
41. Hayashy, Y., S. Tsuji, M. Tsujii, et al 2008. Topical transplantation of mesenchymal stem cells accelerates gastric ulcer healing in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 294: G778-G786.
42. Hayashy, Y., J. Zhang, J.F. Gong, et al 2008. Effects of transplanted bone marrow mesenchymal stem cells on the irradiated intestine of mice. J. Biomed. Sci. 15: 585-594.
43. Mouiseddine, M., S. François, A. Semont, et al 2007. Human mesenchymal stem cells home specifically to radiation-injured tissues in a non-obese diabetes/severe combined immunodeficiency mouse model. Br. J. Radiol. 80: S49-S55.
44. Németh, K., A. Leelahavanichkul, P.S. Yuen, et al 2009. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat. Med. 15: 42-49.
45. Kuo, T.K., S.P. Hung, C.H. Chuang, et al 2008. Stem cell therapy for liver disease: parameters governing the success of using bone marrow mesenchymal stem cells. Gastroenterology 134: 2111-2121.
46. van Poll, D., B. Parekkadan, C.H. Cho, et al 2008. Mesenchymal stem cell-derived molecules directly modulate hepatocellular death and regeneration in vitro and in vivo. Hepatology 47: 1634-1643.
47. Yu, Y., A.H. Yao, N. Chen, et al 2007. Mesenchymal stem cells over-expressing hepatocyte growth factor improve small-for-size liver grafts regeneration. Mol. Ther. 15: 1382-1389.
48. Carvalho, A.B., L.F. Quintanilha, J.V. Dias, et al 2008. Bone marrow multipotent mesenchymal stromal cells do not reduce fibrosis or improve function in a rat model of severe chronic liver injury. Stem. Cells 26: 1307-1314.
49. Zappia, E., S. Casazza, E. Pedemonte, et al 2005. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106: 1755-1761.
50. Zhang, J., Y. Li, J. Chen, et al 2005. Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Exp. Neurol. 195: 16-26.
51. Deng, W., Q. Han, L. Liao, et al 2005. Effect of allogeneic bone marrow-derived mesenchymal stem cells on T and B lymphocytes from BXSB mice. DNA Cell. Biol. 24: 458-463.
52. Djouad, F., V. Fritz, F. Apparailly, et al 2005. Reversal of the immunesuppressive properties of mesenchymal stem cells by tumor necrosis factor alpha in collagen-induced arthritis. Arthritis Rheum. 52: 1595-1603.
53. Jurewicz, M., S. Yang, A. Augello, et al 2010. Congenic mesenchymal stem cell therapy reverses hyperglycemia in experimental type 1 diabetes. Diabetes 59: 3139-3147.
54. Fiorina, P., M. Jurewicz, A. Augello, et al 2009. Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes. J. Immunol. 183: 993-1004.
55. Lee, R.H., M.J. Seo, A.A. Pulin, et al 2006. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/SCID mice. Proc. Natl. Acad. Sci. U. S. A. 103: 17438-17443.
56. Kunter, U., S. Rong, Z. Djuric, et al 2006. Transplanted mesenchymal stemm cells accelerate glomerular healing in experimental glomerulonephritis. J. Am. Soc. Nephrol. 17: 2202-2212.
57. Krampera, M., L. Cosmi, R. Angeli, et al 2006. Role of interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 24: 386-398.
58. Ryan, J.M., F. Barry, J.M. Murphy & B.P. Mahon 2007. Interferon-γ does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin. Exp. Immunol. 149: 353-363.
59. Prockop, D.J. & J.Y. Oh 2012. Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. Mol. Ther. 20: 14-20.
60. Roddy, G.W., J.Y. Oh, R.H. Lee, et al 2011. Action at a distance: systemically administered adult stem/progenitor cells (MSCs) reduce inflammatory damage to the cornea without engraftment and primarily by secretion of TNF- α stimulated gene/protein 6. Stem Cells 29: 1572-1579.
61. Mougiakakos, D., R. Jitschin, C.C. Johansson, et al 2011. The impact of inflammatory licensing on heme oxygenase-1-mediated induction of regulatory T cells by human mesenchymal stem cells. Blood 117: 4826-4835.
62. Dazzi, F. & M. Krampera 2011. Mesenchymal stem cells and autoimmune diseases. Best Pract. Res. Clin. Haematol. 24: 49-57.
63. Ren, G., L. Zhang, X. Zhaon, et al 2008. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2: 141-150.
64. Wynn, R.F., C.A. Hart, C. Corradi-Perini, et al 2004. A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow. Blood 104: 2643-2645.
65. Sordi, V., M.L. Malosio, F. Marchesi, et al 2005. Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 106: 419-427.
66. Larghero, J., D. Farge, A. Braccini, et al 2008. Phenotypical and functional characteristics of in vitro expanded bone marrow mesenchymal stem cells from patients with systemic sclerosis. Ann. Rheum. Dis. 67: 443-449.
67. Bocelli-Tyndall, C., L. Bracci, G. Spagnoli, et al 2007. Bone marrow mesenchymal stromal cells (BM-MSCs) from healthy donors and auto-immune disease patients reduce the proliferation of autologous- and allogeneic-stimulated lymphocytes in vitro. Rheumatology 46: 403-408.
68. Bernardo, M.E., M.A. Avanzini, R. Ciccocioppo, et al 2009. Phenotypical/functional characterization of in vitro expanded mesenchymal stromal cells from Crohn's disease patients. Cytotherapy 11: 825-836.
69. García-Olmo, D., M. García-Arranz, D. Herreros, et al 2005. A phase I clinical trial of the treatment of Crohn's fistula by adipose mesenchymal stem cell transplantation. Dis. Colon. Rectum. 48: 1416-1423.
70. Garcia-Olmo, D., D. Herreros, I. Pascual, et al Expanded adipose-tissue derived stem cells for the treatment of complex perianal fistula: a phase II clinical trial. Dis. Colon. Rectum. 52: 79-86.
71. Garcia-Olmo, D., D. Herreros, P. De-La-Quintana, et al 2010. Adipose-derived stem cells in Crohn's rectovaginal fistula. Case Report Med. 2010: 961758.
72. Ko, I.K., B.G. Kim, A. Awadallah, et al 2010. Targeting improves MSC treatment of inflammatory bowel disease. Mol. Ther. 18: 1365-1372.
73. Lazebnik, L.B., A.G. Konopliannikov, O.V. Kniazev, et al 2010. Use of allogeneic mesenchymal stem cells in the treatment of intestinal inflammatory diseases. Ter. Arkh. 82: 38-43.
74. Mohyeddin Bonab, M., S. Yazdanbakhsh, J. Lotfi, et al 2007. Does mesenchymal stem cell therapy help multiple sclerosis patients? Report of a pilot study. Iran. J. Immunol. 4: 50-57.
75. Karussis, D., C. Karageorgiou, A. Vaknin-Dembinsky, et al 2010. Safety and immunological effect of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch. Neurol. 67: 1187-1194.
76. Freedman, M.S., A. Bar-Or, H.L. Atkins, et al 2010. The therapeutic potential of mesenchymal stem cell transplantation as a treatment for multiple sclerosis: consensus report of the International MSCT Study Group. Mult. Scler. 16: 503-510.
77. Mabed, M. & M Shahin. 2012. Mesenchymal stem cell-based therapy for the treatment of type 1 Diabetes Mellitus. Curr. Stem. Cell. Res. Ther. 7: 179-190.
78. Jaganathan, B.G., V. Tisato, T. Vulliamy, et al 2010. Effects of MSC co-injection on the reconstitution of aplastic anemia patient following hematopoietic stem cell transplantation. Leukemia 24: 1791-1795.
79. Fang, B., N. Li, Y. Song, et al 2009. Cotransplantation of haploidentical mesenchymal stem cells to enhance engraftment of hematopoietic stem cells and to reduce the risk of graft failure in two children with severe aplastic anemia. Pediatr. Transplant 13: 499-502.
80. Hernatti, P. & A. Keating Mesenchymal stromal cells: Basic Biology and Clinical Applications." Section II, chapter 6: "MSCs for gastrointestinal disorders.