Efficacy of immunotherapy with mesenchymal stem cells in man: A systematic review

Expert Review of Clinical Immunology

Volumn 11, Issue 5, 2015, Pages 617-636

  Luk, Franka ^a   De Witte, Samantha Fh ^a   Bramer, Wichor M ^a   Baan, Carla C ^a   Hoogduijn, Martin J ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Organ transplantation

Indexed keywords

C PEPTIDE; CD27 ANTIGEN; CREATININE; GAMMA INTERFERON; HEMOGLOBIN; INSULIN; INTERLEUKIN 10; INTERLEUKIN 11; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; STROMAL CELL DERIVED FACTOR 1ALPHA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

AMYOTROPHIC LATERAL SCLEROSIS; APLASTIC ANEMIA; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL STUDY; CROHN DISEASE; DISEASE SEVERITY; GRAFT VERSUS HOST REACTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOLOGICAL PARAMETERS; IMMUNOMODULATION; IMMUNOPATHOLOGY; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; INSULIN DEPENDENT DIABETES MELLITUS; LIVER CIRRHOSIS; LIVER FAILURE; MEMORY CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MULTIPLE SCLEROSIS; NATURAL KILLER T CELL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SJOEGREN SYNDROME; SYSTEMATIC REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; TH17 CELL; TREATMENT OUTCOME; TREATMENT RESPONSE; ANIMAL; AUTOIMMUNE DISEASES; CLINICAL TRIAL (TOPIC); IMMUNOLOGY; MESENCHYMAL STROMA CELL; PROCEDURES;

ANIMALS; AUTOIMMUNE DISEASES; CLINICAL TRIALS AS TOPIC; HUMANS; IMMUNOMODULATION; IMMUNOTHERAPY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; TREATMENT OUTCOME;

EID: 84928188327     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/1744666X.2015.1029458     Document Type: Review

References (85)

1. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284(5411):143-7
2. Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002;99(10):3838-43
3. Franquesa M, Mensah FK, Huizinga R, et al. Human adipose tissue-derived mesenchymal stem cells abrogate plasmablast formation and induce regulatory B cells independently of T helper cells. Stem Cells 2015;33(3):880-91
4. Maggini J, Mirkin G, Bognanni I, et al. Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile. PLoS One 2010;5(2):e9252
5. Gonzalez MA, Gonzalez-Rey E, Rico L, et al. Adipose-derived mesenchymal stem cells alleviate experimental colitis by inhibiting inflammatory and autoimmune responses. Gastroenterology 2009;136(3): 978-89
6. Nemeth K, Leelahavanichkul A, Yuen PS, et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 2009;15(1):42-9
7. Constantin G, Marconi S, Rossi B, et al. Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells 2009;27(10):2624-35
8. Popp FC, Eggenhofer E, Renner P, et al. Mesenchymal stem cells can induce long-term acceptance of solid organ allografts in synergy with low-dose mycophenolate. Transpl Immunol 2008; 20(1-2):55-60
9. Bernardo ME, Fibbe WE. Safety and efficacy of mesenchymal stromal cell therapy in autoimmune disorders. Ann N Y Acad Sci 2012;1266:107-17
10. Franquesa M, Hoogduijn MJ, Reinders ME, et al. Mesenchymal Stem Cells in Solid Organ Transplantation (MiSOT) Fourth Meeting: lessons learned from first clinical trials. Transplantation 2013;96(3):234-8
11. Le Blanc K, Rasmusson I, Sundberg B, et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004;363(9419):1439-41
12. Lalu MM, McIntyre L, Pugliese C, et al. Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. PLoS One 2012;7(10):e47559
13. Eggenhofer E, Luk F, Dahlke MH, Hoogduijn MJ. The life and fate of mesenchymal stem cells. Front Immunol 2014;5:148
14. Higgins JPT, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0. The Cochrane Collaboration 2011. Available from: www. cochrane-handbook.org [updated March 2011]
15. Xiao Y, Jiang ZJ, Pang Y, et al. Efficacy and safety of mesenchymal stromal cell treatment from related donors for patients with refractory aplastic anemia. Cytotherapy 2013;15(7):760-6
16. Bernardo ME, Ball LM, Cometa AM, et al. Co-infusion of ex vivo-expanded, parental MSCs prevents life-threatening acute GVHD, but does not reduce the risk of graft failure in pediatric patients undergoing allogeneic umbilical cord blood transplantation. Bone Marrow Transplant 2011;46(2):200-7
17. Baron F, Lechanteur C, Willems E, et al. Cotransplantation of Mesenchymal stem cells might prevent death from graft-versus-host disease (GVHD) without Abrogating graft-versus-tumor effects after HLA-mismatched allogeneic transplantation following nonmyeloablative conditioning. Biol Blood Marrow Transplant 2010;16(6): 838-47
18. Ball LM, Bernardo ME, Roelofs H, et al. Cotransplantation 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 2007;110(7):2764-7
19. Weiss DJ, Casaburi R, Flannery R, et al. A placebo-controlled, randomized trial of mesenchymal stem cells in COPD. Chest 2013;143(6):1590-8
20. Hu J, Yu X, Wang Z, et al. Long term effects of the implantation of Wharton's jelly-derived mesenchymal stem cells from the umbilical cord for newly-onset type 1 diabetes mellitus. Endocr J 2013; 60(3):347-57
21. Jitschin R, Mougiakakos D, Von Bahr L, et al. Alterations in the cellular immune compartment of patients treated with third-party mesenchymal stromal cells following allogeneic hematopoietic stem cell transplantation. Stem Cells 2013;31(8): 1715-25
22. Zhang Z, Lin H, Shi M, et al. Human umbilical cord mesenchymal stem cells improve liver function and ascites in decompensated liver cirrhosis patients. J Gastroenterol Hepatol 2012;27(Suppl 2): 112-20
23. Shi M, Zhang Z, Xu RN, et al. Human mesenchymal stem cell transfusion is safe and improves liver function in acute-on-chronic liver failure patients. Stem Cells Transl Med 2012;1(10):725-31
24. Le Blanc K, Frassoni F, Ball L, et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008;371(9624):1579-86
25. Xiong YY, Fan Q, Huang F, et al. Mesenchymal stem cells versus mesenchymal stem cells combined with cord blood for engraftment failure after autologous hematopoietic stem cell transplantation: a pilot prospective, open-label, randomized trial. Biol Blood Marrow Transplant 2014; 20(2):236-42
26. Lucchini G, Introna M, Dander E, et al. Platelet-lysate-expanded mesenchymal stromal cells as a salvage therapy for severe resistant graft-versus-host disease in a pediatric population. Biol Blood Marrow Transplant 2010;16(9):1293-301
27. Introna M, Lucchini G, Dander E, et al. Treatment of graft versus host disease with mesenchymal stromal cells: a phase I study on 40 adult and pediatric patients. Biol Blood Marrow Transplant 2014;20(3): 375-81
28. Liu X, Wu M, Peng Y, et al. Improvement in poor graft function after allogeneic hematopoietic stem cell transplantation upon administration of mesenchymal stem cells from third-party donors: a pilot prospective study. Cell Transplant 2014; 23(9):1087-98
29. Muroi K, Miyamura K, Ohashi K, et al. Unrelated allogeneic bone marrow-derived mesenchymal stem cells for steroid-refractory acute graft-versus-host disease: a phase I/II study. Int J Hematol 2013;98(2):206-13
30. Prasad VK, Lucas KG, Kleiner GI, et al. Efficacy and safety of ex vivo cultured adult human mesenchymal stem cells (Prochymal (trademark)) in Pediatric patients with severe refractory acute graft-versus-host disease in a compassionate use study. Biol Blood Marrow Transplant 2011;17(4): 534-41
31. Kebriaei P, Isola L, Bahceci E, et al. Adult Human Mesenchymal Stem Cells added to corticosteroid therapy for the treatment of acute graft-versus-host disease. Biol Blood Marrow Transplant 2009;15(7):804-11
32. Guo M, Sun Z, Sun QY, et al. a modified haploidentical nonmyeloablative transplantation without t cell depletion for high-risk acute leukemia: successful engraftment and mild GVHD. Biol Blood Marrow Transplant 2009;15(8):930-7
33. Lazarus HM, Koc ON, Devine SM, et al. Cotransplantation of HLA-identical sibling culture-expanded mesenchymal stem cells and hematopoietic stem cells in hematologic malignancy patients. Biol Blood Marrow Transplant 2005;11(5):389-98
34. Wang D, Li J, Zhang Y, et al. Umbilical cord mesenchymal stem cell transplantation in active and refractory systemic lupus erythematosus: A multicenter clinical study. Arthritis Res Ther 2014;16:2
35. Forbes GM, Sturm MJ, Leong RW, et al. A phase 2 study of allogeneic mesenchymal stromal cells for luminal Crohn's disease refractory to biologic therapy. Clin Gastroenterol Hepatol 2014;12(1):64-71
36. Kurtzberg J, Prockop S, Teira P, et al. Allogeneic human mesenchymal stem cell therapy (Remestemcel-L, Prochymal) as a rescue agent for severe refractory acute graft-versus-host disease in pediatric patients. Biol Blood Marrow Transplant 2014;20(2): 229-35
37. Calkoen FGJ, Jol-van der Zijde CM, Mearin ML, et al. Gastrointestinal acute graft-versus-host disease in children: histology for diagnosis, mesenchymal stromal cells for treatment, and biomarkers for prediction of response. Biol Blood Marrow Transplant 2013;19(11):1590-9
38. Vanikar AV, Trivedi HL, Kumar A, et al. Co-infusion of donor adipose tissue-derived mesenchymal and hematopoietic stem cells helps safe minimization of immunosuppression in renal transplantation-single center experience. Ren Fail 2014; 36(9):1376-84
39. Resnick IB, Barkats C, Shapira MY, et al. Treatment of severe steroid resistant acute GVHD with mesenchymal stromal cells (MSC). Am J Blood Res 2013;3(3):225-38
40. Peng Y, Chen X, Liu Q, et al. Mesenchymal stromal cells infusions improve refractory chronic graft versus host disease through an increase of CD5+ regulatory B cells producing interleukin 10. Leukemia 2015;29(3):636-46
41. Weng J, He C, Lai P, et al. Mesenchymal stromal cells treatment attenuates dry eye in patients with chronic graft-versus-host disease. Mol Ther 2012;20(12):2347-54
42. Ringden O, Uzunel M, Rasmusson I, et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 2006;81(10):1390-7
43. Wu Y, Cao Y, Li X, et al. Cotransplantation of haploidentical hematopoietic and umbilical cord mesenchymal stem cells for severe aplastic anemia: successful engraftment and mild GVHD. Stem Cell Res 2014;12(1):132-8
44. Wu Y, Wang Z, Cao Y, et al. Cotransplantation of haploidentical hematopoietic and umbilical cord mesenchymal stem cells with a myeloablative regimen for refractory/ relapsed hematologic malignancy. Ann Hematol 2013;92(12):1675-84
45. Liu K, Chen Y, Zeng Y, et al. Coinfusion of mesenchymal stromal cells facilitates platelet recovery without increasing leukemia recurrence in haploidentical hematopoietic stem cell transplantation: a randomized, controlled clinical study. Stem Cells Dev 2011;20(10):1679-85
46. Ning H, Yang F, Jiang M, et al. The correlation between cotransplantation of mesenchymal stem cells and higher recurrence rate in hematologic malignancy patients: outcome of a pilot clinical study. Leukemia 2008;22(3):593-9
47. Ciccocioppo R, Bernardo ME, Sgarella A, et al. Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 2011; 60(6):788-98
48. Peng L, Xie D, Lin BL, et al. Autologous bone marrow mesenchymal stem cell transplantation in liver failure patients caused by hepatitis B: short-term and long-term outcomes. Hepatology 2011;54: 820-8
49. Peng Y, Ke M, Xu L, et al. Donor-derived mesenchymal stem cells combined with low-dose tacrolimus prevent acute rejection after renal transplantation: a clinical pilot study. Transplantation 2013;95(1):161-8
50. Xu LM, Gong YW, Wang BF, et al. Randomized trial of autologous bone marrow mesenchymal stem cells transplantation for hepatitis B virus cirrhosis: regulation of Treg/Th17 cells. J Gastroenterol Hepatol 2014;29(8):1620-8
51. Amin MA, Sabry D, Rashed LA, et al. Short-term evaluation of autologous transplantation of bone marrow-derived mesenchymal stem cells in patients with cirrhosis: Egyptian study. Clin Transplant 2013;27(4):607-12
52. El-Ansary M, Mogawer S, Abdel-Aziz I, et al. Trial: mesenchymal stem cells transplantation in end stage liver disease. Stem Cell 2010;1(2):22-33
53. Mazzini L, Ferrero I, Luparello V, Rustichelli D. Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: A Phase I clinical trial. Exp Neurol 2010;223(1):229-37
54. Karussis D, Karageorgiou C, Vaknin-Dembinsky A, et al. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 2010;67(10):1187-94
55. Bonab MM, Sahraian MA, Aghsaie A, et al. Autologous mesenchymal stem cell therapy in progressive multiple sclerosis: an open label study. Curr Stem Cell Res Ther 2012; 7(6):407-14
56. Bonab MM, Yazdanbakhsh S, Lotfi J, et al. Does mesenchymal stem cell therapy help multiple sclerosis patients? Report of a pilot study. Iran J Immunol 2007;4(1):50-7
57. Kuzmina LA, Petinati NA, Parovichnikova EN, et al. Multipotent mesenchymal stromal cells for the prophylaxis of acute graft-versus-host disease-A phase II study. Stem Cells Int 2012;2012:968213
58. El-Ansary M, Abdel-Aziz I, Mogawer S, et al. Phase II Trial: undifferentiated Versus differentiated autologous mesenchymal stem cells transplantation in Egyptian patients with HCV induced liver cirrhosis. Stem Cell Rev Rep 2012;8(3):972-81
59. Connick P, Kolappan M, Crawley C, et al. Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: an open-label phase 2a proof-of-concept study. Lancet Neurol 2012;11(2):150-6
60. Yamout B, Hourani R, Salti H, et al. Bone marrow mesenchymal stem cell transplantation in patients with multiple sclerosis: a pilot study. J Neuroimmunol 2010;227(1-2):185-9
61. Mayer L, Pandak WM, Melmed GY, et al. Safety and tolerability of human placenta-derived cells (PDA001) in treatment-resistant Crohn's disease: a phase 1 study. Inflamm Bowel Dis 2013; 19(4):754-60
62. Trivedi HL, Vanikar AV, Dave SD, Thakkar UG. Cotransplantation of adipose tissue-derived insulin-secreting mesenchymal stem cells and hematopoietic stem cells: A novel therapy for insulin-dependent diabetes mellitus. Stem Cells Intl 2010;2010:582382
63. Tan J, Wu W, Xu X, et al. Induction therapy with autologous mesenchymal stem cells in living-related kidney transplants: a randomized controlled trial. J Am Med Assoc 2012;307(11):1169-77
64. Herrmann R, Sturm M, Shaw K, et al. Mesenchymal stromal cell therapy for steroid-refractory acute and chronic graft versus host disease: a phase 1 study. Int J Hematol 2012;95(2):182-8
65. Liang J, Zhang HY, Hua BZ, et al. Allogenic mesenchymal stem cells transplantation in refractory systemic lupus erythematosus: a pilot clinical study. Ann Rheum Dis 2010;69(8):1423-9
66. Sun L, Wang D, Liang J, et al. Umbilical cord mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus. Arthritis Rheum 2010;62(8): 2467-75
67. Galipeau J. The mesenchymal stromal cells dilemma-does a negative phase III trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road? Cytotherapy 2013;15(1):2-8
68. Cell therapy clinical trials failures in 2014. Available from: http://celltrials.info/2015/ 01/04/failures-2014
69. Clinical trial phase multicentric I/II to evaluate safety in patients with amyotrophic sclerosis lateral. Available from: https:// clinicaltrials.gov/ct2/show/NCT02290886
70. Phase 2, randomized, double blind, placebo controlled multicenter study of autologous MSC-NTF cells in patients with ALS (NurOwn). Available from: www. clinicaltrials.gov/ct2/show/NCT02017912
71. A Phase IIa, single-blind, placebo-controlled, crossover, multi-center, randomized study to assess the safety, tolerability, and preliminary efficacy of a single intravenous dose of ischemia-tolerant allogeneic mesenchymal bone marrow cells to subjects with heart failure of non-ischemic etiology. Available from: https://clinicaltrials.gov/ct2/show/ NCT02123706
72. Randomized clinical trial of intravenous infusion umbilical cord mesenchymal stem cells on cardiopathy (RIMECARD). Available from: https://clinicaltrials.gov/ct2/ show/NCT01739777
73. Mesenchymal stem cells to intervene in the development of Type 1 diabetes: a blinded randomized study. Available from: https:// clinicaltrials.gov/ct2/show/NCT02057211
74. Phase I-II clinical trial with autologous bone marrow derived mesenchymal stem cells for the therapy of multiple sclerosis. Available from: https://clinicaltrials.gov/ct2/show/ NCT02035514
75. Yin F, Battiwalla M, Ito S, et al. Bone marrow mesenchymal stromal cells to treat tissue damage in allogeneic stem cell transplant recipients: correlation of biological markers with clinical responses. Stem Cells 2014;32(5):1278-88
76. von Bonin M, Stolzel F, Goedecke A, et al. Treatment of refractory acute GVHD with third-party MSC expanded in platelet lysate-containing medium. Bone Marrow Transplant 2009;43(3):245-51
77. Peng Y, Chen X, Liu Q, et al. Alteration of naive and memory B-cell subset in chronic graft-versus-host disease patients after treatment with mesenchymal stromal cells. Stem Cells Transl Med 2014;3(9):1023-31
78. Weng JY, Du X, Geng SX, et al. Mesenchymal stem cell as salvage treatment for refractory chronic GVHD. Bone Marrow Transplant 2010;45(12):1732-40
79. Perez-Simon JA, Lopez-Villar O, Andreu EJ, et al. Mesenchymal stem cells expanded in vitro with human serum for the treatment of acute and chronic graft-versus-host disease: results of a phase I/II clinical trial. Haematologica 2011;96(7):1072-6
80. Zhang X, Li JY, Cao K, et al. Cotransplantation of HLA-identical mesenchymal stem cells and hematopoietic stem cells in Chinese patients with hematologic diseases. Int J Lab Hematol 2010;32(2):256-64
81. Xu J, Wang D, Liu D, et al. Allogeneic mesenchymal stem cell treatment alleviates experimental and clinical Sjögren syndrome. Blood 2012;120(15):3142-51
82. Gu F, Wang D, Zhang H, et al. Allogeneic mesenchymal stem cell transplantation for lupus nephritis patients refractory to conventional therapy. Clin Rheumatol 2014;33(11):1611-19
83. Wang D, Zhang H, Liang J, et al. Allogeneic mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus: 4 years of experience. Cell Transplant 2013;22(12): 2267-77
84. El-Ansary M, Saadi G, Abd El-Hamid SM. Mesenchymal stem cells are a rescue approach for recovery of deteriorating kidney function. Nephrology 2012;17(7): 650-7
85. Wang D, Akiyama K, Zhang H, et al. Double allogenic mesenchymal stem cells transplantations could not enhance therapeutic effect compared with single transplantation in systemic lupus erythematosus. Clin Dev Immunol 2012;2012:273291