Changes in immunological profile of allogeneic mesenchymal stem cells after differentiation: Should we be concerned?

Stem Cell Research and Therapy

Volumn 5, Issue 4, 2014, Pages

  Lohan, Paul ^a   Coleman, Cynthia M ^a   Murphy, J Mary ^a   Griffin, Matthew D ^a   Ritter, Thomas ^a   Ryan, Aideen E ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROSTAGLANDIN E2;

BONE; BONE DEFECT; CARTILAGE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL INFILTRATION; CELL PROLIFERATION; CELL SURFACE; CELL THERAPY; CHONDROPATHY; HEART; HEART DISEASE; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IN VIVO STUDY; MESENCHYMAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; TISSUE REGENERATION; BIOLOGICAL THERAPY; BONE REGENERATION; CARDIAC MUSCLE; CELLULAR IMMUNITY; CYTOLOGY; GRAFT REJECTION; HUMORAL IMMUNITY; IMMUNOLOGY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; PHYSIOLOGY; REGENERATION;

BONE REGENERATION; CARTILAGE; CELL DIFFERENTIATION; CELL- AND TISSUE-BASED THERAPY; GRAFT REJECTION; HEART; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MYOCARDIUM; REGENERATION;

EID: 84908323131     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt488     Document Type: Review

References (60)

1. Historic landmarks in clinical transplantation: conclusions from the consensus conference at the University of California, Los Angeles. CG Groth, LB Brent, RY Calne, JB Dausset, RA Good, JE Murray, NE Shumway, RS Schwartz, TE Starzl, PI Terasaki, ED Thomas, JJ van Rood, World J Surg 2000 24 834 843 10.1007/s002680010134 10833252
2. Anti-donor immune responses elicited by allogeneic mesenchymal stem cells: what have we learned so far? MD Griffin, AE Ryan, S Alagesan, P Lohan, O Treacy, T Ritter, Immunol Cell Biol 2013 91 40 51 10.1038/icb.2012.67 23207278
3. Autologous and allogeneic mesenchymal stem cells in organ transplantation: what do we know about their safety and efficacy? S Alagesan, MD Griffin, Curr Opin Organ Transplant 2014 19 65 72 10.1097/MOT.0000000000000043 24370985
4. Mechanisms of rejection: current perspectives. KJ Wood, R Goto, Transplantation 2012 93 1 10 10.1097/TP.0b013e31823cab44 22138818
5. Chondrogenic differentiation increases anti-donor immune response to allogeneic mesenchymal stem cell (MSC) transplantation. AE Ryan, P Lohan, L O'Flynn, O Treacy, X Chen, C Coleman, G Shaw, M Murphy, F Barry, MD Griffin, T Ritter, Mol Ther 2013 22 655 667 24184966
6. Differentiation of allogeneic mesenchymal stem cells induces immunogenicity and limits their long-term benefits for myocardial repair. X Huang, Z Sun, Y Miyagi, H McDonald Kinkaid, L Zhang, R Weisel, RK Li, Circulation 2010 122 2419 2429 10.1161/CIRCULATIONAHA.110.955971 21098445
7. The immunogenicity and immunomodulatory function of osteogenic cells differentiated from mesenchymal stem cells. H Liu, DM Kemeny, BC Heng, HW Ouyang, AJ Melendez, T Cao, J Immunol 2006 176 2864 2871 10.4049/jimmunol.176.5.2864 16493043
8. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. C Toma, MF Pittenger, KS Cahill, BJ Byrne, PD Kessler, Circulation 2002 105 93 98 10.1161/hc0102.101442 11772882
9. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. M Dominici, K Le Blanc, I Mueller, I Slaper-Cortenbach, F Marini, D Krause, R Deans, A Keating, D Prockop, E Horwitz, Cytotherapy 2006 8 315 317 10.1080/14653240600855905 16923606
10. Characterization of fibroblastic stromal cells from murine bone marrow. AH Piersma, KG Brockbank, RE Ploemacher, E van Vliet, KM Brakel-van Peer, PJ Visser, Exp Hematol 1985 13 237 243 2580729
11. Mesenchymal stem cell-based therapy: a new paradigm in regenerative medicine. NK Satija, VK Singh, YK Verma, P Gupta, S Sharma, F Afrin, M Sharma, P Sharma, RP Tripathi, GU Gurudutta, J Cell Mol Med 2009 13 4385 4402 19602034
12. Differentiation of human umbilical cord mesenchymal stromal cells into low immunogenic hepatocyte-like cells. Q Zhao, H Ren, X Li, Z Chen, X Zhang, W Gong, Y Liu, T Pang, ZC Han, Cytotherapy 2009 11 414 426 10.1080/14653240902849754 19513901
13. Immunostimulatory effects of mesenchymal stem cell-derived neurons: implications for stem cell therapy in allogeneic transplantations. MD Castillo, KA Trzaska, SJ Greco, NM Ponzio, P Rameshwar, Clin Transl Sci 2008 1 27 34 10.1111/j.1752-8062.2008.00018.x 20443815
14. Immunogenicity of allogeneic mesenchymal stem cells. S Schu, M Nosov, L O'Flynn, G Shaw, O Treacy, F Barry, M Murphy, T O'Brien, T Ritter, J Cell Mol Med 2012 16 2094 2103 22151542
15. Immunomodulatory properties of mesenchymal stromal cells. AJ Nauta, WE Fibbe, Blood 2007 110 3499 3506 10.1182/blood-2007-02-069716 17664353
16. Mesenchymal stem cell inhibition of T-helper 17 cell-differentiation is triggered by cell-cell contact and mediated by prostaglandin E2 via the EP4 receptor. MM Duffy, J Pindjakova, SA Hanley, C McCarthy, GA Weidhofer, EM Sweeney, K English, G Shaw, JM Murphy, FP Barry, BP Mahon, O Belton, R Ceredig, MD Griffin, Eur J Immunol 2011 41 2840 2851 10.1002/eji.201141499 21710489
17. Mechanisms of mesenchymal stromal cell immunomodulation. K English, Immunol Cell Biol 2013 91 19 26 10.1038/icb.2012.56 23090487
18. Preserving prostaglandin E2 level prevents rejection of implanted allogeneic mesenchymal stem cells and restores postinfarction ventricular function. S Dhingra, P Li, XP Huang, J Guo, J Wu, A Mihic, SH Li, WF Zang, D Shen, RD Weisel, PK Singal, RK Li, Circulation 2013 128 69 S78 10.1161/CIRCULATIONAHA.112.000324 24030423
19. Mesenchymal stem cells secrete factors that inhibit inflammatory processes in short-term osteoarthritic synovium and cartilage explant culture. GM van Buul, E Villafuertes, PK Bos, JH Waarsing, N Kops, R Narcisi, H Weinans, JA Verhaar, MR Bernsen, GJ van Osch, Osteoarthritis Cartilage 2012 20 1186 1196 10.1016/j.joca.2012.06.003 22771777
20. Human mesenchymal stem/stromal cells cultured as spheroids are self-activated to produce prostaglandin E2 that directs stimulated macrophages into an anti-inflammatory phenotype. JH Ylostalo, TJ Bartosh, K Coble, DJ Prockop, Stem Cells 2012 30 2283 2296 10.1002/stem.1191 22865689
21. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. G Ren, L Zhang, X Zhao, G Xu, Y Zhang, AI Roberts, RC Zhao, Y Shi, Cell Stem Cell 2008 2 141 150 10.1016/j.stem.2007.11.014 18371435
22. Mesenchymal stromal cells and regulatory T cells: the Yin and Yang of peripheral tolerance? SP Burr, F Dazzi, OA Garden, Immunol Cell Biol 2013 91 12 18 10.1038/icb.2012.60 23146942
23. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. S Beyth, Z Borovsky, D Mevorach, M Liebergall, Z Gazit, H Aslan, E Galun, J Rachmilewitz, Blood 2005 105 2214 2219 10.1182/blood-2004-07-2921 15514012
24. Age of the donor reduces the ability of human adipose-derived stem cells to alleviate symptoms in the experimental autoimmune encephalomyelitis mouse model. BA Scruggs, JA Semon, X Zhang, S Zhang, AC Bowles, AC Pandey, KM Imhof, AV Kalueff, JM Gimble, BA Bunnell, Stem Cells Transl Med 2013 2 797 807 10.5966/sctm.2013-0026 24018793
25. Mesenchymal stem cells from umbilical cord matrix, adipose tissue and bone marrow exhibit different capability to suppress peripheral blood B, natural killer and T cells. A Ribeiro, P Laranjeira, S Mendes, I Velada, C Leite, P Andrade, F Santos, A Henriques, M Grãos, CM Cardoso, A Martinho, M Pais, CL da Silva, J Cabral, H Trindade, A Paiva, Stem Cell Res Ther 2013 4 125 10.1186/scrt336 24406104
26. Mesenchymal stem cells are injured by complement after their contact with serum. Y Li, F Lin, Blood 2012 120 3436 3443 10.1182/blood-2012-03-420612 22966167
27. Stroke CDfHDa. CDC Division for Heart Disease and Stroke Prevention: Data Trends & Maps, [ http://nccd.cdc.gov/DHDSP-DTM/LocationSummary.aspx?state=United+States ]
28. Osteoarthritis. CDC, [ http://www.cdc.gov/arthritis/basics/osteoarthritis.htm ]
29. Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. K Le Blanc, C Gotherstrom, O Ringden, M Hassan, R McMahon, E Horwitz, G Anneren, O Axelsson, J Nunn, U Ewald, S Nordén-Lindeberg, M Jansson, A Dalton, E Aström, M Westgren, Transplantation 2005 79 1607 1614 10.1097/01.TP.0000159029.48678.93 15940052
30. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. EM Horwitz, PL Gordon, WKK Koo, JC Marx, MD Neel, RY McNall, L Muul, T Hofmann, Proc Natl Acad Sci U S A 2002 99 8932 8937 10.1073/pnas.132252399 12084934
31. Bone regeneration potential of allogeneic or autogeneic mesenchymal stem cells loaded onto cancellous bone granules in a rabbit radial defect model. SH Kang, YG Chung, IH Oh, YS Kim, KO Min, JY Chung, Cell Tissue Res 2014 355 81 88 10.1007/s00441-013-1738-z 24169864
32. Allogeneic mesenchymal stem cells regenerate bone in a critical-sized canine segmental defect. TL Arinzeh, SJ Peter, MP Archambault, C van den Bos, S Gordon, K Kraus, A Smith, S Kadiyala, J Bone Joint Surg Am 2003 85-A 1927 1935 14563800
33. From isolation to implantation: a concise review of mesenchymal stem cell therapy in bone fracture repair. L Watson, CM Coleman, SJ Elliman, Stem Cell Res Ther 2014 5 51 10.1186/scrt439 25099622
34. In vivo survival and osteogenic differentiation of allogeneic rat bone marrow mesenchymal stem cells (MSCs). N Kotobuki, Y Katsube, Y Katou, M Tadokoro, M Hirose, H Ohgushi, Cell Transplant 2008 17 705 712 10.3727/096368908786092793 18819258
35. Suppression of the immune system as a critical step for bone formation from allogeneic osteoprogenitors implanted in rats. A Chatterjea, VL Lapointe, J Alblas, S Chatterjea, CA van Blitterswijk, J de Boer, J Cell Mol Med 2013 18 134 142 24237965
36. Allogeneic adipose-derived stem cells with low immunogenicity constructing tissue-engineered bone for repairing bone defects in pigs. ML Ren, W Peng, ZL Yang, XJ Sun, SC Zhang, ZG Wang, B Zhang, Cell Transplant 2012 21 2711 2721 10.3727/096368912X654966 22963757
37. Immunogenicity and immune modulation of osteogenic differentiated mesenchymal stem cells from Banna minipig inbred line. L Wang, XF Lu, YR Lu, J Liu, K Gao, YZ Zeng, YP Li, JQ Cheng, WD Tan, L Wan, Transplant Proc 2006 38 2267 2269 10.1016/j.transproceed.2006.06.048 16980061
38. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. K Le Blanc, C Tammik, K Rosendahl, E Zetterberg, O Ringden, Exp Hematol 2003 31 890 896 10.1016/S0301-472X(03)00110-3 14550804
39. Pre- and postnatal transplantation of fetal mesenchymal stem cells in osteogenesis imperfecta: a two-center experience. C Gotherstrom, M Westgren, SW Shaw, E Astrom, A Biswas, PH Byers, CN Mattar, GE Graham, J Taslimi, U Ewald, NM Fisk, AE Yeoh, JL Lin, PJ Cheng, M Choolani, K Le Blanc, JK Chan, Stem Cells Transl Med 2013 3 255 264 24342908
40. Mesenchymal stem cells and their potential as cardiac therapeutics. M Pittenger, B Martin, Circulation Res 2004 95 9 20 10.1161/01.RES.0000135902.99383.6f 15242981
41. Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. N Nagaya, T Fujii, T Iwase, H Ohgushi, T Itoh, M Uematsu, M Yamagishi, H Mori, K Kangawa, S Kitamura, Am J Physiol Heart Circ Physiol 2004 287 2670 H2676 15284059
42. Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity. HC Quevedo, KE Hatzistergos, BN Oskouei, GS Feigenbaum, JE Rodriguez, D Valdes, PM Pattany, JP Zambrano, Q Hu, I McNiece, AW Heldman, JM Hare, Proc Natl Acad Sci U S A 2009 106 14022 14027 10.1073/pnas.0903201106 19666564
43. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. LC Amado, AP Saliaris, KH Schuleri, M St John, JS Xie, S Cattaneo, DJ Durand, T Fitton, JQ Kuang, G Stewart, S Lehrke, WW Baumgartner, BJ Martin, AW Heldman, JM Hare, Proc Natl Acad Sci U S A 2005 102 11474 11479 10.1073/pnas.0504388102 16061805
44. Intramyocardial injection of allogenic bone marrow-derived mesenchymal stem cells without immunosuppression preserves cardiac function in a porcine model of myocardial infarction. RR Makkar, MJ Price, M Lill, M Frantzen, K Takizawa, T Kleisli, J Zheng, S Kar, R McClelan, T Miyamota, J Bick-Forrester, MC Fishbein, PK Shah, JS Forrester, B Sharifi, PS Chen, M Qayyum, J Cardiovasc Pharmacol Ther 2005 10 225 233 10.1177/107424840501000403 16382259
45. Comparison of intracoronary and transendocardial delivery of allogeneic mesenchymal cells in a canine model of acute myocardial infarction. EC Perin, GV Silva, JA Assad, D Vela, LM Buja, AL Sousa, S Litovsky, J Lin, WK Vaughn, S Coulter, MR Fernandes, JT Willerson, J Mol Cell Cardiol 2008 44 486 495 10.1016/j.yjmcc.2007.09.012 18061611
46. Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium: short- and long-term effects. W Dai, SL Hale, BJ Martin, JQ Kuang, JS Dow, LE Wold, RA Kloner, Circulation 2005 112 214 223 10.1161/CIRCULATIONAHA.104.527937 15998673
47. Imaging the survival and utility of pre-differentiated allogeneic MSC in ischemic heart. C Xia, J Cao, Biochem Biophys Res Commun 2013 438 382 387 10.1016/j.bbrc.2013.07.084 23899528
48. Intracoronary infusion of allogeneic mesenchymal precursor cells directly after experimental acute myocardial infarction reduces infarct size, abrogates adverse remodeling, and improves cardiac function. JH Houtgraaf, R de Jong, K Kazemi, D de Groot, TI van der Spoel, F Arslan, I Hoefer, G Pasterkamp, S Itescu, F Zijlstra, ML Geleijnse, PW Serruys, HJ Duckers, Circ Res 2013 113 153 166 10.1161/CIRCRESAHA.112.300730 23658436
49. Challenges in allogeneic mesenchymal stem cell-mediated cardiac repair. S Dhingra, XP Huang, RK Li, Trends Cardiovasc Med 2010 20 263 268 10.1016/j.tcm.2011.12.002 22433652
50. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. JM Hare, JH Traverse, TD Henry, N Dib, RK Strumpf, SP Schulman, G Gerstenblith, AN DeMaria, AE Denktas, RS Gammon, JB Hermiller Jr, MA Reisman, GL Schaer, W Sherman, J Am Coll Cardiol 2009 54 2277 2286 10.1016/j.jacc.2009.06.055 19958962
51. Mesenchymal stem cells for cartilage repair in osteoarthritis. PK Gupta, AK Das, A Chullikana, AS Majumdar, Stem Cell Res Ther 2012 3 25 10.1186/scrt116 22776206
52. Mesenchymal stem cells in osteoarticular diseases. C Jorgensen, D Noel, Regen Med 2011 6 44 51 10.2217/rme.11.80 21999261
53. Allogeneic mesenchymal stem cell and mesenchymal stem cell-differentiated chondrocyte suppress the responses of type II collagen-reactive T cells in rheumatoid arthritis. ZH Zheng, XY Li, J Ding, JF Jia, P Zhu, Rheumatology (Oxford) 2008 47 22 30 10.1093/rheumatology/kem284
54. Chondrogenic differentiation alters the immunosuppressive property of bone marrow-derived mesenchymal stem cells, and the effect is partially due to the upregulated expression of B7 molecules. X Chen, A McClurg, GQ Zhou, M McCaigue, MA Armstrong, G Li, Stem Cells 2007 25 364 370 10.1634/stemcells.2006-0268 17068184
55. Adipose tissue-derived stem cells show both immunogenic and immunosuppressive properties after chondrogenic differentiation. A Technau, K Froelich, R Hagen, N Kleinsasser, Cytotherapy 2011 13 310 317 10.3109/14653249.2010.504769 20795757
56. Genetic mismatch affects the immunosuppressive properties of mesenchymal stem cells in vitro and their ability to influence the course of collagen-induced arthritis. C Sullivan, JM Murphy, MD Griffin, RM Porter, CH Evans, C O'Flatharta, G Shaw, F Barry, Arthritis Res Ther 2012 14 167 10.1186/ar3916 22812502
57. Pathways of allorecognition: implications for transplantation tolerance. DS Game, RI Lechler, Transpl Immunol 2002 10 101 108 10.1016/S0966-3274(02)00055-2 12216939
58. Pretreatment with interferon-gamma enhances the therapeutic activity of mesenchymal stromal cells in animal models of colitis. M Duijvestein, ME Wildenberg, MM Welling, S Hennink, I Molendijk, VL van Zuylen, T Bosse, AC Vos, ES de Jonge-Muller, H Roelofs, L van der Weerd, HW Verspaget, WE Fibbe, AA te Velde, GR van den Brink, DW Hommes, Stem Cells 2011 29 1549 1558 10.1002/stem.698 21898680
59. Encapsulated islets transplantation: past, present and future. N Sakata, S Sumi, G Yoshimatsu, M Goto, S Egawa, M Unno, World J Gastrointest Pathophysiol 2012 3 19 26 10.4291/wjgp.v3.i1.19 22368783
60. Decline of surface MHC I by adenoviral gene transfer of anti-MHC I intrabodies in human endothelial cells-new perspectives for the generation of universal donor cells for tissue transplantation. F Beyer, C Doebis, A Busch, T Ritter, A Mhashilkar, WM Marasco, H Laube, HD Volk, M Seifert, J Gene Med 2004 6 616 623 10.1002/jgm.548 15170732