The clinical application of mesenchymal stem cells and cardiac stem cells as a therapy for cardiovascular disease

Pharmacology and Therapeutics

Volumn 151, Issue , 2015, Pages 8-15

  Kim, Jiyeon ^a   Shapiro, Linda ^a   Flynn, Aidan ^a,b  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b HARTFORD HOSPITAL   (United States)

Author keywords

Cardiac stem cell; Cardiovascular disease; Clinical trial; Mesenchymal stem cell; Pre conditioning; Therapy

Indexed keywords

PLACEBO; SIMVASTATIN; TRIMETAZIDINE;

ACUTE HEART INFARCTION; ADIPOSE TISSUE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BONE MARROW DERIVED MONONUCLEAR CELL; CARDIAC STEM CELL; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CELL HYPOXIA; CELL POPULATION; CLINICAL EVALUATION; CLINICAL TRIAL (TOPIC); ENGRAFTMENT; HEART FAILURE; HEART MUSCLE; HUMAN; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; PRIORITY JOURNAL; REVIEW; ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; STEM CELL TRANSPLANTATION; TISSUE REPAIR; TRANSLATIONAL RESEARCH; ANIMAL; CARDIOVASCULAR DISEASES; CYTOLOGY; IMMUNOSUPPRESSIVE TREATMENT; MESENCHYMAL STROMA CELL; METABOLISM;

ANIMALS; CARDIOVASCULAR DISEASES; CLINICAL TRIALS AS TOPIC; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MYOCARDIUM; STEM CELL TRANSPLANTATION; TRANSPLANTATION CONDITIONING;

EID: 84930082728     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2015.02.003     Document Type: Review

References (83)

1. L.C. Amado, A.P. Saliaris, K.H. Schuleri, M. St John, J.S. Xie, and S. Cattaneo Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction Proc Natl Acad Sci U S A 102 2005 11474 11479
2. R. Atoui, and R.C. Chiu Concise review: immunomodulatory properties of mesenchymal stem cells in cellular transplantation: update, controversies, and unknowns Stem Cells Transl Med 1 2012 200 205
3. J. Bartunek, A. Behfar, D. Dolatabadi, M. Vanderheyden, M. Ostojic, and J. Dens Cardiopoietic stem cell therapy in heart failure: the C-CURE (Cardiopoietic stem Cell therapy in heart failURE) multicenter randomized trial with lineage-specified biologics J Am Coll Cardiol 61 2013 2329 2338
4. J. Bartunek, J.D. Croissant, W. Wijns, S. Gofflot, A. de Lavareille, and M. Vanderheyden Pretreatment of adult bone marrow mesenchymal stem cells with cardiomyogenic growth factors and repair of the chronically infarcted myocardium Am J Physiol Heart Circ Physiol 292 2007 H1095 H1104
5. A. Behfar, S. Yamada, R. Crespo-Diaz, J.J. Nesbitt, L.A. Rowe, and C. Perez-Terzic Guided cardiopoiesis enhances therapeutic benefit of bone marrow human mesenchymal stem cells in chronic myocardial infarction J Am Coll Cardiol 56 2010 721 734
6. A.P. Beltrami, L. Barlucchi, D. Torella, M. Baker, F. Limana, and S. Chimenti Adult cardiac stem cells are multipotent and support myocardial regeneration Cell 114 2003 763 776
7. R. Bolli, A.R. Chugh, D. D'Amario, J.H. Loughran, M.F. Stoddard, and S. Ikram Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial Lancet 378 2011 1847 1857
8. M. Breitbach, T. Bostani, W. Roell, Y. Xia, O. Dewald, and J.M. Nygren Potential risks of bone marrow cell transplantation into infarcted hearts Blood 110 2007 1362 1369
9. S.M. Chacko, S. Ahmed, K. Selvendiran, M.L. Kuppusamy, M. Khan, and P. Kuppusamy Hypoxic preconditioning induces the expression of prosurvival and proangiogenic markers in mesenchymal stem cells Am J Physiol Cell Physiol 299 2010 C1562 C1570
10. G. Chamberlain, J. Fox, B. Ashton, and J. Middleton Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing Stem Cells 25 2007 2739 2749
11. S.L. Chen, W.W. Fang, F. Ye, Y.H. Liu, J. Qian, and S.J. Shan 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 2004 92 95
12. A.R. Chugh, G.M. Beache, J.H. Loughran, N. Mewton, J.B. Elmore, and J. Kajstura Administration of cardiac stem cells in patients with ischemic cardiomyopathy: the SCIPIO trial: surgical aspects and interim analysis of myocardial function and viability by magnetic resonance Circulation 126 2012 S54 S64
13. Meirelles L. da Silva, P.C. Chagastelles, and N.B. Nardi Mesenchymal stem cells reside in virtually all post-natal organs and tissues J Cell Sci 119 Pt 11 2006 2204 2213
14. R.A. Fenton, E.W. Dickson, and J.G. Dobson Jr. Inhibition of phosphatase activity enhances preconditioning and limits cell death in the ischemic/reperfused aged rat heart Life Sci 77 2005 3375 3388
15. M. Gnecchi, H. He, O.D. Liang, L.G. Melo, F. Morello, and H. Mu Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells Nat Med 11 2005 367 368
16. M. Gnecchi, Z. Zhang, A. Ni, and V.J. Dzau Paracrine mechanisms in adult stem cell signaling and therapy Circ Res 103 2008 1204 1219
17. A.S. Go, D. Mozaffarian, V.L. Roger, E.J. Benjamin, J.D. Berry, and M.J. Blaha Heart disease and stroke statistics - 2014 update: a report from the American Heart Association Circulation 129 2014 e28 e292
18. J.Y. Hahn, H.J. Cho, H.J. Kang, T.S. Kim, M.H. Kim, and J.H. Chung Pre-treatment of mesenchymal stem cells with a combination of growth factors enhances gap junction formation, cytoprotective effect on cardiomyocytes, and therapeutic efficacy for myocardial infarction J Am Coll Cardiol 51 2008 933 943
19. J.M. Hare, J.E. Fishman, G. Gerstenblith, D.L. DiFede Velazquez, J.P. Zambrano, and V.Y. Suncion Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial JAMA 308 22 2012 2369 2379
20. Erratum in: JAMA. 2013 Aug 21;310(7):750
21. P.A. Heidenreich, J.G. Trogdon, O.A. Khavjou, J. Butler, K. Dracup, and M.D. Ezekowitz Forecasting the future of cardiovascular disease in the United States: a policy statement from the American Heart Association Circulation 123 2011 933 944
22. A.W. Heldman, D.L. DiFede, J.E. Fishman, J.P. Zambrano, B.H. Trachtenberg, and V. Karantalis Transendocardial mesenchymal stem cells and mononuclear bone marrow cells for ischemic cardiomyopathy: the TAC-HFT randomized trial J Am Med Assoc 311 2014 62 73
23. D.L. Hoyert, M.P. Heron, S.L. Murphy, and H.C. Kung Deaths: final data for 2003 Natl Vital Stat Rep 54 2006 1 120
24. X. Hu, S.P. Yu, J.L. Fraser, Z. Lu, M.E. Ogle, and J.A. Wang Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis J Thorac Cardiovasc Surg 135 2008 799 808
25. J. Huang, J. Guo, F. Beigi, C.P. Hodgkinson, H.T. Facundo, and Z. Zhang HASF is a stem cell paracrine factor that activates PKC epsilon mediated cytoprotection J Mol Cell Cardiol 66 2014 157 164
26. V. Jeevanantham, M. Butler, A. Saad, A. Abdel-Latif, E.K. Zuba-Surma, and B. Dawn Adult bone marrow cell therapy improves survival and induces long-term improvement in cardiac parameters: a systematic review and meta-analysis Circulation 126 2012 551 568
27. V. Karantalis, D.L. DiFede, G. Gerstenblith, S. Pham, J. Symes, and J.P. Zambrano Autologous mesenchymal stem cells produce concordant improvements in regional function, tissue perfusion, and fibrotic burden when administered to patients undergoing coronary artery bypass grafting: the Prospective Randomized Study of Mesenchymal Stem Cell Therapy in Patients Undergoing Cardiac Surgery (PROMETHEUS) trial Circ Res 114 2014 1302 1310
28. H. Kawada, J. Fujita, K. Kinjo, Y. Matsuzaki, M. Tsuma, and H. Miyatake Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction Blood 104 2004 3581 3587
29. H.W. Kim, H.K. Haider, S. Jiang, and M. Ashraf Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting caspase-8-associated protein 2 J Biol Chem 284 2009 33161 33168
30. K.L. Laugwitz, A. Moretti, J. Lam, P. Gruber, Y. Chen, and S. Woodard Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages Nature 433 2005 647 653
31. K. Le Blanc, and O. Ringden Immunomodulation by mesenchymal stem cells and clinical experience J Intern Med 262 2007 509 525
32. K. Le Blanc, C. Tammik, K. Rosendahl, E. Zetterberg, and O. Ringden HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells Exp Hematol 31 2003 890 896
33. W. Li, N. Ma, L.L. Ong, C. Nesselmann, C. Klopsch, and Y. Ladilov Bcl-2 engineered MSCs inhibited apoptosis and improved heart function Stem Cells 25 2007 2118 2127
34. S.Y. Lim, Y.S. Kim, Y. Ahn, M.H. Jeong, M.H. Hong, and S.Y. Joo The effects of mesenchymal stem cells transduced with Akt in a porcine myocardial infarction model Cardiovasc Res 70 2006 530 542
35. A. Linke, P. Muller, D. Nurzynska, C. Casarsa, D. Torella, and A. Nascimbene Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function Proc Natl Acad Sci U S A 102 2005 8966 8971
36. A.D. Lopez, C.D. Mathers, M. Ezzati, D.T. Jamison, and C.J. Murray Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data Lancet 367 2006 1747 1757
37. R.R. Makkar, R.R. Smith, K. Cheng, K. Malliaras, L.E. Thomson, and D. Berman Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial Lancet 379 2012 895 904
38. K. Malliaras, Y. Zhang, J. Seinfeld, G. Galang, E. Tseliou, and K. Cheng Cardiomyocyte proliferation and progenitor cell recruitment underlie therapeutic regeneration after myocardial infarction in the adult mouse heart EMBO Mol Med 5 2013 191 209
39. A.A. Mangi, N. Noiseux, D. Kong, H. He, M. Rezvani, and J.S. Ingwall Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts Nat Med 9 2003 1195 1201
40. C.M. Martin, A.P. Meeson, S.M. Robertson, T.J. Hawke, J.A. Richardson, and S. Bates Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart Dev Biol 265 2004 262 275
41. T. Matsui, J. Tao, F. del Monte, K.H. Lee, L. Li, and M. Picard Akt activation preserves cardiac function and prevents injury after transient cardiac ischemia in vivo Circulation 104 2001 330 335
42. E. Messina, L. De Angelis, G. Frati, S. Morrone, S. Chimenti, and F. Fiordaliso Isolation and expansion of adult cardiac stem cells from human and murine heart Circ Res 95 2004 911 921
43. Y. Miyahara, N. Nagaya, M. Kataoka, B. Yanagawa, K. Tanaka, and H. Hao Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction Nat Med 12 2006 459 465
44. M. Mollova, K. Bersell, S. Walsh, J. Savla, L.T. Das, and S.Y. Park Cardiomyocyte proliferation contributes to heart growth in young humans Proc Natl Acad Sci U S A 110 2013 1446 1451
45. A. Moretti, L. Caron, A. Nakano, J.T. Lam, A. Bernshausen, and Y. Chen Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification Cell 127 2006 1151 1165
46. L.A. Mylotte, A.M. Duffy, M. Murphy, T. O'Brien, A. Samali, and F. Barry Metabolic flexibility permits mesenchymal stem cell survival in an ischemic environment Stem Cells 26 2008 1325 1336
47. A.J. Nauta, and W.E. Fibbe Immunomodulatory properties of mesenchymal stromal cells Blood 110 2007 3499 3506
48. N. Noiseux, M. Gnecchi, M. Lopez-Ilasaca, L. Zhang, S.D. Solomon, and A. Deb Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation Mol Ther 14 2006 840 850
49. H. Oh, S.B. Bradfute, T.D. Gallardo, T. Nakamura, V. Gaussin, and Y. Mishina Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction Proc Natl Acad Sci U S A 100 2003 12313 12318
50. K.G. Oldroyd, C. Berry, and J. Bartunek Myocardial repair and regeneration: bone marrow or cardiac stem cells? Mol Ther 20 2012 1102 1105
51. D. Orlic, J. Kajstura, S. Chimenti, I. Jakoniuk, S.M. Anderson, and B. Li Bone marrow cells regenerate infarcted myocardium Nature 410 6829 2001 701 705
52. E.C. Perin, G.V. Silva, Y. Zheng, A. Gahremanpour, J. Canales, and D. Patel Randomized, double-blind pilot study of transendocardial injection of autologous aldehyde dehydrogenase-bright stem cells in patients with ischemic heart failure Am Heart J 163 3 2012 415 421
53. O. Pfister, F. Mouquet, M. Jain, R. Summer, M. Helmes, and A. Fine CD31- but not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation Circ Res 97 2005 52 61
54. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, and J.D. Mosca Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147
55. M.J. Price, C.C. Chou, M. Frantzen, T. Miyamoto, S. Kar, and S. Lee Intravenous mesenchymal stem cell therapy early after reperfused acute myocardial infarction improves left ventricular function and alters electrophysiologic properties Int J Cardiol 111 2006 231 239
56. H.C. Quevedo, K.E. Hatzistergos, B.N. Oskouei, G.S. Feigenbaum, J.E. Rodriguez, and D. Valdes Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity Proc Natl Acad Sci U S A 106 2009 14022 14027
57. V. Schächinger, S. Erbs, A. Elsässer, W. Haberbosch, R. Hambrecht, and H. Hölschermann Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction N Engl J Med 355 2006 1210 1221
58. S.E. Senyo, M.L. Steinhauser, C.L. Pizzimenti, V.K. Yang, L. Cai, and M. Wang Mammalian heart renewal by pre-existing cardiomyocytes Nature 493 2013 433 436
59. J.G. Shake, P.J. Gruber, W.A. Baumgartner, G. Senechal, J. Meyers, and J.M. Redmond Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects Ann Thorac Surg 73 2002 1919 1925 (discussion 1926)
60. J. Shujia, H.K. Haider, N.M. Idris, G. Lu, and M. Ashraf Stable therapeutic effects of mesenchymal stem cell-based multiple gene delivery for cardiac repair Cardiovasc Res 77 2008 525 533
61. N. Smart, S. Bollini, K.N. Dube, J.M. Vieira, B. Zhou, and S. Davidson De novo cardiomyocytes from within the activated adult heart after injury Nature 474 2011 640 644
62. B.E. Strauer, and G. Steinhoff 10 years of intracoronary and intramyocardial bone marrow stem cell therapy of the heart: from the methodological origin to clinical practice J Am Coll Cardiol 58 2011 1095 1104
63. V.Y. Suncion, E. Ghersin, J.E. Fishman, J.P. Zambrano, V. Karantalis, and N. Mandel Does transendocardial injection of mesenchymal stem cells improve myocardial function locally or globally?: an analysis from the Percutaneous Stem Cell Injection Delivery Effects on Neomyogenesis (POSEIDON) randomized trial Circ Res 114 2014 1292 1301
64. Y.L. Tang, Y. Tang, Y.C. Zhang, K. Qian, L. Shen, and M.I. Phillips Improved graft mesenchymal stem cell survival in ischemic heart with a hypoxia-regulated heme oxygenase-1 vector J Am Coll Cardiol 46 2005 1339 1350
65. J. Tang, J. Wang, L. Guo, X. Kong, J. Yang, and F. Zheng Mesenchymal stem cells modified with stromal cell-derived factor 1 alpha improve cardiac remodeling via paracrine activation of hepatocyte growth factor in a rat model of myocardial infarction Mol Cells 29 2010 9 19
66. Y.L. Tang, W. Zhu, M. Cheng, L. Chen, J. Zhang, and T. Sun Hypoxic preconditioning enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing CXCR4 expression Circ Res 104 2009 1209 1216
67. T. Thom, N. Haase, W. Rosamond, V.J. Howard, J. Rumsfeld, and T. Manolio Heart disease and stroke statistics - 2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee Circulation 113 2006 e85 e151
68. C. Toma, M.F. Pittenger, K.S. Cahill, B.J. Byrne, and P.D. Kessler Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart Circulation 105 2002 93 98
69. J.H. Traverse, T.D. Henry, S.G. Ellis, C.J. Pepine, J.T. Willerson, and D.X. Zhao Effect of intracoronary delivery of autologous bone marrow mononuclear cells 2 to 3 weeks following acute myocardial infarction on left ventricular function: the LateTIME randomized trial JAMA 306 2011 2110 2119
70. J.H. Traverse, T.D. Henry, C.J. Pepine, J.T. Willerson, D.X. Zhao, and S.G. Ellis Effect of the use and timing of bone marrow mononuclear cell delivery on left ventricular function after acute myocardial infarction TIME Randomized Trial 308 2012 2380 2389
71. A.R. Williams, K.E. Hatzistergos, B. Addicott, F. McCall, D. Carvalho, and V. Suncion Enhanced effect of combining human cardiac stem cells and bone marrow mesenchymal stem cells to reduce infarct size and to restore cardiac function after myocardial infarction Circulation 127 2013 213 223
72. A.R. Williams, V.Y. Suncion, F. McCall, D. Guerra, J. Mather, and J.P. Zambrano Durable scar size reduction due to allogeneic mesenchymal stem cell therapy regulates whole-chamber remodeling J Am Heart Assoc 3 2014 e000140
73. S. Wisel, M. Khan, M.L. Kuppusamy, I.K. Mohan, S.M. Chacko, and B.K. Rivera Pharmacological preconditioning of mesenchymal stem cells with trimetazidine (1-[2,3,4-trimethoxybenzyl]piperazine) protects hypoxic cells against oxidative stress and enhances recovery of myocardial function in infarcted heart through Bcl-2 expression J Pharmacol Exp Ther 329 2009 543 550
74. K.C. Wollert, G.P. Meyer, J. Lotz, S. Ringes-Lichtenberg, P. Lippolt, and C. Breidenbach Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial Lancet 364 2004 141 148
75. K.H. Wu, X.M. Mo, Z.C. Han, and B. Zhou Stem cell engraftment and survival in the ischemic heart Ann Thorac Surg 92 2011 1917 1925
76. G.D. Wu, J.A. Nolta, Y.S. Jin, M.L. Barr, H. Yu, and V.A. Starnes Migration of mesenchymal stem cells to heart allografts during chronic rejection Transplantation 75 2003 679 685
77. M.H. Yacoub, and J. Terrovitis CADUCEUS, SCIPIO, ALCADIA: cell therapy trials using cardiac-derived cells for patients with post myocardial infarction LV dysfunction, still evolving Global Cardiol Sci Pract 1 2013 5 8
78. Z.J. Yang, D.C. Ma, W. Wang, S.L. Xu, Y.Q. Zhang, and B. Chen Experimental study of bone marrow-derived mesenchymal stem cells combined with hepatocyte growth factor transplantation via noninfarct-relative artery in acute myocardial infarction Gene Ther 13 2006 1564 1568
79. Y.J. Yang, H.Y. Qian, J. Huang, J.J. Li, R.L. Gao, and K.F. Dou Combined therapy with simvastatin and bone marrow-derived mesenchymal stem cells increases benefits in infarcted swine hearts Arterioscler Thromb Vasc Biol 29 2009 2076 2082
80. B.A. Yi, O. Wernet, and K.R. Chien Pregenerative medicine: developmental paradigms in the biology of cardiovascular regeneration J Clin Invest 120 2010 20 28
81. Y. Yoshida, and S. Yamanaka iPS cells: a source of cardiac regeneration J Mol Cell Cardiol 50 2011 327 332
82. T. Yoshioka, N. Ageyama, H. Shibata, T. Yasu, Y. Misawa, and K. Takeuchi Repair of infarcted myocardium mediated by transplanted bone marrow-derived CD34+ stem cells in a nonhuman primate model Stem Cells 23 3 2005 355 364
83. B. Zhou, L.B. Honor, Q. Ma, J.H. Oh, R.Z. Lin, and J.M. Melero-Martin Thymosin beta 4 treatment after myocardial infarction does not reprogram epicardial cells into cardiomyocytes J Mol Cell Cardiol 52 2012 43 47