Stem cell-based therapies for heart regeneration: What did the bench teach us?

Cardiovascular and Hematological Disorders - Drug Targets

Volumn 10, Issue 3, 2010, Pages 173-185

  Ferreira, L ^a,b   Pedroso, D C S ^a,b   Vazao H ^a,b   Gomes, R S M ^a,b,c  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b Biocant Biotechnology Innovation Center   (Portugal)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Biomaterials; Heart regeneration; Nanoparticles and magnetic resonance imaging (MRI); Stem cells

Indexed keywords

ALGINIC ACID; BIOMATERIAL; CHONDROITIN SULFATE; COLLAGEN; DEXTRAN; FIBRIN GLUE; HYALURONIC ACID; MACROGOL;

ANGIOGENESIS; ARTICLE; BONE MARROW CELL; CELL ADHESION; CELL REGENERATION; CORD BLOOD STEM CELL TRANSPLANTATION; ELECTROCARDIOGRAM; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; FETAL STEM CELL; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; NONHUMAN; PLURIPOTENT STEM CELL; STEM CELL TRANSPLANTATION;

EID: 78549255903     PISSN: 1871529X     EISSN: None     Source Type: Journal    
DOI: 10.2174/1871529X11006030173     Document Type: Article

References (110)

1. Klug, M.G.; Soonpaa, M.H.; Koh, G.Y.; Field, L.J. Genetically selected cardiomyocytes from differentiating embryonic stem cells form stable intracardiac grafts. J. Clin. Invest., 1996, 98, 216-224.
2. Dimmeler, S.; Burchfield, J.; Zeiher, A.M. Cell-based therapy of myocardial infarction. Arterioscler. Thromb. Vasc. Biol., 2008, 28, 208-216.
3. Segers, V.F.; Lee, R.T. Stem-cell therapy for cardiac disease. Nature, 2008, 451, 937-942.
4. Yang, L.; Soonpaa, M.H.; Adler, E.D.; Roepke, T.K.; Kattman, S.J.; Kennedy, M.; Henckaerts, E.; Bonham, K.; Abbott, G.W.; Linden, R.M.; Field, L.J.; Keller, G.M. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cellderived population. Nature, 2008, 453, 524-528.
5. Laflamme, M.A.; Chen, K.Y.; Naumova, A.V.; Muskheli, V.; Fugate, J.A.; Dupras, S.K.; Reinecke, H.; Xu, C.; Hassanipour, M.; Police, S.; O'Sullivan, C.; Collins, L.; Chen, Y.; Minami, E.; Gill, E.A.; Ueno, S.; Yuan, C.; Gold, J.; Murry, C.E. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol., 2007, 25, 1015-1024.
6. Zwi, L.; Caspi, O.; Arbel, G.; Huber, I.; Gepstein, A.; Park, I.H.; Gepstein, L. Cardiomyocyte differentiation of human induced pluripotent stem cells. Circulation, 2009, 120, 1513-1523.
7. Bu, L.; Jiang, X.; Martin-Puig, S.; Caron, L.; Zhu, S.; Shao, Y.; Roberts, D.J.; Huang, P.L.; Domian, I.J.; Chien, K.R. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature, 2009, 460, 113-117.
8. Zhang, J.; Wilson, G.F.; Soerens, A.G.; Koonce, C.H.; Yu, J.; Palecek, S.P.; Thomson, J.A.; Kamp, T.J. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ. Res., 2009, 104, e30-41.
9. Van Laake, L.; Passier, R.; Monshouwerkloots, J.; Verkleij, A.; Lips, D.; Freund, C.; Denouden, K.; Wardvanoostwaard, D.; Korving, J.; Tertoolen, L. Human embryonic stem cell-derived cardiomyocytes survive and mature in the mouse heart and transiently improve function after myocardial infarction. Stem Cell Res., 2007, 1, 9-24.
10. Leor, J.; Gerecht, S.; Cohen, S.; Miller, L.; Holbova, R.; Ziskind, A.; Shachar, M.; Feinberg, M.S.; Guetta, E.; Itskovitz-Eldor, J. Human embryonic stem cell transplantation to repair the infarcted myocardium. Heart, 2007, 93, 1278-1284.
11. van Laake, L.W.; Passier, R.; den Ouden, K.; Schreurs, C.; Monshouwer-Kloots, J.; Ward-van Oostwaard, D.; van Echteld, C.J.; Doevendans, P.A.; Mummery, C.L. Improvement of mouse cardiac function by hESC-derived cardiomyocytes correlates with vascularity but not graft size. Stem Cell Res. 2009, 3, 106-112.
12. Gnecchi, M.; Zhang, Z.; Ni, A.; Dzau, V.J. Paracrine mechanisms in adult stem cell signaling and therapy. Circ. Res., 2008, 103, 1204-1219.
13. Uemura, R.; Xu, M.; Ahmad, N.; Ashraf, M. Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ. Res., 2006, 98, 1414-1421.
14. Urbich, C.; Aicher, A.; Heeschen, C.; Dernbach, E.; Hofmann, W.K.; Zeiher, A.M.; Dimmeler, S. Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. J. Mol. Cell Cardiol., 2005, 39, 733-742.
15. Gnecchi, M.; He, H.; Liang, O.D.; Melo, L.G.; Morello, F.; Mu, H.; Noiseux, N.; Zhang, L.; Pratt, R.E.; Ingwall, J.S.; Dzau, V.J. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat. Med., 2005, 11, 367-368.
16. Mazhari, R.; Hare, J.M. Mechanisms of action of mesenchymal stem cells in cardiac repair: potential influences on the cardiac stem cell niche. Nat. Clin. Pract. Cardiovasc. Med., 2007, 4 Suppl 1, S21-26.
17. Kocher, A.A.; Schuster, M.D.; Szabolcs, M.J.; Takuma, S.; Burkhoff, D.; Wang, J.; Homma, S.; Edwards, N.M.; Itescu, S. Neovascularization of ischemic myocardium by human bonemarrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat. Med., 2001, 7, 430-436.
18. Kawamoto, A.; Tkebuchava, T.; Yamaguchi, J.-I.; Nishimura, H.; Yoon, Y.-S.; Milliken, C.; Uchida, S.; Masuo, O.; Iwaguro, H.; Ma, H.; Hanley, A.; Silver, M.; Kearney, M.; Losordo, D.W.; Isner, J.M.; Asahara, T. Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation, 2003, 107, 461-468.
19. Beltrami, A.P.; Barlucchi, L.; Torella, D.; Baker, M.; Limana, F.; Chimenti, S.; Kasahara, H.; Rota, M.; Musso, E.; Urbanek, K.; Leri, A.; Kajstura, J.; Nadal-Ginard, B.; Anversa, P. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell, 2003, 114, 763-776.
20. Murry, C.E.; Field, L.J.; Menasche, P. Cell-based cardiac repair: reflections at the 10-year point. Circulation, 2005, 112, 3174-3183.
21. Marelli, D.; Desrosiers, C.; el-Alfy, M.; Kao, R.L.; Chiu, R.C. Cell transplantation for myocardial repair: an experimental approach. Cell Transplant., 1992, 1, 383-390.
22. Koh, G.Y.; Klug, M.G.; Soonpaa, M.H.; Field, L.J. Differentiation and long-term survival of C2C12 myoblast grafts in heart. J. Clin. Invest., 1993, 92, 1548-1554.
23. Muller-Ehmsen, J.; Whittaker, P.; Kloner, R.A.; Dow, J.S.; Sakoda, T.; Long, T.I.; Laird, P.W.; Kedes, L. Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. J. Mol. Cell Cardiol., 2002, 34, 107-116.
24. Hutcheson, K.A.; Atkins, B.Z.; Hueman, M.T.; Hopkins, M.B.; Glower, D.D.; Taylor, D.A. Comparison of benefits on myocardial performance of cellular cardiomyoplasty with skeletal myoblasts and fibroblasts. Cell Transplant., 2000, 9, 359-368.
25. Fujii, T.; Yau, T.M.; Weisel, R.D.; Ohno, N.; Mickle, D.A.; Shiono, N.; Ozawa, T.; Matsubayashi, K.; Li, R.K. Cell transplantation to prevent heart failure: a comparison of cell types. Ann. Thorac. Surg., 2003, 76, 2062-2070; discussion 2070.
26. Meluzin, J.; Mayer, J.; Groch, L.; Janousek, S.; Hornacek, I.; Hlinomaz, O.; Kala, P.; Panovsky, R.; Prasek, J.; Kaminek, M.; Stanicek, J.; Klabusay, M.; Koristek, Z.; Navratil, M.; Dusek, L.; Vinklarkova, J. Autologous transplantation of mononuclear bone marrow cells in patients with acute myocardial infarction: the effect of the dose of transplanted cells on myocardial function. Am. Heart J., 2006, 152, 975 e979-915.
27. Schachinger, V.; Erbs, S.; Elsasser, A.; Haberbosch, W.; Hambrecht, R.; Holschermann, H.; Yu, J.; Corti, R.; Mathey, D.; Hamm, C. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N. Engl. J. Med., 2006, 355, 1210.
28. Strauer, B.E.; Brehm, M.; Zeus, T.; Bartsch, T.; Schannwell, C.; Antke, C.; Sorg, R.V.; Kogler, G.; Wernet, P.; Muller, H.W.; Kostering, M. Regeneration of human infarcted heart muscle by intracoronary autologous bone marrow cell transplantation in chronic coronary artery disease: the IACT Study. J. Am. Coll. Cardiol., 2005, 46, 1651-1658.
29. Yao, K.; Huang, R.; Qian, J.; Cui, J.; Ge, L.; Li, Y.; Zhang, F.; Shi, H.; Huang, D.; Zhang, S.; Sun, A.; Zou, Y.; Ge, J. Administration of intracoronary bone marrow mononuclear cells on chronic myocardial infarction improves diastolic function. Heart, 2008, 94, 1147-1153.
30. Schaefer, A.; Meyer, G.P.; Fuchs, M.; Klein, G.; Kaplan, M.; Wollert, K.C.; Drexler, H. Impact of intracoronary bone marrow cell transfer on diastolic function in patients after acute myocardial infarction: results from the BOOST trial. Eur. Heart J., 2006, 27, 929-935.
31. Passier, R.; Van Laake, L.W.; Mummery, C.L. Stem-cellbased therapy and lessons from the heart. Nature, 2008, 453, 322-329.
32. Zhang, S.; Guo, J.; Zhang, P.; Liu, Y.; Jia, Z.; Ma, K.; Li, W.; Li, L.; Zhou, C. Long-term effects of bone marrow mononuclear cell transplantation on left ventricular function and remodeling in rats. Life Sci., 2004, 74, 2853-2864.
33. Orlic, D.; Kajstura, J.; Chimenti, S.; Limana, F.; Jakoniuk, I.; Quaini, F.; Nadal-Ginard, B.; Bodine, D.M.; Leri, A.; Anversa, P. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc. Natl. Acad. Sci. USA, 2001, 98, 10344-10349.
34. Kawamoto, A.; Iwasaki, H.; Kusano, K.; Murayama, T.; Oyamada, A.; Silver, M.; Hulbert, C.; Gavin, M.; Hanley, A.; Ma, H.; Kearney, M.; Zak, V.; Asahara, T.; Losordo, D.W. CD34-positive cells exhibit increased potency and safety for therapeutic neovascularization after myocardial infarction compared with total mononuclear cells. Circulation, 2006, 114, 2163-2169.
35. Assmus, B.; Schachinger, V.; Teupe, C.; Britten, M.; Lehmann, R.; Dobert, N.; Grunwald, F.; Aicher, A.; Urbich, C.; Martin, H.; Hoelzer, D.; Dimmeler, S.; Zeiher, A.M. Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation, 2002, 106, 3009-3017.
36. Kang, H.J.; Kim, H.S.; Zhang, S.Y.; Park, K.W.; Cho, H.J.; Koo, B.K.; Kim, Y.J.; Soo Lee, D.; Sohn, D.W.; Han, K.S.; Oh, B.H.; Lee, M.M.; Park, Y.B. Effects of intracoronary infusion of peripheral blood stem-cells mobilised with granulocyte-colony stimulating factor on left ventricular systolic function and restenosis after coronary stenting in myocardial infarction: the MAGIC cell randomised clinical trial. Lancet, 2004, 363, 751-756.
37. Ripa, R.S.; Haack-Sorensen, M.; Wang, Y.; Jorgensen, E.; Mortensen, S.; Bindslev, L.; Friis, T.; Kastrup, J. Bone marrow derived mesenchymal cell mobilization by granulocyte-colony stimulating factor after acute myocardial infarction: results from the Stem Cells in Myocardial Infarction (STEMMI) trial. Circulation, 2007, 116, I24-30.
38. Tang, Y.L.; Zhao, Q.; Zhang, Y.C.; Cheng, L.; Liu, M.; Shi, J.; Yang, Y.Z.; Pan, C.; Ge, J.; Phillips, M.I. Autologous mesenchymal stem cell transplantation induce VEGF and neovascularization in ischemic myocardium. Regul. Pept., 2004, 117, 3-10.
39. Breitbach, M.; Bostani, T.; Roell, W.; Xia, Y.; Dewald, O.; Nygren, J.M.; Fries, J.W.; Tiemann, K.; Bohlen, H.; Hescheler, J.; Welz, A.; Bloch, W.; Jacobsen, S.E.; Fleischmann, B.K. Potential risks of bone marrow cell transplantation into infarcted hearts. Blood, 2007, 110, 1362-1369.
40. Oh, H.; Bradfute, S.B.; Gallardo, T.D.; Nakamura, T.; Gaussin, V.; Mishina, Y.; Pocius, J.; Michael, L.H.; Behringer, R.R.; Garry, D.J.; Entman, M.L.; Schneider, M.D. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc. Natl. Acad. Sci. USA, 2003, 100, 12313-12318.
41. Laugwitz, K.-L.; Moretti, A.; Lam, J.; Gruber, P.; Chen, Y.; Woodard, S.; Lin, L.-Z.; Cai, C.-L.; Lu, M.M.; Reth, M.; Platoshyn, O.; Yuan, J.X.-J.; Evans, S.; Chien, K.R. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature, 2005, 433, 647-653.
42. Hierlihy, A.M.; Seale, P.; Lobe, C.G.; Rudnicki, M.A.; Megeney, L.A. The post-natal heart contains a myocardial stem cell population. FEBS Lett., 2002, 530, 239-243.
43. Wu, S.M.; Chien, K.R.; Mummery, C. Origins and fates of cardiovascular progenitor cells. Cell, 2008, 132, 537-543.
44. Cai, C.-L.; Liang, X.; Shi, Y.; Chu, P.-H.; Pfaff, S.L.; Chen, J.; Evans, S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell, 2003, 5, 877-889.
45. Sun, Y.; Liang, X.; Najafi, N.; Cass, M.; Lin, L.; Cai, C.-L.; Chen, J.; Evans, S.M. Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Devel. Biol., 2007, 304, 286-296.
46. Parmacek, M.S.; Epstein, J.A. Pursuing cardiac progenitors: regeneration redux. Cell, 2005, 120, 295-298.
47. Mouquet, F.; Pfister, O.; Jain, M.; Oikonomopoulos, A.; Ngoy, S.; Summer, R.; Fine, A.; Liao, R. Restoration of cardiac progenitor cells after myocardial infarction by self-proliferation and selective homing of bone marrow-derived stem cells. Circ. Res., 2005, 97, 1090-1092.
48. Fazel, S.; Cimini, M.; Chen, L.; Li, S.; Angoulvant, D.; Fedak, P.; Verma, S.; Weisel, R.D.; Keating, A.; Li, R.K. Cardioprotective ckit+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J. Clin. Invest., 2006, 116, 1865-1877.
49. Heeschen, C.; Lehmann, R.; Honold, J.; Assmus, B.; Aicher, A.; Walter, D.H.; Martin, H.; Zeiher, A.M.; Dimmeler, S. Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation, 2004, 109, 1615-1622.
50. Scheubel, R.J.; Zorn, H.; Silber, R.E.; Kuss, O.; Morawietz, H.; Holtz, J.; Simm, A. Age-dependent depression in circulating endothelial progenitor cells in patients undergoing coronary artery bypass grafting. J. Am. Coll. Cardiol., 2003, 42, 2073-2080.
51. Ma, N.; Stamm, C.; Kaminski, A.; Li, W.; Kleine, H.D.; Muller-Hilke, B.; Zhang, L.; Ladilov, Y.; Egger, D.; Steinhoff, G. Human cord blood cells induce angiogenesis following myocardial infarction in NOD/scid-mice. Cardiovasc. Res., 2005, 66, 45-54.
52. Ma, N.; Ladilov, Y.; Moebius, J.M.; Ong, L.; Piechaczek, C.; David, A.; Kaminski, A.; Choi, Y.H.; Li, W.; Egger, D.; Stamm, C.; Steinhoff, G. Intramyocardial delivery of human CD133+ cells in a SCID mouse cryoinjury model: Bone marrow vs. cord bloodderived cells. Cardiovasc. Res., 2006, 71, 158-169.
53. Leor, J.; Guetta, E.; Feinberg, M.S.; Galski, H.; Bar, I.; Holbova, R.; Miller, L.; Zarin, P.; Castel, D.; Barbash, I.M.; Nagler, A. Human umbilical cord blood-derived CD133+ cells enhance function and repair of the infarcted myocardium. Stem Cells, 2006, 24, 772-780.
54. Henning, R.J.; Abu-Ali, H.; Balis, J.U.; Morgan, M.B.; Willing, A.E.; Sanberg, P.R. Human umbilical cord blood mononuclear cells for the treatment of acute myocardial infarction. Cell Transplant., 2004, 13, 729-739.
55. Ma, N.; Ladilov, Y.; Kaminski, A.; Piechaczek, C.; Choi, Y.H.; Li, W.; Steinhoff, G.; Stamm, C. Umbilical cord blood cell transplantation for myocardial regeneration. Transplant. Proc., 2006, 38, 771-773.
56. Leor, J.; Guetta, E.; Chouraqui, P.; Guetta, V.; Nagler, A. Human umbilical cord blood cells: a new alternative for myocardial repair? Cytotherapy, 2005, 7, 251-257.
57. Mummery, C.; Ward-van Oostwaard, D.; Doevendans, P.; Spijker, R.; van den Brink, S.; Hassink, R.; van der Heyden, M.; Opthof, T.; Pera, M.; de la Riviere, A.B.; Passier, R.; Tertoolen, L. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation, 2003, 107, 2733-2740.
58. Kehat, I.; Kenyagin-Karsenti, D.; Snir, M.; Segev, H.; Amit, M.; Gepstein, A.; Livne, E.; Binah, O.; Itskovitz-Eldor, J.; Gepstein, L. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J. Clin. Invest., 2001, 108, 407-414.
59. Xu, C.; Police, S.; Rao, N.; Carpenter, M.K. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ. Res., 2002, 91, 501-508.
60. Ferreira, L.S.; Gerecht, S.; Shieh, H.F.; Watson, N.; Rupnick, M.A.; Dallabrida, S.M.; Vunjak-Novakovic, G.; Langer, R. Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ. Res., 2007, 101, 286-294.
61. Takahashi, K.; Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 2006, 126, 663-676.
62. Martinez-Fernandez, A.; Nelson, T.J.; Yamada, S.; Reyes, S.; Alekseev, A.E.; Perez-Terzic, C.; Ikeda, Y.; Terzic, A. iPS programmed without c-MYC yield proficient cardiogenesis for functional heart chimerism. Circ. Res., 2009, 105, 648-656.
63. Shiba, Y.; Hauch, K.D.; Laflamme, M.A. Cardiac applications for human pluripotent stem cells. Curr. Pharm. Des., 2009, 15, 2791-2806.
64. Zhu, W.Z.; Hauch, K.D.; Xu, C.; Laflamme, M.A. Human embryonic stem cells and cardiac repair. Transplant. Rev. (Orlando). 2009, 23, 53-68.
65. Nakamuta, J.S.; Danoviz, M.E.; Marques, F.L.; dos Santos, L.; Becker, C.; Goncalves, G.A.; Vassallo, P.F.; Schettert, I.T.; Tucci, P.J.; Krieger, J.E. Cell therapy attenuates cardiac dysfunction post myocardial infarction: effect of timing, routes of injection and a fibrin scaffold. PLoS One, 2009, 4, e6005.
66. Suzuki, K.; Smolenski, R.T.; Jayakumar, J.; Murtuza, B.; Brand, N.J.; Yacoub, M.H. Heat shock treatment enhances graft cell survival in skeletal myoblast transplantation to the heart. Circulation, 2000, 102, 216-221.
67. Yang, J.; Zhou, W.; Zheng, W.; Ma, Y.; Lin, L.; Tang, T.; Liu, J.; Yu, J.; Zhou, X.; Hu, J. Effects of myocardial transplantation of marrow mesenchymal stem cells transfected with vascular endothelial growth factor for the improvement of heart function and angiogenesis after myocardial infarction. Cardiology, 2007, 107, 17-29.
68. Tara, S.; Miyamoto, M.; Asoh, S.; Ishii, N.; Yasutake, M.; Takagi, G.; Takano, T.; Ohta, S. Transduction of the anti-apoptotic PTDFNK protein improves the efficiency of transplantation of bone marrow mononuclear cells. J. Mol. Cell Cardiol., 2007, 42, 489-497.
69. Niagara, M.I.; Haider, H.; Jiang, S.; Ashraf, M. Pharmacologically preconditioned skeletal myoblasts are resistant to oxidative stress and promote angiomyogenesis via release of paracrine factors in the infarcted heart. Circ. Res., 2007, 100, 545-555.
70. Haider, H.; Ashraf, M. Strategies to promote donor cell survival: combining preconditioning approach with stem cell transplantation. J. Mol. Cell Cardiol., 2008, 45, 554-566.
71. Mirotsou, M.; Zhang, Z.; Deb, A.; Zhang, L.; Gnecchi, M.; Noiseux, N.; Mu, H.; Pachori, A.; Dzau, V. Secreted frizzled related protein 2 (Sfrp2) is the key Akt-mesenchymal stem cellreleased paracrine factor mediating myocardial survival and repair. Proc. Natl. Acad. Sci. USA, 2007, 104, 1643-1648.
72. Datta, S.R.; Brunet, A.; Greenberg, M.E. Cellular survival: a play in three Akts. Genes Dev. 1999, 13, 2905-2927.
73. Vunjak-Novakovic, G.; Tandon, N.; Godier, A.; Maidhof, R.; Marsano, A.; Martens, T.; Radisic, M. Challenges in cardiac tissue engineering. Tissue Eng. Part B Rev., 2010, 16(2), 169-187.
74. Zimmermann, W.H. Remuscularizing failing hearts with tissue engineered myocardium. Antioxid. Redox Signal., 2009, 11, 2011-2023.
75. Davis, M.E.; Hsieh, P.C.H.; Grodzinsky, A.J.; Lee, R.T. Custom design of the cardiac microenvironment with biomaterials. Circ. Res., 2005, 97, 8-15.
76. Ferreira, L.S.; Gerecht, S.; Fuller, J.; Shieh, H.F.; Vunjak-Novakovic, G.; Langer, R. Bioactive hydrogel scaffolds for controllable vascular differentiation of human embryonic stem cells. Biomaterials, 2007, 28, 2706-2717.
77. Ratner, B.D.; Bryant, S.J. Biomaterials: where we have been and where we are going. Annu. Rev. Biomed. Eng., 2004, 6, 41-75.
78. Christman, K.L.; Lee, R.J. Biomaterials for the treatment of myocardial infarction. J. Am. Coll. Cardiol., 2006, 48, 907-913.
79. Christman, K.L.; Fok, H.H.; Sievers, R.E.; Fang, Q.; Lee, R.J. Fibrin glue alone and skeletal myoblasts in a fibrin scaffold preserve cardiac function after myocardial infarction. Tissue Eng., 2004, 10, 403-409.
80. Jiang, X.J.; Wang, T.; Li, X.Y.; Wu, D.Q.; Zheng, Z.B.; Zhang, J.F.; Chen, J.L.; Peng, B.; Jiang, H.; Huang, C.; Zhang, X.Z. Injection of a novel synthetic hydrogel preserves left ventricle function after myocardial infarction. J. Biomed. Mater. Res. A., 2009, 90, 472-477.
81. Leor, J.; Tuvia, S.; Guetta, V.; Manczur, F.; Castel, D.; Willenz, U.; Petnehazy, O.; Landa, N.; Feinberg, M.S.; Konen, E.; Goitein, O.; Tsur-Gang, O.; Shaul, M.; Klapper, L.; Cohen, S. Intracoronary injection of in situ forming alginate hydrogel reverses left ventricular remodeling after myocardial infarction in Swine. J. Am. Coll. Cardiol., 2009, 54, 1014-1023.
82. Yu, J.; Gu, Y.; Du, K.T.; Mihardja, S.; Sievers, R.E.; Lee, R.J. The effect of injected RGD modified alginate on angiogenesis and left ventricular function in a chronic rat infarct model. Biomaterials, 2009, 30, 751-756.
83. Ryu, J.H.; Kim, I.K.; Cho, S.W.; Cho, M.C.; Hwang, K.K.; Piao, H.; Piao, S.; Lim, S.H.; Hong, Y.S.; Choi, C.Y.; Yoo, K.J.; Kim, B.S. Implantation of bone marrow mononuclear cells using injectable fibrin matrix enhances neovascularization in infarcted myocardium. Biomaterials, 2005, 26, 319-326.
84. Wang, T.; Jiang, X.J.; Tang, Q.Z.; Li, X.Y.; Lin, T.; Wu, D.Q.; Zhang, X.Z.; Okello, E. Bone marrow stem cells implantation with alpha-cyclodextrin/MPEG-PCL-MPEG hydrogel improves cardiac function after myocardial infarction. Acta Biomater., 2009, 5, 2939-2944.
85. Lu, W.N.; Lu, S.H.; Wang, H.B.; Li, D.X.; Duan, C.M.; Liu, Z.Q.; Hao, T.; He, W.J.; Xu, B.; Fu, Q.; Song, Y.C.; Xie, X.H.; Wang, C.Y. Functional improvement of infarcted heart by co-injection of embryonic stem cells with temperature-responsive chitosan hydrogel. Tissue Eng. Part A., 2009, 15, 1437-1447.
86. Silva, G.A.; Czeisler, C.; Niece, K.L.; Beniash, E.; Harrington, D.A.; Kessler, J.A.; Stupp, S.I. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science, 2004, 303, 1352-1355.
87. Davis, M.E.; Motion, J.P.M.; Narmoneva, D.A.; Takahashi, T.; Hakuno, D.; Kamm, R.D.; Zhang, S.; Lee, R.T. Injectable selfassembling peptide nanofibers create intramyocardial microenvironments for endothelial cells. Circulation, 2005, 111, 442-450.
88. Frangioni, J.V.; Hajjar, R.J. In vivo tracking of stem cells for clinical trials in cardiovascular disease. Circulation, 2004, 110, 3378-3383.
89. Zhou, R.; Acton, P.D.; Ferrari, V.A. Imaging stem cells implanted in infarcted myocardium. J. Am. Coll. Cardiol., 2006, 48, 2094-2106.
90. Kraitchman, D.L.; Gilson, W.D.; Lorenz, C.H. Stem cell therapy: MRI guidance and monitoring. J. Magn. Reson. Imaging, 2008, 27, 299-310.
91. Ferreira, L.; Karp, J.M.; Nobre, L.; Langer, R. New opportunities: the use of nanotechnologies to manipulate and track stem cells. Cell Stem Cell, 2008, 3, 136-146.
92. Wang, Y.X.; Hussain, S.M.; Krestin, G.P. Superparamagnetic iron oxide contrast agents: physicochemical characteristics and applications in MR imaging. Eur. Radiol., 2001, 11, 2319-2331.
93. Reimer, P.; Balzer, T. Ferucarbotran (Resovist): a new clinically approved RES-specific contrast agent for contrast-enhanced MRI of the liver: properties, clinical development, and applications. Eur. Radiol., 2003, 13, 1266-1276.
94. Engstrom, M.; Klasson, A.; Pedersen, H.; Vahlberg, C.; Kall, P.O.; Uvdal, K. High proton relaxivity for gadolinium oxide nanoparticles. MAGMA, 2006, 19, 180-186.
95. Srinivas, M.; Morel, P.A.; Ernst, L.A.; Laidlaw, D.H.; Ahrens, E.T. Fluorine-19 MRI for visualization and quantification of cell migration in a diabetes model. Magn. Reson. Med., 2007, 58, 725-734.
96. Bulte, J.W.; Douglas, T.; Witwer, B.; Zhang, S.C.; Lewis, B.K.; van Gelderen, P.; Zywicke, H.; Duncan, I.D.; Frank, J.A. Monitoring stem cell therapy in vivo using magnetodendrimers as a new class of cellular MR contrast agents. Acad. Radiol., 2002, 9 Suppl 2, 332-335.
97. Liu, W.; Frank, J.A. Detection and quantification of magnetically labeled cells by cellular MRI. Eur. J. Radiol., 2009, 70, 258-264.
98. Hill, J.M.; Dick, A.J.; Raman, V.K.; Thompson, R.B.; Yu, Z.-X.; Hinds, K.A.; Pessanha, B.S.S.; Guttman, M.A.; Varney, T.R.; Martin, B.J.; Dunbar, C.E.; McVeigh, E.R.; Lederman, R.J. Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells. Circulation, 2003, 108, 1009-1014.
99. Walczak, P.; Kedziorek, D.A.; Gilad, A.A.; Lin, S.; Bulte, J.W. Instant MR labeling of stem cells using magnetoelectroporation. Magn. Reson. Med., 2005, 54, 769-774.
100. de Vries, I.J.; Lesterhuis, W.J.; Barentsz, J.O.; Verdijk, P.; van Krieken, J.H.; Boerman, O.C.; Oyen, W.J.; Bonenkamp, J.J.; Boezeman, J.B.; Adema, G.J.; Bulte, J.W.; Scheenen, T.W.; Punt, C.J.; Heerschap, A.; Figdor, C.G. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat. Biotechnol., 2005, 23, 1407-1413.
101. Zhu, J.; Zhou, L.; XingWu, F. Tracking neural stem cells in patients with brain trauma. N. Engl. J. Med., 2006, 355, 2376.
102. Garot, J.; Unterseeh, T.; Teiger, E.; Champagne, S.; Chazaud, B.; Gherardi, R.; Hittinger, L.; Gueret, P.; Rahmouni, A. Magnetic resonance imaging of targeted catheter-based implantation of myogenic precursor cells into infarcted left ventricular myocardium. J. Am. Coll. Cardiol., 2003, 41, 1841-1846.
103. Dick, A.J.; Guttman, M.A.; Raman, V.K.; Peters, D.C.; Pessanha, B.S.S.; Hill, J.M.; Smith, S.; Scott, G.; McVeigh, E.R.; Lederman, R.J. Magnetic resonance fluoroscopy allows targeted delivery of mesenchymal stem cells to infarct borders in Swine. Circulation, 2003, 108, 2899-2904.
104. Stuckey, D.J.; Carr, C.A.; Martin-Rendon, E.; Tyler, D.J.; Willmott, C.; Cassidy, P.J.; Hale, S.J.; Schneider, J.E.; Tatton, L.; Harding, S.E.; Radda, G.K.; Watt, S.; Clarke, K. Iron particles for noninvasive monitoring of bone marrow stromal cell engraftment into, and isolation of viable engrafted donor cells from, the heart. Stem Cells, 2006, 24, 1968-1975.
105. Kraitchman, D.L.; Heldman, A.W.; Atalar, E.; Amado, L.C.; Martin, B.J.; Pittenger, M.F.; Hare, J.M.; Bulte, J.W.M. In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation, 2003, 107, 2290-2293.
106. Freyman, T.; Polin, G.; Osman, H.; Crary, J.; Lu, M.; Cheng, L.; Palasis, M.; Wilensky, R.L. A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction. Eur. Heart J., 2006, 27, 1114-1122.
107. Pula, G.; Mayr, U.; Evans, C.; Prokopi, M.; Vara, D.S.; Yin, X.; Astroulakis, Z.; Xiao, Q.; Hill, J.; Xu, Q.; Mayr, M. Proteomics identifies thymidine phosphorylase as a key regulator of the angiogenic potential of colony-forming units and endothelial progenitor cell cultures. Circ. Res., 2009, 104, 32-40.
108. Birkedal-Hansen, H.; Moore, W.G.; Bodden, M.K.; Windsor, L.J.; Birkedal-Hansen, B.; DeCarlo, A.; Engler, J.A. Matrix metalloproteinases: a review. Crit. Rev. Oral. Biol. Med., 1993, 4, 197-250.
109. Kraehenbuehl, T.P.; Ferreira, L.S.; Zammaretti, P.; Hubbell, J.A.; Langer, R. Cell-responsive hydrogel for encapsulation of vascular cells. Biomaterials, 2009, 30, 4318-4324.
110. Li, Z.; Wilson, K.D.; Smith, B.; Kraft, D.L.; Jia, F.; Huang, M.; Xie, X.; Robbins, R.C.; Gambhir, S.S.; Weissman, I.L.; Wu, J.C. Functional and transcriptional characterization of human embryonic stem cell-derived endothelial cells for treatment of myocardial infarction. PLoS One, 2009, 4, e8443.