From ontogenesis to regeneration: Learning how to instruct adult cardiac progenitor cells

Progress in Molecular Biology and Translational Science

Volumn 111, Issue , 2012, Pages 109-137

  Chimenti, Isotta ^a   Forte, Elvira ^b   Angelini, Francesco ^a   Giacomello, Alessandro ^b   Messina, Elisa ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

cardiac cell therapy; cardiac progenitor cells; cardiac regeneration; cardiac stem cell niche

Indexed keywords

EID: 84865322200     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-398459-3.00005-8     Document Type: Chapter

References (123)

1. S. Ausoni, and S. Sartore From fish to amphibians to mammals: in search of novel strategies to optimize cardiac regeneration J Cell Biol 184 2009 357 364
2. D.C. Lo, F. Allen, and J.P. Brockes Reversal of muscle differentiation during urodele limb regeneration Proc Natl Acad Sci USA 90 1993 7230 7234 (Pubitemid 23222423)
3. M. Maden Regeneration: every clot has a thrombin lining Curr Biol 13 2003 R517 R518
4. J.P. Brockes Amphibian limb regeneration: rebuilding a complex structure Science 276 1997 81 87 (Pubitemid 27161247)
5. E.M. Tanaka Regeneration: if they can do it, why can't we? Cell 113 2003 559 562 (Pubitemid 36694180)
6. I. Chimenti, R. Gaetani, L. Barile, E. Forte, V. Ionta, and F. Angelini Evidence for the existence of resident cardiac stem cells I.S. Cohen, R. Glenn, Regenerating the heart 2011 Humana Press Totowa, New Jersey
7. P.C. Hsieh, V.F. Segers, M.E. Davis, C. MacGillivray, J. Gannon, and J.D. Molkentin Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury Nat Med 13 2007 970 974 (Pubitemid 47222045)
8. O. Bergmann, R.D. Bhardwaj, S. Bernard, S. Zdunek, F. Barnabe-Heider, and S. Walsh Evidence for cardiomyocyte renewal in humans Science 324 2009 98 102
9. J. Kajstura, N. Gurusamy, B. Ogorek, P. Goichberg, C. Clavo-Rondon, and T. Hosoda Myocyte turnover in the aging human heart Circ Res 107 2010 1374 1386
10. L. Barile, E. Messina, A. Giacomello, and E. Marban Endogenous cardiac stem cells Prog Cardiovasc Dis 50 2007 31 48 (Pubitemid 47042841)
11. K.D. Poss, L.G. Wilson, and M.T. Keating Heart regeneration in zebrafish Science 298 2002 2188 2190 (Pubitemid 35471243)
12. C. Jopling, E. Sleep, M. Raya, M. Marti, A. Raya, and J.C. Belmonte Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation Nature 464 2010 606 609
13. K. Kikuchi, J.E. Holdway, A.A. Werdich, R.M. Anderson, Y. Fang, and G.F. Egnaczyk Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes Nature 464 2010 601 605
14. J.D. Drenckhahn, Q.P. Schwarz, S. Gray, A. Laskowski, H. Kiriazis, and Z. Ming Compensatory growth of healthy cardiac cells in the presence of diseased cells restores tissue homeostasis during heart development Dev Cell 15 2008 521 533
15. E.R. Porrello, A.I. Mahmoud, E. Simpson, J.A. Hill, J.A. Richardson, and E.N. Olson Transient regenerative potential of the neonatal mouse heart Science 331 2011 1078 1080
16. S. Martin-Puig, Z. Wang, and K.R. Chien Lives of a heart cell: tracing the origins of cardiac progenitors Cell Stem Cell 2 2008 320 331 (Pubitemid 351455247)
17. E. Dodou, M.P. Verzi, J.P. Anderson, S.M. Xu, and B.L. Black Mef2c is a direct transcriptional target of ISL1 and GATA factors in the anterior heart field during mouse embryonic development Development 131 2004 3931 3942 (Pubitemid 39232153)
18. 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 (Pubitemid 40282999)
19. 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 (Pubitemid 44895618)
20. S.J. Kattman, E.D. Adler, and G.M. Keller Specification of multipotential cardiovascular progenitor cells during embryonic stem cell differentiation and embryonic development Trends Cardiovasc Med 17 2007 240 246 (Pubitemid 47532729)
21. C.E. Murry, and G. Keller Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development Cell 132 2008 661 680 (Pubitemid 351260059)
22. A. Bondue, S. Tannler, G. Chiapparo, S. Chabab, M. Ramialison, and C. Paulissen Defining the earliest step of cardiovascular progenitor specification during embryonic stem cell differentiation J Cell Biol 192 2011 751 765
23. S. Kitajima, A. Takagi, T. Inoue, and Y. Saga MesP1 and MesP2 are essential for the development of cardiac mesoderm Development 127 2000 3215 3226 (Pubitemid 30649534)
24. Y. Saga, S. Kitajima, and S. Miyagawa-Tomita Mesp1 expression is the earliest sign of cardiovascular development Trends Cardiovasc Med 10 2000 345 352 (Pubitemid 32448044)
25. Y. Saga, S. Miyagawa-Tomita, A. Takagi, S. Kitajima, J. Miyazaki, and T. Inoue MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube Development 126 1999 3437 3447 (Pubitemid 29396783)
26. M. Mercola, P. Ruiz-Lozano, and M.D. Schneider Cardiac muscle regeneration: lessons from development Genes Dev 25 2011 299 309
27. C. Xu, S. Police, M. Hassanipour, and J.D. Gold Cardiac bodies: a novel culture method for enrichment of cardiomyocytes derived from human embryonic stem cells Stem Cells Dev 15 2006 631 639 (Pubitemid 44748598)
28. L. Yang, M.H. Soonpaa, E.D. Adler, T.K. Roepke, S.J. Kattman, and M. Kennedy Human cardiovascular progenitor cells develop from a KDR + embryonic-stem-cell-derived population Nature 453 2008 524 528 (Pubitemid 351733312)
29. A.C. Foley, and M. Mercola Heart induction by Wnt antagonists depends on the homeodomain transcription factor Hex Genes Dev 19 2005 387 396 (Pubitemid 40189301)
30. S. Yuasa, Y. Itabashi, U. Koshimizu, T. Tanaka, K. Sugimura, and M. Kinoshita Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells Nat Biotechnol 23 2005 607 611 (Pubitemid 41724900)
31. T.M. Schultheiss, J.B. Burch, and A.B. Lassar A role for bone morphogenetic proteins in the induction of cardiac myogenesis Genes Dev 11 1997 451 462 (Pubitemid 27097644)
32. M.S. Rones, K.A. McLaughlin, M. Raffin, and M. Mercola Serrate and Notch specify cell fates in the heart field by suppressing cardiomyogenesis Development 127 2000 3865 3876
33. T. Schroeder, S.T. Fraser, M. Ogawa, S. Nishikawa, C. Oka, and G.W. Bornkamm Recombination signal sequence-binding protein Jkappa alters mesodermal cell fate decisions by suppressing cardiomyogenesis Proc Natl Acad Sci USA 100 2003 4018 4023 (Pubitemid 36418149)
34. T. Schroeder, F. Meier-Stiegen, R. Schwanbeck, H. Eilken, S. Nishikawa, and R. Hasler Activated Notch1 alters differentiation of embryonic stem cells into mesodermal cell lineages at multiple stages of development Mech Dev 123 2006 570 579 (Pubitemid 44176343)
35. I.M. Conboy, and T.A. Rando The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis Dev Cell 3 2002 397 409
36. J. Jensen, E.E. Pedersen, P. Galante, J. Hald, R.S. Heller, and M. Ishibashi Control of endodermal endocrine development by Hes-1 Nat Genet 24 2000 36 44 (Pubitemid 30041417)
37. R. Abu-Issa, and M.L. Kirby Patterning of the heart field in the chick Dev Biol 319 2008 223 233
38. J.K. Takeuchi, M. Ohgi, K. Koshiba-Takeuchi, H. Shiratori, I. Sakaki, and K. Ogura Tbx5 specifies the left/right ventricles and ventricular septum position during cardiogenesis Development 130 2003 5953 5964 (Pubitemid 38008799)
39. T.J. Lints, L.M. Parsons, L. Hartley, I. Lyons, and R.P. Harvey Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants Development 119 1993 969 (Pubitemid 23337435)
40. A. Kaipainen, J. Korhonen, K. Pajusola, O. Aprelikova, M.G. Persico, and B.I. Terman The related FLT4, FLT1, and KDR receptor tyrosine kinases show distinct expression patterns in human fetal endothelial cells J Exp Med 178 1993 2077 2088 (Pubitemid 23344864)
41. J.D. Molkentin, A.B. Firulli, B.L. Black, J.F. Martin, C.M. Hustad, and N. Copeland MEF2B is a potent transactivator expressed in early myogenic lineages Mol Cell Biol 16 1996 3814 3824 (Pubitemid 26199902)
42. M. Heikinheimo, J.M. Scandrett, and D.B. Wilson Localization of transcription factor GATA-4 to regions of the mouse embryo involved in cardiac development Dev Biol 164 1994 361 373 (Pubitemid 24269225)
43. C.T. Kuo, E.E. Morrisey, R. Anandappa, K. Sigrist, M.M. Lu, and M.S. Parmacek GATA4 transcription factor is required for ventral morphogenesis and heart tube formation Genes Dev 11 1997 1048 1060 (Pubitemid 27199883)
44. D. Srivastava, P. Cserjesi, and E.N. Olson A subclass of bHLH proteins required for cardiac morphogenesis Science 270 1995 1995 1999 (Pubitemid 26097190)
45. R.P. Harvey Patterning the vertebrate heart Nat Rev Genet 3 2002 544 556 (Pubitemid 34746879)
46. R. Abu-Issa, K. Waldo, and M.L. Kirby Heart fields: one, two or more? Dev Biol 272 2004 281 285 (Pubitemid 38988257)
47. C.L. Cai, X. Liang, Y. Shi, P.H. Chu, S.L. Pfaff, and J. Chen Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart Dev Cell 5 2003 877 889 (Pubitemid 37527688)
48. R.G. Kelly, N.A. Brown, and M.E. Buckingham The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm Dev Cell 1 2001 435 440 (Pubitemid 33586092)
49. D. Ai, X. Fu, J. Wang, M.F. Lu, L. Chen, and A. Baldini Canonical Wnt signaling functions in second heart field to promote right ventricular growth Proc Natl Acad Sci USA 104 2007 9319 9324 (Pubitemid 47185777)
50. E.D. Cohen, Z. Wang, J.J. Lepore, M.M. Lu, M.M. Taketo, and D.J. Epstein Wnt/beta-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling J Clin Invest 117 2007 1794 1804 (Pubitemid 47036313)
51. A. Klaus, Y. Saga, M.M. Taketo, E. Tzahor, and W. Birchmeier Distinct roles of Wnt/beta-catenin and Bmp signaling during early cardiogenesis Proc Natl Acad Sci USA 104 2007 18531 18536 (Pubitemid 350210731)
52. L. Lin, L. Cui, W. Zhou, D. Dufort, X. Zhang, and C.L. Cai Beta-catenin directly regulates Islet1 expression in cardiovascular progenitors and is required for multiple aspects of cardiogenesis Proc Natl Acad Sci USA 104 2007 9313 9318 (Pubitemid 47185776)
53. S.M. Meilhac, M. Esner, R.G. Kelly, J.F. Nicolas, and M.E. Buckingham The clonal origin of myocardial cells in different regions of the embryonic mouse heart Dev Cell 6 2004 685 698 (Pubitemid 38579352)
54. S.J. Kattman, T.L. Huber, and G.M. Keller Multipotent flk-1 + cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages Dev Cell 11 2006 723 732 (Pubitemid 44644969)
55. M. Ema, S. Takahashi, and J. Rossant Deletion of the selection cassette, but not cis-acting elements, in targeted Flk1-lacZ allele reveals Flk1 expression in multipotent mesodermal progenitors Blood 107 2006 111 117 (Pubitemid 43053531)
56. K.R. Chien, I.J. Domian, and K.K. Parker Cardiogenesis and the complex biology of regenerative cardiovascular medicine Science 322 2008 1494 1497
57. A. Wessels, and D. Sedmera Developmental anatomy of the heart: a tale of mice and man Physiol Genomics 15 2003 165 176 (Pubitemid 38089563)
58. M.R. Hutson, and M.L. Kirby Model systems for the study of heart development and disease. Cardiac neural crest and conotruncal malformations Semin Cell Dev Biol 18 2007 101 110 (Pubitemid 46343796)
59. P. Snider, M. Olaopa, A.B. Firulli, and S.J. Conway Cardiovascular development and the colonizing cardiac neural crest lineage ScientificWorldJournal 7 2007 1090 1113 (Pubitemid 47036152)
60. A.P. Kappetein, A.C. Gittenberger-de Groot, A.H. Zwinderman, J. Rohmer, R.E. Poelmann, and H.A. Huysmans The neural crest as a possible pathogenetic factor in coarctation of the aorta and bicuspid aortic valve J Thorac Cardiovasc Surg 102 1991 830 836
61. T. Nakamura, M.C. Colbert, and J. Robbins Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system Circ Res 98 2006 1547 1554 (Pubitemid 44297078)
62. J.Z. Stoller, and J.A. Epstein Cardiac neural crest Semin Cell Dev Biol 16 2005 704 715 (Pubitemid 41506978)
63. R.W. Stottmann, M. Choi, Y. Mishina, E.N. Meyers, and J. Klingensmith BMP receptor IA is required in mammalian neural crest cells for development of the cardiac outflow tract and ventricular myocardium Development 131 2004 2205 2218 (Pubitemid 38702051)
64. V. El-Helou, P.C. Beguin, J. Assimakopoulos, R. Clement, H. Gosselin, and R. Brugada The rat heart contains a neural stem cell population; role in sympathetic sprouting and angiogenesis J Mol Cell Cardiol 45 2008 694 702
65. E.M. Winter, and A.C. Gittenberger-de Groot Epicardium-derived cells in cardiogenesis and cardiac regeneration Cell Mol Life Sci 64 2007 692 703
66. D.E. Reese, T. Mikawa, and D.M. Bader Development of the coronary vessel system Circ Res 91 2002 761 768 (Pubitemid 35285072)
67. A. Wessels, and J.M. Perez-Pomares The epicardium and epicardially derived cells (EPDCs) as cardiac stem cells Anat Rec A Discov Mol Cell Evol Biol 276 2004 43 57 (Pubitemid 38063877)
68. C.L. Cai, J.C. Martin, Y. Sun, L. Cui, L. Wang, and K. Ouyang A myocardial lineage derives from Tbx18 epicardial cells Nature 454 2008 104 108 (Pubitemid 351931969)
69. B. Zhou, Q. Ma, S. Rajagopal, S.M. Wu, I. Domian, and J. Rivera-Feliciano Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart Nature 454 2008 109 113 (Pubitemid 351931979)
70. I. Bock-Marquette, A. Saxena, M.D. White, J.M. Dimaio, and D. Srivastava Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair Nature 432 2004 466 472 (Pubitemid 39576522)
71. N. Smart, C.A. Risebro, A.A. Melville, K. Moses, R.J. Schwartz, and K.R. Chien Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization Nature 445 2007 177 182 (Pubitemid 46095717)
72. I. Bock-Marquette, S. Shrivastava, G.C. Pipes, J.E. Thatcher, A. Blystone, and J.M. Shelton Thymosin beta4 mediated PKC activation is essential to initiate the embryonic coronary developmental program and epicardial progenitor cell activation in adult mice in vivo J Mol Cell Cardiol 46 2009 728 738
73. K. Urayama, C. Guilini, G. Turkeri, S. Takir, H. Kurose, and N. Messaddeq Prokineticin receptor-1 induces neovascularization and epicardial-derived progenitor cell differentiation Arterioscler Thromb Vasc Biol 28 2008 841 849 (Pubitemid 351544097)
74. F. Limana, A. Zacheo, D. Mocini, A. Mangoni, G. Borsellino, and A. Diamantini Identification of myocardial and vascular precursor cells in human and mouse epicardium Circ Res 101 2007 1255 1265 (Pubitemid 350294642)
75. 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
76. M. Nemir, and T. Pedrazzini Functional role of Notch signaling in the developing and postnatal heart J Mol Cell Cardiol 45 2008 495 504
77. K. Niessen, and A. Karsan Notch signaling in cardiac development Circ Res 102 2008 1169 1181
78. A. Raya, C.M. Koth, D. Buscher, Y. Kawakami, T. Itoh, and R.M. Raya Activation of Notch signaling pathway precedes heart regeneration in zebrafish Proc Natl Acad Sci USA 100 Suppl 1 2003 11889 11895 (Pubitemid 37205900)
79. A. Croquelois, A.A. Domenighetti, M. Nemir, M. Lepore, N. Rosenblatt-Velin, and F. Radtke Control of the adaptive response of the heart to stress via the Notch1 receptor pathway J Exp Med 205 2008 3173 3185
80. N.A. Gude, G. Emmanuel, W. Wu, C.T. Cottage, K. Fischer, and P. Quijada Activation of Notch-mediated protective signaling in the myocardium Circ Res 102 2008 1025 1035 (Pubitemid 351667856)
81. J.L. Russell, S.C. Goetsch, N.R. Gaiano, J.A. Hill, E.N. Olson, and J.W. Schneider A dynamic notch injury response activates epicardium and contributes to fibrosis repair Circ Res 108 2011 51 59
82. 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 (Pubitemid 37186770)
83. 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 USA 100 2003 12313 12318 (Pubitemid 37271557)
84. A.M. Hierlihy, P. Seale, C.G. Lobe, M.A. Rudnicki, and L.A. Megeney The post-natal heart contains a myocardial stem cell population FEBS Lett 530 2002 239 243 (Pubitemid 35248218)
85. 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 (Pubitemid 39435006)
86. C. Bearzi, M. Rota, T. Hosoda, J. Tillmanns, A. Nascimbene, and A. De Angelis Human cardiac stem cells Proc Natl Acad Sci USA 104 2007 14068 14073 (Pubitemid 350003336)
87. S. Dimmeler, A.M. Zeiher, and M.D. Schneider Unchain my heart: the scientific foundations of cardiac repair J Clin Invest 115 2005 572 583 (Pubitemid 40322227)
88. M. Ieda, J.D. Fu, P. Delgado-Olguin, V. Vedantham, Y. Hayashi, and B.G. Bruneau Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors Cell 142 2010 375 386
89. R. David, C. Brenner, J. Stieber, F. Schwarz, S. Brunner, and M. Vollmer MesP1 drives vertebrate cardiovascular differentiation through Dkk-1-mediated blockade of Wnt-signalling Nat Cell Biol 10 2008 338 345 (Pubitemid 351331021)
90. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 2006 663 676 (Pubitemid 44233629)
91. L. Li, and T. Xie Stem cell niche: structure and function Annu Rev Cell Dev Biol 21 2005 605 631 (Pubitemid 41740648)
92. M.R. Walker, K.K. Patel, and T.S. Stappenbeck The stem cell niche J Pathol 217 2009 169 180
93. T. Vazin, and D.V. Schaffer Engineering strategies to emulate the stem cell niche Trends Biotechnol 28 2010 117 124
94. F.M. Watt, and B.L. Hogan Out of Eden: stem cells and their niches Science 287 2000 1427 1430 (Pubitemid 30127126)
95. Y. Qyang, S. Martin-Puig, M. Chiravuri, S. Chen, H. Xu, and L. Bu The renewal and differentiation of Isl1 + cardiovascular progenitors are controlled by a Wnt/beta-catenin pathway Cell Stem Cell 1 2007 165 179 (Pubitemid 47224618)
96. K. Schlessinger, A. Hall, and N. Tolwinski Wnt signaling pathways meet Rho GTPases Genes Dev 23 2009 265 277
97. K. Urbanek, D. Cesselli, M. Rota, A. Nascimbene, A. De Angelis, and T. Hosoda Stem cell niches in the adult mouse heart Proc Natl Acad Sci USA 103 2006 9226 9231 (Pubitemid 43902560)
98. L.M. Popescu, M. Gherghiceanu, C.G. Manole, and M.S. Faussone-Pellegrini Cardiac renewing: interstitial Cajal-like cells nurse cardiomyocyte progenitors in epicardial stem cell niches J Cell Mol Med 13 2009 866 886
99. F. Pampaloni, E.G. Reynaud, and E.H. Stelzer The third dimension bridges the gap between cell culture and live tissue Nat Rev Mol Cell Biol 8 2007 839 845 (Pubitemid 47462131)
100. I.E. Holopainen Organotypic hippocampal slice cultures: a model system to study basic cellular and molecular mechanisms of neuronal cell death, neuroprotection, and synaptic plasticity Neurochem Res 30 2005 1521 1528 (Pubitemid 41813716)
101. R.R. Smith, L. Barile, H.C. Cho, M.K. Leppo, J.M. Hare, and E. Messina Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens Circulation 115 2007 896 908 [CIRCULATIONAHA.106.655209 [pii] 10.1161/CIRCULATIONAHA.106.655209] (Pubitemid 46294730)
102. I. Chimenti, R.R. Smith, T.S. Li, G. Gerstenblith, E. Messina, and A. Giacomello Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice Circ Res 106 2010 971 980
103. T.S. Li, K. Cheng, S.T. Lee, S. Matsushita, D. Davis, and K. Malliaras Cardiospheres recapitulate a niche-like microenvironment rich in stemness and cell-matrix interactions, rationalizing their enhanced functional potency for myocardial repair Stem Cells 28 2010 2088 2098
104. R. Gaetani, M. Ledda, L. Barile, I. Chimenti, F. De Carlo, and E. Forte Differentiation of human adult cardiac stem cells exposed to extremely low-frequency electromagnetic fields Cardiovasc Res 82 2009 411 420 doi:10.1093/cvr/cvp067 cvp067 [pii]
105. S.T. Lee, A.J. White, S. Matsushita, K. Malliaras, C. Steenbergen, and Y. Zhang Intramyocardial injection of autologous cardiospheres or cardiosphere-derived cells preserves function and minimizes adverse ventricular remodeling in pigs with heart failure post-myocardial infarction J Am Coll Cardiol 57 2011 455 465
106. E. Forte, I. Chimenti, L. Barile, R. Gaetani, F. Angelini, and V. Ionta Cardiac cell therapy: the next (re)generation Stem Cell Rev 7 2011 1018 1030
107. R. Gaetani, L. Barile, E. Forte, I. Chimenti, V. Ionta, and A. Di Consiglio New perspectives to repair a broken heart Cardiovasc Hematol Agents Med Chem 7 2009 91 107
108. 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
109. P. Menasche Cardiac cell therapy: lessons from clinical trials J Mol Cell Cardiol 50 2011 258 265
110. E. Martin-Rendon, S.J. Brunskill, C.J. Hyde, S.J. Stanworth, A. Mathur, and S.M. Watt Autologous bone marrow stem cells to treat acute myocardial infarction: a systematic review Eur Heart J 29 2008 1807 1818
111. 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 USA 102 2005 8966 8971 (Pubitemid 40881062)
112. 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
113. 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
114. P.V. Johnston, T. Sasano, K. Mills, R. Evers, S.T. Lee, and R.R. Smith Engraftment, differentiation, and functional benefits of autologous cardiosphere-derived cells in porcine ischemic cardiomyopathy Circulation 120 2009 1075 1083 7 p following 83
115. N. Takehara, Y. Tsutsumi, K. Tateishi, T. Ogata, H. Tanaka, and T. Ueyama Controlled delivery of basic fibroblast growth factor promotes human cardiosphere-derived cell engraftment to enhance cardiac repair for chronic myocardial infarction J Am Coll Cardiol 52 2008 1858 1865
116. K. Tateishi, E. Ashihara, S. Honsho, N. Takehara, T. Nomura, and T. Takahashi Human cardiac stem cells exhibit mesenchymal features and are maintained through Akt/GSK-3beta signaling Biochem Biophys Res Commun 352 2007 635 641 (Pubitemid 44880302)
117. K. Malliaras, and E. Marban Cardiac cell therapy: where we've been, where we are, and where we should be headed Br Med Bull 98 2011 161 185
118. A. Leri, J. Kajstura, and P. Anversa Role of cardiac stem cells in cardiac pathophysiology: a paradigm shift in human myocardial biology Circ Res 109 2011 941 961
119. K. Malliaras, T.S. Li, D. Luthringer, J. Terrovitis, K. Cheng, and T. Chakravarty Safety and efficacy of allogeneic cell therapy in infarcted rats transplanted with mismatched cardiosphere-derived cells Circulation 125 2012 100 112
120. R.R. Smith, I. Chimenti, and E. Marban Unselected human cardiosphere-derived cells are functionally superior to c-Kit- or CD90-purified cardiosphere-derived cells Circulation 118 2008 S420
121. T.S. Li, K. Cheng, K. Malliaras, N. Matsushita, B. Sun, and L. Marban Expansion of human cardiac stem cells in physiological oxygen improves cell production efficiency and potency for myocardial repair Cardiovasc Res 89 2011 157 165
122. T.S. Li, and E. Marban Physiological levels of reactive oxygen species are required to maintain genomic stability in stem cells Stem Cells 28 2010 1178 1185
123. R. Gaetani, G. Rizzitelli, I. Chimenti, L. Barile, E. Forte, and V. Ionta Cardiospheres and tissue engineering for myocardial regeneration: potential for clinical application J Cell Mol Med 14 2010 1071 1077