Biochemistry and biology: Heart-to-heart to investigate cardiac progenitor cells

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 2, 2013, Pages 2459-2469

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

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Calcium signaling; Cardiac progenitor cells; Cardiogenic pharmacological treatments; Cardiogenic small molecules; Hypoxia; Paracrine effects

Indexed keywords

BETA CATENIN; CALCIUM; CHEMOKINE RECEPTOR CXCR4; FIBROBLAST GROWTH FACTOR 2; GLUCOSE; GROWTH FACTOR; NICOTINAMIDE; OXYGEN; REACTIVE OXYGEN METABOLITE; STAGE SPECIFIC EMBRYO ANTIGEN 1; STEM CELL ANTIGEN 1; STEM CELL FACTOR; STROMAL CELL DERIVED FACTOR 1; THROMBIN; VASCULOTROPIN; WNT PROTEIN;

AUTOCRINE EFFECT; CARDIAC PROGENITOR CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL METABOLISM; CELL PROLIFERATION; CELL REGENERATION; CELL RENEWAL; CELLULAR PARAMETERS; ENERGY METABOLISM; EPICARDIALLY DERIVED CELL; EPICARDIUM; GENE; GLUCOSE METABOLISM; HEART FAILURE; HUMAN; INTRACELLULAR SIGNALING; ISLET 1 GENE; METABOLIC REGULATION; NONHUMAN; NUCLEAR REPROGRAMMING; PARACRINE SIGNALING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION; STEMNESS;

HUMANS; MYOCARDIUM; STEM CELLS;

EID: 84872487476     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2012.08.004     Document Type: Review

References (145)

1. P.Z. Gerczuk, D.G. Breckenridge, J.T. Liles, G.R. Budas, J.C. Shryock, L. Belardinelli, R.A. Kloner, and W. Dai An apoptosis signal-regulating kinase 1 inhibitor reduces cardiomyocyte apoptosis and infarct size in a rat ischemia-reperfusion model J. Cardiovasc. Pharmacol. 2012
2. R. Gaetani, L. Barile, E. Forte, I. Chimenti, V. Ionta, A. Di Consiglio, F. Miraldi, G. Frati, E. Messina, and A. Giacomello New perspectives to repair a broken heart Cardiovasc. Hematol. Agents Med. Chem. 7 2009 91 107
3. P. Menasche Cardiac cell therapy: lessons from clinical trials J. Mol. Cell. Cardiol. 50 2011 258 265
4. 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
5. E. Messina, L. De Angelis, G. Frati, S. Morrone, S. Chimenti, F. Fiordaliso, M. Salio, M. Battaglia, M.V. Latronico, M. Coletta, E. Vivarelli, L. Frati, G. Cossu, and A. Giacomello Isolation and expansion of adult cardiac stem cells from human and murine heart Circ. Res. 95 2004 911 921
6. R. Bolli, A.R. Chugh, D. D'Amario, J.H. Loughran, M.F. Stoddard, S. Ikram, G.M. Beache, S.G. Wagner, A. Leri, T. Hosoda, F. Sanada, J.B. Elmore, P. Goichberg, D. Cappetta, N.K. Solankhi, I. Fahsah, D.G. Rokosh, M.S. Slaughter, J. Kajstura, and P. Anversa Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial Lancet 378 9806 Nov 26 2011 1847 1857
7. R.R. Makkar, R.R. Smith, K. Cheng, K. Malliaras, L.E. Thomson, D. Berman, L.S. Czer, L. Marban, A. Mendizabal, P.V. Johnston, S.D. Russell, K.H. Schuleri, A.C. Lardo, G. Gerstenblith, and E. Marban Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial Lancet 379 2012 895 904
8. N. Takehara, Y. Tsutsumi, K. Tateishi, T. Ogata, H. Tanaka, T. Ueyama, T. Takahashi, T. Takamatsu, M. Fukushima, M. Komeda, M. Yamagishi, H. Yaku, Y. Tabata, H. Matsubara, and H. Oh 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
9. P.V. Johnston, T. Sasano, K. Mills, R. Evers, S.T. Lee, R.R. Smith, A.C. Lardo, S. Lai, C. Steenbergen, G. Gerstenblith, R. Lange, and E. Marban Engraftment, differentiation, and functional benefits of autologous cardiosphere-derived cells in porcine ischemic cardiomyopathy Circulation 120 2009 1075 1083 (1077 p following 1083)
10. S.T. Lee, A.J. White, S. Matsushita, K. Malliaras, C. Steenbergen, Y. Zhang, T.S. Li, J. Terrovitis, K. Yee, S. Simsir, R. Makkar, and E. Marban 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
11. E. Forte, I. Chimenti, L. Barile, R. Gaetani, F. Angelini, V. Ionta, E. Messina, and A. Giacomello Cardiac cell therapy: the next (re)generation Stem Cell Rev. 7 2011 1018 1030
12. J. Rehman Empowering self-renewal and differentiation: the role of mitochondria in stem cells J. Mol. Med. 88 2010 981 986
13. R.J. Deberardinis, and C.B. Thompson Cellular metabolism and disease: what do metabolic outliers teach us? Cell 148 2012 1132 1144
14. A.J. Boyle, S.P. Schulman, J.M. Hare, and P. Oettgen Is stem cell therapy ready for patients? Stem cell therapy for cardiac repair. Ready for the next step Circulation 114 2006 339 352
15. H.J. Cho, N. Lee, J.Y. Lee, Y.J. Choi, M. Ii, A. Wecker, J.O. Jeong, C. Curry, G. Qin, and Y.S. Yoon Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart J. Exp. Med. 204 2007 3257 3269
16. H. Reinecke, E. Minami, W.Z. Zhu, and M.A. Laflamme Cardiogenic differentiation and transdifferentiation of progenitor cells Circ. Res. 103 2008 1058 1071
17. K. Guan, and G. Hasenfuss Do stem cells in the heart truly differentiate into cardiomyocytes? J. Mol. Cell. Cardiol. 43 2007 377 387
18. N. Christoforou, and J.D. Gearhart Stem cells and their potential in cell-based cardiac therapies Prog. Cardiovasc. Dis. 49 2007 396 413
19. H.F. Tse, C.W. Siu, S.G. Zhu, L. Songyan, Q.Y. Zhang, W.H. Lai, Y.L. Kwong, J. Nicholls, and C.P. Lau Paracrine effects of direct intramyocardial implantation of bone marrow derived cells to enhance neovascularization in chronic ischaemic myocardium Eur. J. Heart Fail. 9 2007 747 753
20. E. Skobel, A. Schuh, E.R. Schwarz, E.A. Liehn, A. Franke, S. Breuer, K. Gunther, T. Reffelmann, P. Hanrath, and C. Weber Transplantation of fetal cardiomyocytes into infarcted rat hearts results in long-term functional improvement Tissue Eng. 10 2004 849 864
21. 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
22. C.M. Martin, A.P. Meeson, S.M. Robertson, T.J. Hawke, J.A. Richardson, S. Bates, S.C. Goetsch, T.D. Gallardo, and D.J. Garry 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
23. A.P. Beltrami, L. Barlucchi, D. Torella, M. Baker, F. Limana, S. Chimenti, H. Kasahara, M. Rota, E. Musso, K. Urbanek, A. Leri, J. Kajstura, B. Nadal-Ginard, and P. Anversa Adult cardiac stem cells are multipotent and support myocardial regeneration Cell 114 2003 763 776
24. H. Oh, S.B. Bradfute, T.D. Gallardo, T. Nakamura, V. Gaussin, Y. Mishina, J. Pocius, L.H. Michael, R.R. Behringer, D.J. Garry, M.L. Entman, and M.D. Schneider Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction Proc. Natl. Acad. Sci. U. S. A. 100 2003 12313 12318
25. K. Matsuura, T. Nagai, N. Nishigaki, T. Oyama, J. Nishi, H. Wada, M. Sano, H. Toko, H. Akazawa, T. Sato, H. Nakaya, H. Kasanuki, and I. Komuro Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes J. Biol. Chem. 279 2004 11384 11391
26. K.L. Laugwitz, A. Moretti, J. Lam, P. Gruber, Y. Chen, S. Woodard, L.Z. Lin, C.L. Cai, M.M. Lu, M. Reth, O. Platoshyn, J.X. Yuan, S. Evans, and K.R. Chien Postnatal isl1 + cardioblasts enter fully differentiated cardiomyocyte lineages Nature 433 2005 647 653
27. H.C. Ott, T.S. Matthiesen, J. Brechtken, S. Grindle, S.K. Goh, W. Nelson, and D.A. Taylor The adult human heart as a source for stem cells: repair strategies with embryonic-like progenitor cells Nat. Clin. Pract. 4 Suppl. 1 2007 S27 S39
28. F. Limana, A. Zacheo, D. Mocini, A. Mangoni, G. Borsellino, A. Diamantini, R. De Mori, L. Battistini, E. Vigna, M. Santini, V. Loiaconi, G. Pompilio, A. Germani, and M.C. Capogrossi Identification of myocardial and vascular precursor cells in human and mouse epicardium Circ. Res. 101 12 Dec 7 2007 1255 1265
29. R.R. Smith, L. Barile, H.C. Cho, M.K. Leppo, J.M. Hare, E. Messina, A. Giacomello, M.R. Abraham, and E. Marban Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens Circulation 115 2007 896 908
30. D.R. Davis, Y. Zhang, R.R. Smith, K. Cheng, J. Terrovitis, K. Malliaras, T.S. Li, A. White, R. Makkar, and E. Marbán Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue PLoS One 4 2009 e7195
31. R. Mishra, K. Vijayan, E.J. Colletti, D.A. Harrington, T.S. Matthiesen, D. Simpson, S.K. Goh, B.L. Walker, G. Almeida-Porada, D. Wang, C.L. Backer, S.C. Dudley Jr., L.E. Wold, and S. Kaushal Characterization and functionality of cardiac progenitor cells in congenital heart patients Circulation 123 2011 364 373
32. D.R. Davis, Y. Zang, R.R. Smith, K. Cheng, J. Terrovitis, K. Malliaras, T.S. Li, A. White, R. Makkar, and E. Marban Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue PLoS One 4 2009 e7195
33. T.S. Li, K. Cheng, S.T. Lee, S. Matsushita, D. Davis, K. Malliaras, Y. Zhang, N. Matsushita, R.R. Smith, and E. Marban 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
34. Z. Ivanovic Hypoxia or in situ normoxia: the stem cell paradigm J. Cell. Physiol. 219 2009 271 275
35. M.C. Simon, and B. Keith The role of oxygen availability in embryonic development and stem cell function Nat. Rev. Mol. Cell Biol. 9 2008 285 296
36. P.C. Johnson, K. Vandegriff, A.G. Tsai, and M. Intaglietta Effect of acute hypoxia on microcirculatory and tissue oxygen levels in rat cremaster muscle J. Appl. Physiol. 98 2005 1177 1184
37. B.A. McKinley, and B.D. Butler Comparison of skeletal muscle PO2, PCO2, and pH with gastric tonometric P(CO2) and pH in hemorrhagic shock Crit. Care Med. 27 1999 1869 1877
38. D.J. Saltzman, A. Toth, A.G. Tsai, M. Intaglietta, and P.C. Johnson Oxygen tension distribution in postcapillary venules in resting skeletal muscle Am. J. Physiol. Heart Circ. Physiol. 285 2003 H1980 H1985
39. K. Jungermann, and T. Kietzmann Role of oxygen in the zonation of carbohydrate metabolism and gene expression in liver Kidney Int. 51 1997 402 412
40. E.G. Mik, T.G. van Leeuwen, N.J. Raat, and C. Ince Quantitative determination of localized tissue oxygen concentration in vivo by two-photon excitation phosphorescence lifetime measurements J. Appl. Physiol. 97 2004 1962 1969
41. W.J. Welch, H. Baumgartl, D. Lubbers, and C.S. Wilcox Nephron pO2 and renal oxygen usage in the hypertensive rat kidney Kidney Int. 59 2001 230 237
42. J.C. Hemphill III, D. Morabito, M. Farrant, and G.T. Manley Brain tissue oxygen monitoring in intracerebral hemorrhage Neurocrit. Care 3 2005 260 270
43. C.I. Nwaigwe, M.A. Roche, O. Grinberg, and J.F. Dunn Effect of hyperventilation on brain tissue oxygenation and cerebrovenous PO2 in rats Brain Res. 868 2000 150 156
44. D.Y. Yu, S.J. Cringle, and E.N. Su Intraretinal oxygen distribution in the monkey retina and the response to systemic hyperoxia Invest. Ophthalmol. Vis. Sci. 46 2005 4728 4733
45. I. Papandreou, A. Powell, A.L. Lim, and N. Denko Cellular reaction to hypoxia: sensing and responding to an adverse environment Mutat. Res. 569 2005 87 100
46. Y.Y. Jang, and S.J. Sharkis A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche Blood 110 2007 3056 3063
47. S.M. Schieke, M. Ma, L. Cao, J.P. McCoy Jr., C. Liu, N.F. Hensel, A.J. Barrett, M. Boehm, and T. Finkel Mitochondrial metabolism modulates differentiation and teratoma formation capacity in mouse embryonic stem cells J. Biol. Chem. 283 2008 28506 28512
48. D. Furlani, W. Li, E. Pittermann, C. Klopsch, L. Wang, A. Knopp, P. Jungebluth, E. Thedinga, C. Havenstein, I. Westien, M. Ugurlucan, R.K. Li, N. Ma, and G. Steinhoff A transformed cell population derived from cultured mesenchymal stem cells has no functional effect after transplantation into the injured heart Cell Transplant. 18 2009 319 331
49. D.C. van Gent, J.H. Hoeijmakers, and R. Kanaar Chromosomal stability and the DNA double-stranded break connection Nat. Rev. Genet. 2 2001 196 206
50. N.C. Denko Hypoxia, HIF1 and glucose metabolism in the solid tumour Nat. Rev. Cancer 8 2008 705 713
51. B. Keith, and M.C. Simon Hypoxia-inducible factors, stem cells, and cancer Cell 129 2007 465 472
52. T. Ezashi, P. Das, and R.M. Roberts Low O2 tensions and the prevention of differentiation of hES cells Proc. Natl. Acad. Sci. U. S. A. 102 2005 4783 4788
53. Y. Yoshida, K. Takahashi, K. Okita, T. Ichisaka, and S. Yamanaka Hypoxia enhances the generation of induced pluripotent stem cells Cell Stem Cell 5 2009 237 241
54. C. Fehrer, R. Brunauer, G. Laschober, H. Unterluggauer, S. Reitinger, F. Kloss, C. Gully, R. Gassner, and G. Lepperdinger Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan Aging Cell 6 2007 745 757
55. S. Yoshida, M. Sukeno, and Y. Nabeshima A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis Science 317 2007 1722 1726
56. C. Calabrese, H. Poppleton, M. Kocak, T.L. Hogg, C. Fuller, B. Hamner, E.Y. Oh, M.W. Gaber, D. Finklestein, M. Allen, A. Frank, I.T. Bayazitov, S.S. Zakharenko, A. Gajjar, A. Davidoff, and R.J. Gilbertson A perivascular niche for brain tumor stem cells Cancer Cell 11 2007 69 82
57. K.L. Covello, J. Kehler, H. Yu, J.D. Gordan, A.M. Arsham, C.J. Hu, P.A. Labosky, M.C. Simon, and B. Keith HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth Genes Dev. 20 2006 557 570
58. C. Dahlqvist, A. Blokzijl, G. Chapman, A. Falk, K. Dannaeus, C.F. Ibanez, and U. Lendahl Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation Development 130 2003 6089 6099
59. J.L. de la Pompa, A. Wakeham, K.M. Correia, E. Samper, S. Brown, R.J. Aguilera, T. Nakano, T. Honjo, T.W. Mak, J. Rossant, and R.A. Conlon Conservation of the Notch signalling pathway in mammalian neurogenesis Development 124 1997 1139 1148
60. J.D. Gordan, J.A. Bertout, C.J. Hu, J.A. Diehl, and M.C. Simon HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity Cancer Cell 11 2007 335 347
61. E.M. Hansson, U. Lendahl, and G. Chapman Notch signaling in development and disease Semin. Cancer Biol. 14 2004 320 328
62. A. Kaidi, A.C. Williams, and C. Paraskeva Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia Nat. Cell Biol. 9 2007 210 217
63. M. Koshiji, Y. Kageyama, E.A. Pete, I. Horikawa, J.C. Barrett, and L.E. Huang HIF-1alpha induces cell cycle arrest by functionally counteracting Myc EMBO J. 23 2004 1949 1956
64. D. Nofziger, A. Miyamoto, K.M. Lyons, and G. Weinmaster Notch signaling imposes two distinct blocks in the differentiation of C2C12 myoblasts Development 126 1999 1689 1702
65. T.S. Li, K. Cheng, K. Malliaras, N. Matsushita, B. Sun, L. Marban, Y. Zhang, and E. Marban Expansion of human cardiac stem cells in physiological oxygen improves cell production efficiency and potency for myocardial repair Cardiovasc. Res. 89 2010 157 165
66. 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
67. D.C. Slusarski, and F. Pelegri Calcium signaling in vertebrate embryonic patterning and morphogenesis Dev. Biol. 307 2007 1 13
68. M. Puceat, and M. Jaconi Ca2 + signalling in cardiogenesis Cell Calcium 38 2005 383 389
69. W. Liu, K. Yasui, T. Opthof, R. Ishiki, J.K. Lee, K. Kamiya, M. Yokota, and I. Kodama Developmental changes of Ca(2 +) handling in mouse ventricular cells from early embryo to adulthood Life Sci. 71 2002 1279 1292
70. S. Kawano, K. Otsu, S. Shoji, K. Yamagata, and M. Hiraoka Ca(2 +) oscillations regulated by Na(+)-Ca(2 +) exchanger and plasma membrane Ca(2 +) pump induce fluctuations of membrane currents and potentials in human mesenchymal stem cells Cell Calcium 34 2003 145 156
71. S. Kawano, S. Shoji, S. Ichinose, K. Yamagata, M. Tagami, and M. Hiraoka Characterization of Ca(2 +) signaling pathways in human mesenchymal stem cells Cell Calcium 32 2002 165 174
72. S. Kawano, K. Otsu, A. Kuruma, S. Shoji, E. Yanagida, Y. Muto, F. Yoshikawa, Y. Hirayama, K. Mikoshiba, and T. Furuichi ATP autocrine/paracrine signaling induces calcium oscillations and NFAT activation in human mesenchymal stem cells Cell Calcium 39 2006 313 324
73. J.M. Ntambi, and T. Takova Role of Ca2 + in the early stages of murine adipocyte differentiation as evidenced by calcium mobilizing agents Differentiation 60 1996 151 158
74. J. Ferreira-Martins, C. Rondon-Clavo, D. Tugal, J.A. Korn, R. Rizzi, M.E. Padin-Iruegas, S. Ottolenghi, A. De Angelis, K. Urbanek, N. Ide-Iwata, D. D'Amario, T. Hosoda, A. Leri, J. Kajstura, P. Anversa, and M. Rota Spontaneous calcium oscillations regulate human cardiac progenitor cell growth Circ. Res. 105 2009 764 774
75. J. Ferreira-Martins, B. Ogorek, D. Cappetta, A. Matsuda, S. Signore, D. D'Amario, J. Kostyla, E. Steadman, N. Ide-Iwata, F. Sanada, G. Iaffaldano, S. Ottolenghi, T. Hosoda, A. Leri, J. Kajstura, P. Anversa, and M. Rota Cardiomyogenesis in the developing heart is regulated by C-kit-positive cardiac stem cells Circ. Res. 110 2012 701 715
76. C. Altomare, L. Barile, S. Marangoni, M. Rocchetti, M. Alemanni, G. Mostacciuolo, A. Giacomello, E. Messina, and A. Zaza Caffeine-induced Ca(2 +) signaling as an index of cardiac progenitor cells differentiation Basic Res. Cardiol. 105 2010 737 749
77. R. Gaetani, M. Ledda, L. Barile, I. Chimenti, F. De Carlo, E. Forte, V. Ionta, L. Giuliani, E. D'Emilia, G. Frati, F. Miraldi, D. Pozzi, E. Messina, S. Grimaldi, A. Giacomello, and A. Lisi Differentiation of human adult cardiac stem cells exposed to extremely low-frequency electromagnetic fields Cardiovasc. Res. 82 2009 411 420
78. T. Lonergan, C. Brenner, and B. Bavister Differentiation-related changes in mitochondrial properties as indicators of stem cell competence J. Cell. Physiol. 208 2006 149 153
79. C.T. Chen, Y.R. Shih, T.K. Kuo, O.K. Lee, and Y.H. Wei Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells Stem Cells 26 2008 960 968
80. Y.M. Cho, S. Kwon, Y.K. Pak, H.W. Seol, Y.M. Choi, J. Park do, K.S. Park, and H.K. Lee Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells Biochem. Biophys. Res. Commun. 348 2006 1472 1478
81. A. Prigione, B. Fauler, R. Lurz, H. Lehrach, and J. Adjaye The senescence-related mitochondrial/oxidative stress pathway is repressed in human induced pluripotent stem cells Stem Cells 28 2010 721 733
82. V. Gogvadze, S. Orrenius, and B. Zhivotovsky Mitochondria in cancer cells: what is so special about them? Trends Cell Biol. 18 2008 165 173
83. F.L. Crespo, V.R. Sobrado, L. Gomez, A.M. Cervera, and K.J. McCreath Mitochondrial reactive oxygen species mediate cardiomyocyte formation from embryonic stem cells in high glucose Stem Cells 28 2010 1132 1142
84. J.M. Facucho-Oliveira, and J.C. St John The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation Stem Cell Rev. 5 2009 140 158
85. C.D. Folmes, T.J. Nelson, A. Martinez-Fernandez, D.K. Arrell, J.Z. Lindor, P.P. Dzeja, Y. Ikeda, C. Perez-Terzic, and A. Terzic Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming Cell Metab. 14 2011 264 271
86. C.D. Folmes, T.J. Nelson, and A. Terzic Energy metabolism in nuclear reprogramming Biomark. Med. 5 2011 715 729
87. Y. Zhang, T.S. Li, S.T. Lee, K.A. Wawrowsky, K. Cheng, G. Galang, K. Malliaras, M.R. Abraham, C. Wang, and E. Marban Dedifferentiation and proliferation of mammalian cardiomyocytes PLoS One 5 2010 e12559
88. J.J. Lum, D.E. Bauer, M. Kong, M.H. Harris, C. Li, T. Lindsten, and C.B. Thompson Growth factor regulation of autophagy and cell survival in the absence of apoptosis Cell 120 2005 237 248
89. N.G. Frangogiannis, and M.L. Entman Chemokines in myocardial ischemia Trends Cardiovasc. Med. 15 2005 163 169
90. D.E. Wright, E.P. Bowman, A.J. Wagers, E.C. Butcher, and I.L. Weissman Hematopoietic stem cells are uniquely selective in their migratory response to chemokines J. Exp. Med. 195 2002 1145 1154
91. T. Nagasawa, K. Tachibana, and T. Kishimoto A novel CXC chemokine PBSF/SDF-1 and its receptor CXCR4: their functions in development, hematopoiesis and HIV infection Semin. Immunol. 10 1998 179 185
92. J.D. Abbott, Y. Huang, D. Liu, R. Hickey, D.S. Krause, and F.J. Giordano Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury Circulation 110 2004 3300 3305
93. A.T. Askari, S. Unzek, Z.B. Popovic, C.K. Goldman, F. Forudi, M. Kiedrowski, A. Rovner, S.G. Ellis, J.D. Thomas, P.E. DiCorleto, E.J. Topol, and M.S. Penn Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy Lancet 362 2003 697 703
94. K. Pillarisetti, and S.K. Gupta Cloning and relative expression analysis of rat stromal cell derived factor-1 (SDF-1)1: SDF-1 alpha mRNA is selectively induced in rat model of myocardial infarction Inflammation 25 2001 293 300
95. Y.R. Zou, A.H. Kottmann, M. Kuroda, I. Taniuchi, and D.R. Littman Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development Nature 393 1998 595 599
96. D. Kuraitis, P. Zhang, Y. Zhang, D.T. Padavan, K. McEwan, T. Sofrenovic, D. McKee, J. Zhang, M. Griffith, X. Cao, A. Musaro, M. Ruel, and E.J. Suuronen A stromal cell-derived factor-1 releasing matrix enhances the progenitor cell response and blood vessel growth in ischaemic skeletal muscle Eur. Cell Mater. 22 2011 109 123
97. N. Itoh The Fgf families in humans, mice, and zebrafish: their evolutional processes and roles in development, metabolism, and disease Biol. Pharm. Bull. 30 2007 1819 1825
98. N. Rosenblatt-Velin, M.G. Lepore, C. Cartoni, F. Beermann, and T. Pedrazzini FGF-2 controls the differentiation of resident cardiac precursors into functional cardiomyocytes J. Clin. Invest. 115 2005 1724 1733
99. C.E. Murry, H. Reinecke, and L.M. Pabon Regeneration gaps: observations on stem cells and cardiac repair J. Am. Coll. Cardiol. 47 2006 1777 1785
100. S.S. Fazel, L. Chen, D. Angoulvant, S.H. Li, R.D. Weisel, A. Keating, and R.K. Li Activation of c-kit is necessary for mobilization of reparative bone marrow progenitor cells in response to cardiac injury FASEB J. 22 2008 930 940
101. S. Vandervelde, M.J. van Luyn, M.H. Rozenbaum, A.H. Petersen, R.A. Tio, and M.C. Harmsen Stem cell-related cardiac gene expression early after murine myocardial infarction Cardiovasc. Res. 73 2007 783 793
102. F.L. Xiang, X. Lu, L. Hammoud, P. Zhu, P. Chidiac, J. Robbins, and Q. Feng Cardiomyocyte-specific overexpression of human stem cell factor improves cardiac function and survival after myocardial infarction in mice Circulation 120 2009 1065 1074 (1069 p following 1074)
103. C. Bearzi, M. Rota, T. Hosoda, J. Tillmanns, A. Nascimbene, A. De Angelis, S. Yasuzawa-Amano, I. Trofimova, R.W. Siggins, N. Lecapitaine, S. Cascapera, A.P. Beltrami, D.A. D'Alessandro, E. Zias, F. Quaini, K. Urbanek, R.E. Michler, R. Bolli, J. Kajstura, A. Leri, and P. Anversa Human cardiac stem cells Proc. Natl. Acad. Sci. U. S. A. 104 2007 14068 14073
104. I. Chimenti, R. Gaetani, L. Barile, G. Frati, E. Messina, and A. Giacomello c-kit cardiac progenitor cells: what is their potential? Proc. Natl. Acad. Sci. U. S. A. 106 2009 E78 (author reply E79)
105. T.S. Li, K. Cheng, K. Malliaras, R.R. Smith, Y. Zhang, B. Sun, N. Matsushita, A. Blusztajn, J. Terrovitis, H. Kusuoka, L. Marban, and E. Marban Direct comparison of different stem cell types and subpopulations reveals superior paracrine potency and myocardial repair efficacy with cardiosphere-derived cells J. Am. Coll. Cardiol. 59 2012 942 953
106. R.R. Smith, I. Chimenti, E. Marban, Unselected human cardiosphere-derived cells are functionally superior to c-Kit- or CD90-purified cardiosphere-derived cells, in: Circulation (Ed.) AHA Scientific Session 2008, vol. 118, Circulation, Orlando, FL, USA, 2008, pp. S-420.
107. N. Maulik Angiogenic signal during cardiac repair Mol. Cell. Biochem. 264 2004 13 23
108. N. Qipshidze, N. Metreveli, P.K. Mishra, D. Lominadze, and S.C. Tyagi Hydrogen sulfide mitigates cardiac remodeling during myocardial infarction via improvement of angiogenesis Int. J. Biol. Sci. 8 2012 430 441
109. L. Claesson-Welsh, M. Welsh, N. Ito, B. Anand-Apte, S. Soker, B. Zetter, M. O'Reilly, and J. Folkman Angiostatin induces endothelial cell apoptosis and activation of focal adhesion kinase independently of the integrin-binding motif RGD Proc. Natl. Acad. Sci. U. S. A. 95 1998 5579 5583
110. N. Yamaguchi, B. Anand-Apte, M. Lee, T. Sasaki, N. Fukai, R. Shapiro, I. Que, C. Lowik, R. Timpl, and B.R. Olsen Endostatin inhibits VEGF-induced endothelial cell migration and tumor growth independently of zinc binding EMBO J. 18 1999 4414 4423
111. I. Chimenti, R.R. Smith, T.S. Li, G. Gerstenblith, E. Messina, A. Giacomello, and E. Marban Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice Circ. Res. 106 2010 971 980
112. N.E. Tsopanoglou, and M.E. Maragoudakis Thrombin's central role in angiogenesis and pathophysiological processes Eur. Cytokine Netw. 20 2009 171 179
113. M. Caunt, Y.Q. Huang, P.C. Brooks, and S. Karpatkin Thrombin induces neoangiogenesis in the chick chorioallantoic membrane J. Thromb. Haemost. 1 2003 2097 2102
114. P. Zania, M. Papaconstantinou, C.S. Flordellis, M.E. Maragoudakis, and N.E. Tsopanoglou Thrombin mediates mitogenesis and survival of human endothelial cells through distinct mechanisms Am. J. Physiol. Cell Physiol. 294 2008 C1215 C1226
115. C. Fabrizi, F. Angelini, I. Chimenti, E. Pompili, F. Somma, R. Gaetani, E. Messina, L. Fumagalli, A. Giacomello, and G. Frati Thrombin and thrombin-derived peptides promote proliferation of cardiac progenitor cells in the form of cardiospheres without affecting their differentiation potential J. Biol. Regul. Homeost. Agents 25 2011 S43 S51
116. S. Freyberg, Y.H. Song, F. Muehlberg, and E. Alt Thrombin peptide (TP508) promotes adipose tissue-derived stem cell proliferation via PI3 kinase/Akt pathway J. Vasc. Res. 46 2009 98 102
117. I. Bock-Marquette, S. Shrivastava, G.C. Pipes, J.E. Thatcher, A. Blystone, J.M. Shelton, C.L. Galindo, B. Melegh, D. Srivastava, E.N. Olson, and J.M. DiMaio 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
118. N. Smart, S. Bollini, K.N. Dube, J.M. Vieira, B. Zhou, S. Davidson, D. Yellon, J. Riegler, A.N. Price, M.F. Lythgoe, W.T. Pu, and P.R. Riley De novo cardiomyocytes from within the activated adult heart after injury Nature 474 2011 640 644
119. K.G. Aghila Rani, and C.C. Kartha Effects of epidermal growth factor on proliferation and migration of cardiosphere-derived cells expanded from adult human heart Growth Factors 28 2010 157 165
120. E. Willems, P.J. Bushway, and M. Mercola Natural and synthetic regulators of embryonic stem cell cardiogenesis Pediatr. Cardiol. 30 2009 635 642
121. E. Willems, S. Spiering, H. Davidovics, M. Lanier, Z. Xia, M. Dawson, J. Cashman, and M. Mercola Small-molecule inhibitors of the Wnt pathway potently promote cardiomyocytes from human embryonic stem cell-derived mesoderm Circ. Res. 109 2011 360 364
122. M. Lanier, D. Schade, E. Willems, M. Tsuda, S. Spiering, J. Kalisiak, M. Mercola, and J.R. Cashman Wnt inhibition correlates with human embryonic stem cell cardiomyogenesis: a structure-activity relationship study based on inhibitors for the Wnt response J. Med. Chem. 55 2012 697 708
123. H. Wang, J. Hao, and C.C. Hong Cardiac induction of embryonic stem cells by a small molecule inhibitor of Wnt/beta-catenin signaling ACS Chem. Biol. 6 2011 192 197
124. X.H. Parsons, Y.D. Teng, J.F. Parsons, E.Y. Snyder, D.B. Smotrich, and D.A. Moore Efficient derivation of human cardiac precursors and cardiomyocytes from pluripotent human embryonic stem cells with small molecule induction J. Vis. Exp. 2011 e3274
125. M. Stastna, M.R. Abraham, and J.E. Van Eyk Cardiac stem/progenitor cells, secreted proteins, and proteomics FEBS Lett. 583 2009 1800 1807
126. D. Van Hoof, A.J. Heck, J. Krijgsveld, and C.L. Mummery Proteomics and human embryonic stem cells Stem Cell Res. 1 2008 169 182
127. S. Roche, M. Provansal, L. Tiers, C. Jorgensen, and S. Lehmann Proteomics of primary mesenchymal stem cells Regen. Med. 1 2006 511 517
128. R. Hoffrogge, S. Beyer, U. Volker, A.M. Uhrmacher, and A. Rolfs 2-DE proteomic profiling of neuronal stem cells Neurodegener. Dis. 3 2006 112 121
129. M.H. Maurer, R.E. Feldmann Jr., C.D. Futterer, and W. Kuschinsky The proteome of neural stem cells from adult rat hippocampus Proteome Sci. 1 2003 4
130. J. Graumann, N.C. Hubner, J.B. Kim, K. Ko, M. Moser, C. Kumar, J. Cox, H. Scholer, and M. Mann Stable isotope labeling by amino acids in cell culture (SILAC) and proteome quantitation of mouse embryonic stem cells to a depth of 5,111 proteins Mol. Cell. Proteomics 7 2008 672 683
131. M.Y. Choi, Y.J. An, S.H. Kim, S.H. Roh, H.K. Ju, S.S. Hong, J.H. Park, K.J. Cho, D.W. Choi, and S.W. Kwon Mass spectrometry based proteomic analysis of human stem cells: a brief review Exp. Mol. Med. 39 2007 690 695
132. H. Baharvand, M. Hajheidari, R. Zonouzi, S.K. Ashtiani, S. Hosseinkhani, and G.H. Salekdeh Comparative proteomic analysis of mouse embryonic stem cells and neonatal-derived cardiomyocytes Biochem. Biophys. Res. Commun. 349 2006 1041 1049
133. S.M. Ahn, R.J. Goode, and R.J. Simpson Stem cell markers: insights from membrane proteomics? Proteomics 8 2008 4946 4957
134. R.L. Gundry, K.R. Boheler, J.E. Van Eyk, and B. Wollscheid A novel role for proteomics in the discovery of cell-surface markers on stem cells: scratching the surface Proteomics Clin. Appl. 2 2008 892 903
135. K. Nunomura, K. Nagano, C. Itagaki, M. Taoka, N. Okamura, Y. Yamauchi, S. Sugano, N. Takahashi, T. Izumi, and T. Isobe Cell surface labeling and mass spectrometry reveal diversity of cell surface markers and signaling molecules expressed in undifferentiated mouse embryonic stem cells Mol. Cell. Proteomics 4 2005 1968 1976
136. C. Nakanishi, M. Yamagishi, K. Yamahara, I. Hagino, H. Mori, Y. Sawa, T. Yagihara, S. Kitamura, and N. Nagaya Activation of cardiac progenitor cells through paracrine effects of mesenchymal stem cells Biochem. Biophys. Res. Commun. 374 2008 11 16
137. M. Gnecchi, H. He, O.D. Liang, L.G. Melo, F. Morello, H. Mu, N. Noiseux, L. Zhang, R.E. Pratt, J.S. Ingwall, and V.J. Dzau Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells Nat. Med. 11 2005 367 368
138. M. Gnecchi, H. He, N. Noiseux, O.D. Liang, L. Zhang, F. Morello, H. Mu, L.G. Melo, R.E. Pratt, J.S. Ingwall, and V.J. Dzau Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement FASEB J. 20 2006 661 669
139. M. Stastna, I. Chimenti, E. Marban, and J.E. Van Eyk Identification and functionality of proteomes secreted by rat cardiac stem cells and neonatal cardiomyocytes Proteomics 10 2010 245 253
140. M. Shimpo, D.A. Morrow, E.O. Weinberg, M.S. Sabatine, S.A. Murphy, E.M. Antman, and R.T. Lee Serum levels of the interleukin-1 receptor family member ST2 predict mortality and clinical outcome in acute myocardial infarction Circulation 109 2004 2186 2190
141. E.O. Weinberg, M. Shimpo, S. Hurwitz, S. Tominaga, J.L. Rouleau, and R.T. Lee Identification of serum soluble ST2 receptor as a novel heart failure biomarker Circulation 107 2003 721 726
142. E.O. Weinberg, M. Shimpo, G.W. De Keulenaer, C. MacGillivray, S. Tominaga, S.D. Solomon, J.L. Rouleau, and R.T. Lee Expression and regulation of ST2, an interleukin-1 receptor family member, in cardiomyocytes and myocardial infarction Circulation 106 2002 2961 2966
143. J. Schmitz, A. Owyang, E. Oldham, Y. Song, E. Murphy, T.K. McClanahan, G. Zurawski, M. Moshrefi, J. Qin, X. Li, D.M. Gorman, J.F. Bazan, and R.A. Kastelein IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines Immunity 23 2005 479 490
144. S. Sanada, D. Hakuno, L.J. Higgins, E.R. Schreiter, A.N. McKenzie, and R.T. Lee IL-33 and ST2 comprise a critical biomechanically induced and cardioprotective signaling system J. Clin. Invest. 117 2007 1538 1549
145. M. Stastna, and J.E. Van Eyk Secreted proteins as a fundamental source for biomarker discovery Proteomics 12 2012 722 735