Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts (original) (raw)

• Mallory, G.K., White, P.D. & Salcedo-Salgar, J. The speed of healing of myocardial infarcts: a study of the pathologic anatomy in seventy-two cases. Am. Heart J. 18, 647–671 (1939).
  Article Google Scholar
• Rumiantsev, P. Growth and Hyperplasia of Cardiac Muscle Cells (Harwood, London/New York, 1991).
  Google Scholar
• Pasumarthi, K.B. & Field, L.J. Cardiomyocyte cell cycle regulation. Circ. Res. 90, 1044–1054 (2002).
  Article CAS Google Scholar
• Rubart, M. & Field, L.J. Cardiac regeneration: repopulating the heart. Annu. Rev. Physiol. 68, 29–49 (2006).
  Article CAS Google Scholar
• Laflamme, M.A. & Murry, C.E. Regenerating the heart. Nat. Biotechnol. 23, 845–856 (2005).
  Article CAS Google Scholar
• Dimmeler, S., Zeiher, A.M. & Schneider, M.D. Unchain my heart: the scientific foundations of cardiac repair. J. Clin. Invest. 115, 572–583 (2005).
  Article CAS Google Scholar
• Murry, C.E., Field, L.J. & Menasche, P. Cell-based cardiac repair: reflections at the 10-year point. Circulation 112, 3174–3183 (2005).
  Article Google Scholar
• Xu, C., Police, S., Rao, N. & Carpenter, M.K. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ. Res. 91, 501–508 (2002).
  Article CAS Google Scholar
• Mummery, C. et al. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 107, 2733–2740 (2003).
  Article CAS Google Scholar
• Kehat, I. et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J. Clin. Invest. 108, 407–414 (2001).
  Article CAS Google Scholar
• McDevitt, T.C., Laflamme, M.A. & Murry, C.E. Proliferation of cardiomyocytes derived from human embryonic stem cells is mediated via the IGF/PI 3-kinase/Akt signaling pathway. J. Mol. Cell. Cardiol. 39, 865–873 (2005).
  Article CAS Google Scholar
• Snir, M. et al. Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 285, H2355–H2363 (2003).
  Article CAS Google Scholar
• Laflamme, M.A. et al. Formation of human myocardium in the rat heart from human embryonic stem cells. Am. J. Pathol. 167, 663–671 (2005).
  Article CAS Google Scholar
• Kehat, I. et al. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat. Biotechnol. 22, 1282–1289 (2004).
  Article CAS Google Scholar
• Xue, T. et al. Functional integration of electrically active cardiac derivatives from genetically engineered human embryonic stem cells with quiescent recipient ventricular cardiomyocytes: insights into the development of cell-based pacemakers. Circulation 111, 11–20 (2005).
  Article Google Scholar
• Leobon, B. et al. Myoblasts transplanted into rat infarcted myocardium are functionally isolated from their host. Proc. Natl. Acad. Sci. USA 100, 7808–7811 (2003).
  Article CAS Google Scholar
• Rubart, M., Soonpaa, M.H., Nakajima, H. & Field, L.J. Spontaneous and evoked intracellular calcium transients in donor-derived myocytes following intracardiac myoblast transplantation. J. Clin. Invest. 114, 775–783 (2004).
  Article CAS Google Scholar
• Weier, H.U. et al. Two-color hybridization with high complexity chromosome-specific probes and a degenerate alpha satellite probe DNA allows unambiguous discrimination between symmetrical and asymmetrical translocations. Chromosoma 100, 371–376 (1991).
  Article CAS Google Scholar
• Shi, Y., Evans, J.E. & Rock, K.L. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425, 516–521 (2003).
  Article CAS Google Scholar
• Zvibel, I., Smets, F. & Soriano, H. Anoikis: roadblock to cell transplantation? Cell Transplant. 11, 621–630 (2002).
  Article Google Scholar
• Cao, G. et al. In vivo delivery of a Bcl-xL fusion protein containing the TAT protein transduction domain protects against ischemic brain injury and neuronal apoptosis. J. Neurosci. 22, 5423–5431 (2002).
  Article CAS Google Scholar
• Baines, C.P. et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434, 658–662 (2005).
  Article CAS Google Scholar
• Nakagawa, T. et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434, 652–658 (2005).
  Article CAS Google Scholar
• Ardehali, H., O'Rourke, B. & Mitochondrial, K. ATP channels in cell survival and death. J. Mol. Cell. Cardiol. 39, 7–16 (2005).
  Article CAS Google Scholar
• Davis, M.E. et al. Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc. Natl. Acad. Sci. USA 103, 8155–8160 (2006).
  Article CAS Google Scholar
• Montolio, M., Tellez, N., Biarnes, M., Soler, J. & Montanya, E. Short-term culture with the caspase inhibitor z-VAD.fmk reduces beta cell apoptosis in transplanted islets and improves the metabolic outcome of the graft. Cell Transplant. 14, 59–65 (2005).
  Article Google Scholar
• Zhang, M. et al. Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J. Mol. Cell. Cardiol. 33, 907–921 (2001).
  Article CAS Google Scholar
• Zuppinger, C., Eppenberger-Eberhardt, M. & Eppenberger, H.M. N-Cadherin: structure, function and importance in the formation of new intercalated disc-like cell contacts in cardiomyocytes. Heart Fail. Rev. 5, 251–257 (2000).
  Article CAS Google Scholar
• Nussbaum, J. et al. Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response. FASEB J. 21, 1345–1357 (2007).
  Article CAS Google Scholar
• Swijnenburg, R.J. et al. Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium. Circulation 112, I166–I172 (2005).
  PubMed Google Scholar
• Contreras, J.L. et al. Cytoprotection of pancreatic islets before and early after transplantation using gene therapy. Kidney Int. 61, 79–84 (2002).
  Article Google Scholar
• Nakano, M. et al. Caspase-3 inhibitor prevents apoptosis of human islets immediately after isolation and improves islet graft function. Pancreas 29, 104–109 (2004).
  Article CAS Google Scholar
• Schierle, G.S. et al. Caspase inhibition reduces apoptosis and increases survival of nigral transplants. Nat. Med. 5, 97–100 (1999).
  Article CAS Google Scholar
• Emgard, M. et al. Both apoptosis and necrosis occur early after intracerebral grafting of ventral mesencephalic tissue: a role for protease activation. J. Neurochem. 86, 1223–1232 (2003).
  Article CAS Google Scholar
• Guerette, B. et al. Prevention by anti-LFA-1 of acute myoblast death following transplantation. J. Immunol. 159, 2522–2531 (1997).
  CAS PubMed Google Scholar
• Skuk, D., Caron, N.J., Goulet, M., Roy, B. & Tremblay, J.P. Resetting the problem of cell death following muscle-derived cell transplantation: detection, dynamics and mechanisms. J. Neuropathol. Exp. Neurol. 62, 951–967 (2003).
  Article CAS Google Scholar
• Gnecchi, M. et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat. Med. 11, 367–368 (2005).
  Article CAS Google Scholar
• Gnecchi, M. et al. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J. 20, 661–669 (2006).
  Article CAS Google Scholar
• Ebelt, H. et al. Cellular cardiomyoplasty: improvement of left ventricular function correlates with the release of cardioactive cytokines. Stem Cells 25, 236–244 (2007).
  Article CAS Google Scholar
• Kinnaird, T. et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ. Res. 94, 678–685 (2004).
  Article CAS Google Scholar
• Laflamme, M.A., Zbinden, S., Epstein, S.E. & Murry, C.E. Cell-based cardiac repair: pathophysiologic mechanisms. Annu. Rev. Pathol. Mech. Dis. 2, 307–339 (2007).
  Article CAS Google Scholar
• Rubart, M. et al. Physiological coupling of donor and host cardiomyocytes after cellular transplantation. Circ. Res. 92, 1217–1224 (2003).
  Article CAS Google Scholar
• Tallini, Y.N. et al. Imaging cellular signals in the heart in vivo: cardiac expression of the high-signal Ca2+ indicator GCaMP2. Proc. Natl. Acad. Sci. USA 103, 4753–4758 (2006).
  Article CAS Google Scholar
• Smith, J.C., Price, B.M., Van Nimmen, K. & Huylebroeck, D. Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature 345, 729–731 (1990).
  Article CAS Google Scholar
• Nakajima, Y., Yamagishi, T., Ando, K. & Nakamura, H. Significance of bone morphogenetic protein-4 function in the initial myofibrillogenesis of chick cardiogenesis. Dev. Biol. 245, 291–303 (2002).
  Article CAS Google Scholar
• Ladd, A.N., Yatskievych, T.A. & Antin, P.B. Regulation of avian cardiac myogenesis by activin/TGFbeta and bone morphogenetic proteins. Dev. Biol. 204, 407–419 (1998).
  Article CAS Google Scholar
• Sugi, Y. & Lough, J. Activin-A and FGF-2 mimic the inductive effects of anterior endoderm on terminal cardiac myogenesis in vitro. Dev. Biol. 168, 567–574 (1995).
  Article CAS Google Scholar
• Lough, J. et al. Combined BMP-2 and FGF-4, but neither factor alone, induces cardiogenesis in non-precardiac embryonic mesoderm. Dev. Biol. 178, 198–202 (1996).
  Article CAS Google Scholar
• Barron, M., Gao, M. & Lough, J. Requirement for BMP and FGF signaling during cardiogenic induction in non-precardiac mesoderm is specific, transient, and cooperative. Dev. Dyn. 218, 383–393 (2000).
  Article CAS Google Scholar
• Xu, C., Police, S., Hassanipour, M. & Gold, J.D. Cardiac bodies: a novel culture method for enrichment of cardiomyocytes derived from human embryonic stem cells. Stem Cells Dev. 15, 631–639 (2006).
  Article CAS Google Scholar
• Rao, B.M. & Zandstra, P.W. Culture development for human embryonic stem cell propagation: molecular aspects and challenges. Curr. Opin. Biotechnol. 16, 568–576 (2005).
  Article CAS Google Scholar
• Zandstra, P.W. & Nagy, A. Stem cell bioengineering. Annu. Rev. Biomed. Eng. 3, 275–305 (2001).
  Article CAS Google Scholar
• Beqqali, A., Kloots, J., Ward-van Oostwaard, D., Mummery, C. & Passier, R. Genome-wide transcriptional profiling of human embryonic stem cells differentiating to cardiomyocytes. Stem Cells 24, 1956–1967 (2006).
  Article CAS Google Scholar
• Bauwens, C., Yin, T., Dang, S., Peerani, R. & Zandstra, P.W. Development of a perfusion fed bioreactor for embryonic stem cell-derived cardiomyocyte generation: oxygen-mediated enhancement of cardiomyocyte output. Biotechnol. Bioeng. 90, 452–461 (2005).
  Article CAS Google Scholar
• Zandstra, P.W. et al. Scalable production of embryonic stem cell-derived cardiomyocytes. Tissue Eng. 9, 767–778 (2003).
  Article CAS Google Scholar
• Xu, C., Police, S., Hassanipour, M. & Gold, J.D. Cardiac bodies: a novel culture method for enrichment of cardiomyocytes derived from human embryonic stem cells. Stem Cells Dev. 15, 631–639 (2006).
  Article CAS Google Scholar
• Gold, J. et al. Efficient serum-free generation of cardiomyocytes from human embryonic stem cells in the absence of embryoid bodies (abstract). in Circulation 112 (17, Suppl. S), U62–U62 (2005).
  Google Scholar
• Thomson, J.A. et al. Embryonic stem cell lines derived from human blastocysts. Science 282, 1145–1147 (1998).
  Article CAS Google Scholar
• Xu, C. et al. Feeder-free growth of undifferentiated human embryonic stem cells. Nat. Biotechnol. 19, 971–974 (2001).
  Article CAS Google Scholar
• Bialik, S. et al. The mitochondrial apoptotic pathway is activated by serum and glucose deprivation in cardiac myocytes. Circ. Res. 85, 403–414 (1999).
  Article CAS Google Scholar
• Malhotra, R. & Brosius, F.C., III Glucose uptake and glycolysis reduce hypoxia-induced apoptosis in cultured neonatal rat cardiac myocytes. J. Biol. Chem. 274, 12567–12575 (1999).
  Article CAS Google Scholar
• Shimizu, S., Konishi, A., Kodama, T. & Tsujimoto, Y. BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc. Natl. Acad. Sci. USA 97, 3100–3105 (2000).
  Article CAS Google Scholar
• Griffiths, E.J. & Halestrap, A.P. Protection by Cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts. J. Mol. Cell. Cardiol. 25, 1461–1469 (1993).
  Article CAS Google Scholar
• Halestrap, A.P., Connern, C.P., Griffiths, E.J. & Kerr, P.M. Cyclosporin A binding to mitochondrial cyclophilin inhibits the permeability transition pore and protects hearts from ischaemia/reperfusion injury. Mol. Cell. Biochem. 174, 167–172 (1997).
  Article CAS Google Scholar
• Reiss, K. et al. Insulin-like growth factor-1 receptor and its ligand regulate the reentry of adult ventricular myocytes into the cell cycle. Exp. Cell Res. 235, 198–209 (1997).
  Article CAS Google Scholar
• Mehrhof, F.B. et al. In cardiomyocyte hypoxia, insulin-like growth factor-I-induced antiapoptotic signaling requires phosphatidylinositol-3-OH-kinase-dependent and mitogen-activated protein kinase-dependent activation of the transcription factor cAMP response element-binding protein. Circulation 104, 2088–2094 (2001).
  Article CAS Google Scholar
• Vanden Hoek, T., Becker, L.B., Shao, Z.H., Li, C.Q. & Schumacker, P.T. Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ. Res. 86, 541–548 (2000).
  Article CAS Google Scholar
• Akao, M., Ohler, A., O'Rourke, B. & Marban, E. Mitochondrial ATP-sensitive potassium channels inhibit apoptosis induced by oxidative stress in cardiac cells. Circ. Res. 88, 1267–1275 (2001).
  Article CAS Google Scholar
• Akao, M. et al. Differential actions of cardioprotective agents on the mitochondrial death pathway. Circ. Res. 92, 195–202 (2003).
  Article CAS Google Scholar
• Reinecke, H. & Murry, C.E. Cell grafting for cardiac repair. Methods Mol. Biol. 219, 97–112 (2003).
  PubMed Google Scholar
• Murry, C.E. et al. Hematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428, 664–668 (2004).
  Article CAS Google Scholar
• Minami, E., Laflamme, M.A., Saffitz, J.E. & Murry, C.E. Extracardiac progenitor cells repopulate most major cell types in the transplanted human heart. Circulation 112, 2951–2958 (2005).
  Article Google Scholar
• Nicklas, J.A. & Buel, E. Development of an Alu-based, real-time PCR method for quantitation of human DNA in forensic samples. J. Forensic Sci. 48, 936–944 (2003).
  CAS PubMed Google Scholar
• Sambrook, J., Fritsch, E.F. & Maniatis, T. Appendix C: Properties of nucleic acids. in Molecular Cloning, A Laboratory Manual (Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA, 1989).
  Google Scholar