Cobalt protoporphyrin pretreatment protects human embryonic stem cell-derived cardiomyocytes from hypoxia/reoxygenation injury in vitro and increases graft size and vascularization in vivo

Stem Cells Translational Medicine

Volumn 3, Issue 6, 2014, Pages 734-744

  Luo, Jun ^a   Weaver, Matthew S ^a   Cao, Baohong ^a   Dennis, James E ^a   Van Biber, Benjamin ^b   Laflamme, Michael A ^b   Allen, Margaret D ^a,b  

^a BENAROYA RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Acute myocardial infarction; Cell therapy; Heme oxygenase 1; Human embryonic stem cell; Infarct repair; Preconditioning

Indexed keywords

HEME OXYGENASE 1; PROTEIN KINASE B; PROTOPORPHYRIN COBALT; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NKX2.5; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CAPILLARY DENSITY; CELL PROTECTION; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME PHOSPHORYLATION; FEMALE; GRAFT SIZE; GRAFT SURVIVAL; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HYPOXIA; MALE; MORPHOMETRICS; NONHUMAN; PHYSICAL PARAMETERS; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; RAT; REOXYGENATION; UPREGULATION; VASCULARIZATION;

ACUTE MYOCARDIAL INFARCTION; CELL THERAPY; HEME OXYGENASE-1; HUMAN EMBRYONIC STEM CELL; INFARCT REPAIR; PRECONDITIONING;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; EMBRYONIC STEM CELLS; ENZYME INDUCTION; FEMALE; GRAFT SURVIVAL; HEME OXYGENASE-1; HUMANS; MALE; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PROTOPORPHYRINS; RATS; RATS, NUDE; REACTIVE OXYGEN SPECIES; REGENERATION; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84901747545     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2013-0189     Document Type: Article

References (67)

1. Zhang M, Methot D, Poppa V et al. Cardiomyocyte grafting for cardiac repair: Graft cell death and anti-death strategies. J Mol Cell Cardiol 2001;33:907-921.
2. LaflammeMA, Chen KY, NaumovaAV et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 2007;25:1015-1024.
3. Li RK, Mickle DA, Weisel RD et al. Optimal time for cardiomyocyte transplantation to maximize myocardial function after left ventricular injury. Ann Thorac Surg 2001;72:1957-1963.
4. Terrovitis JV, Smith RR, Marbán E. Assessment and optimization of cell engraftment after transplantation into the heart. Circ Res 2010; 106:479-494.
5. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation 1986;74:1124-1136.
6. Bolli R. The late phase of preconditioning. Circ Res 2000;87:972-983.
7. Melo LG, Agrawal R, Zhang L et al. Gene therapy strategy for long-term myocardial protection using adeno-associated virus-mediated delivery of heme oxygenase gene. Circulation 2002;105:602-607.
8. Tang YL, Qian K, Zhang YC et al. A vigilant, hypoxia-regulated hemeoxygenase-1 gene vector in the heart limits cardiac injury after ischemia-reperfusion in vivo. J Cardiovasc Pharmacol Ther 2005;10:251-263.
9. Lin HH, Chen YH, Chang PF et al. Heme oxygenase-1 promotes neovascularization in ischemic heart by coinduction of VEGF and SDF-1. J Mol Cell Cardiol 2008;45:44-55.
10. Kearns-Jonker M, Dai W, Gunthart M et al. Genetically engineered mesenchymal stem cells influence gene expression in donor cardiomyocytes and the recipient heart. J Stem Cell Res Ther 2012;S1. pii:005.
11. Yet SF, Tian R, Layne MD et al. Cardiacspecific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ Res 2001;89:168-173.
12. Araujo JA, Meng L, Tward AD et al. Systemic rather than local heme oxygenase-1 overexpression improves cardiac allograft outcomes in a new transgenic mouse. J Immunol 2003; 171:1572-1580.
13. Wang G, Hamid T, Keith RJ et al. Cardioprotective and antiapoptotic effects of heme oxygenase-1 in the failing heart. Circulation 2010;121:1912-1925.
14. Lakkisto P, Kytö V, Forsten H et al. Heme oxygenase-1 and carbon monoxide promote neovascularization after myocardial infarction by modulating the expression of HIF-1alpha, SDF-1alpha and VEGF-B. Eur J Pharmacol 2010;635:156-164.
15. Lakkisto P, Siren JM, Kytö V et al. Heme oxygenase-1 induction protects the heart and modulates cellular and extracellular remodelling after myocardial infarction in rats. Exp Biol Med (Maywood) 2011;236:1437-1448.
16. Katori M, Buelow R, Ke B et al. Heme oxygenase-1 overexpression protects rat hearts from cold ischemia/reperfusion injury via an antiapoptotic pathway. Transplantation 2002; 73:287-292.
17. Akamatsu Y, Haga M, Tyagi S et al. Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. FASEB J 2004;18: 771-772.
18. Kawamoto S, Flynn JP, Shi Q et al. Heme oxygenase-1 induction enhances cell survival and restores contractility to unvascularized three-dimensional adult cardiomyocyte grafts implanted in vivo. Tissue Eng Part A 2011;17: 1605-1614.
19. Luo J, Weaver M, Van Biber B et al. Heme oxygenase-1 induction protects human embryonic-derived cardiomyocytes against hypoxia/reoxygenation injury and improves cell survival and angiogenesis in vivo. American Heart Association Scientific Sessions, Chicago, IL, November 15, 2010. Circulation 2010;122: A18196 (Abstract)
20. Laflamme MA, Gold J, Xu C et al. Formation ofhumanmyocardium in the rat heart from human embryonic stem cells. AmJ Pathol 2005; 167:663-671.
21. Robey TE, Saiget MK, Reinecke H et al. Systems approaches to preventing transplanted cell death in cardiac repair. J Mol Cell Cardiol 2008;45:567-581.
22. Chimenti I, Smith RR, Li TS et al. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res 2010;106:971-980.
23. Dulak J, Deshane J, Jozkowicz A et al. Heme oxygenase-1 and carbon monoxide in vascular pathobiology: Focus on angiogenesis. Circulation 2008;117:231-241.
24. Brusko TM, Wasserfall CH, Agarwal A et al. An integral role for heme oxygenase-1 and carbon monoxide in maintaining peripheral tolerance by CD4+CD25+ regulatory T cells. J Immunol 2005;174:5181-5186.
25. Tang YL, Tang Y, Zhang YC et al. Protection from ischemic heart injury by a vigilant heme oxygenase-1 plasmid system. Hypertension 2004;43:746-751.
26. Liu X, Simpson JA, Brunt KR et al. Preemptivehemeoxygenase-1 gene delivery reveals reduced mortality and preservation of left ventricular function 1 yr after acute myocardial infarction. Am J Physiol Heart Circ Physiol 2007; 293:H48-H59.
27. Fernandes S, Naumova AV, Zhu WZ et al. Human embryonic stem cell-derived cardiomyocytes engraft but do not alter cardiac remodeling after chronic infarction in rats. J Mol Cell Cardiol 2010;49:941-949.
28. Caspi O, Lesman A, Basevitch Y et al. Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 2007;100:263-272.
29. Trigona WL, Porter CM, Horvath-Arcidiacono JA et al. Could heme-oxygenase-1 have a role in modulating the recipient immune response to embryonic stem cells? Antioxid Redox Signal 2007;9:751-756.
30. Drukker M, Katchman H, Katz G et al. Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. STEM CELLS 2006;24: 221-229.
31. Zhu WZ, Van Biber B, Laflamme MA. Methods for the derivation and use of cardiomyocytes from human pluripotent stem cells. Methods Mol Biol 2011;767:419-431.
32. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145-1147.
33. Xu C, Inokuma MS, Denham J et al. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 2001;19: 971-974.
34. Negroni E, Riederer I, Chaouch S et al. In vivo myogenic potential of human CD133+ muscle-derived stem cells:Aquantitative study. Mol Ther 2009;17:1771-1778.
35. Weiss A, Leinwand LA. The mammalian myosin heavy chain gene family. Annu Rev Cell Dev Biol 1996;12:417-439.
36. Fishbein MC, Maclean D, Maroko PR. Experimental myocardial infarction in the rat: Qualitative and quantitative changes during pathologic evolution. Am J Pathol 1978;90: 57-70.
37. Virag JI, Murry CE. Myofibroblast and endothelial cell proliferation during murine myocardial infarct repair. Am J Pathol 2003;163: 2433-2440.
38. Nicklas JA, Buel E. Development of an Alu-based, real-time PCR method for quantitation of human DNA in forensic samples. J Forensic Sci 2003;48:936-944.
39. Hausenloy DJ, Yellon DM. Survival kinases in ischemic preconditioning and postconditioning. Cardiovasc Res 2006;70:240-253.
40. Dai W, Field LJ, Rubart M et al. Survival and maturation of human embryonic stem cell-derived cardiomyocytes in rat hearts. J Mol Cell Cardiol 2007;43:504-516.
41. Shiba Y, Fernandes S, Zhu WZ et al. HumanES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 2012;489:322-325.
42. Leor J, Gerecht S, Cohen S et al. Human embryonic stem cell transplantation to repair the infarcted myocardium. Heart 2007;93: 1278-1284.
43. Hu X, Wang J, Chen J et al. Optimal temporal delivery of bone marrow mesenchymal stem cells in rats with myocardial infarction. Eur J Cardiothorac Surg 2007;31:438-443.
44. Lee ST, White AJ, Matsushita S et al. Intramyocardial injection of autologous cardiospheres or cardiosphere-derived cells preserves function and minimizes adverse ventricular remodeling in pigs with heart failure postmyocardial infarction. J Am Coll Cardiol 2011;57:455-465.
45. Haider HK, Ashraf M. Strategies to promote donor cell survival: Combining preconditioning approach with stem cell transplantation. J Mol Cell Cardiol 2008;45: 554-566.
46. Jiang S, Haider HK, Idris NM et al. Supportive interaction between cell survival signaling and angiocompetent factors enhances donor cell survival and promotes angiomyogenesis for cardiac repair. Circ Res 2006;99:776-784.
47. Abraham NG, Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 2008;60:79-127.
48. Gozzelino R, Jeney V, Soares MP. Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol 2010;50: 323-354.
49. Bilban M, Haschemi A, Wegiel B et al. Heme oxygenase and carbon monoxide initiate homeostatic signaling. J Mol Med (Berl) 2008; 86:267-279.
50. Piantadosi CA, Carraway MS, Babiker A et al. Hemeoxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ Res 2008;103:1232-1240.
51. Clark JE, Foresti R, Sarathchandra P et al. Heme oxygenase-1-derived bilirubin ameliorates postischemic myocardial dysfunction. Am J Physiol Heart Circ Physiol 2000;278: H643-H651.
52. Pachori AS, Smith A, McDonald P et al. Heme-oxygenase-1-induced protection against hypoxia/reoxygenation is dependent on biliverdin reductase and its interaction with PI3K/Akt pathway. J Mol Cell Cardiol 2007; 43:580-592.
53. Fujimoto H, Ohno M, Ayabe S et al. Carbon monoxide protects against cardiac ischemia-reperfusion injury in vivo via MAPK and Akt-eNOS pathways. Arterioscler Thromb Vasc Biol 2004;24:1848-1853.
54. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: From basic science to therapeutic applications. Physiol Rev 2006;86:583-650.
55. Suliman HB, Carraway MS, Tatro LG et al. A new activating role for CO in cardiac mitochondrial biogenesis. J Cell Sci 2007;120: 299-308.
56. SuttnerDM, Dennery PA. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J 1999;13: 1800-1809.
57. McDevitt TC, Laflamme MA, Murry CE. Proliferation of cardiomyocytes derived from human embryonic stem cells is mediated via the IGF/PI 3-kinase/Akt signaling pathway. J Mol Cell Cardiol 2005;39:865-873.
58. Qiao H, Surti S, Choi SR et al. Death and proliferation time course of stem cells transplanted in the myocardium. Mol Imaging Biol 2009;11:408-414.
59. van Laake LW, van Donselaar EG, Monshouwer-Kloots J et al. Extracellular matrix formation after transplantation of human embryonic stem cell-derived cardiomyocytes. Cell Mol Life Sci 2010;67:277-290.
60. van Laake LW, Passier R, Doevendans PA et al. Humanembryonic stem cell-derived cardiomyocytes and cardiac repair in rodents. Circ Res 2008;102:1008-1010.
61. Brouard S, Otterbein LE, Anrather J et al. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med 2000;192:1015-1026.
62. Fazel S, Cimini M, Chen L et al. Cardioprotective c-kit+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J Clin Invest 2006;116: 1865-1877.
63. Ellison GM, Vicinanza C, Smith AJ et al. Adult c-kit(pos) cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell 2013;154:827-842.
64. Cai C, Teng L, Vu D et al. The heme oxygenase 1 inducer (CoPP) protects human cardiac stem cells against apoptosis through activation of the extracellular signal-regulated kinase (ERK)/NRF2 signaling pathway and cytokine release. J Biol Chem 2012;287:33720-33732.
65. Kehat I, Khimovich L, Caspi O et al. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol 2004;22:1282-1289.
66. Xue T, Cho HC, Akar FG 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 2005;111:11-20.
67. Tang YL, Tang Y, Zhang YC et al. Improved graft mesenchymal stem cell survival in ischemic heart with a hypoxia-regulated heme oxygenase-1 vector. J Am Coll Cardiol 2005; 46:1339-1350.