Preconditioning Human Cardiac Stem Cells with an HO-1 Inducer Exerts Beneficial Effects after Cell Transplantation in the Infarcted Murine Heart

Stem Cells

Volumn 33, Issue 12, 2015, Pages 3596-3607

  Cai, Chuanxi ^a,b   Guo, Yiru ^a   Teng, Lei ^a,b   Nong, Yibing ^a   Tan, Min ^a   Book, Michael J ^a   Zhu, Xiaoping ^a   Wang, Xiao Liang ^a,b   Du, Junjie ^a   Wu, Wen Jian ^a   Xie, Wei ^a   Hong, Kyung U ^a   Li, Qianhong ^a   Bolli, Roberto ^a  

^a University of Louisville School of Medicine   (United States)

^b ALBANY MEDICAL COLLEGE   (United States)

Author keywords

Cell survival; Cobalt protoporphyrin; Heart failure; HO 1 inducer; Human cardiac stem cell; Myocardial infarction; Preconditioning

Indexed keywords

CELL NUCLEUS ANTIGEN; GREEN FLUORESCENT PROTEIN; HEME OXYGENASE 1; PROTOPORPHYRIN COBALT; ENZYME ACTIVATOR; HMOX1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ARTICLE; CARDIAC STEM CELL; CELL LINEAGE; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSPLANTATION; COMPLIANCE (PHYSICAL); CONTROLLED STUDY; CORONARY ARTERY OCCLUSION; GENE EXPRESSION; HEART FUNCTION; HEART INFARCTION; HEART LEFT VENTRICLE DP-DT; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART TRANSPLANTATION; HEART VENTRICLE REMODELING; HLA SYSTEM; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MOUSE; MURINE; NONHUMAN; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SCID MOUSE; TISSUE SECTION; ANIMAL; CARDIAC MUSCLE; ENZYMOLOGY; METABOLISM; MYOCARDIAL INFARCTION; PATHOLOGY; STEM CELL; STEM CELL TRANSPLANTATION; XENOGRAFT;

ANIMALS; ENZYME ACTIVATORS; HEME OXYGENASE-1; HETEROGRAFTS; HUMANS; MICE; MYOCARDIAL INFARCTION; MYOCARDIUM; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84983094265     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2198     Document Type: Article

References (46)

1. Hong KU, Bolli R., Cardiac stem cell therapy for cardiac repair. Curr Treat Options Cardiovasc Med 2014; 16: 324.
2. Sanganalmath SK, Bolli R., Cell therapy for heart failure: A comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ Res 2013; 113: 810-834.
3. Bearzi C, Rota M, Hosoda T, et al., Human cardiac stem cells. Proc Natl Acad Sci USA 2007; 104: 14068-14073.
4. Bolli R, Tang XL, Sanganalmath SK, et al., Intracoronary delivery of autologous cardiac stem cells improves cardiac function in a porcine model of chronic ischemic cardiomyopathy. Circulation 2013; 128: 122-131.
5. Linke A, Muller P, Nurzynska D, et al., Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function. Proc Natl Acad Sci USA 2005; 102: 8966-8971.
6. Fischer KM, Cottage CT, Wu W, et al., Enhancement of myocardial regeneration through genetic engineering of cardiac progenitor cells expressing Pim-1 kinase. Circulation 2009; 120: 2077-2087.
7. Angert D, Berretta RM, Kubo H, et al., Repair of the injured adult heart involves new myocytes potentially derived from resident cardiac stem cells. Circ Res 2011; 108: 1226-1237.
8. Dawn B, Stein AB, Urbanek K, et al., Cardiac stem cells delivered intravascularly traverse the vessel barrier, regenerate infarcted myocardium, and improve cardiac function. Proc Natl Acad Sci USA 2005; 102: 3766-3771.
9. Tang XL, Rokosh G, Sanganalmath SK, et al., Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation 2010; 121: 293-305.
10. Taghavi S, Sharp TE, 3rd, Duran JM, et al., Autologous c-Kit+ mesenchymal stem cell injections provide superior therapeutic benefit as compared to c-Kit+ cardiac-derived stem cells in a feline model of isoproterenol-induced cardiomyopathy. Clin Transl Sci 2015 [Epub ahead of print].
11. Li Q, Guo Y, Ou Q, et al., Intracoronary administration of cardiac stem cells in mice: A new, improved technique for cell therapy in murine models. Basic Res Cardiol 2011; 106: 849-864.
12. Bolli R, Chugh AR, D'Amario D, et al., Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): Initial results of a randomised phase 1 trial. Lancet 2011; 378: 1847-1857.
13. Chugh AR, Beache GM, Loughran JH, et al., Administration of cardiac stem cells in patients with ischemic cardiomyopathy: The SCIPIO trial: Surgical aspects and interim analysis of myocardial function and viability by magnetic resonance. Circulation 2012; 126: S54-64.
14. Hong KU, Li QH, Guo Y, et al., A highly sensitive and accurate method to quantify absolute numbers of c-kit+ cardiac stem cells following transplantation in mice. Basic Res Cardiol 2013; 108: 346.
15. Hong KU, Guo Y, Li QH, et al., c-kit+ Cardiac stem cells alleviate post-myocardial infarction left ventricular dysfunction despite poor engraftment and negligible retention in the recipient heart. PLoS One 2014; 9: e96725.
16. Laflamme MA, Chen KY, Naumova AV, 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.
17. Haider H, Ashraf M., Preconditioning and stem cell survival. J Cardiovasc Transl Res 2010; 3: 89-102.
18. Mohsin S, Khan M, Toko H, et al., Human cardiac progenitor cells engineered with Pim-I kinase enhance myocardial repair. J Am Coll Cardiol 2012; 60: 1278-1287.
19. Ryter SW, Alam J, Choi AM., Heme oxygenase-1/carbon monoxide: From basic science to therapeutic applications. Physiol Rev 2006; 86: 583-650.
20. Tsoyi K, Kim HJ, Shin JS, et al., HO-1 and JAK-2/STAT-1 signals are involved in preferential inhibition of iNOS over COX-2 gene expression by newly synthesized tetrahydroisoquinoline alkaloid, CKD712, in cells activated with lipopolysacchride. Cell Signal 2008; 20: 1839-1847.
21. Li Q, Guo Y, Ou Q, et al., Gene transfer of inducible nitric oxide synthase affords cardioprotection by upregulating heme oxygenase-1 via a nuclear factor-{kappa}B-dependent pathway. Circulation 2009; 120: 1222-1230.
22. Abraham NG, Kappas A., Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 2008; 60: 79-127.
23. Ryter SW, Morse D, Choi AM., Carbon monoxide and bilirubin: Potential therapies for pulmonary/vascular injury and disease. Am J Respir Cell Mol Biol 2007; 36: 175-182.
24. Woo J, Iyer S, Mori N, et al., Alleviation of graft-versus-host disease after conditioning with cobalt-protoporphyrin, an inducer of heme oxygenase-1. Transplantation 2000; 69: 623-633.
25. 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.
26. L'Abbate A, Neglia D, Vecoli C, et al., Beneficial effect of heme oxygenase-1 expression on myocardial ischemia-reperfusion involves an increase in adiponectin in mildly diabetic rats. Am J Physiol Heart Circ Physiol 2007; 293: H3532-3541.
27. 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.
28. Cheng K, Gupta S., Quantitative tools for assessing the fate of xenotransplanted human stem/progenitor cells in chimeric mice. Xenotransplantation 2009; 16: 145-151.
29. He JQ, Vu DM, Hunt G, et al., Human cardiac stem cells isolated from atrial appendages stably express c-kit. PLoS One 2011; 6: e27719.
30. Becker KF, Schott C, Hipp S, et al., Quantitative protein analysis from formalin-fixed tissues: Implications for translational clinical research and nanoscale molecular diagnosis. J Pathol 2007; 211: 370-378.
31. Rosova I, Dao M, Capoccia B, et al., Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 2008; 26: 2173-2182.
32. Pasha Z, Wang Y, Sheikh R, et al., Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovasc Res 2008; 77: 134-142.
33. 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 College Cardiol 2005; 46: 1339-1350.
34. Reinecke H, Zhang M, Bartosek T, et al., Survival, integration, and differentiation of cardiomyocyte grafts: A study in normal and injured rat hearts. Circulation 1999; 100: 193-202.
35. Toma C, Pittenger MF, Cahill KS, et al., Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002; 105: 93-98.
36. Duran JM, Makarewich CA, Sharp TE, et al., Bone-derived stem cells repair the heart after myocardial infarction through transdifferentiation and paracrine signaling mechanisms. Circ Res 2013; 113: 539-552.
37. Williams AR, Hatzistergos KE, Addicott B, et al., Enhanced effect of combining human cardiac stem cells and bone marrow mesenchymal stem cells to reduce infarct size and to restore cardiac function after myocardial infarction. Circulation 2013; 127: 213-223.
38. Mirotsou M, Jayawardena TM, Schmeckpeper J, et al., Paracrine mechanisms of stem cell reparative and regenerative actions in the heart. J Mol Cell Cardiol 2011; 50: 280-289.
39. Zhou P, Wirthlin L, McGee J, et al., Contribution of human hematopoietic stem cells to liver repair. Semin Immunopathol 2009; 31: 411-419.
40. Chen L, Tredget EE, Wu PY, et al., Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 2008; 3: e1886.
41. Gnecchi M, Zhang Z, Ni A, et al., Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008; 103: 1204-1219.
42. Burchfield JS, Dimmeler S., Role of paracrine factors in stem and progenitor cell mediated cardiac repair and tissue fibrosis. Fibrogenesis Tissue Repair 2008; 1: 4.
43. Shintani S, Kusano K, Ii M, et al., Synergistic effect of combined intramyocardial CD34+ cells and VEGF2 gene therapy after MI. Nat Clin Pract Cardiovasc Med 2006; 3 (suppl 1): S123-128.
44. Stastna M, Abraham MR, Van Eyk JE., Cardiac stem/progenitor cells, secreted proteins, and proteomics. FEBS Lett 2009; 583: 1800-1807.
45. Stastna M, Chimenti I, Marban E, et al., Identification and functionality of proteomes secreted by rat cardiac stem cells and neonatal cardiomyocytes. Proteomics 2010; 10: 245-253.
46. Czibik G, Derumeaux G, Sawaki D, et al., Heme oxygenase-1: An emerging therapeutic target to curb cardiac pathology. Basic Res Cardiol 2014; 109: 450.