Heme Oxygenase-1 Gene Therapy Provides Cardioprotection Via Control of Post-Ischemic Inflammation: An Experimental Study in a Pre-Clinical Pig Model

Journal of the American College of Cardiology

Volumn 66, Issue 2, 2015, Pages 154-165

  Hinkel, Rabea ^a,b   Lange, Philipp ^a   Petersen, Björn ^c   Gottlieb, Elena ^a   Ng, Judy King Man ^a,b   Finger, Stefanie ^d   Horstkotte, Jan ^a   Lee, Seungmin ^a   Thormann, Michael ^a   Knorr, Maike ^d   El Aouni, Chiraz ^a   Boekstegers, Peter ^a   Reichart, Bruno ^a   Wenzel, Philip ^d   Niemann, Heiner ^c   Kupatt, Christian ^a,b  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^d German Center for Cardiovascular Research   (Germany)

Author keywords

adenoassociated virus; cardiomyocyte; endothelial; reperfusion; transgenic

Indexed keywords

CD14 ANTIGEN; HEME OXYGENASE 1; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; MYELOPEROXIDASE; PARVOVIRUS VECTOR; HMOX1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CARDIOVASCULAR GENE THERAPY; CARDITIS; CONTROLLED STUDY; DRUG EFFICACY; EXPERIMENTAL STUDY; FLUORESCENCE ACTIVATED CELL SORTING; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PORCINE MODEL; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; ANIMAL; COMPLICATION; DEPENDOPARVOVIRUS; DISEASE MODEL; GENE THERAPY; GENE VECTOR; GENETICS; INFLAMMATION; PIG; PROCEDURES; REPERFUSION INJURY;

ANIMALS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GENETIC THERAPY; GENETIC VECTORS; HEME OXYGENASE-1; INFLAMMATION; MICE; MYOCARDIAL ISCHEMIA; REPERFUSION INJURY; SWINE;

EID: 84939163244     PISSN: 07351097     EISSN: 15583597     Source Type: Journal    
DOI: 10.1016/j.jacc.2015.04.064     Document Type: Article

References (41)

1. K. Hao, H. Hanawa, L. Ding, and et al. Free heme is a danger signal inducing expression of proinflammatory proteins in cultured cells derived from normal rat hearts Mol Immunol 48 2011 1191 1202
2. S.W. Ryter, J. Alam, and A.M.K. Choi Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications Physiol Rev 86 2006 583 650
3. X. Liu, J.A. Simpson, K.R. Brunt, and et al. Preemptive heme oxygenase-1 gene delivery reveals reduced mortality and preservation of left ventricular function 1 yr after acute myocardial infarction Am J Physiol Heart Circ Physiol 293 2007 H48 H59
4. A.S. Pachori, L.G. Melo, L. Zhang, S.D. Solomon, and V.J. Dzau Chronic recurrent myocardial ischemic injury is significantly attenuated by pre-emptive adeno-associated virus heme oxygenase-1 gene delivery J Am Coll Cardiol 47 2006 635 643
5. G. Wang, T. Hamid, R.J. Keith, and et al. Cardioprotective and antiapoptotic effects of heme oxygenase-1 in the failing heart Circulation 121 2010 1912 1925
6. M. Nahrendorf, F.K. Swirski, E. Aikawa, and et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions J Exp Med 204 2007 3037 3047
7. X. Liu, A.S. Pachori, C.A. Ward, and et al. Heme oxygenase-1 (HO-1) inhibits postmyocardial infarct remodeling and restores ventricular function FASEB J 20 2006 207 216
8. L. Timmers, G. Pasterkamp, V.C. de Hoog, F. Arslan, Y. Appelman, and D.P. de Kleijn The innate immune response in reperfused myocardium Cardiovasc Res 94 2012 276 283
9. N.G. Frangogiannis Regulation of the inflammatory response in cardiac repair Circ Res 110 2012 159 173
10. S. Epelman, P.P. Liu, and D.L. Mann Role of innate and adaptive immune mechanisms in cardiac injury and repair Nat Rev Immunol 15 2015 117 129
11. S. Wantha, J.E. Alard, R.T.A. Megens, and et al. Neutrophil-derived cathelicidin promotes adhesion of classical monocytes Circ Res 112 2013 792 801
12. P. Libby, M. Nahrendorf, and F.K. Swirski Monocyte heterogeneity in cardiovascular disease Semin Immunopathol 35 2013 553 562
13. I.M. Seropian, S. Toldo, B.W. Van Tassell, and A. Abbate Anti-inflammatory strategies for ST-elevation acute myocardial infarction ventricular remodeling J Am Coll Cardiol 63 2014 1593 1603
14. S.F. Yet, R. Tian, M.D. Layne, and et al. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice Circ Res 89 2001 168 173
15. Y. Zhao, L. Zhang, Y. Qiao, and et al. Heme oxygenase-1 prevents cardiac dysfunction in streptozotocin-diabetic mice by reducing inflammation, oxidative stress, apoptosis and enhancing autophagy PLoS One 8 2013 e75927
16. J. Xue, and A. Habtezion Carbon monoxide-based therapy ameliorates acute pancreatitis via TLR4 inhibition J Clin Invest 124 2014 437 447
17. L.T. Bish, K. Morine, M.M. Sleeper, and et al. AAV9 provides global cardiac gene transfer superior to AAV1, AAV6, AAV7, and AAV8 in the mouse and rat Hum Gene Ther 19 2008 1359 1368
18. S.F. Yet, M.A. Perrella, M.D. Layne, and et al. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice J Clin Invest 103 1999 R23 R29
19. Y. Zhang, J. Takagawa, R.E. Sievers, and et al. Validation of the wall motion score and myocardial performance indexes as novel techniques to assess cardiac function in mice after myocardial infarction Am J Physiol Heart Circ Physiol 292 2007 H1187 H1192
20. T. Wollenweber, C. Zach, C. Rischpler, and et al. Myocardial perfusion imaging is feasible for infarct size quantification in mice using a clinical single-photon emission computed tomography system equipped with pinhole collimators Mol Imaging Biol 12 2010 427 434
21. J. Horstkotte, T. Perisic, M. Schneider, and et al. Mitochondrial thioredoxin reductase is essential for early postischemic myocardial protection Circulation 124 2011 2892 2902
22. B. Petersen, W. Ramackers, A. Lucas-Hahn, and et al. Transgenic expression of human heme oxygenase-1 in pigs confers resistance against xenograft rejection during ex vivo perfusion of porcine kidneys Xenotransplantation 18 2011 355 368
23. C. Kupatt, R. Hinkel, M.L. von Bruhl, and et al. Endothelial nitric oxide synthase overexpression provides a functionally relevant angiogenic switch in hibernating pig myocardium J Am Coll Cardiol 49 2007 1575 1584
24. C. Kupatt, R. Hinkel, A. Pfosser, and et al. Cotransfection of vascular endothelial growth factor-A and platelet-derived growth factor-B via recombinant adeno-associated virus resolves chronic ischemic malperfusion: role of vessel maturation J Am Coll Cardiol 56 2010 414 422
25. R. Hinkel, D. Penzkofer, S. Zuehlke, and et al. Inhibition of microRNA-92a protects against ischemia-reperfusion injury in a large animal model Circulation 128 2013 1066 1075
26. R. Hinkel, C. El-Aouni, T. Olson, and et al. Thymosin ß 4 is an essential paracrine factor of embryonic endothelial progenitor cell-mediated cardioprotection Circulation 117 2008 2232 2240
27. C. Kupatt, R. Hinkel, M. Lamparter, and et al. Retroinfusion of embryonic endothelial progenitor cells attenuates ischemia-reperfusion injury in pigs: role of phosphatidylinositol 3-kinase/AKT kinase Circulation 112 Suppl 2005 I117 I122
28. C. Kupatt, R. Wichels, J. Horstkotte, F. Krombach, H. Habazettl, and P. Boekstegers Molecular mechanisms of platelet-mediated leukocyte recruitment during myocardial reperfusion J Leukoc Biol 72 2002 455 461
29. J. Takagawa, Y. Zhang, M.L. Wong, and et al. Myocardial infarct size measurement in the mouse chronic infarction model: comparison of area- and length-based approaches J Appl Physiol 102 2007 2104 2111
30. F. Leuschner, P.J. Rauch, T. Ueno, and et al. Rapid monocyte kinetics in acute myocardial infarction are sustained by extramedullary monocytopoiesis J Exp Med 209 2012 123 137
31. M.P. Seldon, G. Silva, N. Pejanovic, and et al. Heme oxygenase-1 inhibits the expression of adhesion molecules associated with endothelial cell activation via inhibition of NF-kappaB RelA phosphorylation at serine 276 J Immunol 179 2007 7840 7851
32. D. Chabannes, M. Hill, E. Merieau, and et al. A role for heme oxygenase-1 in the immunosuppressive effect of adult rat and human mesenchymal stem cells Blood 110 2007 3691 3694
33. M.P. Soares, Y. Lin, J. Anrather, and et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival Nat Med 4 1998 1073 1077
34. S.T. Pleger, C. Shan, J. Ksienzyk, and et al. Cardiac AAV9-S100A1 gene therapy rescues post-ischemic heart failure in a preclinical large animal model Sci Transl Med 3 2011 92ra64
35. A. Asokan, and R.J. Samulski An emerging adeno-associated viral vector pipeline for cardiac gene therapy Hum Gene Ther 24 2013 906 913
36. X.M. Wang, H.P. Kim, K. Nakahira, S.W. Ryter, and A.M.K. Choi The heme oxygenase-1/carbon monoxide pathway suppresses TLR4 signaling by regulating the interaction of TLR4 with caveolin-1 J Immunol 182 2009 3809 3818
37. P. Mandal, S. Roychowdhury, P.H. Park, B.T. Pratt, T. Roger, and L.E. Nagy Adiponectin and heme oxygenase-1 suppress TLR4/MyD88-independent signaling in rat Kupffer cells and in mice after chronic ethanol exposure J Immunol 185 2010 4928 4937
38. G. Li, D. Tang, and M.T. Lotze Menage a trois in stress: DAMPs, redox and autophagy Semin Cancer Biol 23 2013 380 390
39. M. Andrassy, H.C. Volz, J.C. Igwe, and et al. High-mobility group box-1 in ischemia-reperfusion injury of the heart Circulation 117 2008 3216 3226
40. X. Liu, J. Wei, D.H. Peng, M.D. Layne, and S.F. Yet Absence of heme oxygenase-1 exacerbates myocardial ischemia/reperfusion injury in diabetic mice Diabetes 54 2005 778 784
41. J. Ma, C.K. Lau, A. Obed, and et al. A cell penetrating heme oxygenase protein protects heart graft against ischemia/reperfusion injury Gene Ther 16 2009 320 328