Gene transfer as a strategy to achieve permanent cardioprotection II: rAAV-mediated gene therapy with heme oxygenase-1 limits infarct size 1 year later without adverse functional consequences

Basic Research in Cardiology

Volumn 106, Issue 6, 2011, Pages 1367-1377

  Li, Qianhong ^a   Guo, Yiru ^a   Ou, Qinghui ^a   Wu, Wen Jian ^a   Chen, Ning ^a   Zhu, Xiaoping ^a   Tan, Wei ^a   Yuan, Fangping ^a   Dawn, Buddhadeb ^a,b   Luo, Li ^a   Hunt, Gregory N ^a   Bolli, Roberto ^a  

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

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Cardiac function; Gene therapy; Heme oxygenase 1; Mouse; Myocardial infarction

Indexed keywords

BETA GALACTOSIDASE; HEME OXYGENASE 1; PARVOVIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE; GENE EXPRESSION; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART LEFT VENTRICLE FUNCTION; HEART LEFT VENTRICLE SIZE; HEART LEFT VENTRICLE WALL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HEME OXYGENASE 1 GENE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VIVO GENE TRANSFER; MALE; MOUSE; NONHUMAN; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRUS RECOMBINANT;

ADENOVIRIDAE; ANIMALS; BLOTTING, WESTERN; FOLLOW-UP STUDIES; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED ICR; MYOCARDIAL INFARCTION; MYOCARDIAL ISCHEMIA; NITRIC OXIDE SYNTHASE TYPE II; VENTRICULAR FUNCTION, LEFT;

EID: 84856702610     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-011-0208-6     Document Type: Article

References (46)

1. Abraham NG, Asija A, Drummond G, Peterson S (2007) Heme oxygenase-1 gene therapy: recent advances and therapeutic applications. Curr Gene Ther 7:89-108 (Pubitemid 46681767)
2. Abraham NG, Kappas A (2005) Heme oxygenase and the cardiovascular-renal system. Free Radic Biol Med 39:1-25. doi: 10.1016/j.freeradbiomed.2005.03.010 (Pubitemid 40733115)
3. Abraham NG, Kappas A (2008) Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 60:79-127. doi: 10.1124/pr.107.07104 (Pubitemid 351439218)
4. Akagi R, Takahashi T, Sassa S (2005) Cytoprotective effects of heme oxygenase in acute renal failure. Contrib Nephrol 148:70-85. doi:10.1159/000086044 (Pubitemid 43264923)
5. Alam J, Cook JL (2007) How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol 36:166-174. doi:10.1165/rcmb.2006-0340TR (Pubitemid 46233469)
6. Bolli R (2000) The late phase of preconditioning. Circ Res 87:972-983
7. Bolli R, Li QH, Tang XL, Guo Y, Xuan YT, Rokosh G, Dawn B (2007) The late phase of preconditioning and its natural clinical application-gene therapy. Heart Fail Rev 12:189-199. doi: 10.1007/s10741-007-9031-4 (Pubitemid 350176692)
8. Dawn B, Bolli R (2005) HO-1 induction by HIF-1: a new mechanism for delayed cardioprotection? Am J Physiol Heart Circ Physiol 289: H522-H524. doi:10.1152/ajpheart.00274.2005 (Pubitemid 41129364)
9. Flotte TR, Schwiebert EM, Zeitlin PL, Carter BJ, Guggino WB (2005) Correlation between DNA transfer and cystic fibrosis airway epithelial cell correction after recombinant adeno-associated virus serotype 2 gene therapy. Hum Gene Ther 16:921-928. doi:10.1089/hum.2005.16.921 (Pubitemid 41153861)
10. Gardin JM, Siri FM, Kitsis RN, Edwards JG, Leinwand LA (1995) Echocardiographic assessment of left ventricular mass and systolic function in mice. Circ Res 76:907-914
11. Guo Y, Bao W, Wu WJ, Shinmura K, Tang XL, Bolli R (2000) Evidence for an essential role of cyclooxygenase-2 as a mediator of the late phase of ischemic preconditioning in mice. Basic Res Cardiol 95:479-484 (Pubitemid 32013988)
12. Guo Y, Jones WK, Xuan YT, Tang XL, Bao W, Wu WJ, Han H, Laubach VE, Ping P, Yang Z, Qiu Y, Bolli R (1999) The late phase of ischemic preconditioning is abrogated by targeted disruption of the inducible NO synthase gene. Proc Natl Acad Sci USA 96:11507-11512 (Pubitemid 29487411)
13. Guo Y, Stein AB, Wu WJ, Tan W, Zhu X, Li QH, Dawn B, Motterlini R, Bolli R (2004) Administration of a CO-releasing molecule at the time of reperfusion reduces infarct size in vivo. Am J Physiol Heart Circ Physiol 286: H1649-H1653. doi: 10.1152/ajpheart.00971.2003 (Pubitemid 38525450)
14. Guo Y, Wu WJ, Qiu Y, Tang XL, Yang Z, Bolli R (1998) Demonstration of an early and a late phase of ischemic preconditioning in mice. Am J Physiol 275: H1375-H1387
15. Hajjar RJ, Schmidt U, Matsui T, Guerrero JL, Lee KH, Gwathmey JK, Dec. GW, Semigran MJ, Rosenzweig A (1998) Modulation of ventricular function through gene transfer in vivo. Proc Natl Acad Sci USA 95:5251-5256 (Pubitemid 28208584)
16. Hajjar RJ, Zsebo K (2007) AAV vectors and cardiovascular disease: targeting TNF receptor in the heart: clue to way forward with AAV? Gene Ther 14:1611-1612. doi:10.1038/sj.gt.3303047 (Pubitemid 350143186)
17. Hangaishi M, Ishizaka N, Aizawa T, Kurihara Y, Taguchi J, Nagai R, Kimura S, Ohno M (2000) Induction of heme oxygenase-1 can act protectively against cardiac ischemia/reperfusion in vivo. Biochem Biophys Res Commun 279:582-588. doi: 10.1006/bbrc.2000.3973 (Pubitemid 32016758)
18. Henckaerts E, Linden RM (2010) Adeno-associated virus: a key to the human genome? Future Virol 5:555-574. doi:10.2217/fvl.10.48
19. Hester ME, Foust KD, Kaspar RW, Kaspar BK (2009) AAV as a gene transfer vector for the treatment of neurological disorders: novel treatment thoughts for ALS. Curr Gene Ther 9:428-433
20. Heusch G, Boengler K, Schulz R (2008) Cardioprotection: nitric oxide, protein kinases, and mitochondria. Circulation 118:1915-1919. doi:10.1161/CIRCULATIONAHA.108.805242
21. Jiang Y, Chen L, Tang Y, Ma G, Shen C, Qi C, Zhu Q, Yao Y, Liu N (2010) HO-1 gene overexpression enhances the beneficial effects of superparamagnetic iron oxide labeled bone marrow stromal cells transplantation in swine hearts underwent ischemia/reperfusion: an MRI study. Basic Res Cardiol 105:431-442. doi: 10.1007/s00395-009-0079-2
22. Jones JM, Wilson KH, Koch WJ, Milano CA (2002) Adenoviral gene transfer to the heart during cardiopulmonary bypass: effect of myocardial protection technique on transgene expression. Eur J Cardiothorac Surg 21:847-852 pii: S1010794002000787 (Pubitemid 34308943)
23. Kapitulnik J, Maines MD (2009) Pleiotropic functions of biliverdin reductase: cellular signaling and generation of cytoprotective and cytotoxic bilirubin. Trends Pharmacol Sci 30:129-137. doi:10.1016/j.tips.2008.12.003
24. Katori M, Buelow R, Ke B, Ma J, Coito AJ, Iyer S, Southard D, Busuttil RW, Kupiec-Weglinski JW (2002) Heme oxygenase-1 overexpression protects rat hearts from cold ischemia/reperfusion injury via an antiapoptotic pathway. Transplantation 73:287-292 (Pubitemid 34112855)
25. Li Q, Guo Y, Ou Q, Chen N, Wu WJ, Yuan F, O'Brien E, Wang T, Luo L, Hunt GN, Zhu X, Bolli R (2011) Intracoronary administration of cardiac stem cells in mice: a new, improved technique for cell therapy in murine models. Basic Res Cardiol. doi:10.1007/s00395-011-0180-1
26. Li Q, Guo Y, Ou Q, Cui C, Wu WJ, Tan W, Zhu X, Lanceta LB, Sanganalmath SK, Dawn B, Shinmura K, Rokosh GD, Wang S, Bolli R (2009) Gene transfer of inducible nitric oxide synthase affords cardioprotection by upregulating heme oxygenase-1 via a nuclear factor-{kappa}B-dependent pathway. Circulation 120:1222-1230. doi:10.1161/CIRCULATIONAHA.108.778688
27. Li Q, Guo Y, Tan W, Ou Q, Wu WJ, Sturza D, Dawn B, Hunt G, Cui C, Bolli R (2007) Cardioprotection afforded by inducible nitric oxide synthase gene therapy is mediated by cyclooxygenase-2 via a nuclear factor-kappaB dependent pathway. Circulation 116:1577-1584. doi:10.1161/CIRCULATIONAHA.107.689 810 (Pubitemid 47511421)
28. Li Q, Guo Y, Tan W, Stein AB, Dawn B, Wu WJ, Zhu X, Lu X, Xu X, Siddiqui T, Tiwari S, Bolli R (2006) Gene therapy with iNOS provides long-term protection against myocardial infarction without adverse functional consequences. Am J Physiol Heart Circ Physiol 290: H584-H589. doi:10.1152/ajpheart.008 55.2005
29. Li Q, Guo Y, Wu W, Ou Q, Zhu X, Tan W, Yuan F, Chen N, Dawn B, Luo L, O'Brien E, Bolli R (2011) Gene transfer as a strategy to achieve permanent cardioprotection I: rAAV-mediated gene therapy with inducible nitric oxide synthase limits infarct size 1 year later without adverse functional consequences. Basic Res Cardiol (in press)
30. Li Q, Guo Y, Xuan YT, Lowenstein CJ, Stevenson SC, Prabhu SD, Wu WJ, Zhu Y, Bolli R (2003) Gene therapy with inducible nitric oxide synthase protects against myocardial infarction via a cyclooxygenase-2-dependent mechanism. Circ Res 92:741-748 (Pubitemid 36457638)
31. Liu Y, Li P, Lu J, Xiong W, Oger J, Tetzlaff W, Cynader M (2008) Bilirubin possesses powerful immunomodulatory activity and suppresses experimental autoimmune encephalomyelitis. J Immunol 181:1887-1897 pii: 181/3/1887
32. Lu R, Peng J, Xiao L, Deng HW, Li YJ (2002) Heme oxygenase-1 pathway is involved in delayed protection induced by heat stress against cardiac ischemia-reperfusion injury. Int J Cardiol 82:133-140 pii: S016752730100612X (Pubitemid 34164390)
33. Manno CS, Chew AJ, Hutchison S, Larson PJ, Herzog RW, Arruda VR, Tai SJ, Ragni MV, Thompson A, Ozelo M, Couto LB, Leonard DG, Johnson FA, McClelland A, Scallan C, Skarsgard E, Flake AW, Kay MA, High KA, Glader B (2003) AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood 101:2963-2972. doi: 10.1182/blood-2002-10-3296 (Pubitemid 36857981)
34. Marini M, Lapalombella R, Margonato V, Ronchi R, Samaja M, Scapin C, Gorza L, Maraldi T, Carinci P, Ventura C, Veicsteinas A (2007) Mild exercise training, cardioprotection and stress genes profile. Eur J Appl Physiol 99:503-510. doi:10.1007/s00421-006-0369-4 (Pubitemid 46766843)
35. Matsushita T, Elliger S, Elliger C, Podsakoff G, Villarreal L, Kurtzman GJ, Iwaki Y, Colosi P (1998) Adeno-associated virus vectors can be efficiently produced without helper virus. Gene Ther 5:938-945. doi:10.1038/sj.gt.3300680 (Pubitemid 28371911)
36. Melo LG, Agrawal R, Zhang L, Rezvani M, Mangi AA, Ehsan A, Griese DP, Dell'Acqua G, Mann MJ, Oyama J, Yet SF, Layne MD, Perrella MA, Dzau VJ (2002) Gene therapy strategy for long-term myocardial protection using adeno-associated virusmediated delivery of heme oxygenase gene. Circulation 105:602-607 (Pubitemid 34123435)
37. Morse D, Choi AM (2002) Heme oxygenase-1: the "emerging molecule" has arrived. Am J Respir Cell Mol Biol 27:8-16 (Pubitemid 34657385)
38. Muruve DA (2004) The innate immune response to adenovirus vectors. Hum Gene Ther 15:1157-1166. doi:10.1089/hum.2004.15. 1157 (Pubitemid 40052429)
39. Post H, Heusch G (2002) Ischemic preconditioning. Experimental facts and clinical perspective. Minerva Cardioangiol 50:569-605 (Pubitemid 36134529)
40. Samulski RJ, Zhu X, Xiao X, Brook JD, Housman DE, Epstein N, Hunter LA (1991) Targeted integration of adeno-associated virus (AAV) into human chromosome 19. EMBO J 10:3941-3950 (Pubitemid 21905423)
41. Thielmann M, Kottenberg E, Boengler K, Raffelsieper C, Neuhaeuser M, Peters J, Jakob H, Heusch G (2010) Remote ischemic preconditioning reduces myocardial injury after coronary artery bypass surgery with crystalloid cardioplegic arrest. Basic Res Cardiol 105:657-664. doi:10.1007/s00395-010-0104- 5
42. Vivaldi MT, Kloner RA, Schoen FJ (1985) Triphenyltetrazolium staining of irreversible ischemic injury following coronary artery occlusion in rats. Am J Pathol 121:522-530 (Pubitemid 16183372)
43. Wright JF, Qu G, Tang C, Sommer JM (2003) Recombinant adeno-associated virus: formulation challenges and strategies for a gene therapy vector. Curr Opin Drug Discov Devel 6:174-178 (Pubitemid 36368371)
44. Yet SF, Tian R, Layne MD, Wang ZY, Maemura K, Solovyeva M, Ith B, Melo LG, Zhang L, Ingwall JS, Dzau VJ, Lee ME, Perrella MA (2001) Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ Res 89:168-173 (Pubitemid 34135825)
45. Yoshida T, Maulik N, Ho YS, Alam J, Das DK (2001) H (mox-1) constitutes an adaptive response to effect antioxidant cardioprotection: a study with transgenic mice heterozygous for targeted disruption of the heme oxygenase-1 gene. Circulation 103:1695-1701 (Pubitemid 32246619)
46. Zhao HX, Wang XL, Wang YH, Wu Y, Li XY, Lv XP, Zhao ZQ, Zhao RR, Liu HR (2010) Attenuation of myocardial injury by postconditioning: role of hypoxia inducible factor-1alpha. Basic Res Cardiol 105:109-118. doi:10.1007/s00395-009- 0044-0