Targeting sarcoplasmic reticulum calcium ATPase by gene therapy

Human Gene Therapy

Volumn 24, Issue 11, 2013, Pages 937-947

  Gwathmey, Judith K ^a   Yerevanian, Armen ^a   Hajjar, Roger J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CALCIUM; COMPLEMENTARY DNA; HEAT SHOCK PROTEIN 20; LENTIVIRUS VECTOR; LIPOSOME; MESSENGER RNA; NAKED DNA; NANOPARTICLE; OLIGONUCLEOTIDE; PARVOVIRUS VECTOR; PHOSPHOLAMBAN; PHOSPHOPROTEIN PHOSPHATASE 1; PLASMID DNA; POLYMER; PROTEIN S100A1; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SUMO 1 PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS 1; CONGESTIVE CARDIOMYOPATHY; DRUG TARGETING; GENE EXPRESSION; GENE VECTOR; GENETIC MANIPULATION; HEART FAILURE; HEART FUNCTION; HEART VENTRICLE HYPERTROPHY; HUMAN; MORTALITY; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL GENE THERAPY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PROMOTER REGION; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SYMPTOMATOLOGY; TRANSGENE; UPREGULATION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ANIMALS; CALCIUM SIGNALING; CLINICAL TRIALS AS TOPIC; GENETIC THERAPY; GENETIC VECTORS; HEART FAILURE; HUMANS; MYOCARDIUM; PROTEIN INTERACTION MAPS; RETROVIRIDAE; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; TRANSDUCTION, GENETIC;

EID: 84886799951     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2013.2512     Document Type: Review

References (100)

1. Alba, R., Bosch, A., and Chillon, M. (2005). Gutless adenovirus: last-generation adenovirus for gene therapy. Gene Ther. 12, S18-S27. (Pubitemid 41541750)
2. Aoki, H., Richmond, M., Izumo, S., and Sadoshima, J. (2000). Specific role of the extracellular signal-regulated kinase pathway in angiotensin II-induced cardiac hypertrophy in vitro. Biochem. J. 347 Pt 1, 275-284. (Pubitemid 30199067)
3. Asokan, A., Schaffer, D.V., and Samulski, R.J. (2012). The AAV vector toolkit: poised at the clinical crossroads. Mol. Ther. 20, 699-708.
4. Beeri, R. (2002). New efficient catheter-based system for myo-cardial gene delivery. Circulation 106, 1756-1759.
5. Boecker, W., Bernecker, O.Y., Wu, J.C., et al. (2004). Cardiac-specific gene expression facilitated by an enhanced myosin light chain promoter. Mol. Imaging 3, 69-75.
6. Boutin, S., Monteilhet, V., Veron, P., et al. (2010). Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) types 1, 2, 5, 6, 8, and 9 in the healthy population: implications for gene therapy using AAV vectors. Hum. Gene Ther. 21, 704-712.
7. Brophy, J.M., Joseph, L., and Rouleau, J.L. (2001). Beta-blockers in congestive heart failure. A Bayesian meta-analysis. Ann. Intern. Med. 134, 550.
8. Bristow, M.R., Ginsburg, R., Umans, V., et al. (1986). Beta 1-and beta 2-adrenergic-receptor subpopulations in nonfailing and failing human ventricular myocardium: coupling of both receptor subtypes to muscle contraction and selective beta 1-receptor down-regulation in heart failure. Circ. Res. 59, 297-309. (Pubitemid 17178124)
9. Bristow, M.R., O'Connell, J.B., Gilbert, E.M., et al. (1994). Dose-response of chronic beta-blocker treatment in heart failure from either idiopathic dilated or ischemic cardiomyopathy. Bucindolol Investigators. Circulation. 89, 1632-1642. (Pubitemid 24114241)
10. Byrne, M.J., Power, J.M., Preovolos, A., et al. (2008). Recirculating cardiac delivery of AAV2/1SERCA2a improves myocardial function in an experimental model of heart failure in large animals. Gene Ther. 15, 1550-1557.
11. Calcedo, R., Vandenberghe, L.H., Gao, G., et al. (2009). Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses. J. Infect. Dis. 199, 381-390.
12. Carter, P.J., and Samulski, R.J. (2000). Adeno-associated viral vectors as gene delivery vehicles. Int. J. Mol. Med. 6, 17-27.
13. Cavazzana-Calvo, M., Hacein-Bey, S., de Saint Basile, G., et al. (2000). Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288, 669-672. (Pubitemid 30241569)
14. Chapdelaine, P., Pichavant, C., Rousseau, J., et al. (2010). Meganucleases can restore the reading frame of a mutated dystrophin. Gene Ther. 17, 846-858.
15. Davia, K., Hajjar, R.J., Terracciano, C.M., et al. (1999). Functional alterations in adult rat myocytes after overexpression of phospholamban with use of adenovirus. Physiol. Genomics 1, 41-50. (Pubitemid 129622450)
16. Davidson, M.J., Jones, J.M., Emani, S.M., et al. (2001). Cardiac gene delivery with cardiopulmonary bypass. Circulation 104, 131-133. (Pubitemid 32655825)
17. del Monte, F., Harding, S.E., Schmidt, U., et al. (1999). Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation 100, 2308-2311.
18. del Monte, F., Harding, S.E., Dec, G.W., et al. (2002a). Targeting phospholamban by gene transfer in human heart failure. Circulation 105, 904-907. (Pubitemid 34184564)
19. del Monte, F., Johnson, C.M., Stepanek, A.C., et al. (2002b). Defects in calcium control. J. Card. Fail. 8, S421-S431. (Pubitemid 36083094)
20. Di Paolo, N.C., et al. (2009). Virus binding to a plasma membrane receptor triggers interleukin-1 alpha-mediated proinflammatory macrophage response in vivo. Immunity 31, 110-121.
21. Dulin, N.O., Alexander, L.D., Harwalkar, S., et al. (1998). Phos-pholipase A2-mediated activation of mitogen-activated protein kinase by angiotensin II. Proc. Natl. Acad. Sci. USA 95, 8098-8102. (Pubitemid 28326072)
22. Fish, K.M., Ladage, D., Kawase, Y., et al. (2013). AAV9.I-1c delivered via direct coronary infusion in a porcine model of heart failure improves contractility and mitigates adverse remodeling. Circ. Heart Fail. 6, 310-317.
23. French, B.A., Mazur, W., Ali, N.M., et al. (1994a). Percutaneous transluminal in vivo gene transfer by recombinant adenovirus in normal porcine coronary arteries, atherosclerotic arteries, and two models of coronary restenosis. Circulation 90, 2402-2413. (Pubitemid 24354328)
24. French, B.A., Mazur, W., Geske, R.S., and Bolli, R. (1994b). Direct in vivo gene transfer into porcine myocardium using replication-deficient adenoviral vectors. Circulation 90, 2414-2424.
25. Giacca, M., and Zacchigna, S. (2012). VEGF gene therapy: therapeutic angiogenesis in the clinic and beyond. Gene Ther. 19, 622-629.
26. Gupta, R., Tongers, J., and Losordo, D.W. (2009). Human studies of angiogenic gene therapy. Circ. Res. 105, 724-736.
27. Gwathmey, J.K., Copelas, L., MacKinnon, R., et al. (1987). Abnormal intracellular calcium handling in myocardium from patients with end-stage heart failure. Circ. Res. 61, 70-76. (Pubitemid 17133480)
28. Gwathmey, J.K., Bentivegna, L.A., Ransil, B.J., et al. (1993). Relationship of abnormal intracellular calcium mobilisation to myocyte hypertrophy in human ventricular myocardium. Cardiovasc. Res. 27, 199-203. (Pubitemid 23070328)
29. Gwathmey, J.K., Kim, C.S., Hajjar, R.J., et al. (1999). Cellular and molecular remodeling in a heart failure model treated with the b-blocker Carteolol. Am. J. Physiol. 276, H1678-H1690. (Pubitemid 29246557)
30. Hacein-Bey-Abina, S., Von Kalle, C., Schmidt, M., et al. (2003). LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302, 415-419. (Pubitemid 37296260)
31. 2+-ATPase. Circ. Res. 81, 145-153. (Pubitemid 27342481)
32. Hajjar, R.J., Schmidt, U., Matsui, T., Guerrero, J.L., Lee, K.H., Gwathmey, J.K., Dec, G.W., Semigran, M.J. and Rosenzweig, A. (1998). Modulation of ventricular function through gene transfer in vivo. Proc. Natl. Acad. Sci. USA 95, 5251-5256. (Pubitemid 28208584)
33. Han, Y., Chen, Y.S., Liu, Z., et al. (2006). Overexpression of HAX-1 protects cardiac myocytes from apoptosis through caspase-9 inhibition. Circ. Res. 99, 415-423. (Pubitemid 44253698)
34. 2+-ATPase in failing and nonfailing human myocardium. Circ. Res. 75, 434-442.
35. Hayase, M., del Monte, F., Kawase, Y., MacNeill, B.D., McGregor, J., Yoneyama, R., Hoshino, K., Tsuji, T., De Grand, A.M., Gwathmey, J.K., Frangioni, J.V. and Hajjar, R.J. (2005). Cather-based antegrade intracoronary viral gene delivery with coronary venous blockade. Am. J. Physiol. Heart Circ. Physiol. 288, H2295-H3000.
36. 2+-ATPase activity and cardiac myocyte contractility. Circulation 100, 974-980. (Pubitemid 29407179)
37. He, Q., Wang, D., Yang, X.P., et al. (2001). Inducible regulation of human brain natriuretic peptide promoter in transgenic mice. Am. J. Physiol. Heart Circ. Physiol. 280, H368-H376.
38. Herrmann, J., Lerman, L.O., and Lerman, A. (2007). Ubiquitin and ubiquitin-like proteins in protein regulation. Circ. Res. 100, 1276-1291. (Pubitemid 46742918)
39. Ho, K.K., Anderson, K.M., Kannel, W.B., et al. (1993). Survival after the onset of congestive heart failure in Framingham Heart Study subjects. Circulation 88, 107-115. (Pubitemid 23195439)
40. Ishikawa, K., Tilemann, L., Fish, K., and Hajjar, R.J. (2011). Gene delivery methods in cardiac gene therapy. J. Gene Med. 13, 566-572.
41. Ishikawa, K., Aguero, J., Naim, C., et al. (2013). Percutaneous approaches for efficient cardiac gene delivery. J. Cardiovasc. Transl. Res. 6, 649-659.
42. Jacobson, S.G., Cideciyan, A.V., Ratnakaram, R., et al. (2012). Gene therapy for leber congenital amaurosis caused by RPE65 mutations: safety and efficacy in 15 children and adults followed up to 3 years. Arch. Ophthalmol. 130, 9-24.
43. Jessup, M., Greenberg, B., Mancini, D., et al.; Calcium Upregu-lation by Percutaneous Administration of Gene Therapy in Cardiac Disease (CUPID) Investigators. (2011). Calcium up-regulation by percutaneous administration of gene therapy in cardiac disease (CUPID): a phase 2 trial of intracoronary gene therapy of sarcoplasmic reticulum Ca2+-ATPase in patients with advanced heart failure. Circulation 124, 304-313.
44. Jiang, B., Qian, K., Du, L., et al. (2011). Helper-dependent ade-novirus is superior to first-generation adenovirus for expressing transgenes in atherosclerosis-prone arteries. Arterioscler. Thromb. Vasc. Biol. 31, 1317-1325.
45. Karakikes, I., Hadri, L., Rapti, K., et al. (2012). Concomitant intravenous nitroglycerin with intracoronary delivery of AAV1.SERCA2a enhances gene transfer inporcine hearts. Mol. Ther. 20, 565-571.
46. Kawase, Y., Ly, H.Q., Prunier, F., et al. (2008). Reversal of cardiac dysfunction after long-term expression of SERCA2a by gene transfer in a pre-clinical model of heart failure. J. Am. Coll. Cardiol. 51, 1112-1119. (Pubitemid 351374774)
47. Kaye, D.M., Preovolos, A., Marshall, T., et al. (2007). Percutaneous cardiac recirculation-mediated gene transfer of an inhibitory phospholamban peptide reverses advanced heart failure in large animals. J. Am. Coll. Cardiol. 50, 253-260. (Pubitemid 47031573)
48. Kettlewell, S., Most, P., Currie, S., et al. (2005). S100A1 increases the gain of excitation-contraction coupling in isolated rabbit ventricular cardiomyocytes. J. Mol. Cell Cardiol. 39, 900-910. (Pubitemid 41572323)
49. Kho, C., Lee, A., Jeong, D., et al. (2011). SUMO1-dependent modulation of SERCA2a in heart failure. Nature 477, 601-605.
50. Klug, A. (2010). The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu. Rev. Biochem. 79, 213-231.
51. Konno, T., Chang, S., Seidman, J.G., and Seidman, C.E. (2010). Genetics of hypertrophic cardiomyopathy. Curr. Opin. Car-diol. 25, 205-209.
52. Konstam, M.A., Rousseau, M.F., Kronenberg, M.W., et al. (1992). Effects of the angiotensin converting enzyme inhibitor en-alapril on the long-term progression of left ventricular dysfunction in patients with heart failure. SOLVD Investigators. Circulation 86, 431-438.
53. Kranias, E.G., and Hajjar, R.J. (2012). Modulation of cardiac contractility by the phospholamban/SERCA2a regulatome. Circ. Res. 110, 1646-1660.
54. Ladage, D., Turnbull, I.C., Ishikawa, K., et al. (2011). Delivery of gelfoam-enabled cells and vectors into the pericardial space using a percutaneous approach in a porcine model. Gene Ther. 18, 979-985.
55. Lai, N.C., Roth, D.M., Gao, M.H., et al. (2004). Intracoronary adenovirus encoding adenylyl cyclase VI increases left ventricular function in heart failure. Circulation 110, 330-336. (Pubitemid 38955502)
56. LaPointe, M.C., Yang, X.P., Carretero, O.A., and He, Q. (2002). Left ventricular targeting of reporter gene expression in vivo by human BNP promoter in an adenoviral vector. Am. J. Physiol. Heart Circ. Physiol. 283, H1439-H1445.
57. Lederman, R.J., Guttman, M.A., Peteres, D.C., Thompson, R.B., Sorger, J.M., Dick, A.J., Raman, V.K. and McVeigh, E.R. (2002) Catheter-based endomyocardial injection with realtime magnetic resonance imaging. Circulation. 105, 1282-1284. (Pubitemid 34260416)
58. Lymperopoulos, A., Rengo, G., and Koch, W.J. (2013). Adre-nergic nervous system in heart failure: pathophysiology and therapy. Circ. Res. 113, 739-753.
59. Manno, C.S., Pierce, G.F., Arruda, V.R., et al. (2006). Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat. Med. 12, 342-347. (Pubitemid 43355084)
60. Meyer, M., Bluhm, W.F., He, H., et al. (1999). Phospholamban-to-SERCA2 ratio controls the force-frequency relationship. Am. J. Physiol. 276, H779-H785. (Pubitemid 29157448)
61. Miller, D.G., Adam, M.A., and Miller, A.D. (1990). Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection. Mol. Cell Biol. 10, 4239-4242.
62. Minamisawa, S., Hoshijima, M., Chu, G., et al. (1999). Chronic phospholamban-sarcoplasmic reticulum calcium ATPase interaction is the critical calcium cycling defect in dilated car-diomyopathy. Cell 99, 313-322. (Pubitemid 29519910)
63. Miyamoto, M.I., del Monte, F., Schmidt, U., et al. (2000). Ade-noviral gene transfer of SERCA2a improves left-ventricular function in aortic-banded rats in transition to heart failure. Proc. Natl. Acad. Sci. USA 97, 793-798. (Pubitemid 30070389)
64. Most, P., and Koch, W.J. (2007). S100A1: a calcium-modulating inotropic prototype for future clinical heart failure therapy. Future Cardiol. 3, 5-11. (Pubitemid 46157665)
65. Neumann, J., Eschenhagen, T., Jones, L.R., et al. (1997). Increased expression of cardiac phosphatases in patients with end-stage heart failure. J. Mol. Cell Cardiol. 29, 265-272. (Pubitemid 27129150)
66. Pacak, C.A., Mah, C.S., Thattaliyath, B.D., et al. (2006). Re-combinant adenoassociated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ. Res. 99, e3-e9. (Pubitemid 44255502)
67. Paques, F., and Duchateau, P. (2007). Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy. Curr. Gene Ther. 7, 49-66. (Pubitemid 46322288)
68. Phillips, M.I., and Kimura, B. (2005). Gene therapy for hypertension: antisense inhibition of the renin-angiotensin system. Methods Mol. Med. 108, 363-379.
69. Pleger, S.T., Most, P., Boucher, M., et al. (2007). Stable myocardial-specific AAV6-S100A1 gene therapy results in chronic functional heart failure rescue. Circulation 115, 2506-2515. (Pubitemid 46763224)
70. Pleger, S.T., Shan, C., Ksienzyk, J., et al. (2011). Cardiac AAV9-S100A1 gene therapy rescues post-ischemic heart failure in a preclinical large animal model. Sci. Transl. Med. 3, 92ra64.
71. Qian, J., Ren, X., Wang, X., et al. (2009). Blockade of Hsp20 phosphorylation exacerbates cardiac ischemia/reperfusion injury by suppressed autophagy and increased cell death. Circ. Res. 105, 1223-1231.
72. Raake, P.W., Vinge, L.E., Gao, E., et al. (2008). G protein-coupled receptor kinase 2 ablation in cardiac myocytes before or after myocardial infarction prevents heart failure. Circ. Res. 103, 413-422.
73. Remppis, A., Greten, T., Schafer, B.W., et al. (1996). Altered expression of the ca(2+)-binding protein S100A1 in human cardiomyopathy. Biochim. Biophys. Acta. 1313, 253-257. (Pubitemid 26342956)
74. Roques, C., Salmon, A., Fiszman, M.Y., et al. (2007). In-trapericardial administration of novel DNA formulations based on thermosensitive Poloxamer 407 gel. Int. J. Pharm. 331, 220-223. (Pubitemid 46216676)
75. Ruan, H., Su, H., Hu, L., et al. (2001). A hypoxia-regulated adeno-associated virus vector for cancer-specific gene therapy. Neoplasia 3, 255-263. (Pubitemid 32747574)
76. Rydén, L., Ariniego, R., Arnman, K., et al. (1983). A double-blind trial of metoprolol in acute myocardial infarction. Effects on ventricular tachyarrhythmias. N. Engl. J. Med. 308, 614-618. (Pubitemid 13152324)
77. Sarge, K.D., and Park-Sarge, O.K. (2009). Sumoylation and human disease pathogenesis. Trends Biochem. Sci. 34, 200-205.
78. Schalch, P., Rahman, G.F., Patejunas, G., et al. (2004). Adenoviral-mediated transfer of vascular endothelial growth factor 121 cDNA enhances myocardial perfusion and exercise performance in the nonischemic state. J. Thorac. Cardiovasc. Surg. 127, 535-540. (Pubitemid 38176660)
79. Schmidt, U., Hajjar, R.J., Helm, P.A., et al. (1998). Contribution of abnormal sarcoplasmic reticulum ATPase activity to systolic and diastolic dysfunction in human heart failure. J. Mol. Cell Cardiol. 30, 1929-1937. (Pubitemid 28495319)
80. Schmidt, U., Hajjar, R.J., Kim, C.S., et al. (1999). Human heart failure: cAMP stimulation of SR Ca(2+)-ATPase activity and phosphorylation level of phospholamban. Am. J. Physiol. 277, H474-H480. (Pubitemid 29415959)
81. Snyder, R., and Moullier, P., eds. (2011). Adeno-Associated Virus: Methods and Protocols. Methods in Molecular Biology Series, vol. 807 (Humana Press, New York, NY).
82. Stewart, D.J., Kutryk, M.J., Fitchett, D., et al.; NORTHERN Trial Investigators. (2009). VEGF gene therapy fails to improve perfusion of ischemic myocardium in patients with advanced coronary disease: results of the NORTHERN trial. Mol. Ther. 17, 1109-1115.
83. Su, H., and Kan, Y.W. (2007). Adeno-associated viral vector-delivered hypoxia-inducible gene expression in ischemic hearts. Methods Mol. Biol. 366, 331-342. (Pubitemid 350183485)
84. Swedberg, K., Hjalmarson, A., Waagstein, F., et al. (1980). Beneficial effects of long-term beta-blockade in congestive car-diomyopathy. Br. Heart. J. 44, 117-133. (Pubitemid 10000987)
85. Sylvius, N., Bilinska, Z.T., Veinot, J.P., et al. (2005). In vivo and in vitro examination of the functional significances of novel lamin gene mutations in heart failure patients. J. Med. Genet. 42, 639-647. (Pubitemid 41129036)
86. Tilemann, L., Ishikawa, K., Weber, T., and Hajjar, R.J. (2012). Gene therapy for heart failure. Circ. Res. 110, 777-793.
87. Vafiadaki, E., Sanoudou, D., Arvanitis, D.A., et al. (2007). Phospholamban interacts with HAX-1, a mitochondrial protein with anti-apoptotic function. J. Mol. Biol. 367, 65-79. (Pubitemid 46274703)
88. Vassalli, G., Bueler, H., Dudler, J., et al. (2003). Adeno-associated virus (AAV) vectors achieve prolonged transgene expression in mouse myocardium and arteries in vivo: a comparative study with adenovirus vectors. Int. J. Cardiol. 90, 229-238. (Pubitemid 37087882)
89. Vodicka, M.A. (2001). Determinants for lentiviral infection of non-dividing 764 cells. Somat. Cell. Mol. Genet. 26, 35-49. (Pubitemid 35332978)
90. Wang, Z., Zhu, T., Qiao, C., Zhou, L., Wang, B., Zhang, J., Chen, C, Li, J. and Xiao, X. (2005). Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat. Biotechnol. 23, 321-328. (Pubitemid 41094420)
91. Washington, B., Butler, K., Doye, A.A., et al. (2001). Heart function challenged with b-receptor agonism and antagonism in a heart failure model. Cardiovasc. Drugs Ther. 15, 479-486. (Pubitemid 34163934)
92. White, J.D., Thesier, D.M., Swain, J.B., et al. (2011). Myocardial gene delivery using molecular cardiac surgery with recombinant adeno-associated virus vectors in vivo. Gene Ther. 18, 546-552.
93. Wu, Z., Asokan, A., and Samulski, R.J. (2006). Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol. Ther. 14, 316-327. (Pubitemid 44184972)
94. Ye, X., Rivera, V.M., Zoltick, P., et al. (1999). Regulated delivery of therapeutic proteins after in vivo somatic cell gene transfer. Science 283, 88-91. (Pubitemid 29045765)
95. Ying, Y., Muller, O.J., Goehringer, C., et al. (2010). Heart-targeted adeno-associated viral vectors selected by in vivo biopanning of a random viral display peptide library. Gene Ther. 17, 980-990.
96. Zaiss, A.K., Liu, Q., Bowen, G.P., Wong N.C.W., Bartlett J.S. and Muruve, D.A. (2002). Differential activation of innate immune responses by adenovirus and adeno-associated virus vectors. J. Virol. 76, 4580-4590. (Pubitemid 34309593)
97. Zangi, L., Lui, K.O., von Gise, A., et al. (2013). Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat. Biotechnol. 31:898-907.
98. Zhang, Y.Q., and Sarge, K.D. (2008). Sumoylation regulates lamin A function and is lost in lamin A mutants associated with familial cardiomyopathies. J. Cell Biol. 182, 35-39. (Pubitemid 352008619)
99. Zhu, Y.H., and Wang, X. (2005). Overexpression of heat-shock protein 20 in rat heart myogenic cells confers protection against simulated ischemia/reperfusion injury. Acta Pharmacol. Sin. 26, 1076-1080. (Pubitemid 41296947)
100. Zincarelli, C., Soltys, S., Rengo, G., and Rabinowitz, J.E. (2008). Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol. Ther. 16, 1073-1080. (Pubitemid 351737072)