Molecular targets in heart failure gene therapy: Current controversies and translational perspectives

Annals of the New York Academy of Sciences

Volumn 1254, Issue 1, 2012, Pages 42-50

  Kairouz, Victor ^a   Lipskaia, Larissa ^b   Hajjar, Roger J ^b   Chemaly, Elie R ^b  

^a UNIVERSITY AT BUFFALO   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Adenylyl cyclase; Calcium handling; Gene therapy; Heart failure; Phospholamban; Protein phosphatase 1

Indexed keywords

ADENOVIRUS VECTOR; ADENYLATE CYCLASE; BETA ADRENERGIC RECEPTOR; CALCIUM; CELL PROTEIN; CHEMOKINE RECEPTOR CXCR4; CYCLIC AMP; LENTIVIRUS VECTOR; MICRORNA; PARVOVIRUS VECTOR; PHOSPHOLAMBAN; PHOSPHOPROTEIN PHOSPHATASE 1; RYANODINE RECEPTOR; S100A1 PROTEIN; SERCA2A PROTEIN; STROMAL CELL DERIVED FACTOR 1; SUMO 1 PROTEIN; UNCLASSIFIED DRUG; VIRUS VECTOR;

ADRENERGIC SYSTEM; CALCIUM SIGNALING; HEART FAILURE; HEART MUSCLE CELL; HUMAN; MOLECULARLY TARGETED THERAPY; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TRANSLATION INITIATION; VIRAL GENE THERAPY;

EID: 84860437342     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2012.06520.x     Document Type: Review

References (62)

1. Lipskaia, L., E.R. Chemaly, L. Hadri, et al 2010. Sarcoplasmic reticulum Ca(2+) ATPase as a therapeutic target for heart failure. Expert Opin. Biol. Ther. 10: 29-41.
2. Roger, V.L., A.S. Go, D.M. Lloyd-Jones, et al 2011. Heart disease and stroke statistics-2011 update: a report from the American Heart Association. Circulation 123: e18-e209.
3. Gheorghiade, M., A.P. Ambrosy, M. Ferrandi & P. Ferrari 2011. Combining SERCA2a activation and Na-K ATPase inhibition: a promising new approach to managing acute heart failure syndromes with low cardiac output. Discov. Med. 12: 141-151.
4. Hasenfuss, G. & J.R. Teerlink 2011. Cardiac inotropes: current agents and future directions. Eur. Heart J. 32: 1838-1845.
5. Jessup, M., B. Greenberg, D. Mancini, et al 2011. Calcium upregulation 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.
6. Lompre, A.M., R.J. Hajjar, S.E. Harding, et al 2010. Ca2+ cycling and new therapeutic approaches for heart failure. Circulation 121: 822-830.
7. Kawase, Y., D. Ladage & R.J. Hajjar 2011. Rescuing the failing heart by targeted gene transfer. J. Am. Coll. Cardiol. 57: 1169-1180.
8. Hambleton, M., H. Hahn, S.T. Pleger, et al 2006. Pharmacological- and gene therapy-based inhibition of protein kinase Calpha/beta enhances cardiac contractility and attenuates heart failure. Circulation 114: 574-582.
9. Ladage, D., L. Tilemann, K. Ishikawa, et al 2011. Inhibition of PKCα/β with ruboxistaurin antagonizes heart failure in pigs after myocardial infarction injury. Circ. Res. 109: 1396-1400.
10. Prunier, F., Y. Kawase, D. Gianni, et al 2008. Prevention of ventricular arrhythmias with sarcoplasmic reticulum Ca2+ ATPase pump overexpression in a porcine model of ischemia reperfusion. Circulation 118: 614-624.
11. Gwathmey, J.K., A.I. Yerevanian & R.J. Hajjar 2011. Cardiac gene therapy with SERCA2a: from bench to bedside. J. Mol. Cell Cardiol. 50: 803-812.
12. Lyon, A.R., M.L. Bannister, T. Collins, et al 2011. SERCA2a gene transfer decreases sarcoplasmic reticulum calcium leak and reduces ventricular arrhythmias in a model of chronic heart failure. Circ. Arrhythm Electrophysiol. 4: 362-372.
13. Jaski, B.E., M.L. Jessup, D.M. Mancini, et al 2009. Calcium upregulation by percutaneous administration of gene therapy in cardiac disease (CUPID Trial), a first-in-human phase 1/2 clinical trial. J. Card. Fail. 15: 171-181.
14. Minamisawa, S., M. Hoshijima, G. Chu, et al 1999. Chronic phospholamban-sarcoplasmic reticulum calcium ATPase interaction is the critical calcium cycling defect in dilated cardiomyopathy. Cell 99: 313-322.
15. del Monte, F., S.E. Harding, G.W. Dec, et al 2002. Targeting phospholamban by gene transfer in human heart failure. Circulation 105: 904-907.
16. Suckau, L., H. Fechner, E. Chemaly, et al 2009. Long-term cardiac-targeted RNA interference for the treatment of heart failure restores cardiac function and reduces pathological hypertrophy. Circulation 119: 1241-1252.
17. Ziolo, M.T., J.L. Martin, J. Bossuyt, et al 2005. Adenoviral gene transfer of mutant phospholamban rescues contractile dysfunction in failing rabbit myocytes with relatively preserved SERCA function. Circ. Res. 96: 815-817.
18. Kaye, D.M., A. Preovolos, T. Marshall, 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.
19. Lockamy, E.L., R.L. Cornea, C.B. Karim & D.D. Thomas 2011. Functional and physical competition between phospholamban and its mutants provides insight into the molecular mechanism of gene therapy for heart failure. Biochem. Biophys. Res. Commun. 408: 388-392.
20. Kiriazis, H., Y. Sato, V.J. Kadambi, et al 2002. Hypertrophy and functional alterations in hyperdynamic phospholamban-knockout mouse hearts under chronic aortic stenosis. Cardiovasc. Res. 53: 372-381.
21. Haghighi, K., F. Kolokathis, L. Pater, et al 2003. Human phospholamban null results in lethal dilated cardiomyopathy revealing a critical difference between mouse and human. J. Clin. Invest. 111: 869-876.
22. Bish, L.T., M.M. Sleeper, C. Reynolds, et al 2011. Cardiac gene transfer of short hairpin RNA directed against phospholamban effectively knocks down gene expression but causes cellular toxicity in canines. Hum. Gene. Ther. 22: 969-977.
23. Ha, K.N., N.J. Traaseth, R. Verardi, et al 2007. Controlling the inhibition of the sarcoplasmic Ca2+-ATPase by tuning phospholamban structural dynamics. J. Biol. Chem. 282: 37205-37214.
24. Kadambi, V.J., S. Ponniah, J.M. Harrer, et al 1996. Cardiac-specific overexpression of phospholamban alters calcium kinetics and resultant cardiomyocyte mechanics in transgenic mice. J. Clin. Invest. 97: 533-539.
25. Chemaly, E.R., L. Hadri, S. Zhang, et al 2011. Long-term in vivo resistin overexpression induces myocardial dysfunction and remodeling in rats. J. Mol. Cell Cardiol. 51: 144-155.
26. Wittkopper, K., D. Dobrev, T. Eschenhagen & A. El-Armouche 2011. Phosphatase-1 inhibitor-1 in physiological and pathological beta-adrenoceptor signalling. Cardiovasc. Res. 91: 392-401.
27. Pathak, A., F. del Monte, W. Zhao, et al 2005. Enhancement of cardiac function and suppression of heart failure progression by inhibition of protein phosphatase 1. Circ. Res. 96: 756-766.
28. Kho, C., A. Lee, D. Jeong, et al 2011. SUMO1-dependent modulation of SERCA2a in heart failure. Nature 477: 601-605.
29. Pleger, S.T., C. Shan, J. Ksienzyk, et al 2011. Cardiac AAV9-S100A1 gene therapy rescues post-ischemic heart failure in a preclinical large animal model. Sci. Transl. Med. 3: 92ra64.
30. Belmonte, S.L., K.B. Margulies & B.C. Blaxall 2011. S100A1: another step toward therapeutic development for heart failure. J. Am. Coll. Cardiol. 58: 974-976.
31. Brinks, H., D. Rohde, M. Voelkers, et al 2011. S100A1 genetically targeted therapy reverses dysfunction of human failing cardiomyocytes. J. Am. Coll. Cardiol. 58: 966-973.
32. Feldman, D.S., C.A. Carnes, W.T. Abraham & M.R. Bristow 2005. Mechanisms of disease: beta-adrenergic receptors-alterations in signal transduction and pharmacogenomics in heart failure. Nat. Clin. Pract. Cardiovasc. Med. 2: 475-483.
33. Lipskaia, L., H. Ly, Y. Kawase, et al 2007. Treatment of heart failure by calcium cycling gene therapy. Future Cardiol. 3: 413-423.
34. Vinge, L.E., P.W. Raake & W.J. Koch 2008. Gene therapy in heart failure. Circ. Res. 102: 1458-1470.
35. Gao, M.H., N.C. Lai, D.M. Roth, et al 1999. Adenylylcyclase increases responsiveness to catecholamine stimulation in transgenic mice. Circulation 99: 1618-1622.
36. Regitz-Zagrosek, V., R. Hertrampf, C. Steffen, et al 1994. Myocardial cyclic AMP and norepinephrine content in human heart failure. Eur. Heart J. 15(Suppl. D): 7-13.
37. Lohse, M.J., S. Engelhardt & T. Eschenhagen 2003. What is the role of beta-adrenergic signaling in heart failure? Circ. Res. 93: 896-906.
38. Ostrom, R.S., S.R. Post & P.A. Insel 2000. Stoichiometry and compartmentation in G protein-coupled receptor signaling: implications for therapeutic interventions involving G(s). J. Pharmacol. Exp. Ther. 294: 407-412.
39. Defer, N., M. Best-Belpomme & J. Hanoune 2000. Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase. Am J. Physiol. Renal Physiol. 279: F400-416.
40. Hanoune, J. & N. Defer 2001. Regulation and role of adenylyl cyclase isoforms. Annu. Rev. Pharmacol. Toxicol. 41: 145-174.
41. Puceat, M., C. Bony, M. Jaconi & G. Vassort 1998. Specific activation of adenylyl cyclase V by a purinergic agonist. FEBS Letters 431: 189-194.
42. Stark, J.C., S.F. Haydock, R. Foo, et al 2004. Effect of overexpressed adenylyl cyclase VI on beta 1- and beta 2-adrenoceptor responses in adult rat ventricular myocytes. Br. J. Pharmacol. 143: 465-476.
43. Hu, C.L., R. Chandra, H. Ge, et al 2009. Adenylyl cyclase type 5 protein expression during cardiac development and stress. Am. J. Physiol. Heart Circ. Physiol. 297: H1776-H1782.
44. Espinasse, I., V. Iourgenko, C. Richer, et al 1999. Decreased type VI adenylyl cyclase mRNA concentration and Mg(2+)-dependent adenylyl cyclase activities and unchanged type V adenylyl cyclase mRNA concentration and Mn(2+)-dependent adenylyl cyclase activities in the left ventricle of rats with myocardial infarction and longstanding heart failure. Cardiovasc. Res. 42: 87-98.
45. Tepe, N.M., J.N. Lorenz, A. Yatani, et al 1999. Altering the receptor-effector ratio by transgenic overexpression of type V adenylyl cyclase: enhanced basal catalytic activity and function without increased cardiomyocyte beta-adrenergic signalling. Biochemistry 38: 16706-16713.
46. Vatner, S.F., L. Yan, Y. Ishikawa, et al 2009. Adenylyl cyclase type 5 disruption prolongs longevity and protects the heart against stress. Circ. J. 73: 195-200.
47. Okumura, S., G. Takagi, J. Kawabe, et al 2003. Disruption of type 5 adenylyl cyclase gene preserves cardiac function against pressure overload. Proc. Natl. Acad. Sci. U. S. A. 100: 9986-9990.
48. Tang, T., H.K. Hammond, A. Firth, et al 2011. Adenylyl cyclase 6 improves calcium uptake and left ventricular function in aged hearts. J. Am. Coll. Cardiol. 57: 1846-1855.
49. Gao, M.H., T. Tang, T. Guo, et al 2008. Adenylyl cyclase type VI increases Akt activity and phospholamban phosphorylation in cardiac myocytes. J. Biol. Chem. 283: 33527-33535.
50. Gao, M.H., T. Tang, A. Miyanohara, et al 2010. beta(1)-Adrenergic receptor vs adenylyl cyclase 6 expression in cardiac myocytes: differences in transgene localization and intracellular signaling. Cell. Signal. 22: 584-589.
51. Lipskaia, L., N. Defer, G. Esposito, et al 2000. Enhanced cardiac function in transgenic mice expressing a Ca(2+)-stimulated adenylyl cyclase. Circ. Res. 86: 795-801.
52. Lipskaia, L., N. Mougenot, A. Jacquet, et al 2011. Compartmentalization of cAMP increase at the level of sarcoplasmic reticulum results in dilated and hypertrophic cardiomyopathy in aged transgenic mice. Eur. Heart J. 32(Suppl. 1): 999.
53. Georget, M., P. Mateo, G. Vandecasteele, et al 2002. Augmentation of cardiac contractility with no change in L-type Ca2+ current in transgenic mice with a cardiac-directed expression of the human adenylyl cyclase type 8 (AC8). FASEB J. 16: 1636-1638.
54. Georget, M., P. Mateo, G. Vandecasteele, et al 2003. Cyclic AMP compartmentation due to increased cAMP-phosphodiesterase activity in transgenic mice with a cardiac-directed expression of the human adenylyl cyclase type 8 (AC8). FASEB J. 17: 1380-1391.
55. Levin, S.D., D.W. Taft, C.S. Brandt, et al 2011. Vstm3 is a member of the CD28 family and an important modulator of T-cell function. Eur. J. Immunol. 41: 902-915.
56. Lyon, A.R., M. Sato, R.J. Hajjar, et al 2008. Gene therapy: targeting the myocardium. Heart (British Cardiac Society) 94: 89-99.
57. Ghadge, S.K., S. Muhlstedt, C. Ozcelik & M. Bader 2011. SDF-1alpha as a therapeutic stem cell homing factor in myocardial infarction. Pharmacol. Ther. 129: 97-108.
58. Pyo, R.T., J. Sui, A. Dhume, et al 2006. CXCR4 modulates contractility in adult cardiac myocytes. J. Mol. Cell Cardiol. 41: 834-844.
59. Chen, J., E. Chemaly, L. Liang, et al 2010. Effects of CXCR4 gene transfer on cardiac function after ischemia-reperfusion injury. Am. J. Pathol. 176: 1705-1715.
60. LaRocca, T.J., M. Schwarzkopf, P. Altman, et al 2010. beta2-Adrenergic receptor signaling in the cardiac myocyte is modulated by interactions with CXCR4. J. Cardiovasc. Pharmacol. 56: 548-559.
61. van Rooij, E. 2011. The art of microRNA research. Circ. Res. 108: 219-234.
62. Karakikes, I., A. Chaanine, J. Kim, et al 2010. Abstract 20916: therapeutic cardiac-targeted delivery of Mir-1 reverses hypertrophy and preserves cardiac function in a pressure overload animal model. Circulation 122: A20916.