SERCA2a: A prime target for modulation of cardiac contractility during heart failure

BMB Reports

Volumn 46, Issue 5, 2013, Pages 237-243

  Park, Woo Jin ^a   Oh, Jae Gyun ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

Author keywords

Inhibitor 1; Phospholamban; PKC ; Protein phosphatase 1; SERCA2a

Indexed keywords

CALCIUM; CALCIUM BINDING PROTEIN; CARDIOVASCULAR AGENT; PHOSPHOLAMBAN; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL; ARTICLE; GENE EXPRESSION REGULATION; GENE THERAPY; GENETICS; HEART CONTRACTION; HEART FAILURE; HUMAN; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CALCIUM-BINDING PROTEINS; CARDIOVASCULAR AGENTS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENETIC THERAPY; HEART FAILURE; HUMANS; MYOCARDIAL CONTRACTION; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SIGNAL TRANSDUCTION;

EID: 84880577354     PISSN: 19766696     EISSN: 1976670X     Source Type: Journal    
DOI: 10.5483/BMBRep.2013.46.5.077     Document Type: Article

References (46)

1. Braz, J. C., Gregory, K., Pathak, A., Zhao, W., Sahin, B., Klevitsky, R., Kimball, T. F., Lorenz, J. N., Nairn, A. C., S. B., Bodi, I., Wang, S., Schwartz, A., Lakatta, E. G., DePaoli-Roach, A. A., Robbins, J., Hewett, T. E., Bibb, J. A., Westfall, M. V., Kranias, E. G. and Molkentin, J. D. (2004) PKC-alpha regulates cardiac contractility and pro- pensity toward heart failure. Nat. Med. 10, 248-254.
2. Byrne, M. J., Power, J. M., Preovolos, A., Mariani, J. A., Hajjar, R. J. and Kaye, D. M. (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.
3. Carr, A. N., Schmidt, A. G., Suzuki, Y., del Monte, F., Sato, Y., Lanner, C., Breeden, K., Jing, S. L., Allen, P. B., Greengard, P., Yatani, A., Hoit, B. D., Grupp, I. L., Hajjar, R. J., DePaoli-Roach, A. A. and Kranias, E. G. (2002) Type 1 phosphatase, a negative regulator of cardiac function. Mol. Cell. Biol. 22, 4124-4135.
4. del Monte, F., Hajjar, R. J. and Harding, S. E. (2001) Overwhelming evidence of the beneficial effects of SERCA gene transfer in heart failure. Circ. Res. 88, E66-67.
5. del Monte, F., Harding, S. E., Schmidt, U., Matsui, T., Kang, Z. B., Dec, G. W., Gwathmey, J. K., Rosenzweig, A. and Hajjar, R. J. (1999) Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation 100, 2308-2311.
6. El-Armouche, A., Rau, T., Zolk, O., Ditz, D., Pamminger, T., Zimmermann, W. H., Jäckel, E., Harding, S. E., Boknik, P., Neumann, J. and Eschenhagen, T. (2003) Evidence for protein phosphatase inhibitor-1 playing an amplifier role in beta-adrenergic signaling in cardiac myocytes. FASEB J. 17, 437-439.
7. Endo, S., Zhou, X., Connor, J., Wang, B. and Shenolikar, S. (1996) Multiple structural elements define the specific- ity of recombinant human inhibitor-1 as a protein phos- phatase-1 inhibitor. Biochemistry 35, 5220-5228.
8. Gupta, R. C., Neumann, J., Watanabe, A. M., Lesch, M. and Sabbah, H. N. (1996) Evidence for presence and hormonal regulation of protein phosphatase inhibitor-1 in ven- tricular cardiomyocyte. Am. J. Physiol. 270, H1159-1164.
9. Gwathmey, J. K., Copelas, L., MacKinnon, R., Schoen, F. J., Feldman, M. D., Grossman, W. and Morgan, J. P. (1987) Abnormal intracellular calcium handling in my- ocardium from patients with end-stage heart failure. Circ. Res. 61, 70-76.
10. Haghighi, K., Kolokathis, F., Pater, L., Lynch, R. A., Asahi, M., Gramolini, A. O., Fan, G. C., Tsiapras, D., Hahn, H. S., Adamopoulos, S., Liggett, S. B., Dorn, G. W. 2nd, MacLennan, D. H., Kremastinos, D. T. and Kranias, E. G. (2003) Human phospholamban null results in lethal di- lated cardiomyopathy revealing a critical difference be- tween mouse and human. J. Clin. Invest. 111, 869-876.
11. Hajjar, R. J., Schmidt, U., Kang, J. X., Matsui, T. and Rosenzweig, A. (1997) Adenoviral gene transfer of phospholamban in isolated rat cardiomyocytes. Rescue effects by concomitant gene transfer of sarcoplasmic reticulum Ca(2+)-ATPase. Circ. Res. 81, 145-153.
12. 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.U.S.A. 95, 5251-5256.
13. Hambleton, M., Hahn, H., Pleger, S. T., Kuhn, M. C., Klevitsky, R., Carr, A. N., Kimball, T. F., Hewett, T. E., Dorn, G. W. 2nd, Koch, W. J. and Molkentin, J. D. (2006) Pharmacological- and gene therapy-based inhibition of protein kinase Calpha/beta enhances cardiac contractility and attenuates heart failure. Circulation 114, 574-582.
14. Hasenfuss, G., Reinecke, H., Studer, R., Meyer, M., Pieske, B., Holtz, J., Holubarsch, C., Posival, H., Just, H. and Drexler, H. (1994) Relation between myocardial function and expression of sarcoplasmic reticulum Ca(2+)- ATPase in failing and nonfailing human myocardium. Circ. Res. 75, 434-442.
15. Houser, S. R., Piacentino, V. 3rd and Weisser, J. (2000) Abnormalities of calcium cycling in the hypertrophied and failing heart. J. Mol. Cell Cardiol. 32, 1595-1607.
16. Jaski, B. E., Jessup, M. L., Mancini, D. M., Cappola, T. P., Pauly, D. F., Greenberg, B., Borow, K., Dittrich, H., Zsebo, K. M. and Hajjar, R. J. (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.
17. Jessup, M., Greenberg, B., Mancini, D., Cappola, T., Pauly, D. F., Jaski, B., Yaroshinsky, A., Zsebo, K. M., Dittrich, H. and Hajjar, R. J. (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.
18. Ji, Y., Lalli, M. J., Babu, G. J., Xu, Y., Kirkpatrick, D. L., Liu, L. H., Chiamvimonvat, N., Walsh, R. A., Shull, G. E. and Periasamy, M. (2000) Disruption of a single copy of the SERCA2 gene results in altered Ca2+ homeostasis and cardiomyocyte function. J. Biol. Chem. 275, 38073-38080.
19. Kadambi, V. J., Ponniah, S., Harrer, J. M., Hoit, B. D., Dorn, G. W. 2nd, Walsh, R. A. and Kranias, E. G. (1996) Cardiac-specific overexpression of phospholamban alters calcium kinetics and resultant cardiomyocyte mechanics in transgenic mice. J. Clin. Invest. 97, 533-539.
20. Kawase, Y., Ly, H. Q., Prunier, F., Lebeche, D., Shi, Y., Jin, H., Hadri, L., Yoneyama, R., Hoshino, K., Takewa, Y., Sakata, S., Peluso, R., Zsebo, K., Gwathmey, J. K., Tardif, J. C., Tanguay, J. F. and Hajjar, R. J. (2008) Reversal of cardiac dysfunction after longterm expression of SERCA2a by gene transfer in a pre-clinical model of heart failure. J. Am. Coll. Cardiol. 51, 1112-1119.
21. Kho, C., Lee, A., Jeong, D., Oh, J. G., Chaanine, A. H., Kizana, E., Park, W. J. and Hajjar, R. J. (2011) SUMO1- dependent modulation of SERCA2a in heart failure. Nature 477, 601-605.
22. Ladage, D., Tilemann, L., Ishikawa, K., Correll, R. N., Kawase, Y., Houser, S. R., Molkentin, J. D. and Hajjar, R. J. (2011) Inhibition of PKCalpha/beta with ruboxistaurin antagonizes heart failure in pigs after myocardial in- farction injury. Circ. Res. 109, 1396-1400.
23. Lehnart, S. E. (2007) Novel targets for treating heart and muscle disease: stabilizing ryanodine receptors and pre- venting intracellular calcium leak. Curr. Opin. Pharmacol. 7, 225-232.
24. Lehnart, S. E., Maier, L. S. and Hasenfuss, G. (2009) Abnormalities of calcium metabolism and myocardial contractility depression in the failing heart. Heart. Fail. Rev. 14, 213-224.
25. Limas, C. J., Olivari, M. T., Goldenberg, I. F., Levine, T. B., Benditt, D. G. and Simon, A. (1987) Calcium uptake by cardiac sarcoplasmic reticulum in human dilated cardiomyopathy. Cardiovasc Res. 21, 601-605.
26. Liu, Q., Chen, X., Macdonnell, S. M., Kranias, E. G., Lorenz, J. N., Leitges, M., Houser, S. R. and Molkentin, J. D. (2009) Protein kinase C{alpha}, but not PKC{beta} or PKC{gamma}, regulates contractility and heart failure susceptibility: implications for ruboxistaurin as a novel therapeutic approach. Circ. Res. 105, 194-200.
27. Lopez, A. D., Mathers, C. D., Ezzati, M., Jamison, D. T. and Murray, C. J. (2006) Global and regional burden of disease and risk factors, 2001: systematic analysis of pop- ulation health data. Lancet 367, 1747-1757.
28. Luo, W., Grupp, I. L., Harrer, J., Ponniah, S., Grupp, G., Duffy, J. J., Doetschman, T. and Kranias, E. G. (1994) Targeted ablation of the phospholamban gene is associated with markedly enhanced myocardial contractility and loss of beta-agonist stimulation. Circ. Res. 75, 401-409.
29. Luo, W., Wolska, B. M., Grupp, I. L., Harrer, J. M., Hag-highi, K., Ferguson, D. G., Slack, J. P., Grupp, G., Doets-chman, T., Solaro, R. J. and Kranias, E. G. (1996) Phos- pholamban gene dosage effects in the mammalian heart. Circ. Res. 78, 839-847.
30. MacDougall, L. K., Jones, L. R. and Cohen, P. (1991) Identification of the major protein phosphatases in mammalian cardiac muscle which dephosphorylate phospholamban. Eur. J. Biochem. 196, 725-734.
31. Mathers, C. D., Boerma, T. and Ma Fat, D. (2009) Global and regional causes of death. Br. Med. Bull. 92, 7-32.
32. Mathers, C. D. and Loncar, D. (2006) Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med. 3, e442.
33. Mercadier, J. J., Lompre, A. M., Duc, P., Boheler, K. R., Fraysse, J. B., Wisnewsky, C., Allen, P. D., Komajda, M. and Schwartz, K. (1990) Altered sarcoplasmic reticulum Ca2(+)-ATPase gene expression in the human ventricle during end-stage heart failure. J. Clin. Invest. 85, 305-309.
34. Movsesian, M. A., Leveille, C., Krall, J., Colyer, J., Wang, J. H. and Campbell, K. P. (1990) Identification and characterization of proteins in sarcoplasmic reticulum from normal and failing human left ventricles. J. Mol. Cell Cardiol. 22, 1477-1485.
35. Neumann, J., Eschenhagen, T., Jones, L. R., Linck, B., Schmitz, W., Scholz, H. and Zimmermann, N. (1997) Increased expression of cardiac phosphatases in patients with end-stage heart failure. J. Mol. Cell Cardiol. 29, 265-272.
36. Neumann, J. Gupta, R. C., Schmitz, W., Scholz, H., Nairn, A. C. and Watanabe, A. M. (1991) Evidence for iso-proterenol-induced phosphorylation of phosphatase inhibitor-1 in the intact heart. Circ. Res. 69, 1450-1457.
37. Nicolaou, P., Rodriguez, P., Ren, X., Zhou, X., Qian, J., Sadayappan, S., Mitton, B., Pathak, A., Robbins, J., Hajjar, R. J., Jones, K. and Kranias, E. G. (2009) Inducible expression of active protein phosphatase-1 inhibitor-1 enhances basal cardiac function and protects against ischemia/reperfusion injury. Circ. Res. 104, 1012-1020.
38. Oh, J. G., Kim, J., Jang, S. P., Nguen, M., Yang, D. K., Jeong, D., Park, Z. Y., Park, S. G., Hajjar, R. J. and Park, W. J. (2013) Decoy peptides targeted to protein phosphatase 1 inhibit dephosphorylation of phospholamban in cardiomyocytes. J. Mol. Cell Cardiol. 56, 63-71.
39. Pathak, A., del Monte, F., Zhao, W., Schultz, J. E., Lorenz, J. N., Bodi, I., Weiser, D., Hahn, H., Carr, A. N., Syed, F., Mavila, N., Jha, L., Qian, J., Marreez, Y., Chen, G., McGraw, D. W., Heist, E. K., Guerrero, J. L., DePaoli-Roach, A. A., Hajjar, R. J. and Kranias, E. G. (2005) Enhancement of cardiac function and suppression of heart failure progression by inhibition of protein phosphatase 1. Circ. Res. 96, 756-766.
40. Periasamy, M., Reed, T. D., Liu, L. H., Ji, Y., Loukianov, E., Paul, R. J., Nieman, M. L., Riddle, T., Duffy, J. J., Doetschman, T., Lorenz, J. N. and Shull, G. E. (1999) Impaired cardiac performance in heterozygous mice with a null mutation in the sarco(endo)plasmic reticulum Ca2+-ATPase isoform 2 (SERCA2) gene. J. Biol. Chem. 274, 2556-2562.
41. Prunier, F., Kawase, Y., Gianni, D., Scapin, C., Danik, S. B., Ellinor, P. T., Hajjar, R. J. and Del Monte, F. (2008) Prevention of ventricular arrhythmias with sarcoplasmic reticulum Ca2+ ATPase pump overexpression in a porcine model of ischemia reperfusion. Circulation 118, 614-624.
42. Rodriguez, P., Mitton, B., Nicolaou, P., Chen, G. and Kranias, E. G. (2007) Phosphorylation of human inhibitor-1 at Ser67 and/or Thr75 attenuates stimulatory effects of protein kinase A signaling in cardiac myocytes. Am. J. Physiol. Heart. Circ. Physiol. 293, H762-769.
43. Rodriguez, P., Mitton, B., Waggoner, J. R. and Kranias, E. G. (2006) Identification of a novel phosphorylation site in protein phosphatase inhibitor-1 as a negative regulator of cardiac function. J. Biol. Chem. 281, 38599-38608.
44. Schultz Jel, J., Glascock, B. J., Witt, S. A., Nieman, M. L., Nattamai, K. J., Liu, L. H., Lorenz, J. N., Shull, G. E., Kimball, T. R. and Periasamy, M. (2004) Accelerated onset of heart failure in mice during pressure overload with chronically decreased SERCA2 calcium pump activity. Am. J. Physiol. Heart. Circ. Physiol. 286, H1146-1153.
45. Steenaart, N. A., Ganim, J. R., Di Salvo, J. and Kranias, E. G. (1992) The phospholamban phosphatase associated with cardiac sarcoplasmic reticulum is a type 1 enzyme. Arch. Biochem. Biophys. 293, 17-24.
46. Yano, M., Yamamoto, T., Ikemoto, N. and Matsuzaki, M. (2005) Abnormal ryanodine receptor function in heart failure. Pharmacol. Ther. 107, 377-391.