Overexpression of the Na+/K+ ATPase α2 But Not α1 isopathological cardiac hypertrophy and remodelingform Attenuates

Circulation Research

Volumn 114, Issue 2, 2014, Pages 249-256

  Correll, Robert N ^a   Eder, Petra ^a,c   Burr, Adam R ^a   Despa, Sanda ^d   Davis, Jennifer ^a   Bers, Donald M ^d   Molkentin, Jeffery D ^a,b  

^a UNIVERSITY OF CINCINNATI   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Calcium signaling; Cardiac; Hypertrophy; Myocardial contraction; Myocytes; Sodium

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM) ALPHA1; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM) ALPHA2; ATRIAL NATRIURETIC FACTOR; BRAIN NATRIURETIC PEPTIDE; CALCIUM ION; MESSENGER RNA; MYOSIN HEAVY CHAIN ALPHA; MYOSIN HEAVY CHAIN BETA; PHOSPHOLAMBAN; RYANODINE RECEPTOR 2; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM ION; UNCLASSIFIED DRUG; ATP1A1 PROTEIN, RAT; ATP1A2 PROTEIN, RAT; CALCIUM; CALCIUM BINDING PROTEIN; ISOENZYME; NCX1 PROTEIN, MOUSE; SODIUM; SODIUM CALCIUM EXCHANGER 1; SODIUM-CALCIUM EXCHANGER 1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; ECHOCARDIOGRAPHY; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; HEART; HEART FAILURE; HEART MUSCLE CELL; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE PERFORMANCE; HEART VENTRICLE REMODELING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOPLASMIC RETICULUM; WESTERN BLOTTING; ANIMAL; CARDIOMEGALY; CELL CULTURE; DISEASE MODEL; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HEART CONTRACTION; HEART MUSCLE; HYPERTROPHY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; RAT; TIME; TRANSGENIC MOUSE; UPREGULATION;

CALCIUM SIGNALING; HYPERTROPHY; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; SODIUM;

ANIMALS; CALCIUM; CALCIUM-BINDING PROTEINS; CARDIOMEGALY; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ISOENZYMES; MICE; MICE, TRANSGENIC; MYOCARDIUM; PHOSPHORYLATION; RATS; SODIUM; SODIUM-CALCIUM EXCHANGER; SODIUM-POTASSIUM-EXCHANGING ATPASE; TIME FACTORS; TRANSFECTION; UP-REGULATION; VENTRICULAR REMODELING;

EID: 84897116242     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.114.302293     Document Type: Article

References (41)

1. Bers DM, Despa S. Cardiac myocytes Ca2+ and Na+ regulation in normal and failing hearts. J Pharmacol Sci. 2006;100:315-322.
2. Pogwizd SM, Sipido KR, Verdonck F, Bers DM. Intracellular Na in animal models of hypertrophy and heart failure: contractile function and arrhythmogenesis. Cardiovasc Res. 2003;57:887-896.
3. Pieske B, Maier LS, Piacentino V III, Weisser J, Hasenfuss G, Houser S. Rate dependence of [Na+]i and contractility in nonfailing and failing human myocardium. Circulation. 2002;106:447-453.
4. Goonasekera SA, Molkentin JD. Unraveling the secrets of a double life: contractile versus signaling Ca2+ in a cardiac myocyte. J Mol Cell Cardiol. 2012;52:317-322.
5. Despa S, Islam MA, Weber CR, Pogwizd SM, Bers DM. Intracellular Na(+) concentration is elevated in heart failure but Na/K pump function is unchanged. Circulation. 2002;105:2543-2548.
6. Baartscheer A, Schumacher CA, van Borren MM, Belterman CN, Coronel R, Fiolet JW. Increased Na+/H+-exchange activity is the cause of increased [Na+]i and underlies disturbed calcium handling in the rabbit pressure and volume overload heart failure model. Cardiovasc Res. 2003;57:1015-1024.
7. Maltsev VA, Sabbah HN, Higgins RS, Silverman N, Lesch M, Undrovinas AI. Novel, ultraslow inactivating sodium current in human ventricular cardiomyocytes. Circulation. 1998;98:2545-2552.
8. Yokoyama H, Gunasegaram S, Harding SE, Avkiran M. Sarcolemmal Na+/H+ exchanger activity and expression in human ventricular myocardium. J Am Coll Cardiol. 2000;36:534-540.
9. Valdivia CR, Chu WW, Pu J, Foell JD, Haworth RA, Wolff MR, Kamp TJ, Makielski JC. Increased late sodium current in myocytes from a canine heart failure model and from failing human heart. J Mol Cell Cardiol. 2005;38:475-483.
10. Nakamura TY, Iwata Y, Arai Y, Komamura K, Wakabayashi S. Activation of Na+/H+ exchanger 1 is sufficient to generate Ca2+ signals that induce cardiac hypertrophy and heart failure. Circ Res. 2008;103:891-899.
11. Sossalla S, Maier LS. Role of ranolazine in angina, heart failure, arrhythmias, and diabetes. Pharmacol Ther. 2012;133:311-323.
12. Sossalla S, Maurer U, Schotola H, Hartmann N, Didié M, Zimmermann WH, Jacobshagen C, Wagner S, Maier LS. Diastolic dysfunction and arrhythmias caused by overexpression of CaMKIIδ(c) can be reversed by inhibition of late Na(+) current. Basic Res Cardiol. 2011;106:263-272.
13. Dostanic I, Schultz Jel J, Lorenz JN, Lingrel JB. The alpha 1 isoform of Na, K-ATPase regulates cardiac contractility and functionally interacts and co-localizes with the Na/Ca exchanger in heart. J Biol Chem. 2004;279:54053-54061.
14. Lederer WJ, Niggli E, Hadley RW. Sodium-calcium exchange in excitable cells: fuzzy space. Science. 1990;248:283.
15. Swift F, Tovsrud N, Sjaastad I, Sejersted OM, Niggli E, Egger M. Functional coupling of alpha(2)-isoform Na(+)/K(+)-ATPase and Ca(2+) extrusion through the Na(+)/Ca(2+)-exchanger in cardiomyocytes. Cell Calcium. 2010;48:54-60.
16. Verdonck F, Mubagwa K, Sipido KR. [Na(+)] in the subsarcolemmal 'fuzzy' space and modulation of [Ca(2+)](i) and contraction in cardiac myocytes. Cell Calcium. 2004;35:603-612.
17. Rahimtoola SH, Tak T. The use of digitalis in heart failure. Curr Probl Cardiol. 1996;21:781-853.
18. Schwinger RH, Wang J, Frank K, Müller-Ehmsen J, Brixius K, McDonough AA, Erdmann E. Reduced sodium pump alpha1, alpha3, and beta1-isoform protein levels and Na+, K+-ATPase activity but unchanged Na+-Ca2+ exchanger protein levels in human heart failure. Circulation. 1999;99:2105-2112.
19. Bossuyt J, Ai X, Moorman JR, Pogwizd SM, Bers DM. Expression and phosphorylation of the na-pump regulatory subunit phospholemman in heart failure. Circ Res. 2005;97:558-565.
20. El-Armouche A, Wittköpper K, Fuller W, Howie J, Shattock MJ, Pavlovic D. Phospholemman-dependent regulation of the cardiac Na/K-ATPase activity is modulated by inhibitor-1 sensitive type-1 phosphatase. FASEB J. 2011;25:4467-4475.
21. James PF, Grupp IL, Grupp G, Woo AL, Askew GR, Croyle ML, Walsh RA, Lingrel JB. Identification of a specific role for the Na, KATPase alpha 2 isoform as a regulator of calcium in the heart. Mol Cell. 1999;3:555-563.
22. Berry RG, Despa S, Fuller W, Bers DM, Shattock MJ. Differential distribution and regulation of mouse cardiac Na+/K+-ATPase alpha1 and alpha2 subunits in T-tubule and surface sarcolemmal membranes. Cardiovasc Res. 2007;73:92-100.
23. Despa S, Lingrel JB, Bers DM. Na(+)/K)+)-ATPase α2-isoform preferentially modulates Ca2(+) transients and sarcoplasmic reticulum Ca2(+) release in cardiac myocytes. Cardiovasc Res. 2012;95:480-486.
24. Clifford RJ, Kaplan JH. Regulation of Na, K-ATPase subunit abundance by translational repression. J Biol Chem. 2009;284:22905-22915.
25. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR, Molkentin JD. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res. 2004;94:110-118.
26. Wu X, Chang B, Blair NS, Sargent M, York AJ, Robbins J, Shull GE, Molkentin JD. Plasma membrane Ca2+-ATPase isoform 4 antagonizes cardiac hypertrophy in association with calcineurin inhibition in rodents. J Clin Invest. 2009;119:976-985.
27. Despa S, Bossuyt J, Han F, Ginsburg KS, Jia LG, Kutchai H, Tucker AL, Bers DM. Phospholemman-phosphorylation mediates the beta-adrenergic effects on Na/K pump function in cardiac myocytes. Circ Res. 2005;97:252-259.
28. Pritchard TJ, Parvatiyar M, Bullard DP, Lynch RM, Lorenz JN, Paul RJ. Transgenic mice expressing Na+-K+-ATPase in smooth muscle decreases blood pressure. Am J Physiol Heart Circ Physiol. 2007;293:1172-1182.
29. McDonough AA, Zhang Y, Shin V, Frank JS. Subcellular distribution of sodium pump isoform subunits in mammalian cardiac myocytes. Am J Physiol. 1996;270:1221-1227.
30. Nakayama H, Otsu K, Yamaguchi O, Nishida K, Date MO, Hongo K, Kusakari Y, Toyofuku T, Hikoso S, Kashiwase K, Takeda T, Matsumura Y, Kurihara S, Hori M, Tada M. Cardiac-specific overexpression of a high Ca2+ affinity mutant of SERCA2a attenuates in vivo pressure overload cardiac hypertrophy. FASEB J. 2003;17:61-63.
31. Kimura J, Miyamae S, Noma A. Identification of sodium-calcium exchange current in single ventricular cells of guinea-pig. J Physiol. 1987;384:199-222.
32. Cheung JY, Zhang XQ, Song J, Gao E, Rabinowitz JE, Chan TO, Wang J. Phospholemman: A novel cardiac stress protein. Clin Transl Sci. 2010;3:189-196.
33. Song J, Zhang XQ, Ahlers BA, Carl LL, Wang J, Rothblum LI, Stahl RC, Mounsey JP, Tucker AL, Moorman JR, Cheung JY. Serine 68 of phospholemman is critical in modulation of contractility, [Ca2+]i transients, and Na+/Ca2+ exchange in adult rat cardiac myocytes. Am J Physiol Heart Circ Physiol. 2005;288:2342-2354.
34. Zhang XQ, Ahlers BA, Tucker AL, Song J, Wang J, Moorman JR, Mounsey JP, Carl LL, Rothblum LI, Cheung JY. Phospholemman inhibition of the cardiac Na+/Ca2+ exchanger. Role of phosphorylation. J Biol Chem. 2006;281:7784-7792.
35. Song J, Gao E, Wang J, Zhang XQ, Chan TO, Koch WJ, Shang X, Joseph JI, Peterson BZ, Feldman AM, Cheung JY. Constitutive overexpression of phosphomimetic phospholemman S68E mutant results in arrhythmias, early mortality, and heart failure: potential involvement of Na+/Ca2+ exchanger. Am J Physiol Heart Circ Physiol. 2012;302:770-781.
36. Dorn GW II, Molkentin JD. Manipulating cardiac contractility in heart failure: Data from mice and men. Circulation. 2004;109:150-158.
37. Jordan MC, Henderson SA, Han T, Fishbein MC, Philipson KD, Roos KP. Myocardial function with reduced expression of the sodium-calcium exchanger. J Card Fail. 2010;16:786-796.
38. Sawyer DB, Suter TM, Apstein CS. The sting of salt on an old, but open, wound-is Na(+) the cause of mitochondrial and myocardial inju ry during ischemia/reperfusion? J Mol Cell Cardiol. 2002;34:699-702.
39. Iwai T, Tanonaka K, Inoue R, Kasahara S, Kamo N, Takeo S. Mitochondrial damage during ischemia determines post-ischemic contractile dysfunction in perfused rat heart. J Mol Cell Cardiol. 2002;34:725-738.
40. Imahashi K, Pott C, Goldhaber JI, Steenbergen C, Philipson KD, Murphy E. Cardiac-specific ablation of the Na+-Ca2+ exchanger confers protection against ischemia/reperfusion injury. Circ Res. 2005;97:916-921.
41. Liu T, O'Rourke B. Enhancing mitochondrial Ca2+ uptake in myocytes from failing hearts restores energy supply and demand matching. Circ Res. 2008;103:279-288.