Cardiac sodium transport and excitation-contraction coupling

Journal of Molecular and Cellular Cardiology

Volumn 61, Issue , 2013, Pages 11-19

  Aronsen, J M ^a,b,c   Swift, F ^a,b   Sejersted, O M ^a,b  

^a ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c BJØRKNES UNIVERSITY COLLEGE   (Norway)

Author keywords

Calcium; EC coupling; Microdomains; Sodium

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALCIUM ION; PROTEIN NKA ALPHA2; PROTEIN SERCA2; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM ION; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

BIOPHYSICS; CALCIUM HOMEOSTASIS; CALCIUM INDUCED CALCIUM RELEASE; CALCIUM TRANSPORT; EXCITATION CONTRACTION COUPLING; HEART MUSCLE CELL; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SODIUM CELL LEVEL; SODIUM TRANSPORT; TRANSVERSE TUBULAR SYSTEM;

CALCIUM; EC-COUPLING; MICRODOMAINS; SODIUM;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; EXCITATION CONTRACTION COUPLING; HUMANS; ION CHANNEL GATING; MEMBRANE MICRODOMAINS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; SODIUM; SODIUM-CALCIUM EXCHANGER; SODIUM-POTASSIUM-EXCHANGING ATPASE; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84880333396     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.06.003     Document Type: Review

References (106)

1. Withering W. An account of the foxglove, and some of its medicinal uses: with practical remarks on dropsy and other diseases 1785, G.G.J. & J. Robinson, London.
2. Schatzmann H.J. Herzglycoside als Hemmstoffe für den aktiven Kalium und Natrium Transport durch die Erythrocytenmembran. Helv Physiol Pharmacol Acta 1953, 11:346-354.
3. Skou J.C. The influence of some cations on an adenosine triphosphatase from peripheral nerves. Biochim Biophys Acta 1957, 23:394-401.
4. + across cell membrane. Physiol Rev 1965, 45:596-617.
5. Blaustein M.P., Lederer W.J. Sodium/calcium exchange: its physiological implications. Physiol Rev 1999, 79:763-854.
6. Reuter H., Seitz N. The dependence of calcium efflux from cardiac muscle on temperature and external ion composition. J Physiol 1968, 195:451-470.
7. 2+ electrochemical gradients in cardiac muscle and their relationship to force development. J Gen Physiol 1982, 80:325-351.
8. 2+ exchanger. Science 1990, 250:562-565.
9. 2+ exchange inhibitors. Circ Res 2002, 91:90-92.
10. Wasserstrom J.A., Schwartz D.J., Fozzard H.A. Relation between intracellular sodium and twitch tension in sheep cardiac Purkinje strands exposed to cardiac glycosides. Circ Res 1983, 52:697-705.
11. Ellingsen Ø., Sejersted O.M., Vengen Ø.A., Ilebekk A. In vivo quantification of myocardial Na-K pump rate during β-adrenergic stimulation of intact pig hearts. Acta Physiol Scand 1989, 135:493-503.
12. Wasserstrom J.A., Aistrup G.L. Digitalis: new actions for an old drug. Am J Physiol Heart Circ Physiol 2005, 289:H1781-H1793.
13. +-ATPase alpha2-isoform regulates cardiac contractility in rat cardiomyocytes. Cardiovasc Res 2007, 75:109-117.
14. Fabiato A. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 1983, 245:C1-C14.
15. Lee C.O., Dagostino M. Effect of strophanthidin on intracellular Na ion activity and twitch tension of constantly driven canine cardiac Purkinje fibers. Biophys J 1982, 40:185-198.
16. i and contractility in nonfailing and failing human myocardium. Circulation 2002, 106:447-453.
17. + regulation in cardiac myocytes. Cardiovasc Res 2003, 57:897-912.
18. Bossuyt J., Despa S., Han F., Hou Z., Robia S.L., Lingrel J.B., et al. Isoform specificity of the Na/K-ATPase association and regulation by phospholemman. J Biol Chem 2009, 284:26749-26757.
19. Saint D.A., Ju Y.K., Gage P.W. A persistent sodium current in rat ventricular myocytes. J Physiol 1992, 453:219-231.
20. Makielski J.C., Farley A.L. Na(+) current in human ventricle: implications for sodium loading and homeostasis. J Cardiovasc Electrophysiol 2006, 17(Suppl. 1):S15-S20.
21. Maier L.S., Sossalla S. The late Na current as a therapeutic target: where are we?. J Mol Cell Cardiol 2013, 10.
22. + pump rate in rat and rabbit ventricular myocytes. J Physiol 2002, 539:133-143.
23. Maack C., O'Rourke B. Excitation-contraction coupling and mitochondrial energetics. Basic Res Cardiol 2007, 102:369-392.
24. Boyman L., Williams G.S., Khananshvili D., Sekler I., Lederer W.J. NCLX: the mitochondrial sodium calcium exchanger. J Mol Cell Cardiol 2013, 59:205-213. [Epub;%2013 Mar 26.:205-13]. 10.1016/j.yjmcc.2013.03.012.
25. Carl S.L., Felix K., Caswell A.H., Brandt N.R., Ball W.J., Vaghy P.L., et al. Immunolocalization of sarcolemmal dihydropyridine receptor and sarcoplasmic reticular triadin and ryanodine receptor in rabbit ventricle and atrium. J Cell Biol 1995, 129:673-682.
26. Sun X.H., Protasi F., Takahashi M., Takeshima H., Ferguson D.G., Franzini-Armstrong C. Molecular architecture of membranes involved in excitation-contraction coupling of cardiac muscle. J Cell Biol 1995, 129:659-671.
27. Lederer W.J., Niggli E., Hadley R.W. Sodium-calcium exchange in excitable cells: fuzzy space. Science 1990, 248:283.
28. Cheng H., Lederer W.J. Calcium sparks. Physiol Rev 2008, 88:1491-1545.
29. Louch W.E., Hake J., Mork H.K., Hougen K., Skrbic B., Ursu D., et al. Slow Ca(2+) sparks de-synchronize Ca(2+) release in failing cardiomyocytes: evidence for altered configuration of Ca(2+) release units?. J Mol Cell Cardiol 2013, 58:41-52.
30. ++ exchanger in the human heart. J Clin Invest 1996, 98:1650-1658.
31. + channel. J Clin Invest 1989, 84:331-336.
32. + channels in the developing mouse heart. J Physiol 2005, 564:683-696.
33. Haufe V., Chamberland C., Dumaine R. The promiscuous nature of the cardiac sodium current. J Mol Cell Cardiol 2007, 42:469-477.
34. + channels: primary structure and function of two isoforms and alternatively spliced variants. Am J Physiol Heart Circ Physiol 2002, 282:H1007-H1017.
35. 2+ exchanger isoforms NCX1, NCX2, and NCX3 in rat. Am J Physiol 1997, 272:C1250-C1261.
36. Scriven D.R., Dan P., Moore E.D. Distribution of proteins implicated in excitation-contraction coupling in rat ventricular myocytes. Biophys J 2000, 79:2682-2691.
37. Scriven D.R., Moore E.D. Ca(2+) channel and Na(+)/Ca(2+) exchange localization in cardiac myocytes. J Mol Cell Cardiol 2012, 58:22-31.
38. Despa S., Brette F., Orchard C.H., Bers D.M. Na/Ca exchange and Na/K-ATPase function are equally concentrated in transverse tubules of rat ventricular myocytes. Biophys J 2003, 85:3388-3396.
39. 2+ exchange activity is localized in the T-tubules of rat ventricular myocytes. Circ Res 2002, 91:315-322.
40. Swift F., Franzini-Armstrong C., Oyehaug L., Enger U.H., Andersson K.B., Christensen G., et al. Extreme sarcoplasmic reticulum volume loss and compensatory T-tubule remodeling after Serca2 knockout. Proc Natl Acad Sci U S A 2012, 109:3997-4001.
41. Jayasinghe I.D., Cannell M.B., Soeller C. Organization of ryanodine receptors, transverse tubules, and sodium-calcium exchanger in rat myocytes. Biophys J 2009, 97:2664-2673.
42. 2+-exchanger in normal and detubulated rat cardiomyocytes. J Mol Cell Cardiol 2003, 35:1325-1337.
43. 2+ exchange protein in mammalian cardiac myocytes: an immunofluorescence and immunocolloidal gold-labeling study. J Cell Biol 1992, 117:337-345.
44. 2+ exchange protein in developing rabbit myocytes. Am J Physiol 1995, 268:C1126-C1132.
45. Kieval R.S., Bloch R.J., Lindenmayer G.E., Ambesi A., Lederer W.J. Immunofluorescence localization of the Na-Ca exchanger in heart cells. Am J Physiol 1992, 263:C545-C550.
46. Schulson M.N., Scriven D.R., Fletcher P., Moore E.D. Couplons in rat atria form distinct subgroups defined by their molecular partners. J Cell Sci 2011, 124:1167-1174.
47. 2+ exchanger and ryanodine receptor during development. Biophys J 2007, 93:2504-2518.
48. Dostanic I., Lorenz J.N., Schultz J.J., Grupp I.L., Neumann J.C., Wani M.A., et al. The alpha2 isoform of Na, K-ATPase mediates ouabain-induced cardiac inotropy in mice. J Biol Chem 2003, 278:53026-53034.
49. Dostanic I., Schultz J.J., Lorenz J.N., Lingrel J.B. 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.
50. Mohler P.J., Davis J.Q., Bennett V. Ankyrin-B coordinates the Na/K ATPase, Na/Ca exchanger, and InsP3 receptor in a cardiac T-tubule/SR microdomain. PLoS Biol 2005, 3:e423.
51. +-ATPase alpha2-isoform in heart failure. Cardiovasc Res 2008, 78:71-78.
52. +-ATPase alpha1 and alpha2 subunits in T-tubule and surface sarcolemmal membranes. Cardiovasc Res 2007, 73:92-100.
53. Lingrel J.B., Kuntzweiler T. Na+, K(+)-ATPase. J Biol Chem 1994, 269:19659-19662.
54. McDonough A.A., Zhang Y., Shin V., Frank J.S. Subcellular distribution of sodium pump isoform subunits in mammalian cardiac myocytes. Am J Physiol 1996, 270:C1221-C1227.
55. +-ATPase in cardiac myocytes: isoform specificity and effect of phospholemman. Am J Physiol Cell Physiol 2009, 297:C699-C705.
56. Price E.M., Lingrel J.B. Structure-function relationships in the Na, K-ATPase alpha subunit: site-directed mutagenesis of glutamine-111 to arginine and asparagine-122 to aspartic acid generates a ouabain-resistant enzyme. Biochemistry 1988, 27:8400-8408.
57. Jewell E.A., Lingrel J.B. Comparison of the substrate dependence properties of the rat Na, K-ATPase alpha 1, alpha 2, and alpha 3 isoforms expressed in HeLa cells. J Biol Chem 1991, 266:16925-16930.
58. +-ATPase isoform distribution in rat ventricular myocytes. Am J Physiol Cell Physiol 2007, 293:C321-C327.
59. Swift F., Tovsrud N., Sjaastad I., Sejersted O.M., 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.
60. 2+ release in cardiac myocytes. Cardiovasc Res 2012, 95:480-486.
61. 2+ transients in mouse ventricular myocytes. J Mol Cell Cardiol 2005, 39:113-120.
62. Scott J.D., Santana L.F. A-kinase anchoring proteins: getting to the heart of the matter. Circulation 2010, 121:1264-1271.
63. Lowe J.S., Palygin O., Bhasin N., Hund T.J., Boyden P.A., Shibata E., et al. Voltage-gated Nav channel targeting in the heart requires an ankyrin-G dependent cellular pathway. J Cell Biol 2008, 180:173-186.
64. Mohler P.J., Schott J.J., Gramolini A.O., Dilly K.W., Guatimosim S., duBell W.H., et al. Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature 2003, 421:634-639.
65. Stern M.D. Theory of excitation-contraction coupling in cardiac muscle. Biophys J 1992, 63:497-517.
66. 2+ ions in the dyadic cleft; continuous versus random walk description of diffusion. Biophys J 2008, 94:4184-4201.
67. Leblanc N., Hume J.R. Sodium current-induced release of calcium from cardiac sarcoplasmic reticulum. Science 1990, 248:372-376.
68. i and contraction in cardiac myocytes. Cell Calcium 2004, 35:603-612.
69. Silverman B., Warley A., Miller J.I., James A.F., Shattock M.J. Is there a transient rise in sub-sarcolemmal Na and activation of Na/K pump current following activation of I(Na) in ventricular myocardium?. Cardiovasc Res 2003, 57:1025-1034.
70. Wendt-Gallitelli M.F., Voigt T., Isenberg G. Microheterogeneity of subsarcolemmal sodium gradients. Electron probe microanalysis in guinea-pig ventricular myocytes. J Physiol (Lond) 1993, 472:33-44.
71. Kushmerick M.J., Podolsky R.J. Ionic mobility in muscle cells. Science 1969, 166:1297-1298.
72. Despa S., Kockskamper J., Blatter L.A., Bers D.M. Na/K pump-induced [Na](i) gradients in rat ventricular myocytes measured with two-photon microscopy. Biophys J 2004, 87:1360-1368.
73. 2+ signaling during acidosis in the ventricular myocyte. Biophys J 2013, 104(2, S1):362a. [Ref Type: Abstract].
74. Dlugosz M., Trylska J. Diffusion in crowded biological environments: applications of Brownian dynamics. BMC Biophys 2011, 4:3.
75. Hall D., Hoshino M. Effects of macromolecular crowding on intracellular diffusion from a single particle perspective. Biophys Rev 2010, 2:39-53.
76. 2+ regulates T-cell receptor activation by modulating the charge property of lipids. Nature 2013, 493:111-115.
77. Scriven D.R.L., Asghari P., Moore E.D.W. Microarchitecture of the dyad. Cardiovasc Res 2013, 98(2):169-176.
78. Neco P., Rose B., Huynh N., Zhang R., Bridge J.H., Philipson K.D., et al. Sodium-calcium exchange is essential for effective triggering of calcium release in mouse heart. Biophys J 2010, 99:755-764.
79. 2+ transient: evidence from NCX knockout mice. J Physiol 2010, 588:3267-3276.
80. Brette F., Orchard C.H. No apparent requirement for neuronal sodium channels in excitation-contraction coupling in rat ventricular myocytes. Circ Res 2006, 98:667-674.
81. + channels. J Physiol 2010, 588:4249-4260.
82. Noujaim S.F., Kaur K., Milstein M., Jones J.M., Furspan P., Jiang D., et al. A null mutation of the neuronal sodium channel NaV1.6 disrupts action potential propagation and excitation-contraction coupling in the mouse heart. FASEB J 2012, 26:63-72.
83. 2+ exchange in activation of excitation-contraction coupling in rat ventricular myocytes. J Physiol (Lond) 1996, 493(Pt 2):529-542.
84. Bouchard R.A., Clark R.B., Giles W.R. Role of sodium-calcium exchange in activation of contraction in rat ventricle. J Physiol 1993, 472:391-413.
85. 2+ exchange. Science 1992, 255:850-853.
86. 2+ exchange. Circ Res 1997, 81:1034-1044.
87. Bouchard R.A., Clark R.B., Giles W.R. Regulation of unloaded cell shortening by sarcolemmal sodium-calcium exchange in isolated rat ventricular myocytes. J Physiol 1993, 469:583-599.
88. 2+] during the cardiac action potential. Circ Res 2002, 90:182-189.
89. 2+ release in cardiomyocytes. Biophys J 2006, 91:779-792.
90. 2+ exchange: cardiac-specific knockout of NCX1. Circ Res 2004, 95:604-611.
91. 2+ flux. Circ Res 2005, 97:1288-1295.
92. James P.F., Grupp I.L., Grupp G., Woo A.L., Askew G.R., Croyle M.L., et al. Identification of a specific role for the Na, K-ATPase alpha 2 isoform as a regulator of calcium in the heart. Mol Cell 1999, 3:555-563.
93. Rindler T.N., Lasko V.M., Nieman M.L., Okada M., Lorenz J.N., Lingrel J.B. Knockout of the Na, K-ATPase α2-isoform in cardiac myocytes delays pressure overload-induced cardiac dysfunction. Am J Physiol Heart Circ Physiol 2013, 304:H1147-H1158.
94. 2+ exchange currents in mouse ventricular myocytes. Am J Physiol 1998, 275:H1808-H1817.
95. + pump low and high ouabain affinity alpha subunit isoforms are differently distributed in cells. Proc Natl Acad Sci U S A 1997, 94:1800-1805.
96. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
97. Bokenes J., Aronsen J.M., Birkeland J.A., Henriksen U.L., Louch W.E., Sjaastad I., et al. Slow contractions characterize failing rat hearts. Basic Res Cardiol 2008, 103:328-344.
98. Louch W.E., Hougen K., Mork H.K., Swift F., Aronsen J.M., Sjaastad I., et al. Sodium accumulation promotes diastolic dysfunction in end-stage heart failure following Serca2 knockout. J Physiol 2010, 588:465-478.
99. Andersson K.B., Birkeland J.A., Finsen A.V., Louch W.E., Sjaastad I., Wang Y., et al. Moderate heart dysfunction in mice with inducible cardiomyocyte-specific excision of the Serca2 gene. J Mol Cell Cardiol 2009, 47:180-187.
100. 2+ exchanger function during early and late relaxation in ventricular myocytes. Am J Physiol 1997, 273:H2765-H2773.
101. i in a restricted space of guinea-pig ventricular cells. J Physiol 1998, 509(Pt 2):457-470.
102. 2+ exchanger-mediated relaxation in rabbit ventricular myocytes. J Physiol 2001, 533:165-173.
103. +-pump rate in heart and skeletal muscle. Acta Physiol Scand 1996, 156:213-225.
104. Despa S., Bers D.M. Na/K pump current and [Na](i) in rabbit ventricular myocytes: local [Na](i) depletion and Na buffering. Biophys J 2003, 84:4157-4166.
105. + pump by reversal of an inhibitory oxidative modification. Circulation 2010, 122:2699-2708.
106. + pump regulation. Circ Res 2009, 105:185-193.