Importance of the Voltage Dependence of Cardiac Na/K ATPase Isozymes

Biophysical Journal

Volumn 109, Issue 9, 2015, Pages 1852-1862

  Stanley, Christopher M ^a   Gagnon, Dominique G ^a   Bernal, Adam ^a   Meyer, Dylan J ^a   Rosenthal, Joshua J ^b   Artigas, Pablo ^a  

^a TEXAS TECH UNIVERSITY   (United States)

^b UNIVERSITY OF PUERTO RICO   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ISOENZYME; MONOVALENT CATION; POTASSIUM;

ANIMAL; CARDIAC MUSCLE CELL; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HEART VENTRICLE; HUMAN; MEMBRANE POTENTIAL; METABOLISM; OOCYTE; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; RAT; TUMOR CELL LINE; WESTERN BLOTTING; XENOPUS;

ANIMALS; BLOTTING, WESTERN; CATIONS, MONOVALENT; CELL LINE, TUMOR; FLUORESCENT ANTIBODY TECHNIQUE; HEART VENTRICLES; HUMANS; ISOENZYMES; MEMBRANE POTENTIALS; MYOCYTES, CARDIAC; OOCYTES; PATCH-CLAMP TECHNIQUES; POTASSIUM; RATS; SODIUM-POTASSIUM-EXCHANGING ATPASE; XENOPUS;

EID: 84947597954     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.09.015     Document Type: Article

References (74)

1. A.K. Sen, and R.L. Post Stoichiometry and localization of adenosine triphosphate-dependent sodium and potassium transport in the erythrocyte J. Biol. Chem. 239 1964 345 352
2. K. Geering The functional role of beta subunits in oligomeric P-type ATPases J. Bioenerg. Biomembr. 33 2001 425 438
3. G. Blanco Na,K-ATPase subunit heterogeneity as a mechanism for tissue-specific ion regulation Semin. Nephrol. 25 2005 292 303
4. J. Wang, and R.H. Schwinger A.A. McDonough Regional expression of sodium pump subunits isoforms and Na+-Ca++ exchanger in the human heart J. Clin. Invest. 98 1996 1650 1658
5. J. Orlowski, and J.B. Lingrel Tissue-specific and developmental regulation of rat Na,K-ATPase catalytic alpha isoform and beta subunit mRNAs J. Biol. Chem. 263 1988 10436 10442
6. R. Zahler, and W. Sun M. Kashgarian Na-K-ATPase alpha-isoform expression in heart and vascular endothelia: cellular and developmental regulation Am. J. Physiol. 270 1996 C361 C371
7. M. Juhaszova, and M.P. Blaustein Na+ pump low and high ouabain affinity alpha subunit isoforms are differently distributed in cells Proc. Natl. Acad. Sci. USA 94 1997 1800 1805
8. A.E. Moseley, and S.P. Lieske J.B. Lingrel The Na,K-ATPase alpha 2 isoform is expressed in neurons, and its absence disrupts neuronal activity in newborn mice J. Biol. Chem. 278 2003 5317 5324
9. P. Bøttger, and Z. Tracz K. Lykke-Hartmann Distribution of Na/K-ATPase alpha 3 isoform, a sodium-potassium P-type pump associated with rapid-onset of dystonia parkinsonism (RDP) in the adult mouse brain J. Comp. Neurol. 519 2011 376 404
10. A. Parekh, and A.J. Campbell S.N. Lawson Immunostaining for the α3 isoform of the Na+/K+-ATPase is selective for functionally identified muscle spindle afferents in vivo J. Physiol. 588 2010 4131 4143
11. K.J. Sweadner, and V.L. Herrera K.R. Repke Immunologic identification of Na+,K(+)-ATPase isoforms in myocardium. Isoform change in deoxycorticosterone acetate-salt hypertension Circ. Res. 74 1994 669 678
12. G. Blanco, and R.W. Mercer Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function Am. J. Physiol. 275 1998 F633 F650
13. C.B. Hensley, and M.M. Bersohn A.A. McDonough Amiodarone decreases Na,K-ATPase alpha 2 and beta 2 expression specifically in cardiac ventricle J. Mol. Cell. Cardiol. 26 1994 417 424
14. K. Harada, and H. Lin M. Inoue Subunit composition and role of Na+,K+-ATPases in ventricular myocytes J. Physiol. Sci. 56 2006 113 121
15. S. Bibert, and C.C. Liu H.H. Rasmussen FXYD proteins reverse inhibition of the Na+-K+ pump mediated by glutathionylation of its beta1 subunit J. Biol. Chem. 286 2011 18562 18572
16. S. Bibert, and S. Roy K. Geering Phosphorylation of phospholemman (FXYD1) by protein kinases A and C modulates distinct Na,K-ATPase isozymes J. Biol. Chem. 283 2008 476 486
17. G. Crambert, and M. Fuzesi K. Geering Phospholemman (FXYD1) associates with Na,K-ATPase and regulates its transport properties Proc. Natl. Acad. Sci. USA 99 2002 11476 11481
18. P. De Weer, D.C. Gadsby, and R.F. Rakowski Voltage dependence of the Na-K pump Annu. Rev. Physiol. 50 1988 225 241
19. F. Bezanilla How membrane proteins sense voltage Nat. Rev. Mol. Cell Biol. 9 2008 323 332
20. D.C. Gadsby, and M. Nakao Steady-state current-voltage relationship of the Na/K pump in guinea pig ventricular myocytes J. Gen. Physiol. 94 1989 511 537
21. C. Li, and O. Capendeguy J.D. Horisberger A third Na+-binding site in the sodium pump Proc. Natl. Acad. Sci. USA 102 2005 12706 12711
22. S. Yaragatupalli, and J.F. Olivera P. Artigas Altered Na+ transport after an intracellular alpha-subunit deletion reveals strict external sequential release of Na+ from the Na/K pump Proc. Natl. Acad. Sci. USA 106 2009 15507 15512
23. I.M. Ratheal, and G.K. Virgin P. Artigas Selectivity of externally facing ion-binding sites in the Na/K pump to alkali metals and organic cations Proc. Natl. Acad. Sci. USA 107 2010 18718 18723
24. G. Crambert, and U. Hasler K. Geering Transport and pharmacological properties of nine different human Na, K-ATPase isozymes J. Biol. Chem. 275 2000 1976 1986
25. J.D. Horisberger, and S. Kharoubi-Hess Functional differences between alpha subunit isoforms of the rat Na,K-ATPase expressed in Xenopus oocytes J. Physiol. 539 2002 669 680
26. M. Nakao, and D.C. Gadsby [Na] and [K] dependence of the Na/K pump current-voltage relationship in guinea pig ventricular myocytes J. Gen. Physiol. 94 1989 539 565
27. R.D. Peluffo, and J.R. Berlin Electrogenic K+ transport by the Na(+)-K+ pump in rat cardiac ventricular myocytes J. Physiol. 501 1997 33 40
28. R.D. Peluffo, Y. Hara, and J.R. Berlin Quaternary organic amines inhibit Na,K pump current in a voltage-dependent manner: direct evidence of an extracellular access channel in the Na,K-ATPase J. Gen. Physiol. 123 2004 249 263
29. F. Han, and A.L. Tucker D.M. Bers Extracellular potassium dependence of the Na+-K+-ATPase in cardiac myocytes: isoform specificity and effect of phospholemman Am. J. Physiol. Cell Physiol. 297 2009 C699 C705
30. S. Despa, and D.M. Bers Functional analysis of Na+/K+-ATPase isoform distribution in rat ventricular myocytes Am. J. Physiol. Cell Physiol. 293 2007 C321 C327
31. R.G. Berry, and S. Despa M.J. Shattock Differential distribution and regulation of mouse cardiac Na+/K+-ATPase alpha1 and alpha2 subunits in T-tubule and surface sarcolemmal membranes Cardiovasc. Res. 73 2007 92 100
32. J. Gao, and R.T. Mathias G.J. Baldo Two functionally different Na/K pumps in cardiac ventricular myocytes J. Gen. Physiol. 106 1995 995 1030
33. T.J. Mitchell, and C. Zugarramurdi P. Artigas Sodium and proton effects on inward proton transport through Na/K pumps Biophys. J. 106 2014 2555 2565
34. E.R. Liman, J. Tytgat, and P. Hess Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs Neuron 9 1992 861 871
35. E.M. Price, and J.B. Lingrel 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 27 1988 8400 8408
36. N. Vedovato, and D.C. Gadsby The two C-terminal tyrosines stabilize occluded Na/K pump conformations containing Na or K ions J. Gen. Physiol. 136 2010 63 82
37. N.N. Tavraz, and T. Friedrich M. Dichgans Diverse functional consequences of mutations in the Na+/K+-ATPase alpha2-subunit causing familial hemiplegic migraine type 2 J. Biol. Chem. 283 2008 31097 31106
38. C.M. Armstrong, R.P. Swenson Jr., and S.R. Taylor Block of squid axon K channels by internally and externally applied barium ions J. Gen. Physiol. 80 1982 663 682
39. W. Fuller, and P. Eaton M.J. Shattock Differential centrifugation separates cardiac sarcolemmal and endosomal membranes from Langendorff-perfused rat hearts Anal. Biochem. 293 2001 216 223
40. T.A. Pressley Phylogenetic conservation of isoform-specific regions within alpha-subunit of Na(+)-K(+)-ATPase Am. J. Physiol. 262 1992 C743 C751
41. G. Galarza-Muñoz, and S.I. Soto-Morales J.J. Rosenthal Physiological adaptation of an Antarctic Na+/K+-ATPase to the cold J. Exp. Biol. 214 2011 2164 2174
42. J.P. Castillo, and D. De Giorgis F. Bezanilla Energy landscape of the reactions governing the Na+ deeply occluded state of the Na+/K+-ATPase in the giant axon of the Humboldt squid Proc. Natl. Acad. Sci. USA 108 2011 20556 20561
43. T. Friedrich, E. Bamberg, and G. Nagel Na+,K(+)-ATPase pump currents in giant excised patches activated by an ATP concentration jump Biophys. J. 71 1996 2486 2500
44. G.E. Shull, J. Greeb, and J.B. Lingrel Molecular cloning of three distinct forms of the Na+,K+-ATPase alpha-subunit from rat brain Biochemistry 25 1986 8125 8132
45. W.J. O'Brien, J.B. Lingrel, and E.T. Wallick Ouabain binding kinetics of the rat alpha two and alpha three isoforms of the sodium-potassium adenosine triphosphate Arch. Biochem. Biophys. 310 1994 32 39
46. P.A. Lucchesi, and K.J. Sweadner Postnatal changes in Na,K-ATPase isoform expression in rat cardiac ventricle. Conservation of biphasic ouabain affinity J. Biol. Chem. 266 1991 9327 9331
47. A.A. McDonough, and Y. Zhang J.S. Frank Subcellular distribution of sodium pump isoform subunits in mammalian cardiac myocytes Am. J. Physiol. 270 1996 C1221 C1227
48. S. Despa, and J. Bossuyt D.M. Bers Phospholemman-phosphorylation mediates the beta-adrenergic effects on Na/K pump function in cardiac myocytes Circ. Res. 97 2005 252 259
49. W. Fuller, and J. Howie M.J. Shattock FXYD1 phosphorylation in vitro and in adult rat cardiac myocytes: threonine 69 is a novel substrate for protein kinase C Am. J. Physiol. Cell Physiol. 296 2009 C1346 C1355
50. F. Han, and J. Bossuyt D.M. Bers Role of phospholemman phosphorylation sites in mediating kinase-dependent regulation of the Na+-K+-ATPase Am. J. Physiol. Cell Physiol. 299 2010 C1363 C1369
51. J. Bossuyt, and S. Despa D.M. Bers Isoform specificity of the Na/K-ATPase association and regulation by phospholemman J. Biol. Chem. 284 2009 26749 26757
52. P. Artigas, and S.J. Al'aref O.S. Andersen 2,3-butanedione monoxime affects cystic fibrosis transmembrane conductance regulator channel function through phosphorylation-dependent and phosphorylation-independent mechanisms: the role of bilayer material properties Mol. Pharmacol. 70 2006 2015 2026
53. E. Tokhtaeva, and R.J. Clifford O. Vagin Subunit isoform selectivity in assembly of Na,K-ATPase α-β heterodimers J. Biol. Chem. 287 2012 26115 26125
54. G. Blanco The NA/K-ATPase and its isozymes: what we have learned using the baculovirus expression system Front. Biosci. 10 2005 2397 2411
55. E.A. Jewell, and J.B. Lingrel 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. 266 1991 16925 16930
56. J.B. Koenderink, and S. Geibel T. Friedrich Electrophysiological analysis of the mutated Na,K-ATPase cation binding pocket J. Biol. Chem. 278 2003 51213 51222
57. + clearance and volume responses Glia 62 2014 608 622
58. S. Koumi, and C.L. Backer R. Sato beta-Adrenergic modulation of the inwardly rectifying potassium channel in isolated human ventricular myocytes. Alteration in channel response to beta-adrenergic stimulation in failing human hearts J. Clin. Invest. 96 1995 2870 2881
59. T.L. Radzyukevich, and J.C. Neumann J.A. Heiny Tissue-specific role of the Na,K-ATPase α2 isozyme in skeletal muscle J. Biol. Chem. 288 2013 1226 1237
60. C.B. Thompson, and A.A. McDonough Skeletal muscle Na,K-ATPase alpha and beta subunit protein levels respond to hypokalemic challenge with isoform and muscle type specificity J. Biol. Chem. 271 1996 32653 32658
61. R. Gruener, and L.Z. Stern C. Gerdes Electrophysiologic properties of intercostal muscle fibers in human neuromuscular diseases Muscle Nerve 2 1979 165 172
62. M. Di Franco, H. Hakimjavadi, J.B. Lingrel, and J.A. Heiny Na,K-ATPase alpha2 activity in mammalian skeletal muscle T-tubules is acutely stimulated by extracellular K J. Gen. Physiol. 146 2015 281 294
63. F. Jaisser, and P. Jaunin J.D. Horisberger Modulation of the Na,K-pump function by beta subunit isoforms J. Gen. Physiol. 103 1994 605 623
64. G. Blanco, and J.C. Koster R.W. Mercer Kinetic properties of the alpha 2 beta 1 and alpha 2 beta 2 isozymes of the Na,K-ATPase Biochemistry 34 1995 319 325
65. W. Withering An Account of the Foxglove and Some of its Medical Uses: With Practical Remarks on Dropsy and Other Diseases 1785 J and J Robinson London
66. P.F. Baker, and M.P. Blaustein R.A. Steinhardt The influence of calcium on sodium efflux in squid axons J. Physiol. 200 1969 431 458
67. W.G. Wier, and P. Hess Excitation-contraction coupling in cardiac Purkinje fibers. Effects of cardiotonic steroids on the intracellular [Ca2+] transient, membrane potential, and contraction J. Gen. Physiol. 83 1984 395 415
68. A. Katz, and Y. Lifshitz S.J. Karlish Selectivity of digitalis glycosides for isoforms of human Na,K-ATPase J. Biol. Chem. 285 2010 19582 19592
69. P.J. Mohler, J.Q. Davis, and V. Bennett Ankyrin-B coordinates the Na/K ATPase, Na/Ca exchanger, and InsP3 receptor in a cardiac T-tubule/SR microdomain PLoS Biol. 3 2005 e423
70. I. Dostanic, and Jel. J. Schultz J.B. Lingrel 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. 279 2004 54053 54061
71. H. Song, and M.Y. Lee M.P. Blaustein An N-terminal sequence targets and tethers Na+ pump alpha2 subunits to specialized plasma membrane microdomains J. Biol. Chem. 281 2006 12929 12940
72. V. Golovina, and H. Song M. Blaustein Regulation of Ca2+ signaling by Na+ pump alpha-2 subunit expression Ann. N. Y. Acad. Sci. 986 2003 509 513
73. S. Despa, J.B. Lingrel, and D.M. Bers Na(+)/K)+)-ATPase α2-isoform preferentially modulates Ca2(+) transients and sarcoplasmic reticulum Ca2(+) release in cardiac myocytes Cardiovasc. Res. 95 2012 480 486
74. J.M. Aronsen, and J. Skogestad I. Sjaastad Hypokalaemia induces Ca(2+) overload and Ca(2+) waves in ventricular myocytes by reducing Na(+),K(+)-ATPase α2 activity J. Physiol. 593 2015 1509 1521