Accessory subunits alter the temperature sensitivity of Kv4.3 channel complexes

Journal of Molecular and Cellular Cardiology

Volumn 56, Issue 1, 2013, Pages 8-18

  Radicke, S ^a   Riedel, T ^a   Cotella, D ^b   Turnow, K ^c   Ravens, U ^c   Schaefer, M ^a   Wettwer, E ^c  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

subunits; Kv4.3 channel; Markov model; Temperature dependence; Transient outward current

Indexed keywords

POTASSIUM CHANNEL; POTASSIUM CHANNEL DPP6; POTASSIUM CHANNEL KCNE1; POTASSIUM CHANNEL KCNE2; POTASSIUM CHANNEL KV4.3; PROTEIN KCHIP2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHO CELL; COMPLEX FORMATION; CONTROLLED STUDY; FEMALE; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; KINETICS; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; ROOM TEMPERATURE; SIMULATION; STATISTICAL MODEL; TEMPERATURE DEPENDENCE; TEMPERATURE SENSITIVITY; THERMODYNAMICS; VOLTAGE CLAMP;

ACTION POTENTIALS; ANIMALS; CHO CELLS; CRICETINAE; DIPEPTIDYL-PEPTIDASES AND TRIPEPTIDYL-PEPTIDASES; HUMANS; ION CHANNEL GATING; KINETICS; MARKOV CHAINS; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTEIN STABILITY; PROTEIN SUBUNITS; SHAL POTASSIUM CHANNELS; THERMODYNAMICS;

EID: 84872798796     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2012.12.017     Document Type: Article

References (44)

1. Sah R., Ramirez R.J., Oudit G.Y., Gidrewicz D., Trivieri M.G., Zobel C., et al. Regulation of cardiac excitation-contraction coupling by action potential repolarization: role of the transient outward potassium current (I(to)). J Physiol (Lond.) 2003, 546:5-18.
2. Li L., Zhang L., Si Y., Xiao F., Li D., Gao S., et al. Effects of acute cooling/rewarming on membrane potential and K(+) currents in rat ventricular myocytes. Sheng Li Xue Bao 2008, 60:311-319.
3. Brouillette J., Clark R.B., Giles W.R., Fiset C. Functional properties of K+ currents in adult mouse ventricular myocytes. J Physiol (Lond.) 2004, 559:777-798.
4. Wettwer E., Amos G.J., Posival H., Ravens U. Transient outward current in human ventricular myocytes of subepicardial and subendocardial origin. Circ Res 1994, 75:473-482.
5. Näbauer M., Beuckelmann D.J., Uberfuhr P., Steinbeck G. Regional differences in current density and rate-dependent properties of the transient outward current in subepicardial and subendocardial myocytes of human left ventricle. Circulation 1996, 93:168-177.
6. An W.F., Bowlby M.R., Betty M., Cao J., Ling H.P., Mendoza G., et al. Modulation of A-type potassium channels by a family of calcium sensors. Nature 2000, 403:553-556.
7. Deschênes I., Tomaselli G.F. Modulation of Kv4.3 current by accessory subunits. FEBS Lett 2002, 528:183-188.
8. Nadal M.S., Ozaita A., Amarillo Y., de Vega-Saenz Miera E., Ma Y., Mo W., et al. The CD26-related dipeptidyl aminopeptidase-like protein DPPX is a critical component of neuronal A-type K+ channels. Neuron 2003, 37:449-461.
9. Radicke S., Cotella D., Graf E.M., Ravens U., Wettwer E. Expression and function of dipeptidyl-aminopeptidase-like protein 6 as a putative beta-subunit of human cardiac transient outward current encoded by Kv4.3. J Physiol (Lond.) 2005, 565:751-756.
10. Shibata R., Misonou H., Campomanes C.R., Anderson A.E., Schrader L.A., Doliveira L.C., et al. A fundamental role for KChIPs in determining the molecular properties and trafficking of Kv4.2 potassium channels. J Biol Chem 2003, 278:36445-36454.
11. Rosati B., Pan Z., Lypen S., Wang H.S., Cohen I., Dixon J.E., et al. Regulation of KChIP2 potassium channel beta subunit gene expression underlies the gradient of transient outward current in canine and human ventricle. J Physiol (Lond.) 2001, 533:119-125.
12. McCrossan Z.A., Abbott G.W. The MinK-related peptides. Neuropharmacology 2004, 47:787-821.
13. Radicke S., Cotella D., Graf E.M., Banse U., Jost N., Varró A., et al. Functional modulation of the transient outward current Ito by KCNE beta-subunits and regional distribution in human non-failing and failing hearts. Cardiovasc Res 2006, 71:695-703.
14. Greenstein J.L., Wu R., Po S., Tomaselli G.F., Winslow R.L. Role of the calcium-independent transient outward current I(to1) in shaping action potential morphology and duration. Circ Res 2000, 87:1026-1033.
15. Christ T., Wettwer E., Voigt N., Hala O., Radicke S., Matschke K., et al. Pathology-specific effects of the IKur/Ito/IK, ACh blocker AVE0118 on ion channels in human chronic atrial fibrillation. Br J Pharmacol 2008, 154:1619-1630.
16. Milescu L.S., Akk G., Sachs F. Maximum likelihood estimation of ion channel kinetics from macroscopic currents. Biophys J 2005, 88:2494-2515.
17. Fernández J.A., Skryma R., Bidaux G., Magleby K.L., Scholfield C.N., McGeown J.G., et al. Voltage- and cold-dependent gating of single TRPM8 ion channels. J Gen Physiol 2011, 137:173-195.
18. Feng J., Xu D., Wang Z., Nattel S. Ultrarapid delayed rectifier current inactivation in human atrial myocytes: properties and consequences. Am J Physiol 1998, 275:H1717-H1725.
19. Hille B. Ion channels of excitable membranes 2001, Sinauer, Sunderland, Mass. 3rd ed.
20. Campbell D.L., Rasmusson R.L., Qu Y., Strauss H.C. The calcium-independent transient outward potassium current in isolated ferret right ventricular myocytes. I. Basic characterization and kinetic analysis. J Gen Physiol 1993, 101:571-601.
21. Rich T.C., Yeola S.W., Tamkun M.M., Snyders D.J. Mutations throughout the S6 region of the hKv1.5 channel alter the stability of the activation gate. Am J Physiol Cell Physiol 2002, 282:C161-C171.
22. Ruff R.L. Effects of temperature on slow and fast inactivation of rat skeletal muscle Na(+) channels. Am J Physiol 1999, 277:C937-C947.
23. Iftinca M., McKay B.E., Snutch T.P., McRory J.E., Turner R.W., Zamponi G.W. Temperature dependence of T-type calcium channel gating. Neuroscience 2006, 142:1031-1042.
24. Vandenberg J.I., Varghese A., Lu Y., Bursill J.A., Mahaut-Smith M.P., Huang C.L. Temperature dependence of human ether-a-go-go-related gene K+ currents. Am J Physiol Cell Physiol 2006, 291:C165-C175.
25. Rodríguez B.M., Sigg D., Bezanilla F. Voltage gating of Shaker K+ channels. The effect of temperature on ionic and gating currents. J Gen Physiol 1998, 112:223-242.
26. Seebohm G., Lerche C., Busch A.E., Bachmann A. Dependence of I(Ks) biophysical properties on the expression system. Pflugers Arch 2001, 442:891-895.
27. Christé G., Simurdová M., Simurda J. Use-dependent features of 4-aminopyridine block of transient outward current in rat ventricular myocytes. Gen Physiol Biophys 1995, 14:75-89.
28. Petersen K.R., Nerbonne J.M. Expression environment determines K+ current properties: Kv1 and Kv4 alpha-subunit-induced K+ currents in mammalian cell lines and cardiac myocytes. Pflugers Arch 1999, 437:381-392.
29. Bertaso F., Sharpe C.C., Hendry B.M., James A.F. Expression of voltage-gated K+ channels in human atrium. Basic Res Cardiol 2002, 97:424-433.
30. Zhang M., Liu J., Jiang M., Wu D., Sonawane K., Guy H.R., et al. Interactions between charged residues in the transmembrane segments of the voltage-sensing domain in the hERG channel. J Membr Biol 2005, 207:169-181.
31. Unsöld B., Kerst G., Brousos H., Hübner M., Schreiber R., Nitschke R., et al. KCNE1 reverses the response of the human K+ channel KCNQ1 to cytosolic pH changes and alters its pharmacology and sensitivity to temperature. Pflugers Arch 2000, 441:368-378.
32. Wu D., Pan H., Delaloye K., Cui J. KCNE1 remodels the voltage sensor of Kv7.1 to modulate channel function. Biophys J 2010, 99:3599-3608.
33. Nadal M.S., Amarillo Y., de Vega-Saenz Miera E., Rudy B. Differential characterization of three alternative spliced isoforms of DPPX. Brain Res 2006, 1094:1-12.
34. Pongs O., Schwarz J.R. Ancillary subunits associated with voltage-dependent K+ channels. Physiol Rev 2010, 90:755-796.
35. Hale S.L., Kloner R.A. Mild hypothermia as a cardioprotective approach for acute myocardial infarction: laboratory to clinical application. J Cardiovasc Pharmacol Ther 2011, 16:131-139.
36. Radicke S., Cotella D., Sblattero D., Ravens U., Santoro C., Wettwer E. The transmembrane beta-subunits KCNE1, KCNE2, and DPP6 modify pharmacological effects of the antiarrhythmic agent tedisamil on the transient outward current Ito. Naunyn Schmiedebergs Arch Pharmacol 2009, 379:617-626.
37. Pourrier M., Schram G., Nattel S. Properties, expression and potential roles of cardiac K+ channel accessory subunits: MinK, MiRPs, KChIP, and KChAP. J Membr Biol 2003, 194:141-152.
38. Maguy A., Hebert T.E., Nattel S. Involvement of lipid rafts and caveolae in cardiac ion channel function. Cardiovasc Res 2006, 69:798-807.
39. Oudit G.Y., Kassiri Z., Sah R., Ramirez R.J., Zobel C., Backx P.H. The molecular physiology of the cardiac transient outward potassium current (I(to)) in normal and diseased myocardium. J Mol Cell Cardiol 2001, 33:851-872.
40. Workman A.J., Marshall G.E., Rankin A.C., Smith G.L., Dempster J. Transient outward K+ current reduction prolongs action potentials and promotes afterdepolarisations: a dynamic-clamp study in human and rabbit cardiac atrial myocytes. J Physiol (Lond.) 2012, 590:4289-4305.
41. Liu B., Arlock P., Wohlfart B., Johansson B.W. Temperature effects on the Na and Ca currents in rat and hedgehog ventricular muscle. Cryobiology 1991, 28:96-104.
42. Puglisi J.L., Yuan W., Bassani J.W., Bers D.M. Ca(2+) influx through Ca(2+) channels in rabbit ventricular myocytes during action potential clamp: influence of temperature. Circ Res 1999, 85:e7-e16.
43. Morita H., Zipes D.P., Morita S.T., Wu J. Temperature modulation of ventricular arrhythmogenicity in a canine tissue model of Brugada syndrome. Heart Rhythm 2007, 4:188-197.
44. Li G., Lau C., Ducharme A., Tardif J., Nattel S. Transmural action potential and ionic current remodeling in ventricles of failing canine hearts. Am J Physiol Heart Circ Physiol 2002, 283:H1031-H1041.