727
Views
6
CrossRef citations to date
0
Altmetric
Research Paper

Interaction of local anesthetics with the K+ channel pore domain

KcsA as a model for drug-dependent tetramer stability

, &
Pages 182-193 | Received 14 Jan 2013, Accepted 26 Mar 2013, Published online: 01 Apr 2013

References

  • Nau C, Wang GK. Interactions of local anesthetics with voltage-gated Na+ channels. J Membr Biol 2004; 201:1 - 8; http://dx.doi.org/10.1007/s00232-004-0702-y; PMID: 15635807
  • Catterall WA. Common modes of drug action on Na+ channels: local anesthetics, antiarrhythmics and anticonvulsants. Trends Pharmacol Sci 1987; 8:57 - 65; http://dx.doi.org/10.1016/0165-6147(87)90011-3
  • Catterall WA. Voltage-gated sodium channels at 60: structure, function and pathophysiology. J Physiol 2012; 590:2577 - 89; http://dx.doi.org/10.1113/jphysiol.2011.224204; PMID: 22473783
  • Armstrong CM. Interaction of tetraethylammonium ion derivatives with the potassium channels of giant axons. J Gen Physiol 1971; 58:413 - 37; http://dx.doi.org/10.1085/jgp.58.4.413; PMID: 5112659
  • French RJ, Shoukimas JJ. Blockage of squid axon potassium conductance by internal tetra-N-alkylammonium ions of various sizes. Biophys J 1981; 34:271 - 91; http://dx.doi.org/10.1016/S0006-3495(81)84849-7; PMID: 7236852
  • Kindler CH, Yost CS. Two-pore domain potassium channels: new sites of local anesthetic action and toxicity. Reg Anesth Pain Med 2005; 30:260 - 74; http://dx.doi.org/10.1016/j.rapm.2004.12.001; PMID: 15898030
  • Sanguinetti MC, Mitcheson JS. Predicting drug-hERG channel interactions that cause acquired long QT syndrome. Trends Pharmacol Sci 2005; 26:119 - 24; http://dx.doi.org/10.1016/j.tips.2005.01.003; PMID: 15749156
  • Sanguinetti MC, Tristani-Firouzi M. hERG potassium channels and cardiac arrhythmia. Nature 2006; 440:463 - 9; http://dx.doi.org/10.1038/nature04710; PMID: 16554806
  • Carlsson L, Duker G, Jacobson I. New pharmacological targets and treatments for atrial fibrillation. Trends Pharmacol Sci 2010; 31:364 - 71; http://dx.doi.org/10.1016/j.tips.2010.05.001; PMID: 20605645
  • Schumacher SM, McEwen DP, Zhang L, Arendt KL, Van Genderen KM, Martens JR. Antiarrhythmic drug-induced internalization of the atrial-specific k+ channel kv1.5. Circ Res 2009; 104:1390 - 8; http://dx.doi.org/10.1161/CIRCRESAHA.108.192773; PMID: 19443837
  • Khodakhah K, Melishchuk A, Armstrong CM. Killing K channels with TEA+. Proc Natl Acad Sci U S A 1997; 94:13335 - 8; http://dx.doi.org/10.1073/pnas.94.24.13335; PMID: 9371846
  • Gomez-Lagunas F. Quinidine interaction with Shab K+ channels: pore block and irreversible collapse of the K+ conductance. J Physiol 2010; 588:2691 - 706; http://dx.doi.org/10.1113/jphysiol.2010.193128; PMID: 20547671
  • Ficker E, Obejero-Paz CA, Zhao S, Brown AM. The binding site for channel blockers that rescue misprocessed human long QT syndrome type 2 ether-a-gogo-related gene (HERG) mutations. J Biol Chem 2002; 277:4989 - 98; http://dx.doi.org/10.1074/jbc.M107345200; PMID: 11741928
  • Ficker E, Dennis A, Kuryshev Y, Wible BA, Brown AM. HERG channel trafficking. Novartis Found Symp 2005; 266:57 - 69, discussion 70-4, 95-9; http://dx.doi.org/10.1002/047002142X.ch6; PMID: 16050262
  • Sanguinetti MC. HERG1 channelopathies. Pflugers Arch 2010; 460:265 - 76; http://dx.doi.org/10.1007/s00424-009-0758-8; PMID: 20544339
  • Rajamani S, Eckhardt LL, Valdivia CR, Klemens CA, Gillman BM, Anderson CL, et al. Drug-induced long QT syndrome: hERG K+ channel block and disruption of protein trafficking by fluoxetine and norfluoxetine. Br J Pharmacol 2006; 149:481 - 9; http://dx.doi.org/10.1038/sj.bjp.0706892; PMID: 16967046
  • Mitcheson JS, Chen J, Lin M, Culberson C, Sanguinetti MC. A structural basis for drug-induced long QT syndrome. Proc Natl Acad Sci U S A 2000; 97:12329 - 33; http://dx.doi.org/10.1073/pnas.210244497; PMID: 11005845
  • Chen J, Seebohm G, Sanguinetti MC. Position of aromatic residues in the S6 domain, not inactivation, dictates cisapride sensitivity of HERG and eag potassium channels. Proc Natl Acad Sci U S A 2002; 99:12461 - 6; http://dx.doi.org/10.1073/pnas.192367299; PMID: 12209010
  • Sánchez-Chapula JA, Navarro-Polanco RA, Culberson C, Chen J, Sanguinetti MC. Molecular determinants of voltage-dependent human ether-a-go-go related gene (HERG) K+ channel block. J Biol Chem 2002; 277:23587 - 95; http://dx.doi.org/10.1074/jbc.M200448200; PMID: 11960982
  • Kamiya K, Niwa R, Mitcheson JS, Sanguinetti MC. Molecular determinants of HERG channel block. Mol Pharmacol 2006; 69:1709 - 16; http://dx.doi.org/10.1124/mol.105.020990; PMID: 16474003
  • Massaeli H, Guo J, Xu J, Zhang S. Extracellular K+ is a prerequisite for the function and plasma membrane stability of HERG channels. Circ Res 2010; 106:1072 - 82; http://dx.doi.org/10.1161/CIRCRESAHA.109.215970; PMID: 20133899
  • Guo J, Massaeli H, Xu J, Jia Z, Wigle JT, Mesaeli N, et al. Extracellular K+ concentration controls cell surface density of IKr in rabbit hearts and of the HERG channel in human cell lines. J Clin Invest 2009; 119:2745 - 57; http://dx.doi.org/10.1172/JCI39027; PMID: 19726881
  • Robertson GA. Endocytic control of ion channel density as a target for cardiovascular disease. J Clin Invest 2009; 119:2531 - 4; http://dx.doi.org/10.1172/JCI40427; PMID: 19726880
  • Wible BA, Hawryluk P, Ficker E, Kuryshev YA, Kirsch G, Brown AM. HERG-Lite: a novel comprehensive high-throughput screen for drug-induced hERG risk. J Pharmacol Toxicol Methods 2005; 52:136 - 45; http://dx.doi.org/10.1016/j.vascn.2005.03.008; PMID: 15950494
  • Decher N, Pirard B, Bundis F, Peukert S, Baringhaus K-H, Busch AE, et al. Molecular basis for Kv1.5 channel block: conservation of drug binding sites among voltage-gated K+ channels. J Biol Chem 2004; 279:394 - 400; http://dx.doi.org/10.1074/jbc.M307411200; PMID: 14578345
  • Tamargo J, Caballero R, Gómez R, Delpón EI. I(Kur)/Kv1.5 channel blockers for the treatment of atrial fibrillation. Expert Opin Investig Drugs 2009; 18:399 - 416; http://dx.doi.org/10.1517/13543780902762850; PMID: 19335273
  • Beshore DC, Liverton NJ, McIntyre CJ, Claiborne CF, Libby B, Culberson JC, et al. Discovery of triarylethanolamine inhibitors of the Kv1.5 potassium channel. Bioorg Med Chem Lett 2010; 20:2493 - 6; http://dx.doi.org/10.1016/j.bmcl.2010.03.005; PMID: 20304642
  • Long SB, Campbell EB, Mackinnon R. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 2005; 309:897 - 903; http://dx.doi.org/10.1126/science.1116269; PMID: 16002581
  • Andér M, Luzhkov VB, Aqvist J. Ligand binding to the voltage-gated Kv1.5 potassium channel in the open state--docking and computer simulations of a homology model. Biophys J 2008; 94:820 - 31; http://dx.doi.org/10.1529/biophysj.107.112045; PMID: 17905851
  • Yang Q, Du L, Wang X, Li M, You Q. Modeling the binding modes of Kv1.5 potassium channel and blockers. J Mol Graph Model 2008; 27:178 - 87; http://dx.doi.org/10.1016/j.jmgm.2008.04.002; PMID: 18485768
  • Valenzuela C, Delpón E, Tamkun MM, Tamargo J, Snyders DJ. Stereoselective block of a human cardiac potassium channel (Kv1.5) by bupivacaine enantiomers. Biophys J 1995; 69:418 - 27; http://dx.doi.org/10.1016/S0006-3495(95)79914-3; PMID: 8527655
  • Steidl JV, Yool AJ. Distinct mechanisms of block of Kv1.5 channels by tertiary and quaternary amine clofilium compounds. Biophys J 2001; 81:2606 - 13; http://dx.doi.org/10.1016/S0006-3495(01)75904-8; PMID: 11606274
  • Aréchiga IA, Barrio-Echavarria GF, Rodríguez-Menchaca AA, Moreno-Galindo EG, Decher N, Tristani-Firouzi M, et al. Kv1.5 open channel block by the antiarrhythmic drug disopyramide: molecular determinants of block. J Pharmacol Sci 2008; 108:49 - 55; http://dx.doi.org/10.1254/jphs.08084FP; PMID: 18818480
  • Almers W, Armstrong CM. Survival of K+ permeability and gating currents in squid axons perfused with K+-free media. J Gen Physiol 1980; 75:61 - 78; http://dx.doi.org/10.1085/jgp.75.1.61; PMID: 7359118
  • Heinz A, Passow H. Role of external potassium in the calcium-induced potassium efflux from human red blood cell ghosts. J Membr Biol 1980; 57:119 - 31; http://dx.doi.org/10.1007/BF01868998; PMID: 6259362
  • Vergara C, Alvarez O, Latorre R. Localization of the K+ lock-In and the Ba2+ binding sites in a voltage-gated calcium-modulated channel. Implications for survival of K+ permeability. J Gen Physiol 1999; 114:365 - 76; http://dx.doi.org/10.1085/jgp.114.3.365; PMID: 10469727
  • Ambriz-Rivas M, Islas LD, Gomez-Lagunas F. K+-dependent stability and ion conduction of Shab K+ channels: a comparison with Shaker channels. Pflugers Arch 2005; 450:255 - 61; http://dx.doi.org/10.1007/s00424-005-1411-9; PMID: 15909181
  • Gómez-Lagunas F. Shaker B K+ conductance in Na+ solutions lacking K+ ions: a remarkably stable non-conducting state produced by membrane depolarizations. J Physiol 1997; 499:3 - 15; PMID: 9061636
  • Gómez-Lagunas F. Na(+) interaction with the pore of Shaker B K(+) channels: zero and low K(+) conditions. J Gen Physiol 2001; 118:639 - 48; http://dx.doi.org/10.1085/jgp.118.6.639; PMID: 11723158
  • Wang L, Dennis AT, Trieu P, Charron F, Ethier N, Hebert TE, et al. Intracellular potassium stabilizes human ether-à-go-go-related gene channels for export from endoplasmic reticulum. Mol Pharmacol 2009; 75:927 - 37; http://dx.doi.org/10.1124/mol.108.053793; PMID: 19139152
  • Krishnan MN, Bingham J-P, Lee SH, Trombley P, Moczydlowski EG. Functional role and affinity of inorganic cations in stabilizing the tetrameric structure of the KcsA K+ channel. J Gen Physiol 2005; 126:271 - 83; http://dx.doi.org/10.1085/jgp.200509323; PMID: 16129774
  • Krishnan MN, Trombley P, Moczydlowski EG. Thermal stability of the K+ channel tetramer: cation interactions and the conserved threonine residue at the innermost site (S4) of the KcsA selectivity filter. Biochemistry 2008; 47:5354 - 67; http://dx.doi.org/10.1021/bi702281p; PMID: 18419132
  • Zhou Y, MacKinnon R. The occupancy of ions in the K+ selectivity filter: charge balance and coupling of ion binding to a protein conformational change underlie high conduction rates. J Mol Biol 2003; 333:965 - 75; http://dx.doi.org/10.1016/j.jmb.2003.09.022; PMID: 14583193
  • Jiang Y, MacKinnon R. The barium site in a potassium channel by x-ray crystallography. J Gen Physiol 2000; 115:269 - 72; http://dx.doi.org/10.1085/jgp.115.3.269; PMID: 10694255
  • Morais-Cabral JH, Zhou Y, MacKinnon R. Energetic optimization of ion conduction rate by the K+ selectivity filter. Nature 2001; 414:37 - 42; http://dx.doi.org/10.1038/35102000; PMID: 11689935
  • Zhou Y, Morais-Cabral JH, Kaufman A, MacKinnon R. Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 A resolution. Nature 2001; 414:43 - 8; http://dx.doi.org/10.1038/35102009; PMID: 11689936
  • Pagliuca C, Goetze TA, Wagner R, Thiel G, Moroni A, Parcej D. Molecular properties of Kcv, a virus encoded K+ channel. Biochemistry 2007; 46:1079 - 90; http://dx.doi.org/10.1021/bi061530w; PMID: 17240991
  • Chatelain FC, Gazzarrini S, Fujiwara Y, Arrigoni C, Domigan C, Ferrara G, et al. Selection of inhibitor-resistant viral potassium channels identifies a selectivity filter site that affects barium and amantadine block. PLoS One 2009; 4:e7496; http://dx.doi.org/10.1371/journal.pone.0007496; PMID: 19834614
  • Wang S, Alimi Y, Tong A, Nichols CG, Enkvetchakul D. Differential roles of blocking ions in KirBac1.1 tetramer stability. J Biol Chem 2009; 284:2854 - 60; http://dx.doi.org/10.1074/jbc.M807474200; PMID: 19033439
  • Taylor RE. Effect of procaine on electrical properties of squid axon membrane. Am J Physiol 1959; 196:1071 - 8; PMID: 13649934
  • Uysal S, Cuello LG, Cortes DM, Koide S, Kossiakoff AA, Perozo E. Mechanism of activation gating in the full-length KcsA K+ channel. Proc Natl Acad Sci U S A 2011; 108:11896 - 9; http://dx.doi.org/10.1073/pnas.1105112108; PMID: 21730186
  • Cuello LG, Jogini V, Cortes DM, Perozo E. Structural mechanism of C-type inactivation in K(+) channels. Nature 2010; 466:203 - 8; http://dx.doi.org/10.1038/nature09153; PMID: 20613835
  • Bruhova I, Zhorov BS. KvAP-based model of the pore region of shaker potassium channel is consistent with cadmium- and ligand-binding experiments. Biophys J 2005; 89:1020 - 9; http://dx.doi.org/10.1529/biophysj.105.062240; PMID: 15908577
  • Zhou M, Morais-Cabral JH, Mann S, MacKinnon R. Potassium channel receptor site for the inactivation gate and quaternary amine inhibitors. Nature 2001; 411:657 - 61; http://dx.doi.org/10.1038/35079500; PMID: 11395760
  • Tikhonov DB, Zhorov BS. Sodium channels: ionic model of slow inactivation and state-dependent drug binding. Biophys J 2007; 93:1557 - 70; http://dx.doi.org/10.1529/biophysj.106.100248; PMID: 17496040
  • Bruhova I, Tikhonov DB, Zhorov BS. Access and binding of local anesthetics in the closed sodium channel. Mol Pharmacol 2008; 74:1033 - 45; http://dx.doi.org/10.1124/mol.108.049759; PMID: 18653802
  • Lenaeus MJ, Vamvouka M, Focia PJ, Gross A. Structural basis of TEA blockade in a model potassium channel. Nat Struct Mol Biol 2005; 12:454 - 9; http://dx.doi.org/10.1038/nsmb929; PMID: 15852022
  • Faraldo-Gómez JD, Kutluay E, Jogini V, Zhao Y, Heginbotham L, Roux B. Mechanism of intracellular block of the KcsA K+ channel by tetrabutylammonium: insights from X-ray crystallography, electrophysiology and replica-exchange molecular dynamics simulations. J Mol Biol 2007; 365:649 - 62; http://dx.doi.org/10.1016/j.jmb.2006.09.069; PMID: 17070844
  • Yohannan S, Hu Y, Zhou Y. Crystallographic study of the tetrabutylammonium block to the KcsA K+ channel. J Mol Biol 2007; 366:806 - 14; http://dx.doi.org/10.1016/j.jmb.2006.11.081; PMID: 17196615
  • Lu Z, Klem AM, Ramu Y. Ion conduction pore is conserved among potassium channels. Nature 2001; 413:809 - 13; http://dx.doi.org/10.1038/35101535; PMID: 11677598
  • Kutluay E, Roux B, Heginbotham L. Rapid intracellular TEA block of the KcsA potassium channel. Biophys J 2005; 88:1018 - 29; http://dx.doi.org/10.1529/biophysj.104.052043; PMID: 15556975
  • Langerman L, Bansinath M, Grant GJ. The partition coefficient as a predictor of local anesthetic potency for spinal anesthesia: evaluation of five local anesthetics in a mouse model. Anesth Analg 1994; 79:490 - 4; http://dx.doi.org/10.1213/00000539-199409000-00015; PMID: 8067553
  • Butterworth JF 4th, Strichartz GR. Molecular mechanisms of local anesthesia: a review. Anesthesiology 1990; 72:711 - 34; http://dx.doi.org/10.1097/00000542-199004000-00022; PMID: 2157353
  • Åqvist J, Luzhkov V. Ion permeation mechanism of the potassium channel. Nature 2000; 404:881 - 4; http://dx.doi.org/10.1038/35009114; PMID: 10786795
  • Thompson AN, Kim I, Panosian TD, Iverson TM, Allen TW, Nimigean CM. Mechanism of potassium-channel selectivity revealed by Na(+) and Li(+) binding sites within the KcsA pore. Nat Struct Mol Biol 2009; 16:1317 - 24; http://dx.doi.org/10.1038/nsmb.1703; PMID: 19946269
  • Hille B. Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor reaction. J Gen Physiol 1977; 69:497 - 515; http://dx.doi.org/10.1085/jgp.69.4.497; PMID: 300786
  • Strichartz GR, Ritchie JM. The action of local anesthetics on ion channels of excitable tissues. In: Strichartz GR, ed. Handbook of Experimental Pharmacology, Volume 81. New York: Springer-Verlag, 1987:21-52.
  • Garden DP, Zhorov BS. Docking flexible ligands in proteins with a solvent exposure- and distance-dependent dielectric function. J Comput Aided Mol Des 2010; 24:91 - 105; http://dx.doi.org/10.1007/s10822-009-9317-9; PMID: 20119653
  • Krissinel E, Henrick K. Inference of macromolecular assemblies from crystalline state. J Mol Biol 2007; 372:774 - 97; http://dx.doi.org/10.1016/j.jmb.2007.05.022; PMID: 17681537
  • Krissinel E. Crystal contacts as nature’s docking solutions. J Comput Chem 2010; 31:133 - 43; http://dx.doi.org/10.1002/jcc.21303; PMID: 19421996
  • Heginbotham L, Odessey E, Miller C. Tetrameric stoichiometry of a prokaryotic K+ channel. Biochemistry 1997; 36:10335 - 42; http://dx.doi.org/10.1021/bi970988i; PMID: 9254633
  • Weiner SJ, Kollman PA, Case DA, Singh UC, Chio C, Alagona G, et al. A new force field for molecular mechanical simulation of nucleic acids and proteins. J Am Chem Soc 1984; 106:765 - 84; http://dx.doi.org/10.1021/ja00315a051
  • Weiner SJ, Kollman PA, Nguyen DT, Case DA. An all atom force field for simulations of proteins and nucleic acids. J Comput Chem 1986; 7:230 - 52; http://dx.doi.org/10.1002/jcc.540070216
  • Dewar MJS, Zoebisch EG, Healy EF, Stewart JJP. AM1: A new general purpose quantum mechanical model. J Am Chem Soc 1985; 107:3902 - 9; http://dx.doi.org/10.1021/ja00299a024
  • Zhorov BS. Vector method for calculating derivatives of energy of atom-atom interactions of complex molecules according to generalized coordinates. J Struct Chem 1981; 22:4 - 8; http://dx.doi.org/10.1007/BF00745970
  • Zhorov BS. Vector method for calculating derivatives of the energy deformation of valence angles and torsion energy of complex molecules according to generalized coordinates. J Struct Chem 1983; 23:649 - 55; http://dx.doi.org/10.1007/BF00746185
  • Li Z, Scheraga HA. Monte Carlo-minimization approach to the multiple-minima problem in protein folding. Proc Natl Acad Sci U S A 1987; 84:6611 - 5; http://dx.doi.org/10.1073/pnas.84.19.6611; PMID: 3477791

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.