Targeting cardiac potassium channels for state-of-the-art drug discovery

Bibliography

• Snyders DJ. Structure and function of cardiac potassium channels. Cardiovasc Res 1999;42:377–90
   PubMed Web of Science ®Google Scholar
• Tamargo J, Caballero R, Gomez R, et al. Pharmacology of cardiac potassium channels. Cardiovasc Res 2004;62:9–33
   PubMed Web of Science ®Google Scholar
• Wulff H, Castle NA, Pardo LA. Voltage-gated potassium channels as therapeutic targets. Nat Rev Drug Discov 2009;8:982–1001
   PubMed Web of Science ®Google Scholar
• Schmitt N, Grunnet M, Olesen S-P. Cardiac potassium channel subtypes: new roles in repolarization and arrhythmia. Physiol Rev 2014;94:609–53
   PubMed Web of Science ®Google Scholar
• Nattel S, Qi XY. Calcium-dependent potassium channels in the heart: clarity and confusion. Cardiovasc Res 2014;101:185–6
   PubMed Web of Science ®Google Scholar
• Gurney A, Manoury B. Two-pore potassium channels in the cardiovascular system. Eur Biophys J 2009;38:305–18
   PubMed Web of Science ®Google Scholar
• Savelieva I, Camm J. Anti-arrhythmic drug therapy for atrial fibrillation: current anti-arrhythmic drugs, investigational agent and innovative approaches. Europace 2008;10:647–65
   PubMed Web of Science ®Google Scholar
• Conway EL, Musco S, Kowey PR. Drug therapy for atrial fibrillation. Cardiol Clin 2009;27:109–23
   PubMed Web of Science ®Google Scholar
• Chugh SS, Havmoeller R, Narayanan K, et al. Worldwide epidemiology of atrial fibrillation: a global burden of disease 2010 study. Circulation 2014;129:837–8
   PubMed Web of Science ®Google Scholar
• Sanguinetti MC, Curran ME, Zou A, et al. Coassembly of KVLQT1 and minK (IsK) proteins to form cardiac IKs potassium channel. Nature 1996;384:80–3
   PubMed Web of Science ®Google Scholar
• Barhanin J, Lesage F, Guillemare E, et al. KvLQT1 and IsK (minK) proteins associate to form the IKs cardiac potassium current. Nature 1996;384:78–80
   PubMed Web of Science ®Google Scholar
• An WF, Bowlby MR, Betty M, et al. Modulation of A-type potassium channels by a family of calcium sensors. Nature 2000;403:553–6
   PubMed Web of Science ®Google Scholar
• Shibata R, Misonou H, Campomanes CR, et al. A fundamental role for KChIPs in determining the molecular properties and trafficking of Kv4.2 potassium channels. J Biol Chem 2003;278:36445–54
   PubMed Web of Science ®Google Scholar
• Hibino H, Inanobe A, Furutani K, et al. Inward rectifying potassium channels: their structure, function and physiological roles. Physiol Rev 2010;90:291–366
   PubMed Web of Science ®Google Scholar
• Dascal N. Signalling via the G protein-activated K+ channels. Cell Signal 1997;9:551–73
   PubMed Web of Science ®Google Scholar
• Flagg TP, Enkvetchakul D, Koster JC, Nichols CG. Muscle KATP channels: recent insights to energy sensing and myoprotection. Physiol Rev 2010;90:799–829
   Google Scholar
• Noma A. ATP-regulated K+ channels in cardiac muscle. Nature 1983;305:147–8
   PubMed Web of Science ®Google Scholar
• Grover GJ, Garlid KD. ATP-sensitive potassium channels: a review of their cardioprotective pharmacology. J Mol Cell Cardiol 2000;32:677–95
   PubMed Web of Science ®Google Scholar
• Gross GJ, Peart JN. KATP channels and myocardial preconditioning: an update. Am J Physiol Heart Circ Physiol 2003;285:H921–30
   PubMed Web of Science ®Google Scholar
• Olszewska A, Szewczyk A. Mitochondria as a pharmacological target: magnum overview. IUBMB Life 2013;65:273–81
   PubMed Web of Science ®Google Scholar
• Yang T, Kanki H, Roden DM. Phosphorylation of the IKs channel complex inhibits drug block: novel mechanism underlying variable antiarrhythmic drug actions. Circulation 2003;108:132–4
   PubMed Web of Science ®Google Scholar
• Macias A, de la Cruz A, Prieto A, et al. PKC inhibition results in a Kv1.5+Kvbeta1.3 pharmacology closer to Kv1.5 channels. Br J Pharmacol 2014;171:4914–20
   PubMed Web of Science ®Google Scholar
• Walsh KB, Kass RS. Regulation of a heart potassium channel by protein kinase A and C. Science 1988;242:67–9
   PubMed Web of Science ®Google Scholar
• Kurokawa J, Abriel H, Kass RS. Molecular basis of the delayed rectifier current IKs in heart. J Mol Cell Cardiol 2001;33:873–82
   PubMed Web of Science ®Google Scholar
• Marx SO, Kurokawa J, Reiken S, et al. Requirement of a macromolecular signaling complex for beta-adrenergic receptor modulation of the KCNQ1-KCNE1 potassium channel. Science 2002;295:496–9
   PubMed Web of Science ®Google Scholar
• Varnum MD, Busch AE, Bond CT, et al. The minK channel underlies the cardiac potassium current IKs and mediates species-specific responses to protein kinase C. Proc Natl Acad Sci USA 1993;90:11528–32
   PubMed Web of Science ®Google Scholar
• Apkon M, Nerbonne JM. Alpha 1-adrenergic agonists selectively suppress voltage-dependent K+ currents in rat ventricular myocytes. Proc Natl Acad Sci USA 1988;85:8756–60
   PubMed Web of Science ®Google Scholar
• Braun AP, Fedida D, Clark RB, Giles WR. Intracellular mechanisms for alpha 1-adrenergic regulation of the transient outward current in rabbit atrial myocytes. J Physiol 1990;431:689–712
   PubMed Web of Science ®Google Scholar
• Nakamura TY, Coetzee WA, Vega-Saenz de Miera E, et al. Modulation of Kv4 channels, key components of rat ventricular transient outward K+ current, by PKC. Am J Physiol 1997;273:H1775–86
   Google Scholar
• Jiménez-Vargas JM, Restano-Cassulini R, Possani LD. Toxin modulators and blockers of hERG K+ channels. Toxicon 2012;60:492–501
   PubMed Web of Science ®Google Scholar
• Sanguinetti MC, Johnson JH, Hammerland LG, et al. Heteropodatoxins: peptides isolated from spider venom that block Kv4.2 potassium channels. Mol Pharmacol 1997;51:491–8
   PubMed Web of Science ®Google Scholar
• Diochot S, Drici MD, Moinier D, et al. Effects of phrixotoxins on the Kv4 family of potassium channels and implications for the role of Ito1 in cardiac electrogenesis. Br J Pharmacol 1999;126:251–63
   PubMed Web of Science ®Google Scholar
• Jin W, Lu Z. A novel high-affinity inhibitor for inward-rectifier K+ channels. Biochemistry 1998;37:13291–9
   PubMed Web of Science ®Google Scholar
• Escoubas P, Diochot S, Célérier ML, et al. Novel tarantula toxins for subtypes of voltage-dependent potassium channels in the Kv2 and Kv4 subfamilies. Mol Pharmacol 2002;62:48–57
   PubMed Web of Science ®Google Scholar
• GlobalData. Atrial Fibrillation Therapeutics Pipeline Assessment and Market Forecasts to 2017. 2011
   Google Scholar
• Roden DM. Long-QT syndrome. N Engl J Med 2008;358:169–76
   PubMed Web of Science ®Google Scholar
• Kannankeril P, Roden DM, Darbar D. Drug-induced long QT syndrome. Pharmacol Rev 2010;62:760–81
   PubMed Web of Science ®Google Scholar
• Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318:1917–20
   PubMed Web of Science ®Google Scholar
• Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861–72
   PubMed Web of Science ®Google Scholar
• Yang L, Soonpaa MH, Adler ED, et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 2008;453:524–8
   PubMed Web of Science ®Google Scholar
• Graichen R, Xu X, Braam SR, et al. Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK. Differentiation 2008;76:357–70
   PubMed Web of Science ®Google Scholar
• Lian X, Hsiao C, Wilson G, et al. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc Natl Acad Sci USA 2012;109:E1848–57
   PubMed Web of Science ®Google Scholar
• Braam SR, Passier R, Mummery CL. Cardiomyocytes from human pluripotent stem cells in regenerative medicine and drug discovery. Trends Pharmacol Sci 2009;30:536–45
   PubMed Web of Science ®Google Scholar
• Lieu DK, Turnbull IC, Costa KD, Li RA. Engineered human pluripotent stem cell-derived cardiac cells and tissues for electrophysiological studies. Drug Discov Today Dis Models 2012;9:e209–17
   Google Scholar
• Ma J, Guo L, Fiene SJ, et al. High purity human-induced pluripotent stem cell-derived cardiomyocytes: electrophysiological properties of action potentials and ionic currents. Am J Physiol Heart Circ Physiol 2011;301:H2006–17
   PubMed Web of Science ®Google Scholar
• Moretti A, Bellin M, Welling A, et al. Patient-specific induced pluripotent stem-cell models for Long-QT syndrome. N Engl J Med 2010;363:1397–409
   PubMed Web of Science ®Google Scholar
• Itzhaki I, Maizels L, Huber I, et al. Modelling the long QT syndrome with induced pluripotent stem cells. Nature 2011;471:225–9
   PubMed Web of Science ®Google Scholar
• Tang W, Kang J, Wu X, et al. Development and evaluation of high throughput functional assay methods for hERG potassium channel. J Biomol Screen 2001;6:325–31
   PubMed Web of Science ®Google Scholar
• Dorn A, Hermann F, Ebneth A, et al. Evaluation of a high-throughput fluorescence assay method for hERG potassium channel inhibition. J Biomol Screen 2005;10:339–47
   PubMed Web of Science ®Google Scholar
• Arkhammar P, Wahl P, Gerlach B, et al. Establishment and application of in vitro membrane potential assays in cell lines with endogenous or recombinant expression of ATP-sensitive potassium channels (Kir6.2/SUR1) using a fluorescent probe kit. J Biomol Screen 2004;9:382–90
   PubMed Web of Science ®Google Scholar
• Whiteaker KL, vis-Taber R, Scott VES, Gopalakrishnan M. Fluorescence-based functional assay for sarcolemmal ATP-sensitive potassium channel activation in cultured neonatal rat ventricular myocytes. J Pharmacol Toxicol Methods 2007;46:45–50
   Google Scholar
• Walsh KB. A real-time screening assay for GIRK1/4 channel blockers. J Biomol Screen 2010;15:1229–37
   PubMed Web of Science ®Google Scholar
• Terstappen GC. Functional analysis of native and recombinant ion channels using a high-capacity nonradioactive rubidium efflux assay. Anal Biochem 1999;272:149–55
   PubMed Web of Science ®Google Scholar
• Karczewski J, Kiss L, Kane SA, et al. High-throughput analysis of drug binding interactions for the human cardiac channel, Kv1.5. Biochem Pharmacol 2009;77:177–85
   PubMed Web of Science ®Google Scholar
• Rezazadeh S, Hesketh JC, Fedida D. Rb+ flux through hERG channels affects the potency of channel blocking drugs: correlation with data obtained using a high-throughput Rb+ efflux assay. J Biomol Screen 2004;9:588–97
   PubMed Web of Science ®Google Scholar
• Jow F, Tseng E, Maddox T, et al. Rb+ efflux through functional activation of cardiac KCNQ1/minK channels by the benzodiazepine R-L3. Assay Drug Dev Technol 2006;4:443–50
   PubMed Web of Science ®Google Scholar
• Weaver CD, Harden D, Dworetzky SI, et al. A thallium-sensitive, fluorescence-based assay for detecting and characterizing potassium channel modulators in mammalian cells. J Biomol Screen 2004;9:671–7
   PubMed Web of Science ®Google Scholar
• Raphemot R, Lonergan DF, Nguyen TT, et al. Discovery, characterization and structure-activity relationships of an inhibitor of inward rectifier potassium (Kir) channels with preference for Kir2.3, Kir3.X and Kir7.1. Front Pharmacol 2011;2:75
   Google Scholar
• Ramos-Hunter SJ, Engers DW, Kaufmann K, et al. Discovery and SAR of a novel series of GIRK1/2 and GIRK1/4 activators. Bioorg Med Chem Lett 2013;23:5195–8
   PubMed Web of Science ®Google Scholar
• Bridal TR, Margulis M, Wang X, et al. Comparison of human ether-á-go-go related gene screening assays based on IonWorks Quattro and thallium flux. Assay Drug Dev Technol 2010;8:755–65
   PubMed Web of Science ®Google Scholar
• Schmalhoffer WA, Swensen AM, Thomas BS, et al. A pharmacologically validated, high capacity, functional thallium flux assay for the human ether-à-go-go related gene potassium channel. ASSAY Drug Dev Technol 2010;8:714–26
   PubMed Web of Science ®Google Scholar
• Dunlop J, Bowlby M, Peri R, et al. High-throughput electrophysiology: an emerging paradigm for ion-channel screening and physiology. Nat Rev Drug Discov 2008;7:358–68
   PubMed Web of Science ®Google Scholar
• Möller C, Slack M. Impact of new technologies for cellular screening along the drug value chain. Drug Discov Today 2010;15:384–90
   PubMed Web of Science ®Google Scholar
• Milligan CJ, Li J, Sukumar P, et al. Robotic multiwell planar patch-clamp for native and primary mammalian cells. Nat Protoc 2009;4:244–55
   PubMed Web of Science ®Google Scholar
• Stoelzle S, Haythornthwaite A, Kettenhofen R, et al. Automated patch clamp on mESC-derived cardiomyocytes for cardiotoxicity prediction. J Biomol Screen 2011;16:910–16
   PubMed Web of Science ®Google Scholar
• Becker N, Stoelzle S, Göpel S, et al. Minimized cell usage for stem cell-derived and primary cells on an automated patch clamp system. J Pharmacol Toxicol Methods 2013;68:82–7
   PubMed Web of Science ®Google Scholar
• Herrington J, Solly K, Ratliff KS, et al. Identification of novel and selective Kv2 channel inhibitors. Mol Pharmacol 2011;80:959–64
   PubMed Web of Science ®Google Scholar
• Comley J. Eight years of surveying ion channel screening - has anything changed? Drug Discov World 2011;12:45–62
   Google Scholar
• Reppel M, Pillekamp F, Lu ZJ, et al. Microelectrode arrays: a new tool to measure embryonic heart activity. J Electrocardiol 2004;37(Suppl):104–9
   PubMedGoogle Scholar
• Meyer T, Leisgen C, Gonser B, Gunther E. QT-Screen: high-throughput cardiac safety pharmacology by extracellular electrophysiology on primary cardiac myocytes. ASSAY Drug Dev Technol 2004;2:507–14
   PubMed Web of Science ®Google Scholar
• Reppel M, Igelmund P, Egert U, et al. Effect of cardioactive drugs on action potential generation and propagation in embryonic stem cell-derived cardiomyocytes. Cell Physiol Biochem 2007;19:213–24
   PubMed Web of Science ®Google Scholar
• Caspi O, Itzhaki I, Kehat I, et al. In vitro electrophysiological drug testing using human embryonic stem cell derived cardiomyocytes. Stem Cells Dev 2009;18:161–72
   PubMed Web of Science ®Google Scholar
• Navarrete EG, Liang P, Lan F, et al. Screening drug-induced arrhythmia using human induced pluripotent stem cell−derived cardiomyocytes and low-impedance microelectrode arrays. Circulation 2013;128:S3–S13
   PubMed Web of Science ®Google Scholar
• Robertson C, Tran DD, George SC. Concise review: maturation phases of human pluripotent stem cell-derived cardiomyocytes. Stem Cells 2013;31:829–37
   PubMed Web of Science ®Google Scholar
• Chaniotakis N, Sofikiti N. Novel semiconductor materials for the development of chemical sensors and biosensors: a review. Anal Chim Acta 2008;615:1–9
   PubMed Web of Science ®Google Scholar
• Bratov A, Abramova N, Ipatov A. Recent trends in potentiometric sensor arrays - a review. Anal Chim Acta 2010;678:149–59
   PubMed Web of Science ®Google Scholar
• Lee C-S, Kim SK, Kim M. Ion-sensitive field-effect transistors for biological sensing. Sensors 2009;9:7111–31
   PubMed Web of Science ®Google Scholar
• Poghossian A, Ingebrandt S, Offenäusser A, Schöning MJ. Field-effect devices for detecting cellular signals. Semin Cell Dev Biol 2009;20:41–8
   PubMed Web of Science ®Google Scholar
• Wang W, Watanabe M, Nakamura T, et al. Properties and expression of Ca2+-activated K+ channels in H9c2 cells derived from rat ventricle. Am J Physiol 1999;276:H1559–66
   PubMed Web of Science ®Google Scholar
• Latorre R, Oberhauser A, Labarca P, Alvarez O. Varieties of calcium-activated potassium channels. Annu Rev Physiol 1989;51:385–99
   PubMed Web of Science ®Google Scholar
• Wrobel G, Seifert R, Ingebrandt S, et al. Cell-transistor coupling: investigation of potassium currents recorded with p- and n-channel FETs. Biophys J 2005;89:3628–38
   PubMed Web of Science ®Google Scholar
• Burnett P, Robertson JK, Palmer JM, et al. Fluorescence imaging of electrically stimulated cells. J Biomol Screen 2003;8:660–7
   PubMed Web of Science ®Google Scholar
• Huang CJ, Harootunian A, Maher MP, et al. Characterization of voltage-gated sodium-channel blockers by electrical stimulation and fluorescence detection of membrane potential. Nat Biotechnol 2006;24:439–46
   PubMed Web of Science ®Google Scholar
• Lee BC, Kim HJ, Park SH, et al. Development of cell-based assay system that utilizes a hyperactive channel mutant for high-throughput screening of BKCa channel modulators. J Biotechnol 2013;167:41–6
   PubMed Web of Science ®Google Scholar
• Du F, Yu H, Zou B, et al. hERGCentral: a large database to store, retrieve, and analyze compound-human Ether-à-go-go related gene channel interactions to facilitate cardiotoxicity assessment in drug development. Assay Drug Dev Technol 2011;9:580–8
   PubMed Web of Science ®Google Scholar
• Jonsson MKB, Duker G, Tropp C, et al. Quantified proarrhythmic potential of selected human embryonic stem cell-derived cardiomyocytes. Stem Cell Res 2010;4:189–200
   PubMed Web of Science ®Google Scholar
• Jonsson MKB, Vos MA, Mirams GR, et al. Application of human stem cell-derived cardiomyocytes in safety pharmacology requires caution beyond hERG. J Mol Cell Cardiol 2012;52:998–1008
   PubMed Web of Science ®Google Scholar
• Cohen-Karni T, Qing Q, Li Q, et al. Graphene and nanowire transistors for cellular interfaces and electrical recording. Nano Lett 2010;10:1098–102
   PubMed Web of Science ®Google Scholar
• Hess LH, Jansen M, Maybeck V, et al. Graphene transistor arrays for recording action potentials from electrogenic cells. Adv Mater 2011;23:5045–9
   PubMed Web of Science ®Google Scholar
• Tolan NV, Genes LI, Spence DM. Merging microfluidics with microtitre technology for more efficient drug discovery. JALA Charlottesv Va 2008;13:275–9
   PubMedGoogle Scholar
• Natarajan A, Stancescu M, Dhir V, et al. Patterned cardiomyocytes on microelectrode arrays as a functional, high information content drug screening platform. Biomaterials 2011;32:4267–74
   PubMed Web of Science ®Google Scholar
• Kuila T, Bose S, Khanra P, et al. Recent advances in graphene-based biosensors. Biosens Bioelectron 2011;26:4637–48
   PubMed Web of Science ®Google Scholar
• Zhang D, Shadrin IY, Lam J, et al. Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 2013;34:5813–20
   PubMed Web of Science ®Google Scholar
• Nerbonne JM. Molecular basis of functional voltage-gated K+ channel diversity in the mammalian myocardium. J Physiol 2000;525(Pt 2):285–98
   PubMed Web of Science ®Google Scholar
• London B, Wang DW, Hill JA, Bennett PB. The transient outward current in mice lacking the potassium channel gene Kv1.4. J Physiol 1998;509(Pt 1):171–82
   PubMed Web of Science ®Google Scholar
• Wang Z, Fermini B, Nattel S. Sustained depolarization-induced outward current in human atrial myocytes. Circ Res 1993;73:1061–76
   PubMed Web of Science ®Google Scholar
• Snyders DJ, Tamkun MM, Bennett PB. A rapidly activating and slowly inactivating potassium channel cloned from human heart. Functional analysis after stable mammalian cell culture expression. J Gen Physiol 1993;101:513–43
   PubMed Web of Science ®Google Scholar
• Wang Z, Kiehn J, Yang Q, et al. Comparison of binding and block produced by alternatively spliced Kvbeta1 subunits. J Biol Chem 1996;271:28311–17
   PubMed Web of Science ®Google Scholar
• Sanguinetti MC, Jurkiewicz NK. Two components of cardiac delayed rectifier K+ current. Differential sensitivity to block by class III antiarrhythmic agents. J Gen Physiol 1990;96:195–215
   PubMed Web of Science ®Google Scholar
• Sanguinetti MC, Jiang C, Curran ME, Keating MT. A mechanistic link between an inherited and an acquired cardiac arrhythmia: hERG encodes the IKr potassium channel. Cell 1995;81:299–307
   PubMed Web of Science ®Google Scholar
• Abbott GW, Sesti F, Splawski I, et al. MiRP1 forms IKr potassium channels with hERG and is associated with cardiac arrhythmia. Cell 1999;97:175–87
   PubMed Web of Science ®Google Scholar
• Nakamura TY, Artman M, Rudy B, Coetzee WA. Inhibition of rat ventricular IK1 with antisense oligonucleotides targeted to Kir2.1 mRNA. Am J Physiol 1998;274:H892–900
   PubMed Web of Science ®Google Scholar
• Zaritsky JJ, Redell JB, Tempel BL, Schwarz TL. The consequences of disrupting cardiac inwardly rectifying K+ current (IK1) as revealed by the targeted deletion of the murine Kir2.1 and Kir2.2 genes. J Physiol 2001;533:697–710
   PubMed Web of Science ®Google Scholar
• Sakura H, Ämmälä C, Smith PA, et al. Cloning and functional expression of the cDNA encoding a novel ATP-sensitive potassium channel subunit expressed in pancreatic beta-cells, brain, heart and skeletal muscle. FEBS Lett 1995;377:338–44
   PubMed Web of Science ®Google Scholar
• Kubo Y, Reuveny E, Slesinger PA, et al. Primary structure and functional expression of a rat G-protein-coupled muscarinic potassium channel. Nature 1993;364:802–6
   PubMed Web of Science ®Google Scholar
• Krapivinsky G, Gordon EA, Wickman K, et al. The G-protein-gated atrial K+ channel IKAch is a heteromultimer of two inwardly rectifying K+-channel proteins. Nature 1995;374:135–41
   PubMed Web of Science ®Google Scholar
• Tinker A, Harmer SC. K+ channels in the heart: new insights and therapeutic implications. Expert Rev Clin Pharmacol 2010;3(3):305–19
   PubMedGoogle Scholar