The resting membrane potential of hSC-CM in a syncytium is more hyperpolarised than that of isolated cells

References

• Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663–676.
   PubMed Web of Science ®Google Scholar
• Burridge PW, Matsa E, Shukla P, et al. Chemically defined generation of human cardiomyocytes. Nat Methods. 2014;11(8):855–860.
   PubMed Web of Science ®Google Scholar
• Ferri N, Siegl P, Corsini A, et al. Drug attrition during pre-clinical and clinical development: understanding and managing drug-induced cardiotoxicity. Pharmacol Ther. 2013;138(3):470–484.
   PubMed Web of Science ®Google Scholar
• Kopljar I, Lu HR, Van Ammel K, et al. Development of a human iPSC cardiomyocyte-based scoring system for cardiac hazard identification in early drug safety de-risking. Stem Cell Reports. 2018;11(6):1365–1377.
   PubMed Web of Science ®Google Scholar
• Kijlstra JD, Hu D, Mittal N, et al. Integrated analysis of contractile kinetics, force generation, and electrical activity in single human stem cell-derived cardiomyocytes. Stem Cell Reports. 2015;5(6):1226–1238.
   PubMed Web of Science ®Google Scholar
• Giles WR, Noble D. Rigorous phenotyping of cardiac iPSC preparations requires knowledge of their resting potential(s). Biophys J. 2016;110(1):278–280.
   PubMed Web of Science ®Google Scholar
• Bett GC, Kaplan AD, Lis A, et al. Electronic “expression” of the inward rectifier in cardiocytes derived from human-induced pluripotent stem cells. Heart Rhythm. 2013;10(12):1903–1910.
   PubMed Web of Science ®Google Scholar
• Chen Z, Xian W, Bellin M, et al. Subtype-specific promoter-driven action potential imaging for precise disease modelling and drug testing in hiPSC-derived cardiomyocytes. Eur Heart J. 2017;38(4):292–301.
   PubMed Web of Science ®Google Scholar
• Davis RP, Casini S, van den Berg CW, et al. Cardiomyocytes derived from pluripotent stem cells recapitulate electrophysiological characteristics of an overlap syndrome of cardiac sodium channel disease. Circulation. 2012;125(25):3079–3091.
   PubMed Web of Science ®Google Scholar
• Doss MX, Di Diego JM, Goodrow RJ, et al. Maximum diastolic potential of human induced pluripotent stem cell-derived cardiomyocytes depends critically on I(Kr). PLoS One. 2012;7(7):e40288.
   PubMed Web of Science ®Google Scholar
• Herron TJ, Rocha AM, Campbell KF, et al. Extracellular matrix-mediated maturation of human pluripotent stem cell-derived cardiac monolayer structure and electrophysiological function. Circ Arrhythm Electrophysiol. 2016;9(4):e003638.
   PubMed Web of Science ®Google Scholar
• Liang P, Lan F, Lee AS, et al. Drug screening using a library of human induced pluripotent stem cell-derived cardiomyocytes reveals disease-specific patterns of cardiotoxicity. Circulation. 2013;127(16):1677–1691.
   PubMed Web of Science ®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(5):H2006–17.
   PubMed Web of Science ®Google Scholar
• Vaidyanathan R, Markandeya YS, Kamp TJ, et al. IK1-enhanced human-induced pluripotent stem cell-derived cardiomyocytes: an improved cardiomyocyte model to investigate inherited arrhythmia syndromes. Am J Physiol Heart Circ Physiol. 2016;310(11):H1611–21.
   PubMed Web of Science ®Google Scholar
• Dhamoon AS, Jalife J. The inward rectifier current (IK1) controls cardiac excitability and is involved in arrhythmogenesis. Heart Rhythm. 2005;2(3):316–324.
   PubMed Web of Science ®Google Scholar
• Horvath A, Lemoine MD, Loser A, et al. Low resting membrane potential and low inward rectifier potassium currents are not inherent features of hipsc-derived cardiomyocytes. Stem Cell Reports. 2018;10(3):822–833.
   PubMed Web of Science ®Google Scholar
• Wilson JR, Clark RB, Banderali U, et al. Measurement of the membrane potential in small cells using patch clamp methods. Channels (Austin). 2011;5(6):530–537.
   PubMed Web of Science ®Google Scholar
• Koumi S, Backer CL, Arentzen CE. Characterization of inwardly rectifying K + channel in human cardiac myocytes. Circulation. 1995;92(2):164–174.
   PubMed Web of Science ®Google Scholar
• Henriquez AP, Vogel R, Muller-Borer BJ, et al. Influence of dynamic gap junction resistance on impulse propagation in ventricular myocardium: A computer simulation study. Biophys J. 2001;81(4):2112–2121.
   PubMed Web of Science ®Google Scholar
• Adermark L, Lovinger DM. Electrophysiological properties and gap junction coupling of striatal astrocytes. Neurochem Int. 2008;52(7):1365–1372.
   PubMed Web of Science ®Google Scholar
• Strausberg RL, Feingold EA, Grouse LH, et al. Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc Natl Acad Sci U S A. 2002;99:16899–16903.
   PubMed Web of Science ®Google Scholar
• Sun Y, Timofeyev V, Dennis A, et al. A singular role of IK1 promoting the development of cardiac automaticity during cardiomyocyte differentiation by IK1–induced activation of pacemaker current. Stem Cell Rev Rep. 2017;13(5):631–643.
   PubMed Web of Science ®Google Scholar
• Desplantez T, Verma V, Leybaert L, et al. Gap26, a connexin mimetic peptide, inhibits currents carried by connexin43 hemichannels and gap junction channels. Pharmacol Res. 2012;65(5):546–552.
   PubMed Web of Science ®Google Scholar
• Iyyathurai J, D’Hondt C, Wang N, et al. Peptides and peptide-derived molecules targeting the intracellular domains of Cx43: gap junctions versus hemichannels. Neuropharmacology. 2013;75:491–505.
   PubMed Web of Science ®Google Scholar
• Leybaert L, Lampe PD, Dhein S, et al. Connexins in cardiovascular and neurovascular health and disease: Pharmacological implications. Pharmacol Rev. 2017;69:396–478.
   PubMed Web of Science ®Google Scholar
• Kane C, Terracciano CMN. Concise review: Criteria for chamber-specific categorization of human cardiac myocytes derived from pluripotent stem cells. Stem Cells. 2017;35(8):1881–1897.
   PubMed Web of Science ®Google Scholar
• Lemoine MD, Mannhardt I, Breckwoldt K, et al. Human iPSC-derived cardiomyocytes cultured in 3D engineered heart tissue show physiological upstroke velocity and sodium current density. Sci Rep. 2017;7(1):5464.
   PubMedGoogle Scholar
• Abdelsayed M, Peters CH, Ruben PC. Differential thermosensitivity in mixed syndrome cardiac sodium channel mutants. J Physiol. 2015;593(18):4201–4223.
   PubMed Web of Science ®Google Scholar
• Irvine LA, Jafri MS, Winslow RL. Cardiac sodium channel markov model with temperature dependence and recovery from inactivation. Biophys J. 1999;76(4):1868–1885.
   PubMed Web of Science ®Google Scholar
• Rook MB, Bezzina Alshinawi C, Groenewegen WA, et al. Human SCN5A gene mutations alter cardiac sodium channel kinetics and are associated with the brugada syndrome. Cardiovasc Res. 1999;44(3):507–517.
   PubMed Web of Science ®Google Scholar
• Van de Sande DV, Kopljar I, Teisman A, et al. Pharmacological profile of the sodium current in human stem cell-derived cardiomyocytes compares to heterologous Nav1.5+beta1 model. Front Pharmacol. 2019;10:1374.
   PubMed Web of Science ®Google Scholar
• Buzatu S. The temperature-induced changes in membrane potential. Riv Biol. 2009;102(2):199–217.
   PubMedGoogle Scholar
• Coyne MD, Kim CS, Cameron JS, et al. Effects of temperature and calcium availability on ventricular myocardium from rainbow trout. Am J Physiol Regul Integr Comp Physiol. 2000;278(6):R1535–44.
   PubMed Web of Science ®Google Scholar
• Marshall JM. Effects of low temperatures on transmembrane potentials of single fibers of the rabbit atrium. Circ Res. 1957;5(6):664–669.
   PubMed Web of Science ®Google Scholar
• Ma B, Buckalew R, Du Y, et al. Gap junction coupling confers isopotentiality on astrocyte syncytium. Glia. 2016;64(2):214–226.
   PubMed Web of Science ®Google Scholar
• Kiyoshi CM, Du Y, Zhong S, et al. Syncytial isopotentiality: A system-wide electrical feature of astrocytic networks in the brain. Glia. 2018;66(12):2756–2769.
   PubMed Web of Science ®Google Scholar
• Goldberg GS, Moreno AP, Bechberger JF, et al. Evidence that disruption of connexon particle arrangements in gap junction plaques is associated with inhibition of gap junctional communication by a glycyrrhetinic acid derivative. Exp Cell Res. 1996;222(1):48–53.
   PubMed Web of Science ®Google Scholar
• Abudara V, Bechberger J, Freitas-Andrade M, et al. The connexin43 mimetic peptide Gap19 inhibits hemichannels without altering gap junctional communication in astrocytes. Front Cell Neurosci. 2014;8:306.
   PubMed Web of Science ®Google Scholar
• Kopljar I, De Bondt A, Vinken P, et al. Chronic drug-induced effects on contractile motion properties and cardiac biomarkers in human induced pluripotent stem cell-derived cardiomyocytes. Br J Pharmacol. 2017;174(21):3766–3779.
   PubMed Web of Science ®Google Scholar
• Wang N, De Bock M, Antoons G, et al. Connexin mimetic peptides inhibit Cx43 hemichannel opening triggered by voltage and intracellular Ca2+ elevation. Basic Res Cardiol. 2012;107(6):304.
   PubMed Web of Science ®Google Scholar
• Wang N, De Bock M, Decrock E, et al. Connexin targeting peptides as inhibitors of voltage- and intracellular Ca2+-triggered Cx43 hemichannel opening. Neuropharmacology. 2013;75:506–516.
   PubMed Web of Science ®Google Scholar
• Hibino H, Inanobe A, Furutani K, et al. Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev. 2010;90(1):291–366.
   PubMed Web of Science ®Google Scholar
• Gamper N, Stockand JD, Shapiro MS. The use of Chinese hamster ovary (CHO) cells in the study of ion channels. J Pharmacol Toxicol Methods. 2005;51(3):177–185.
   PubMedGoogle Scholar
• Ross GR, Rizvi F, Emelyanova L, et al. Prolonged post-differentiation culture influences the expression and biophysics of Na(+) and Ca(2+) channels in induced pluripotent stem cell-derived ventricular-like cardiomyocytes. Cell Tissue Res. 2019;378(1):59–66.
   PubMed Web of Science ®Google Scholar
• Lee HA, Hyun SA, Byun B, et al. Electrophysiological mechanisms of vandetanib-induced cardiotoxicity: comparison of action potentials in rabbit Purkinje fibers and pluripotent stem cell-derived cardiomyocytes. PLoS One. 2018;13(4):e0195577.
   PubMed Web of Science ®Google Scholar
• El-Battrawy I, Lan H, Cyganek L, et al. Modeling short QT syndrome using human-induced pluripotent stem cell-derived cardiomyocytes. J Am Heart Assoc. 2018;7.
   Web of Science ®Google Scholar
• Verkerk AO, Veerman CC, Zegers JG, et al. Patch-clamp recording from human induced pluripotent stem cell-derived cardiomyocytes: Improving action potential characteristics through dynamic clamp. Int J Mol Sci. 2017;18(9):18.
   Web of Science ®Google Scholar
• Mitcheson JS, Hancox JC, Levi AJ. Cultured adult cardiac myocytes: future applications, culture methods, morphological and electrophysiological properties. Cardiovasc Res. 1998;39(2):280–300.
   PubMed Web of Science ®Google Scholar
• Hoekstra M, Mummery CL, Wilde AA, et al. Induced pluripotent stem cell derived cardiomyocytes as models for cardiac arrhythmias. Front Physiol. 2012;3:346.
   PubMed Web of Science ®Google Scholar
• Jonsson MK, 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(5):998–1008.
   PubMed Web of Science ®Google Scholar
• Magyar J, Iost N, Kortvely A, et al. Effects of endothelin-1 on calcium and potassium currents in undiseased human ventricular myocytes. Pflugers Arch. 2000;441(1):144–149.
   PubMed Web of Science ®Google Scholar
• Clark RB, Tremblay A, Melnyk P, et al. T-tubule localization of the inward-rectifier K(+) channel in mouse ventricular myocytes: a role in K(+) accumulation. J Physiol. 2001;537(3):979–992.
   PubMed Web of Science ®Google Scholar
• Ponce-Balbuena D, Guerrero-Serna G, Valdivia CR, et al. Cardiac Kir2.1 and NaV1.5 channels traffic together to the sarcolemma to control excitability. Circ Res. 2018;122(11):1501–1516.
   PubMed Web of Science ®Google Scholar
• Utrilla RG, Nieto-Marin P, Alfayate S, et al. Kir2.1-Nav1.5 channel complexes are differently regulated than Kir2.1 and Nav1.5 channels alone. Front Physiol. 2017;8:903.
   PubMed Web of Science ®Google Scholar
• Garg P, Garg V, Shrestha R, et al. Human induced pluripotent stem cell-derived cardiomyocytes as models for cardiac channelopathies: A primer for non-electrophysiologists. Circ Res. 2018;123(2):224–243.
   PubMed Web of Science ®Google Scholar
• Yang X, Pabon L, Murry CE. Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Res. 2014;114(3):511–523.
   PubMed Web of Science ®Google Scholar
• Vermij SH, Rougier JS, Agullo-Pascual E, et al. Single-molecule localization of the cardiac voltage-gated sodium channel reveals different modes of reorganization at cardiomyocyte membrane domains. Circ Arrhythm Electrophysiol. 2020;13(7):e008241.
   PubMed Web of Science ®Google Scholar
• Kim C, Majdi M, Xia P, et al. Non-cardiomyocytes influence the electrophysiological maturation of human embryonic stem cell-derived cardiomyocytes during differentiation. Stem Cells Dev. 2010;19(6):783–795.
   PubMed Web of Science ®Google Scholar
• Nunes SS, Miklas JW, Liu J, et al. Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Nat Methods. 2013;10(8):781–787.
   PubMed Web of Science ®Google Scholar
• Sala L, Ward-van Oostwaard D, Tertoolen LGJ, et al. Electrophysiological analysis of human Pluripotent Stem Cell-derived Cardiomyocytes (hPSC-CMs) using Multi-electrode Arrays (MEAs). J Vis Exp. 2017; 123. DOI: https://doi.org/10.3791/55587.
   Google Scholar
• Jonsson MK, Wang QD, Becker B. Impedance-based detection of beating rhythm and proarrhythmic effects of compounds on stem cell-derived cardiomyocytes. Assay Drug Dev Technol. 2011;9(6):589–599.
   PubMed Web of Science ®Google Scholar