Structural and functional screening in human induced-pluripotent stem cell-derived cardiomyocytes accurately identifies cardiotoxicity of multiple drug types

Abassi, 2012, Dynamic monitoring of beating periodicity of stem cell-derived cardiomyocytes as a predictive tool for preclinical safety assessment, Br. J. Pharmacol., 165, 1424, 10.1111/j.1476-5381.2011.01623.x Arola, 2000, Acute doxorubicin cardiotoxicity involves cardiomyocyte apoptosis, Cancer Res., 60, 1789 Brueggemann, 2010, Novel actions of nonsteroidal anti-inflammatory drugs on vascular ion channels: accounting for cardiovascular side effects and identifying new therapeutic applications, Mol. Cell. Pharmacol., 2, 15 Cardinale, 2010, Role of biomarkers in chemotherapy-induced cardiotoxicity, Prog. Cardiovasc. Dis., 53, 121, 10.1016/j.pcad.2010.04.002 Cohen, 2011, Use of human stem cell derived cardiomyocytes to examine sunitinib mediated cardiotoxicity and electrophysiological alterations, Toxicol. Appl. Pharmacol., 257, 74, 10.1016/j.taap.2011.08.020 Colombo, 2013, Cardiac toxicity of anticancer agents, Curr. Cardiol. Rep., 15, 362, 10.1007/s11886-013-0362-6 Deavall, 2012, Drug-induced oxidative stress and toxicity, J. Toxicol., 2012, 645460, 10.1155/2012/645460 Doherty, 2013, Multi-parameter in vitro toxicity testing of crizotinib, sunitinib, erlotinib, and nilotinib in human cardiomyocytes, Toxicol. Appl. Pharmacol., 272, 245, 10.1016/j.taap.2013.04.027 Eisner, 1989, The effects of metabolic inhibition on intracellular calcium and pH in isolated rat ventricular cells, J. Physiol., 411, 393, 10.1113/jphysiol.1989.sp017580 Ernande, 2010, Impaired myocardial radial function in asymptomatic patients with type 2 diabetes mellitus: a speckle-tracking imaging study, J. Am. Soc. Echocardiogr., 23, 1266, 10.1016/j.echo.2010.09.007 FDA, 2013 Force, 2011, Cardiotoxicity of kinase inhibitors: the prediction and translation of preclinical models to clinical outcomes, Nat. Rev. Drug Discov., 10, 111, 10.1038/nrd3252 Glenn, 2007, Lipids and the heart: neither feast nor famine, Hypertension, 50, 463, 10.1161/HYPERTENSIONAHA.107.095612 Guo, 2011, Estimating the risk of drug-induced proarrhythmia using human induced pluripotent stem cell-derived cardiomyocytes, Toxicol. Sci., 123, 281, 10.1093/toxsci/kfr158 Guo, 2013, Refining the human iPSC-cardiomyocyte arrhythmic risk assessment model, Toxicol. Sci., 136, 581, 10.1093/toxsci/kft205 ICH S7A, 2000 ICH S7B, 2005 Harrigan, 2004, A randomized evaluation of the effects of six antipsychotic agents on QTc, in the absence and presence of metabolic inhibition, J. Clin. Psychopharmacol., 24, 62, 10.1097/01.jcp.0000104913.75206.62 Hartigan-Go, 1996, Concentration-related pharmacodynamic effects of thioridazine and its metabolites in humans, Clin. Pharmacol. Ther., 60, 543, 10.1016/S0009-9236(96)90150-2 Hasinoff, 2010, Mechanisms of myocyte cytotoxicity induced by the multikinase inhibitor sorafenib, Cardiovasc. Toxicol., 10, 1, 10.1007/s12012-009-9056-0 Hull, 1986, Toxic cardiomyopathy: the effect of antipsychotic-antidepressant drugs and calcium on myocardial protein degradation and structural integrity, Toxicol. Appl. Pharmacol., 86, 308, 10.1016/0041-008X(86)90061-X Jonsson, 2011, Impedance-based detection of beating rhythm and proarrhythmic effects of compounds on stem cell-derived cardiomyocytes, Assay Drug Dev. Technol., 9, 589, 10.1089/adt.2011.0396 Kelly, 1963, Thioridazine and electrocardiographic abnormalities, Can. Med. Assoc. J., 89, 1297 Kerkela, 2006, Cardiotoxicity of the cancer therapeutic agent imatinib mesylate, Nat. Med., 12, 908, 10.1038/nm1446 Kerkela, 2009, Sunitinib-induced cardiotoxicity is mediated by off-target inhibition of AMP-activated protein kinase, Clin. Transl. Sci., 2, 15, 10.1111/j.1752-8062.2008.00090.x Khan, 2013, The case for induced pluripotent stem cell-derived cardiomyocytes in pharmacological screening, Br. J. Pharmacol., 169, 304, 10.1111/j.1476-5381.2012.02118.x Korantzopoulos, 2007, The role of oxidative stress in the pathogenesis and perpetuation of atrial fibrillation, Int. J. Cardiol., 115, 135, 10.1016/j.ijcard.2006.04.026 Lamore, 2013, Cellular impedance assays for predictive preclinical drug screening of kinase inhibitor cardiovascular toxicity, Toxicol. Sci., 135, 402, 10.1093/toxsci/kft167 Laverty, 2011, How can we improve our understanding of cardiovascular safety liabilities to develop safer medicines?, Br. J. Pharmacol., 163, 675, 10.1111/j.1476-5381.2011.01255.x Lipshultz, 1991, Late cardiac effects of doxorubicin therapy for acute lymphoblastic leukemia in childhood, N. Engl. J. Med., 324, 808, 10.1056/NEJM199103213241205 Ma, 2011, High purity human-induced pluripotent stem cell-derived cardiomyocytes: electrophysiological properties of action potentials and ionic currents, Am. J. Physiol. Heart Circ. Physiol., 301, H2006, 10.1152/ajpheart.00694.2011 MacDonald, 2009, Toxicity testing in the 21st century: a view from the pharmaceutical industry, Toxicol. Sci., 110, 40, 10.1093/toxsci/kfp088 Minotti, 2004, Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity, Pharmacol. Rev., 56, 185, 10.1124/pr.56.2.6 Morton, 2014, Predicting changes in cardiac myocyte contractility during early drug discovery with in vitro assays, Toxicol. Appl. Pharmacol., 279, 87, 10.1016/j.taap.2014.06.005 Newby, 2011, Am. Heart J., 162, 64, 10.1016/j.ahj.2011.04.005 Ng, 2009, Findings from left ventricular strain and strain rate imaging in asymptomatic patients with type 2 diabetes mellitus, Am. J. Cardiol., 104, 1398, 10.1016/j.amjcard.2009.06.063 Orphanos, 2009, Cardiotoxicity induced by tyrosine kinase inhibitors, Acta Oncol., 48, 964, 10.1080/02841860903229124 Paakkari, 2002, Cardiotoxicity of new antihistamines and cisapride, Toxicol. Lett., 127, 279, 10.1016/S0378-4274(01)00510-0 Palmer, 2013, Establishment and assessment of a new human embryonic stem cell-based biomarker assay for developmental toxicity screening, Birth Defects Res. B Dev. Reprod. Toxicol., 98, 343, 10.1002/bdrb.21078 Park, 2013, The impact of drug-related QT prolongation on FDA regulatory decisions, Int. J. Cardiol., 168, 4975, 10.1016/j.ijcard.2013.07.136 Peters, 2015, Human stem cell-derived cardiomyocytes in cellular impedance assays: bringing cardiotoxicity screening to the front line, Cardiovasc. Toxicol., 15, 317, 10.1007/s12012-014-9268-9 Pointon, 2013, Phenotypic profiling of structural cardiotoxins in vitro reveals dependency on multiple mechanisms of toxicity, Toxicol. Sci., 132, 317, 10.1093/toxsci/kft005 Redfern, 2003, Relationships between preclinical cardiac electrophysiology, clinical QT interval prolongation and torsade de pointes for a broad range of drugs: evidence for a provisional safety margin in drug development, Cardiovasc. Res., 58, 32, 10.1016/S0008-6363(02)00846-5 Sager, 2014, Rechanneling the cardiac proarrhythmia safety paradigm: a meeting report from the Cardiac Safety Research Consortium, Am. Heart J., 167, 292, 10.1016/j.ahj.2013.11.004 Salvo, 2014, Cardiovascular events associated with the long-term use of NSAIDs: a review of randomized controlled trials and observational studies, Expert Opin. Drug Saf., 13, 573, 10.1517/14740338.2014.907792 Sawyer, 2010, Mechanisms of anthracycline cardiac injury: can we identify strategies for cardioprotection?, Prog. Cardiovasc. Dis., 53, 105, 10.1016/j.pcad.2010.06.007 Seidman, 2002, Cardiac dysfunction in the trastuzumab clinical trials experience, J. Clin. Oncol., 20, 1215, 10.1200/JCO.2002.20.5.1215 Shapiro, 2009, An ion channel hypothesis to explain divergent cardiovascular safety of cyclooxygenase-2 inhibitors: the answer to a hotly debated puzzle?, Mol. Pharmacol., 76, 942, 10.1124/mol.109.059683 Simunek, 2009, Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron, Pharmacol. Rep., 61, 154, 10.1016/S1734-1140(09)70018-0 Sirenko, 2013, Assessment of beating parameters in human induced pluripotent stem cells enables quantitative in vitro screening for cardiotoxicity, Toxicol. Appl. Pharmacol., 273, 500, 10.1016/j.taap.2013.09.017 Stone, 2015, Was there really any evidence that rosiglitazone increased the risk of myocardial infarction or death from cardiovascular causes?, Pharmacoepidemiol. Drug Saf., 24, 223, 10.1002/pds.3736 Sugamura, 2011, Reactive oxygen species in cardiovascular disease, Free Radic. Biol. Med., 51, 978, 10.1016/j.freeradbiomed.2011.05.004 Szczepaniak, 2007, Forgotten but not gone: the rediscovery of fatty heart, the most common unrecognized disease in America, Circ. Res., 101, 759, 10.1161/CIRCRESAHA.107.160457 ter Keurs, 2001, Damage induced arrhythmias: mechanisms and implications, Can. J. Physiol. Pharmacol., 79, 73, 10.1139/y00-114 Thomas, 1994, Drugs, QT interval abnormalities and ventricular arrhythmias, Adverse Drug React. Toxicol. Rev., 13, 77 van de Water, 2011, High content screening analysis of phospholipidosis: validation of a 96-well assay with CHO-K1 and HepG2 cells for the prediction of in vivo based phospholipidosis, Toxicol. In Vitro, 25, 1870, 10.1016/j.tiv.2011.05.026 Volkova, 2011, Anthracycline cardiotoxicity: prevalence, pathogenesis and treatment, Curr. Cardiol. Rev., 7, 214, 10.2174/157340311799960645 Whelan, 2010, Cell death in the pathogenesis of heart disease: mechanisms and significance, Annu. Rev. Physiol., 72, 19, 10.1146/annurev.physiol.010908.163111 Wolf, 2011, Preclinical evaluation of potential nilotinib cardiotoxicity, Leuk. Res., 35, 631, 10.1016/j.leukres.2010.11.001 Yeh, 2004, Cardiovascular complications of cancer therapy: diagnosis, pathogenesis, and management, Circulation, 109, 3122, 10.1161/01.CIR.0000133187.74800.B9