In Vivo and in Silico Investigation into Mechanisms of Frequency Dependence of Repolarization Alternans in Human Ventricular Cardiomyocytes

Circulation Research

Volumn 118, Issue 2, 2016, Pages 266-278

  Zhou, Xin ^a   Bueno Orovio, Alfonso ^a   Orini, Michele ^b   Hanson, Ben ^b,c   Hayward, Martin ^d   Taggart, Peter ^b   Lambiase, Pier D ^b   Burrage, Kevin ^a   Rodriguez, Blanca ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

^d QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

calcium; calibration; electrophysiology; pericardium; sarcoplasmic reticulum

Indexed keywords

SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; CALCIUM CHANNEL L TYPE; SODIUM CALCIUM EXCHANGE PROTEIN;

ACTION POTENTIAL DURATION; ADULT; AORTA VALVE REPLACEMENT; ARRHYTHMOGENESIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM CONDUCTANCE; CALCIUM CURRENT; CLINICAL ARTICLE; COMPUTER MODEL; CORONARY ARTERY BYPASS GRAFT; ELECTROGRAPHY; EPICARDIUM; FEMALE; FREQUENCY DEPENDENCE; HEART MUSCLE CELL; HEART VENTRICLE; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MEMBRANE STEADY POTENTIAL; MIDDLE AGED; PRIORITY JOURNAL; REPOLARIZATION ALTERNANS; TRIANGULATION; ACTION POTENTIAL; AGED; ARRHYTHMIAS, CARDIAC; BIOLOGICAL MODEL; CALCIUM SIGNALING; CARDIAC MUSCLE CELL; COMPUTER SIMULATION; HEART FUNCTION TEST; HEART RATE; METABOLISM; PATHOPHYSIOLOGY; PREDICTIVE VALUE; SIGNAL PROCESSING;

ACTION POTENTIALS; AGED; ARRHYTHMIAS, CARDIAC; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; COMPUTER SIMULATION; ELECTROPHYSIOLOGIC TECHNIQUES, CARDIAC; FEMALE; HEART RATE; HEART VENTRICLES; HUMANS; MALE; MIDDLE AGED; MODELS, CARDIOVASCULAR; MYOCYTES, CARDIAC; PREDICTIVE VALUE OF TESTS; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SIGNAL PROCESSING, COMPUTER-ASSISTED; SODIUM-CALCIUM EXCHANGER;

EID: 84955243411     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.307836     Document Type: Article

References (38)

1. Merchant FM, Armoundas AA., Role of substrate and triggers in the genesis of cardiac alternans, from the myocyte to the whole heart: implications for therapy. Circulation 2012;125:539-549. doi: 10.1161/CIRCULATIONAHA.111.033563.
2. Armoundas AA, Tomaselli GF, Esperer HD., Pathophysiological basis and clinical application of T-wave alternans. J Am Coll Cardiol 2002;40:207-217
3. Armoundas AA, Hohnloser SH, Ikeda T, Cohen RJ., Can microvolt T-wave alternans testing reduce unnecessary defibrillator implantation? Nat Clin Pract Cardiovasc Med 2005;2 522:528. doi: 10.1038/ncpcardio0323.
4. Qu Z, Xie Y, Garfinkel A, Weiss JN., T-wave alternans and arrhythmogenesis in cardiac diseases. Front Physiol 2010-1 154. doi: 10.3389/fphys.2010.00154.
5. Clancy Sato D., Cardiac Electrophysiological Dynamics From the Cellular Level to the Organ Level. Biomed Eng Comput Biol 2013;69
6. Fox JJ, McHarg JL, Gilmour RF Jr., Ionic mechanism of electrical alternans. Am J Physiol Heart Circ Physiol 2002:282-H516 H530. doi: 10.1152/ajpheart.00612.2001.
7. Narayan SM, Franz MR, Lalani G, Kim J, Sastry A., T-wave alternans, restitution of human action potential duration, and outcome. J Am Coll Cardiol 2007;50:2385-2392. doi: 10.1016/j.jacc.2007.10.011.
8. Pruvot EJ, Katra RP, Rosenbaum DS, Laurita KR., Role of calcium cycling versus restitution in the mechanism of repolarization alternans. Circ Res 2004;94:1083-1090. doi: 10.1161/01.RES.0000125629.72053.95.
9. Goldhaber JI, Xie LH, Duong T, Motter C, Khuu K, Weiss JN., Action potential duration restitution and alternans in rabbit ventricular myocytes: the key role of intracellular calcium cycling. Circ Res 2005;96:459-466. doi: 10.1161/01.RES.0000156891.66893.83.
10. Cutler MJ, Rosenbaum DS., Risk stratification for sudden cardiac death: is there a clinical role for T wave alternans? Heart Rhythm 2009;6 S56:S61. doi: 10.1016/j.hrthm.2009.05.025.
11. Diáz ME, O'Neill SC, Eisner DA., Sarcoplasmic reticulum calcium content fluctuation is the key to cardiac alternans. Circ Res 2004-94 650 656. doi: 10.1161/01.RES.0000119923.64774.72.
12. Picht E, DeSantiago J, Blatter LA, Bers DM., Cardiac alternans do not rely on diastolic sarcoplasmic reticulum calcium content fluctuations. Circ Res 2006;99:740-748. doi: 10.1161/01.RES.0000244002.88813.91.
13. Wang L, Myles RC, De Jesus NM, Ohlendorf AK, Bers DM, Ripplinger CM., Optical mapping of sarcoplasmic reticulum Ca2+ in the intact heart: ryanodine receptor refractoriness during alternans and fibrillation. Circ Res 2014;114:1410-1421. doi: 10.1161/CIRCRESAHA.114.302505.
14. Kanaporis G, Blatter LA., The mechanisms of calcium cycling and action potential dynamics in cardiac alternans. Circ Res 2015;116:846-856. doi: 10.1161/CIRCRESAHA.116.305404.
15. Cutler MJ, Wan X, Laurita KR, Hajjar RJ, Rosenbaum DS., Targeted SERCA2a gene expression identifies molecular mechanism and therapeutic target for arrhythmogenic cardiac alternans. Circ Arrhythm Electrophysiol 2009;2 686:694. doi: 10.1161/CIRCEP.109.863118.
16. Valdivia HH., Mechanisms of cardiac alternans in atrial cells: intracellular Ca2+ disturbances lead the way. Circ Res 2015-116 778 780. doi: 10.1161/CIRCRESAHA.115.305923.
17. Jeyaraj D, Haldar SM, Wan X, Circadian rhythms govern cardiac repolarization and arrhythmogenesis. Nature 2012;483:96-99. doi: 10.1038/nature10852.
18. Taggart P, Boyett MR, Logantha S, Lambiase PD., Anger, emotion, and arrhythmias: from brain to heart. Front Physiol 2011;2 67. doi: 10.3389/fphys.2011.00067.
19. Groenendaal W, Ortega FA, Kherlopian AR, Zygmunt AC, Krogh-Madsen T, Christini DJ., Cell-specific cardiac electrophysiology models. PLoS Comput Biol 2015:11-e1004242. doi: 10.1371/journal.pcbi.1004242.
20. Sobie EA., Parameter sensitivity analysis in electrophysiological models using multivariable regression. Biophys J 2009;96:1264-1274. doi: 10.1016/j.bpj.2008.10.056.
21. Walmsley J, Rodriguez JF, Mirams GR, Burrage K, Efimov IR, Rodriguez B., mRNA expression levels in failing human hearts predict cellular electrophysiological remodeling: a population-based simulation study. PLoS One 2013;8 e56359. doi: 10.1371/journal.pone.0056359.
22. Britton OJ, Bueno-Orovio A, Van Ammel K, Lu HR, Towart R, Gallacher DJ, Rodriguez B., Experimentally calibrated population of models predicts and explains intersubject variability in cardiac cellular electrophysiology. Proc Natl Acad Sci USA 2013:110-E2098 E2105. doi: 10.1073/pnas.1304382110.
23. Nash MP, Mourad A, Clayton RH, Sutton PM, Bradley CP, Hayward M, Paterson DJ, Taggart P., Evidence for multiple mechanisms in human ventricular fibrillation. Circulation 2006;114:536-542. doi: 10.1161/CIRCULATIONAHA.105.602870.
24. Taggart P, Orini M, Hanson B, Hayward M, Clayton R, Dobrzynski H, Yanni J, Boyett M, Lambiase PD., Developing a novel comprehensive framework for the investigation of cellular and whole heart electrophysiology in the in situ human heart: historical perspectives, current progress and future prospects. Prog Biophys Mol Biol 2014;115:252-260. doi: 10.1016/j.pbiomolbio.2014.06.004.
25. Potse M, Vinet A, Opthof T, Coronel R., Validation of a simple model for the morphology of the T wave in unipolar electrograms. Am J Physiol Heart Circ Physiol 2009;297:H792-H801. doi: 10.1152/ajpheart.00064.2009.
26. Bueno-Orovio A, Hanson BM, Gill JS, Taggart P, Rodriguez B., In vivo human left-to-right ventricular differences in rate adaptation transiently increase pro-arrhythmic risk following rate acceleration. PLoS One 2012;7 e52234. doi: 10.1371/journal.pone.0052234.
27. O'Hara T, Virág L, Varró A, Rudy Y., Simulation of the undiseased human cardiac ventricular action potential: model formulation and experimental validation. PLoS Comput Biol 2011:7 e1002061. doi: 10.1371/journal.pcbi.1002061.
28. McKay MD, Beckman RJ, Conover WJ., A Comparison of Three Methods for Selecting Values of Input Variables in the Analysis of Output from a Computer Code. Technometrics 1979-21 239 245
29. Pinz I, Zhu M, Mende U, Ingwall JS., An improved isolation procedure for adult mouse cardiomyocytes. Cell Biochem Biophys 2011;61:93-101. doi: 10.1007/s12013-011-9165-9.
30. Pitt-Francis J, Pathmanathan P, Bernabeu MO, Bordas R, Cooper J, Fletcher AG, Mirams GR, Murray P, Osborne JM, Walter A, Chapman SJ, Garny A, van Leeuwen IMM, Maini PK, Rodríguez B, Chaste: A test-driven approach to software development for biological modelling. Comput Phys Commun 2009;180:2452-2471
31. Wan X, Cutler M, Song Z, Karma A, Matsuda T, Baba A, Rosenbaum DS., New experimental evidence for mechanism of arrhythmogenic membrane potential alternans based on balance of electrogenic I(NCX)/I(Ca) currents. Heart Rhythm 2012;9 1698:1705. doi: 10.1016/j.hrthm.2012.06.031.
32. Eisner DA, Choi HS, Diáz ME, O'Neill SC, Trafford AW., Integrative analysis of calcium cycling in cardiac muscle. Circ Res 2000-87 1087 1094
33. Xie LH, Sato D, Garfinkel A, Qu Z, Weiss JN., Intracellular Ca alternans: coordinated regulation by sarcoplasmic reticulum release, uptake, and leak. Biophys J 2008;95:3100-3110. doi: 10.1529/biophysj.108.130955.
34. Cutler MJ, Wan X, Plummer BN, Liu H, Deschenes I, Laurita KR, Hajjar RJ, Rosenbaum DS., Targeted sarcoplasmic reticulum Ca2+ ATPase 2a gene delivery to restore electrical stability in the failing heart. Circulation 2012;126:2095-2104. doi: 10.1161/CIRCULATIONAHA.111.071480.
35. Rovetti R, Cui X, Garfinkel A, Weiss JN, Qu Z., Spark-induced sparks as a mechanism of intracellular calcium alternans in cardiac myocytes. Circ Res 2010;106:1582-1591. doi: 10.1161/CIRCRESAHA.109.213975.
36. Qu Z, Nivala M, Weiss JN., Calcium alternans in cardiac myocytes: order from disorder. J Mol Cell Cardiol 2013;58:100-109. doi: 10.1016/j.yjmcc.2012.10.007.
37. Escobar AL, Valdivia HH., Cardiac alternans and ventricular fibrillation: a bad case of ryanodine receptors reneging on their duty. Circ Res 2014;114:1369-1371. doi: 10.1161/CIRCRESAHA.114.303823.
38. Jost N, Nagy N, Corici C, Kohajda Z, Horváth A, Acsai K, Biliczki P, Levijoki J, Pollesello P, Koskelainen T, Otsomaa L, Tóth A, Papp JG, Varró A, Virág L., ORM-10103, a novel specific inhibitor of the Na+/Ca2+ exchanger, decreases early and delayed afterdepolarizations in the canine heart. Br J Pharmacol 2013;170:768-778. doi: 10.1111/bph.12228.