Increased vulnerability of human ventricle to re-entrant excitation in hERG-linked variant 1 short QT syndrome

PLoS Computational Biology

Volumn 7, Issue 12, 2011, Pages

  Adeniran, Ismail ^a   McPate, Mark J ^b,c   Witchel, Harry J ^b,d   Hancox, Jules C ^b   Zhang, Henggui ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b School of Medical Sciences   (United Kingdom)

^c NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^d BRIGHTON AND SUSSEX MEDICAL SCHOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRIC RECTIFIERS; MARKOV PROCESSES;

3D TISSUES; DELAYED RECTIFIER; EXCITATION WAVES; HETEROGENEOUS CONDITIONS; HUMAN VENTRICLES; REPOLARIZATION; SIMULATION STUDIES; SUDDEN DEATHS; TISSUE MODELS; TRANSMURAL HETEROGENEITY;

TISSUE;

POTASSIUM CHANNEL HERG; ERG1 POTASSIUM CHANNEL;

ACTION POTENTIAL; AMINO ACID SUBSTITUTION; ARRHYTHMOGENESIS; ARTICLE; CONTROLLED STUDY; HEART REPOLARIZATION; HEART RIGHT VENTRICLE OUTFLOW TRACT; HEART VENTRICLE; HODGKIN HUXLEY EQUATION; HUMAN; ION CURRENT; MEMBRANE POTENTIAL; PROBABILITY; QRS COMPLEX; QT INTERVAL; SHORT QT SYNDROME; STEADY STATE; T WAVE AMPLITUDE; BIOLOGICAL MODEL; ELECTROCARDIOGRAPHY; GENETICS; HEART; HEART VENTRICLE FUNCTION; METABOLISM; MUTATION; PHYSIOLOGY;

ACTION POTENTIALS; ELECTROCARDIOGRAPHY; ETHER-A-GO-GO POTASSIUM CHANNELS; HEART; HEART VENTRICLES; HUMANS; MARKOV CHAINS; MODELS, CARDIOVASCULAR; MUTATION; VENTRICULAR FUNCTION;

EID: 84855272382     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002313     Document Type: Article

References (58)

1. Maury P, Extramiana F, Sbragia P, Giustetto C, Schimpf R, et al. (2008) Short QT syndrome. Update on a recent entity. Arch Cardiovasc Dis 101: 779-786.
2. Modell SM, Lehmann MH, (2006) The long QT syndrome family of cardiac ion channelopathies: A HuGE review. Genet Med 8: 143-155.
3. Gussak I, Brugada P, Brugada J, Wright RS, Kopecky SL, et al. (2000) Idiopathic short QT interval: A new clinical syndrome? Cardiology 94: 99-102.
4. Patel C, Antzelevitch C, (2008) Cellular basis for arrhythmogenesis in an experimental model of the SQT1 form of the short QT syndrome. Heart Rhythm 5: 585-590.
5. Schimpf R, Wolpert C, Gaita F, Giustetto C, Borggrefe M, (2005) Short QT syndrome. Cardiovasc Res 67: 357-366.
6. Bellocq C, van Ginneken ACG, Bezzina CR, Alders M, Escande D, et al. (2004) Mutation in the KCNQ1 gene leading to the short QT-interval syndrome. Circulation 109: 2394-2397.
7. Brugada R, Hong K, Dumaine R, Cordeiro J, Gaita F, et al. (2004) Sudden death associated with short-QT syndrome linked to mutations in HERG. Circulation 109: 30-35.
8. Hong K, Bjerregaard P, Gussak I, Brugada R, (2005) Short QT syndrome and atrial fibrillation caused by mutation in KCNH2. J Cardiovasc Electrophysiol 16: 394-396.
9. Hong K, Piper DR, Diaz-Valdecantos A, Brugada J, Oliva A, et al. (2005) De novo KCNQ1 mutation responsible for atrial fibrillation and short QT syndrome in utero. Cardiovasc Res 68: 433-440.
10. Priori SG, Pandit SV, Rivolta I, Berenfeld O, Ronchetti E, et al. (2005) A novel form of short QT syndrome (SQT3) is caused by a mutation in the KCNJ2 gene. Circ Res 96: 800-807.
11. Cordeiro JM, Brugada R, Wu YS, Hong K, Dumaine R, (2005) Modulation of I-Kr inactivation by mutation N588K in KCNH2: A link to arrhythmogenesis in short QT syndrome. Cardiovasc Res 67: 498-509.
12. McPate MJ, Duncan RS, Milnes JT, Witchel HJ, Hancox JC, (2005) The N588K-HERG K+ channel mutation in the 'short QT syndrome': Mechanism of gain-in-function determined at 37 degrees C. Biochem Biophys Res Commun 334: 441-449.
13. McPate MJ, Zhang H, Adeniran I, Cordeiro JM, Witchel HJ, et al. (2009) Comparative Effects of the short QT N588K mutation at 37 degrees C on hERG K(+) channel during ventricular, purkinje firbre and atrial action potentials: an action potential clamp study. J Physiol Pharmacol 60: 23-41.
14. Mitcheson JS, Sanguinetti MC, (1999) Biophysical properties and molecular basis of cardiac rapid and slow delayed rectifier potassium channels. Cell Physiol Biochem 9: 201-216.
15. Antzelevitch C, Sicouri S, (1994) Clinical relevance of cardiac arrhythmias generated by afterdepolarizations- Role of M cells in generation of U waves, triggered activity and torsade de pointes. J Am Coll Cardiol 23: 259-277.
16. Extramiana F, Antzelevitch C, (2004) Amplified transmural dispersion of repolarization as the basis for arrhythmogenesis in a canine ventricular-wedge model of short-QT syndrome. Circulation 110: 3661-3666.
17. Itoh H, Horie M, Ito M, Imoto K, (2006) Arrhythmogenesis in the short-QT syndrome associated with combined HERG channel gating defects- A simulation study. Circ J 70: 502-508.
18. Weiss DL, Seemann G, Sachse FB, Dossel O, (2005) Modelling of short QT syndrome in a heterogeneous model of the human ventricular wall. Europace 7: S105-S117.
19. Zhang H, Kharche S, Holden AV, Hancox JC, (2008) Repolarisation and vulnerability to re-entry in the human heart with short QT syndrome arising from KCNQ1 mutation- A simulation study. Prog Biophys Mol Biol 96: 112-131.
20. Zhang HG, Hancox JC, (2004) In silico study of action potential and QT interval shortening due to loss of inactivation of the cardiac rapid delayed rectifier potassium current. Biochem Biophys Res Commun 322: 693-699.
21. Lu Y, Mahaut-Smith MP, Varghese A, Huang CLH, Kemp PR, et al. (2001) Effects of premature stimulation on HERG K+ channels. J Physiol 537: 843-851.
22. Grandi E, Pasqualini FS, Bers DM, (2010) A novel computational model of the human ventricular action potential and Ca transient. J Mol Cell Cardiol 48: 112-121.
23. O'Hara T, Virag L, Varro A, Rudy Y, (2011) Simulation of the Undiseased Human Cardiac Ventricular Action Potential: Model Formulation and Experimental Validation. PloS Comput Biol 7: e1002061.
24. Szabo G, Szentandrassy N, Biro T, Toth BI, Czifra G, et al. (2005) Asymmetrical distribution of ion channels in canine and human left-ventricular wall: epicardium versus midmyocardium. Pflugers Arch 450: 307-316.
25. Giustetto C, Di Monte F, Wolpert C, Borggrefe M, Schimpf R, et al. (2006) Short QT syndrome: clinical findings and diagnostic-therapeutic implications. Eur Heart J 27: 2440-2447.
26. Gollob MH, Redpath CJ, Roberts JD, (2011) The Short QT Syndrome Proposed Diagnostic Criteria. J Am Coll Cardiol 57: 802-812.
27. Watanabe H, Makiyama T, Koyama T, Kannankeril PJ, Seto S, et al. (2010) High prevalence of early repolarization in short QT syndrome. Heart Rhythm 7: 647-652.
28. Gima K, Rudy Y, (2002) Ionic current basis of electrocardiographic waveforms- A model study. Circ Res 90: 889-896.
29. Keller DUJ, Kalayciyan R, Dossel O, Seemann G, (2009) Fast creation of endocardial stimulation profiles for the realistic simulation of body surface ECGs. IFMBE World Congr Med Phys Biomed Eng 25: 145-148.
30. Kogan BY, Karplus WJ, Billett BS, Pang AT, Khan SS, et al. (1991) The role of diastolic outward current deactivation kinetics on the induction of spiral waves. Pacing Clin Electrophysiol 14: 1688-1693.
31. ten Tusscher K, Noble D, Noble PJ, Panfilov AV, (2004) A model for human ventricular tissue. Am J Physiol Heart Circ Physiol 286: H1573-H1589.
32. ten Tusscher K, Panfilov AV, (2006) Alternans and spiral breakup in a human ventricular tissue model. Am J Physiol Heart Circ Physiol 291: H1088-H1100.
33. Li GR, Feng J, Yue L, Carrier M, (1998) Transmural heterogeneity of action potentials and Ito1 in myocytes isolated from the human right ventricle. Am J Physiol 275: H369-377.
34. Taggart P, Sutton PMI, Opthof T, Coronel R, Trimlett R, et al. (2000) Inhomogeneous transmural conduction during early ischaemia in patients with coronary artery disease. J Mol Cell Cardiol 32: 621-630.
35. Seemann G, Keller DUJ, Weiss DL, Dossel O, (2006) Modeling human ventricular geometry and fiber orientation based on diffusion tensor MRI. Proc Comput Cardiol 33: 801-804.
36. Kiehn J, Lacerda AE, Brown AM, (1999) Pathways of HERG inactivation. Am J Physiol Heart Circ Physiol 277: H199-H210.
37. Clancy CE, Rudy Y, (2001) Cellular consequences of HERG mutations in the long QT syndrome: precursors to sudden cardiac death. Cardiovasc Res 50: 301-313.
38. Wang SM, Liu SG, Morales MJ, Strauss HC, Rasmusson RL, (1997) A quantitative analysis of the activation and inactivation kinetics of HERG expressed in Xenopus oocytes. J Physiol 502: 45-60.
39. McPate MJ, Duncan RS, Hancox JC, Witchel HJ, (2008) Pharmacology of the short QT syndrome N588K-hERG K(+) channel mutation: differential impact on selected class I and class III antiarrhythmic drugs. Br J Pharmacol 155: 957-966.
40. Rudy Y, Silva JR, (2006) Computational biology in the study of cardiac ion channels and cell electrophysiology. Q Rev Biophys 39: 57-116.
41. Broyden CG, (1970) The convergence of a class of double-rank minimization algorithms 1. General considerations. IMA J Appl Math 6: 76-90.
42. Xia L, Zhang Y, Zhang HG, Wei Q, Liu F, et al. (2006) Simulation of Brugada syndrome using cellular and three-dimensional whole-heart modeling approaches. Physiol Meas 27: 1125-1142.
43. Rush S, Larsen H, (1978) A practical algorithm for solving dynamic membrane equations. IEEE Trans Biomed Eng 25: 389-392.
44. Workman AJ, Kane AK, Rankin AC, (2001) The contribution of ionic currents to changes in refractoriness of human atrial myocytes associated with chronic atrial fibrillation. Cardiovasc Res 52: 226-235.
45. Rudy Y, Luo CH, (1993) Cellular responses to elctrical stimulation: a study using a model of the ventricular cardiac action potential. Adv Exp Med Biol 346: 79-90.
46. Zeng JL, Laurita KR, Rosenbaum DS, Rudy Y, (1995) Two components of the delayed rectifier K(+) current in ventricular myocytes of the guinea pig type. Theoretical formulation and their role in repolarization. Circ Res 77: 140-152.
47. Bett GCL, Zhou QL, Rasmusson RL, (2011) Models of HERG Gating. Biophys J 101: 631-642.
48. Clements JC, Nenonen J, Li PKJ, Horacek BM, (2004) Activation dynamics in anisotropic cardiac tissue via decoupling. Ann Biomed Eng 32: 984-990.
49. Colli-Franzone P, Pavarino LF, Taccardi B, (2005) Simulating patterns of excitation, repolarization and action potential duration with cardiac Bidomain and Monodomain models. Math Biosci 197: 35-66.
50. Drouin E, Charpentier F, Gauthier C, Laurent K, Lemarec H, (1995) Electrophysiologic characteristics of cells spanning the left-ventricular wall of human heart- evidence for presence of M cells. J Am Coll Cardiol 26: 185-192.
51. Feigenbaum H, (1994) Echocardiography Philadelphia Lee and Febiger.
52. Yan GX, Shimizu W, Antzelevitch C, (1998) Characteristics and distribution of M cells in arterially perfused canine left ventricular wedge preparations. Circulation 98: 1921-1927.
53. Sundnes J, Lines GT, Tveito A, (2005) An operator splitting method for solving the bidomain equations coupled to a volume conductor model for the torso. Math Biosci 194: 233-248.
54. Bangerth W, Hartmann R, Kanschat G, (2007) deal. II- A general-purpose object-oriented finite element library. ACM Trans Math Softw 33.
55. Burnett DS, (1988) Finite Element Analysis: From Concepts to Applications Reading, Masachusetts Addison-Wesley.
56. Hackbusch W, (1994) Iterative Solution of Large Sparse Systems of Equations Springer-Verlag.
57. Hoberock J, Bell N, (2010) Thrust: A Parallel Template Library. Version 1.3.0. Available: http://www.meganewtons.com/. Accessed 10 November 2011.
58. Durrer D, Vandam RT, Freud GE, Janse MJ, Meijler FL, et al. (1970) Total excitation of the isolated human heart. Circulation 41: 899-912.