An analysis of deformation-dependent electromechanical coupling in the mouse heart

Journal of Physiology

Volumn 590, Issue 18, 2012, Pages 4553-4569

  Land, Sander ^a   Niederer, Steven A ^b   Aronsen, Jan Magnus ^c,d   Espe, Emil K S ^c,d   Zhang, Lili ^c,d   Louch, William E ^c,d   Sjaastad, Ivar ^c,d   Sejersted, Ole M ^c,d   Smith, Nicolas P ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

^d UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

TROPOMYOSIN; TROPONIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING KINETICS; BODY TEMPERATURE MONITORING; CALCIUM BINDING; CELL KINETICS; CONTROLLED STUDY; EXCITATION CONTRACTION COUPLING; FEEDBACK SYSTEM; HEART CONTRACTION; HEART HEMODYNAMICS; HEART MUSCLE CELL; HEART MUSCLE RELAXATION; HEART PACING; HEART RATE VARIABILITY; HEART VENTRICLE PRESSURE; HEART VOLUME; MOUSE; MUSCLE FIBER CONTRACTION; MUSCLE ISOMETRIC CONTRACTION; MUSCLE TWITCH; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL;

ANIMALS; HEART; HEMODYNAMICS; MICE; MODELS, CARDIOVASCULAR; MYOCARDIAL CONTRACTION;

EID: 84866412672     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.231928     Document Type: Article

References (60)

1. Andersson K, Birkeland J, Finsen A, Louch W, Sjaastad I, Wang Y, Chen J, Molkentin J, Chien K, Sejersted O & Christensen G (2009). Moderate heart dysfunction in mice with inducible cardiomyocyte-specific excision of the serca2 gene. J Mol Cell Cardiol 47, 180-187.
2. Baker LC, London B, Choi B, Koren G & Salama G (2000). Enhanced dispersion of repolarization and refractoriness in transgenic mouse hearts promotes reentrant ventricular tachycardia. Circ Res 86, 396-407.
3. Blanchard E, Seidman C, Seidman JG, LeWinter M & Maughan D (1999). Altered crossbridge kinetics in the alphaMHC403/+ mouse model of familial hypertrophic cardiomyopathy. Circ Res 84, 475-483.
4. Bluhm WF, Kranias EG, Dillmann WH & Meyer M (2000). Phospholamban: a major determinant of the cardiac force-frequency relationship. Am J Physiol Heart Circ Physiol 278, H249-H255.
5. 2+-ATPase improves cardiac contractile function in hypothyroid mice. Cardiovasc Res 43, 382-388.
6. Campbell KB, Razumova MV, Kirkpatrick RD & Slinker BK (2001). Nonlinear myofilament regulatory processes affect frequency-dependent muscle fber stifness. Biophys J 81, 2278-2296.
7. Campbell K (2011). Impact of myocyte strain on cardiac myofilament activation. Pfugers Arch 462, 3-14.
8. Campbell SG, Flaim SN, Leem CH & McCulloch AD (2008). Mechanisms of transmurally varying myocyte electromechanics in an integrated computational model. Philos Transact A Math Phys Eng Sci. 366, 3361-3380.
9. Cazorla O & Lacampagne A (2011). Regional variation in myofilament length-dependent activation. Pfugers Arch 462, 15-28.
10. Davis JP, Norman C, Kobayashi T, Solaro RJ, Swartz DR & Tikunova SB (2007). Effects of thin and thick filament proteins on calcium binding and exchange with cardiac troponin c. Biophys J 92, 3195-3206.
11. Dobesh DP, Konhilas JP & de Tombe PP (2002). Cooperative activation in cardiac muscle: impact of sarcomere length. Am J Physiol Heart Circ Physiol 282, H1055-H1062.
12. Farman G, Allen E, Schoenfelt K, Backx P & de Tombe P (2010). The role of thin filament cooperativity in cardiac length-dependent calcium activation. Biophys J 99, 2978-2986.
13. 2+ sensitivity in intact versus skinned rat ventricular muscle. Circ Res 74, 408-415.
14. 2+ binding to cardiac troponin c: effects of temperature and pH on mammalian and salmonid isoforms. Am J Physiol Regul Integr Comp Physiol 279, R1707-R1715.
15. Guccione JM, McCulloch AD & Waldman LK (1991). Passive material properties of intact ventricular myocardium determined from a cylindrical model. J Biomech Eng 113, 42-55.
16. Hanft LM, Korte FS & McDonald KS (2008). Cardiac function and modulation of sarcomeric function by length. Cardiovasc Res 77, 627-636.
17. Holzapfel GA & Ogden RW (2009). Constitutive modelling of passive myocardium: a structurally based framework for material characterization. Philos Transact A Math Phys Eng Sci 367, 3445.
18. Hunter PJ, McCulloch AD & ter Keurs H (1998). Modelling the mechanical properties of cardiac muscle. Prog Biophys Mol Biol 69, 289-331.
19. Jiang Y, Pandya K, Smithies O & Hsu E (2004). Three-dimensional diffusion tensor microscopy of fixed mouse hearts. Magn Reson Med 52, 453-460.
20. Joho S, Ishizaka S, Sievers R, Foster E, Simpson P & Grossman W (2007). Left ventricular pressure-volume relationship in conscious mice. Am J Physiol Heart Circ Physiol 292, H369-H377.
21. Kawai M, Saeki Y & Zhao Y (1993). Crossbridge scheme and the kinetic constants of elementary steps deduced from chemically skinned papillary and trabecular muscles of the ferret. Circ Res 73, 35-50.
22. Kawai M & Brandt PW (1980). Sinusoidal analysis: a high resolution method for correlating biochemical reactions with physiological processes in activated skeletal muscles of rabbit, frog and crayfsh. J Muscle Res Cell Motil 1, 279-303.
23. Keldermann RH, Nash MP, Gelderblom H, Wang VY & Panflov AV (2010). Electro-mechanical wavebreak in a model of the human left ventricle. Am J Physiol Heart Circ Physiol 299, H134-143.
24. Kerckhofs RC, Omens JH, McCulloch AD & Mulligan LJ (2010). Ventricular dilation and electrical dyssynchrony synergistically increase regional mechanical nonuniformity but not mechanical dyssynchrony: A computational model. Circ Heart Fail 3, 528-536.
25. Kreutziger K, Piroddi N, McMichael J, Tesi C, Poggesi C & Regnier M (2011). Calcium binding kinetics of troponin c strongly modulate cooperative activation and tension kinetics in cardiac muscle. J Mol Cell Cardiol 50, 165-174.
26. Land S, Niederer S & Smith N (2012). Effcient computational methods for strongly coupled cardiac electromechanics. IEEE Trans Biomed Eng 59, 1219-1228.
27. Lee EJ, Peng J, Radke M, Gotthardt M & Granzier HL (2010). Calcium sensitivity and the Frank-Starling mechanism of the heart are increased in titin N2B region-defcient mice. J Mol Cell Cardiol 49, 449-458.
28. Levy C & Landesberg A (2006). Cross-bridge dependent cooperativity determines the cardiac force-length relationship. J Mol Cell Cardiol 40, 639-647.
29. Li L, Louch W, Niederer S, Andersson K, Christensen G, Sejersted O & Smith N (2011). Calcium dynamics in the ventricular myocytes of SERCA2 knockout mice: A modeling study. Biophys J 100, 322-331.
30. 2+ sensitivity of tension at short sarcomere length. Circ Res 77, 199-205.
31. McKillop DF & Geeves MA (1993). Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament. Biophys J 65, 693-701.
32. Nickerson D, Smith N & Hunter P (2005). New developments in a strongly coupled cardiac electromechanical model. Europace 7(Suppl 2), S118-127.
33. Niederer SA, Fink M, Noble D & Smith NP (2009). A meta-analysis of cardiac electrophysiology computational models. Exp Physiol 94, 486-495.
34. Niederer SA, Hunter PJ & Smith NP (2006). A quantitative analysis of cardiac myocyte relaxation: a simulation study. Biophys J 90, 1697-1722.
35. Niederer S & Smith N (2009). The role of the Frank-Starling law in the transduction of cellular work to whole organ pump function: A computational modeling analysis. PLoS Comput Biol 5, e1000371.
36. Omens JH, Rockman HA & Covell JW (1994). Passive ventricular mechanics in tight-skin mice. Am J Physiol Heart Circ Physiol 266, H1169-H1176.
37. Palmer BM (2010). A strain-dependency of myosin off-rate must be sensitive to frequency to predict the B-process of sinusoidal analysis. Adv Exp Med Biol 682, 57-75.
38. Palmer BM, Fishbaugher DE, Schmitt JP, Wang Y, Alpert NR, Seidman CE, Seidman JG, VanBuren P & Maughan DW (2004a). Differential cross-bridge kinetics of FHC myosin mutations R403Q and R453C in heterozygous mouse myocardium. Am J Physiol Heart Circ Physiol 287, H91-H99.
39. Palmer BM, Georgakopoulos D, Janssen PM, Wang Y, Alpert NR, Belardi DF, Harris SP, Moss RL, Burgon PG, Seidman CE, Seidman JG, Maughan DW & Kass DA (2004b). Role of cardiac myosin binding protein c in sustaining left ventricular systolic stiffening. Circ Res 94, 1249-1255.
40. Palmer BM, Suzuki T, Wang Y, Barnes WD, Miller MS & Maughan DW (2007). Two-state model of acto-myosin attachment-detachment predicts C-process of sinusoidal analysis. Biophys J 93, 760-769.
41. Rice J & de Tombe P (2004). Approaches to modeling crossbridges and calcium-dependent activation in cardiac muscle. Progr Biophys Mol Biol 85, 179-195.
42. Rice J, Wang F, Bers D & de Tombe P (2008). Approximate model of cooperative activation and crossbridge cycling in cardiac muscle using ordinary differential equations. Biophys J 95, 2368-2390.
43. Segers P, Rietzschel ER, Buyzere MLD, Stergiopulos N, Westerhof N, Bortel LMV, Gillebert T & Verdonck PR (2008). Three-and four-element windkessel models: assessment of their fitting performance in a large cohort of healthy middle-aged individuals. Proc Inst Mech Eng H 222, 417-428.
44. Segers P, Georgakopoulos D, Afanasyeva M, Champion HC, Judge DP, Millar HD, Verdonck P, Kass DA, Stergiopulos N & Westerhof N (2005). Conductance catheter-based assessment of arterial input impedance, arterial function, and ventricular-vascular interaction in mice. Am J Physiol Heart Circ Physiol 288, H1157-H1164.
45. Sermesant M, Delingette H & Ayache N (2006). An electromechanical model of the heart for image analysis and simulation. IEEE Trans Med Imaging 25, 612-625.
46. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, Mujica AO, Thomas M, Harrow J, Cox T, Jackson D, Severin J, Biggs P, Fu J, Nefedov M, de Jong PJ, Stewart AF & Bradley A (2011). A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474, 337-342.
47. Solaro RJ (2007). Mechanisms of the Frank-Starling law of the heart: The beat goes on. Biophys J 93, 4095-4096.
48. Stull LB, Hiranandani N, Kelley MA, Leppo MK, Marbán E & Janssen PML (2006). Murine strain differences in contractile function are temperature- and frequency-dependent. Pflugers Arch 452, 140-145.
49. Stull LB, Leppo MK, Marbán E & Janssen PML (2002). Physiological determinants of contractile force generation and calcium handling in mouse myocardium. J Mol Cell Cardiol 34, 1367-1376.
50. 2+ on force generation by mouse cardiac muscle. J Physiol 544, 817-830.
51. Sun Y, Lou F & Irving M (2009). Calcium- and myosin-dependent changes in troponin structure during activation of heart muscle. J Physiol 587, 155-163.
52. Tamaddon HS, Vaidya D, Simon AM, Paul DL, Jalife J & Morley GE (2000). High-resolution optical mapping of the right bundle branch in connexin40 knockout mice reveals slow conduction in the specialized conduction system. Circ Res 87, 929-936.
53. Tobacman LS & Sawyer D (1990). Calcium binds cooperatively to the regulatory sites of the cardiac thin filament. J Biol Chem 265, 931-939.
54. Toorop GP, Westerhof N & Elzinga G (1987). Beat-to-beat estimation of peripheral resistance and arterial compliance during pressure transients. Am J Physiol Heart Circ Physiol 252, H1275-H1283.
55. Usyk TP, Mazhari R & McCulloch AD (2000). Effect of laminar orthotropic myofber architecture on regional stress and strain in the canine left ventricle. J Elasticity 61, 143-164.
56. Wang VY, Lam HI, Ennis DB, Cowan BR, Young AA & Nash MP (2009). Modelling passive diastolic mechanics with quantitative MRI of cardiac structure and function. Med Image Anal 13, 773-784.
57. Westerhof N & Elzinga G (1991). Normalized input impedance and arterial decay time over heart period are independent of animal size. Am J Physiol Regul Integr Comp Physiol 261, R126-133.
58. Xi J, Lamata P, Shi W, Niederer S, Land S, Rueckert D, Duckett S, Shetty A, Rinaldi C, Razavi R & Smith N (2011a). An automatic data assimilation framework for patient-specific myocardial mechanical parameter estimation Vol. 6666 LNCS.
59. Xi J, Lamata P, Lee J, Moireau P, Chapelle D & Smith N (2011b). Myocardial transversely isotropic material parameter estimation from in-silico measurements based on a reduced-order unscented kalman flter. J Mech Behav Biomed Mater 4, 1090-1102.
60. Yadid M & Landesberg A (2010). Stretch increases the force by decreasing cross-bridge weakening rate in the rat cardiac trabeculae. J Mol Cell Cardiol 49, 962-971.