Modelling the cardiac transverse-axial tubular system.

The transverse-axial tubular system (TATS) of cardiac ventricular myocytes is a complex network of tubules that arises as invaginations of the surface membrane; it appears to form a specialised region of cell membrane that is particularly important for excitation-contraction coupling. However, much remains unknown about the structure and role of the TATS. In this brief review we use experimental data and computer modelling to address the following key questions: (i) What fraction of the cell membrane is within the TATS? (ii) Is the composition of the TATS membrane the same as the surface membrane? (iii) How good is electrical coupling between the surface and TATS membranes? (iv) What fraction of each current is within the TATS? (v) How important is the complex structure of the TATS network? (vi) What is the effect of current inhomogeneity on lumenal ion concentrations? (vii) Does the TATS contribute to the functional changes observed in heart failure? Although there are many areas in which experimental evidence is lacking, computer models provide a method to assess and predict the possible function of the TATS; such models suggest that although the surface and TATS membranes are electrically well coupled, concentration of ion flux pathways within the TATS, coupled to restricted diffusion, may result in the ionic composition in the TATS lumen being different from that in the bulk extracellular space, and varying with activity and in pathological conditions.

[1]  Denis Noble,et al.  The IUPS human physiome project , 2002, Pflügers Archiv.

[2]  W. Schilling,et al.  TRPC3 channels colocalize with Na+/Ca2+ exchanger and Na+ pump in axial component of transverse-axial tubular system of rat ventricle. , 2007, American journal of physiology. Heart and circulatory physiology.

[3]  C. Orchard,et al.  Differential Modulation of L-type Ca2+ Current by SR Ca2+ Release at the T-Tubules and Surface Membrane of Rat Ventricular Myocytes , 2004, Circulation research.

[4]  S. Harrison,et al.  Cellular distribution of calcium current is unaltered during compensated hypertrophy in the spontaneously hypertensive rat , 2006, Pflügers Archiv - European Journal of Physiology.

[5]  C. Orchard,et al.  T‐Tubule Function in Mammalian Cardiac Myocytes , 2003, Circulation research.

[6]  C. Soeller,et al.  Effect of changes in action potential spike configuration, junctional sarcoplasmic reticulum micro-architecture and altered t-tubule structure in human heart failure , 2006, Journal of Muscle Research & Cell Motility.

[7]  C. Souchier,et al.  Transverse‐axial tubular system in guinea pig ventricular cardiomyocyte: 3D reconstruction, quantification and its possible role in K+ accumulation‐depletion phenomenon in single cells , 1995 .

[8]  K. Sipido,et al.  Something old, something new: changing views on the cellular mechanisms of heart failure. , 2005, Cardiovascular research.

[9]  E. White,et al.  Caveolae modulate excitation-contraction coupling and beta2-adrenergic signalling in adult rat ventricular myocytes. , 2006, Cardiovascular research.

[10]  D. Bers.  Early transient depletion of extracellular Ca during individual cardiac muscle contractions. , 1983, The American journal of physiology.

[11]  W. Lederer,et al.  Heart Failure After Myocardial Infarction: Altered Excitation-Contraction Coupling , 2001, Circulation.

[12]  G. Christé.  Localization of K(+) channels in the tubules of cardiomyocytes as suggested by the parallel decay of membrane capacitance, IK(1) and IK(ATP) during culture and by delayed IK(1) response to barium. , 1999, Journal of molecular and cellular cardiology.

[13]  E. Niggli,et al.  Confocal near-membrane detection of calcium in cardiac myocytes. , 1998, Cell calcium.

[14]  C. Orchard,et al.  Density and sub-cellular distribution of cardiac and neuronal sodium channel isoforms in rat ventricular myocytes. , 2006, Biochemical and biophysical research communications.

[15]  K. Kamiya,et al.  Contribution of potassium accumulation in narrow extracellular spaces to the genesis of nicorandil-induced large inward tail current in guinea-pig ventricular cells , 2004, Pflügers Archiv.

[16]  D. Uttenweiler,et al.  Numerical analysis of Ca2+ depletion in the transverse tubular system of mammalian muscle. , 2001, Biophysical journal.

[17]  Yuri E. Korchev,et al.  Functional localization of single active ion channels on the surface of a living cell , 2000, Nature Cell Biology.

[18]  Kai Simons,et al.  Cholesterol, lipid rafts, and disease. , 2002, The Journal of clinical investigation.

[19]  M. Pásek,et al.  Quantification of t-tubule area and protein distribution in rat cardiac ventricular myocytes. , 2008, Progress in biophysics and molecular biology.

[20]  Michal Pásek,et al.  The functional role of cardiac T-tubules explored in a model of rat ventricular myocytes , 2006, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[21]  F. Brette,et al.  beta-adrenergic stimulation restores the Ca transient of ventricular myocytes lacking t-tubules. , 2004, Journal of molecular and cellular cardiology.

[22]  C. Orchard,et al.  Quantification of calcium entry at the T-tubules and surface membrane in rat ventricular myocytes. , 2006, Biophysical journal.

[23]  D. Demandolx,et al.  Multicolour analysis and local image correlation in confocal microscopy , 1997 .

[24]  R. Winslow,et al.  Electrophysiological modeling of cardiac ventricular function: from cell to organ. , 2000, Annual review of biomedical engineering.

[25]  I. Sjaastad,et al.  Slow diffusion of K+ in the T tubules of rat cardiomyocytes. , 2006, Journal of applied physiology.

[26]  M. Pásek,et al.  A quantitative model of the cardiac ventricular cell incorporating the transverse-axial tubular system. , 2003, General physiology and biophysics.

[27]  James B. Bassingthwaighte,et al.  Strategies for the Physiome Project , 2000, Annals of Biomedical Engineering.

[28]  N. Shepherd,et al.  Ionic diffusion in transverse tubules of cardiac ventricular myocytes. , 1998, American journal of physiology. Heart and circulatory physiology.

[29]  C. Hidalgo,et al.  Immunological and biochemical properties of transverse tubule membranes isolated from rabbit skeletal muscle. , 1981, The Journal of biological chemistry.

[30]  Jose L Puglisi,et al.  Modeling the isolated cardiac myocyte. , 2004, Progress in biophysics and molecular biology.

[31]  V Avdonin,et al.  A beta2 adrenergic receptor signaling complex assembled with the Ca2+ channel Cav1.2. , 2001, Science.

[32]  J. Foell,et al.  Reduction in density of transverse tubules and L-type Ca(2+) channels in canine tachycardia-induced heart failure. , 2001, Cardiovascular research.

[33]  Peter Hunter,et al.  A strategy for integrative computational physiology. , 2005, Physiology.

[34]  Y Rudy,et al.  Electrophysiologic effects of acute myocardial ischemia. A mechanistic investigation of action potential conduction and conduction failure. , 1997, Circulation research.

[35]  Godfrey L. Smith,et al.  Myocardial Infarction Causes Increased Expression But Decreased Activity of the Myocardial Na+—Ca2+ Exchanger in the Rabbit , 2003, The Journal of physiology.

[36]  W. Wallinga,et al.  Modelling action potentials and membrane currents of mammalian skeletal muscle fibres in coherence with potassium concentration changes in the T-tubular system , 1999, European Biophysics Journal.

[37]  P. Hunter,et al.  Computational physiology and the physiome project , 2004, Experimental physiology.

[38]  Ole Petter Ottersen,et al.  Localization and function of the Na+/Ca2+-exchanger in normal and detubulated rat cardiomyocytes. , 2003, Journal of molecular and cellular cardiology.

[39]  Y. Tourneur,et al.  SR47063, A potent channel opener, activates KATP and a time-dependent current likely due to potassium accumulation , 1994, The Journal of Membrane Biology.

[40]  R. Haworth,et al.  Depletion of T-tubules and specific subcellular changes in sarcolemmal proteins in tachycardia-induced heart failure. , 2003, Cardiovascular research.

[41]  A. Marks,et al.  Molecular determinants of altered contractility in heart failure , 2004, Annals of medicine.

[42]  W. Lederer,et al.  ATP-sensitive potassium channel modulation of the guinea pig ventricular action potential and contraction. , 1991, Circulation research.

[43]  A. Klimek,et al.  The Molecular Architecture of Calcium Microdomains in Rat Cardiomyocytes , 2002, Annals of the New York Academy of Sciences.

[44]  J. Daut.  The passive electrical properties of guinea‐pig ventricular muscle as examined with a voltage‐clamp technique. , 1982, The Journal of physiology.

[45]  Willem Flameng,et al.  Reduced synchrony of Ca2+ release with loss of T-tubules-a comparison to Ca2+ release in human failing cardiomyocytes. , 2004, Cardiovascular research.

[46]  James B Bassingthwaighte,et al.  The Computational Integrated Myocyte: A View into the Virtual Heart , 2004, Annals of the New York Academy of Sciences.

[47]  F. Protasi,et al.  Shape, size, and distribution of Ca(2+) release units and couplons in skeletal and cardiac muscles. , 1999, Biophysical journal.

[48]  C. Soeller,et al.  Examination of the transverse tubular system in living cardiac rat myocytes by 2-photon microscopy and digital image-processing techniques. , 1999, Circulation research.

[49]  W. Giles,et al.  T‐tubule localization of the inward‐rectifier K+ channel in mouse ventricular myocytes: a role in K+ accumulation , 2001, The Journal of physiology.

[50]  A. Marks.  A guide for the perplexed: towards an understanding of the molecular basis of heart failure. , 2003, Circulation.

[51]  M. Dunn,et al.  Genomics, proteomics and bioinformatics of human heart failure , 2004, Journal of Muscle Research & Cell Motility.

[52]  E Page,et al.  Quantitative ultrastructural analysis in cardiac membrane physiology. , 1978, The American journal of physiology.

[53]  N V Thakor,et al.  Simulation of action potentials from metabolically impaired cardiac myocytes. Role of ATP-sensitive K+ current. , 1996, Circulation research.

[54]  C. Mcpherson,et al.  ATP-regulated K+ channels protect the myocardium against ischemia/reperfusion damage. , 1991 .

[55]  R. Coronado,et al.  Membrane cholesterol modulates dihydropyridine receptor function in mice fetal skeletal muscle cells , 2004, The Journal of physiology.

[56]  C. Biskup,et al.  Anoxia generates rapid and massive opening of KATP channels in ventricular cardiac myocytes. , 1999, Cardiovascular research.

[57]  R. Tunin,et al.  Transcriptomic profiling of the canine tachycardia-induced heart failure model: global comparison to human and murine heart failure. , 2006, Journal of molecular and cellular cardiology.

[58]  D M Bers,et al.  Na/Ca exchange and Na/K-ATPase function are equally concentrated in transverse tubules of rat ventricular myocytes. , 2003, Biophysical journal.

[59]  Daniel A. Beard,et al.  Computational Framework for Generating Transport Models from Databases of Microvascular Anatomy , 2001, Annals of Biomedical Engineering.

[60]  Eric A Sobie,et al.  Calcium Biology of the Transverse Tubules in Heart , 2005, Annals of the New York Academy of Sciences.

[61]  Eric A Sobie,et al.  Orphaned ryanodine receptors in the failing heart. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[62]  W. Freygang,et al.  The After-Potential that Follows Trains of Impulses in Frog Muscle Fibers , 1964, The Journal of general physiology.

[63]  A. Yao,et al.  The restriction of diffusion of cations at the external surface of cardiac myocytes varies between species. , 1997, Cell calcium.

[64]  R. Hullin,et al.  Increased availability and open probability of single L-type calcium channels from failing compared with nonfailing human ventricle. , 1998, Circulation.

[65]  J. Weiss,et al.  Metabolic regulation of cardiac ATP-sensitive K+ channels , 1993, Cardiovascular Drugs and Therapy.

[66]  Michal Pásek,et al.  A model of the guinea-pig ventricular cardiac myocyte incorporating a transverse-axial tubular system. , 2008, Progress in biophysics and molecular biology.

[67]  M. Cannell,et al.  Ca2+ influx during the cardiac action potential in guinea pig ventricular myocytes. , 1996, Circulation research.

[68]  D. Attwell,et al.  Membrane potential and ion concentration stability conditions for a cell with a restricted extracellular space , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[69]  Daniel A Beard,et al.  Computational modeling of physiological systems. , 2005, Physiological genomics.

[70]  P. L. Becker,et al.  Gs and adenylyl cyclase in transverse tubules of heart: implications for cAMP-dependent signaling. , 1999, American journal of physiology. Heart and circulatory physiology.

[71]  M. Pásek,et al.  Modelling the distribution of [Ca2+] within the cardiact-tubule: effects of Ca2+ current distribution and changes inextracellular [Ca2+] , 2004 .

[72]  G. Sumnicht,et al.  Lipid composition of transverse tubular membranes from normal and dystrophic skeletal muscle. , 1982, Archives of biochemistry and biophysics.

[73]  D. Bers,et al.  Surface:volume relationship in cardiac myocytes studied with confocal microscopy and membrane capacitance measurements: species-dependence and developmental effects. , 1996, Biophysical journal.

[74]  T. Shimada,et al.  The internal and external protein scaffold of the T-tubular system in cardiomyocytes , 1998, Cell and Tissue Research.

[75]  O. Rougier,et al.  Excitation-contraction coupling in skeletal muscle. , 1985, Progress in biophysics and molecular biology.

[76]  C. Orchard,et al.  No Apparent Requirement for Neuronal Sodium Channels in Excitation-Contraction Coupling in Rat Ventricular Myocytes , 2006, Circulation research.