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Computational and Mathematical Methods in Medicine
Volume 2013, Article ID 238676, 9 pages
http://dx.doi.org/10.1155/2013/238676
Research Article

Excitation-Contraction Coupling between Human Atrial Myocytes with Fibroblasts and Stretch Activated Channel Current: A Simulation Study

Department of Biomedical Engineering, Zhejiang University, Hangzhou 310027, China

Received 2 May 2013; Revised 13 July 2013; Accepted 13 July 2013

Academic Editor: Zhonghua Sun

Copyright © 2013 Heqing Zhan and Ling Xia. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. A. MacCannell, H. Bazzazi, L. Chilton, Y. Shibukawa, R. B. Clark, and W. R. Giles, “A mathematical model of electrotonic interactions between ventricular myocytes and fibroblasts,” Biophysical Journal, vol. 92, no. 11, pp. 4121–4132, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. F. B. Sachse, A. P. Moreno, G. Seemann, and J. A. Abildskov, “A model of electrical conduction in cardiac tissue including fibroblasts,” Annals of Biomedical Engineering, vol. 37, no. 5, pp. 874–889, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Kohl and U. Ravens, “Cardiac mechano-electric feedback: past, present, and prospect,” Progress in Biophysics and Molecular Biology, vol. 82, no. 1–3, pp. 3–9, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. N. A. Trayanova and J. J. Rice, “Cardiac electromechanical models: from cell to organ,” Frontiers in Physiology, vol. 2, p. 43, 2011. View at Google Scholar
  5. N. A. Trayanova, “Whole-heart modeling: applications to cardiac electrophysiology and electromechanics,” Circulation Research, vol. 108, no. 1, pp. 113–128, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. N. A. Trayanova, J. Constantino, and V. Gurev, “Electromechanical models of the ventricles,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 301, no. 2, pp. H279–H286, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. R. H. Clayton, O. Bernus, E. M. Cherry et al., “Models of cardiac tissue electrophysiology: progress, challenges and open questions,” Progress in Biophysics and Molecular Biology, vol. 104, no. 1–3, pp. 22–48, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Carusi, K. Burrage, and B. Rodriguez, “Bridging experiments, models and simulations: an integrative approach to validation in computational cardiac electrophysiology,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 303, no. 2, pp. H144–H155, 2012. View at Google Scholar
  9. E. M. Cherry and F. H. Fenton, “Effects of boundaries and geometry on the spatial distribution of action potential duration in cardiac tissue,” Journal of Theoretical Biology, vol. 285, no. 1, pp. 164–176, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. N. H. Kuijpers, E. Hermeling, P. H. Bovendeerd, T. Delhaas, and F. W. Prinzen, “Modeling cardiac electromechanics and mechanoelectrical coupling in dyssynchronous and failing hearts: insight from adaptive computer models,” Journal of Cardiovascular Translational Research, vol. 5, no. 2, pp. 159–169, 2012. View at Google Scholar
  11. S. A. Niederer and N. P. Smith, “The role of the Frank-Starling law in the transduction of cellular work to whole organ pump function: a computational modeling analysis,” PLoS Computational Biology, vol. 5, no. 4, Article ID e1000371, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. S. A. Niederer and N. P. Smith, “An improved numerical method for strong coupling of excitation and contraction models in the heart,” Progress in Biophysics and Molecular Biology, vol. 96, no. 1–3, pp. 90–111, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Xia, M. Huo, Q. Wei, F. Liu, and S. Crozier, “Analysis of cardiac ventricular wall motion based on a three-dimensional electromechanical biventricular model,” Physics in Medicine and Biology, vol. 50, no. 8, pp. 1901–1917, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. R. C. P. Kerckhoffs, J. H. Omens, A. D. McCulloch, and L. J. Mulligan, “Ventricular dilation and electrical dyssynchrony synergistically increase regional mechanical nonuniformity but not mechanical dyssynchrony: a computational model,” Circulation, vol. 3, no. 4, pp. 528–536, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. X.-C. Yang and F. Sachs, “Characterization of stretch-activated ion channels in Xenopus oocytes,” Journal of Physiology, vol. 431, pp. 103–122, 1990. View at Google Scholar · View at Scopus
  16. K. Naruse and M. Sokabe, “Involvement of stretch-activated ion channels in Ca2+ mobilization to mechanical stretch in endothelial cells,” American Journal of Physiology. Cell Physiology, vol. 264, no. 4, pp. C1037–C1044, 1993. View at Google Scholar · View at Scopus
  17. W. Craelius, V. Chen, and N. El-Sherif, “Stretch activated ion channels in ventricular myocytes,” Bioscience Reports, vol. 8, no. 5, pp. 407–414, 1988. View at Google Scholar · View at Scopus
  18. J. O. Bustamante, A. Ruknudin, and F. Sachs, “Stretch-activated channels in heart cells: relevance to cardiac hypertrophy,” Journal of Cardiovascular Pharmacology, vol. 17, supplement 2, pp. S110–S113, 1991. View at Google Scholar · View at Scopus
  19. I. Manabe, T. Shindo, and R. Nagai, “Gene expression in fibroblasts and fibrosis involvement in cardiac hypertrophy,” Circulation Research, vol. 91, no. 12, pp. 1103–1113, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. V. S. Petrov, G. V. Osipov, and J. Kurths, “Fibroblasts alter spiral wave stability,” Chaos, vol. 20, no. 4, Article ID 045103, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. J. M. T. De Bakker and H. M. V. Van Rijen, “Continuous and discontinuous propagation in heart muscle,” Journal of Cardiovascular Electrophysiology, vol. 17, no. 5, pp. 567–573, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. M. S. Spach, J. F. Heidlage, P. C. Dolber, and R. C. Barr, “Mechanism of origin of conduction disturbances in aging human atrial bundles: experimental and model study,” Heart Rhythm, vol. 4, no. 2, pp. 175–185, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Xie, A. Garfinkel, P. Camelliti, P. Kohl, J. N. Weiss, and Z. Qu, “Effects of fibroblast-myocyte coupling on cardiac conduction and vulnerability to reentry: a computational study,” Heart Rhythm, vol. 6, no. 11, pp. 1641–1649, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. M. A. Rossi, “Connective tissue skeleton in the normal left ventricle and in hypertensive left ventricular hypertrophy and chronic chagasic myocarditis,” Medical Science Monitor, vol. 7, no. 4, pp. 820–832, 2001. View at Google Scholar · View at Scopus
  25. M. Miragoli, G. Gaudesius, and S. Rohr, “Electrotonic modulation of cardiac impulse conduction by myofibroblasts,” Circulation Research, vol. 98, no. 6, pp. 801–810, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Zlochiver, V. Muñoz, K. L. Vikstrom, S. M. Taffet, O. Berenfeld, and J. Jalife, “Electrotonic myofibroblast-to-myocyte coupling increases propensity to reentrant arrhythmias in two-dimensional cardiac monolayers,” Biophysical Journal, vol. 95, no. 9, pp. 4469–4480, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. V. Jacquemet and C. S. Henriquez, “Loading effect of fibroblast-myocyte coupling on resting potential, impulse propagation, and repolarization: insights from a microstructure model,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 294, no. 5, pp. H2040–H2052, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Xie, A. Garfinkel, J. N. Weiss, and Z. Qu, “Cardiac alternans induced by fibroblast-myocyte coupling: mechanistic insights from computational models,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 297, no. 2, pp. H775–H784, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. F. B. Sachse, A. P. Moreno, and J. A. Abildskov, “Electrophysiological modeling of fibroblasts and their interaction with myocytes,” Annals of Biomedical Engineering, vol. 36, no. 1, pp. 41–56, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Courtemanche, R. J. Ramirez, and S. Nattel, “Ionic mechanisms underlying human atrial action potential properties: insights from a mathematical model,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 275, no. 1, part 2, pp. H301–H321, 1998. View at Google Scholar · View at Scopus
  31. N. H. Kuijpers, P. A. J. Hilbers, H. M. M. ten Eikelder, and M. G. J. Arts, Cardiac electrophysiology and mechanoelectric feedback: modeling and simulation [Ph.D. thesis], Technische Universiteit Eindhoven, Eindhoven, The Netherlands, 2008.
  32. J. J. Rice, F. Wang, D. M. Bers, and P. P. De Tombe, “Approximate model of cooperative activation and crossbridge cycling in cardiac muscle using ordinary differential equations,” Biophysical Journal, vol. 95, no. 5, pp. 2368–2390, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. M. M. Maleckar, J. L. Greenstein, W. R. Giles, and N. A. Trayanova, “Electrotonic coupling between human atrial myocytes and fibroblasts alters myocyte excitability and repolarization,” Biophysical Journal, vol. 97, no. 8, pp. 2179–2190, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. M. P. Nash and A. V. Panfilov, “Electromechanical model of excitable tissue to study reentrant cardiac arrhythmias,” Progress in Biophysics and Molecular Biology, vol. 85, no. 2-3, pp. 501–522, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. R. A. Brown, R. Prajapati, D. A. McGrouther, I. V. Yannas, and M. Eastwood, “Tensional homeostasis in dermal fibroblasts: mechanical responses to mechanical loading in three-dimensional substrates,” Journal of Cellular Physiology, vol. 175, no. 3, pp. 323–332, 1998. View at Google Scholar
  36. L. Chilton, S. Ohya, D. Freed et al., “K+ currents regulate the resting membrane potential, proliferation, and contractile responses in ventricular fibroblasts and myofibroblasts,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 288, no. 6, pp. H2931–H2939, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. Y. Shibukawa, E. L. Chilton, K. A. MacCannell, R. B. Clark, and W. R. Giles, “K+ currents activated by depolarization in cardiac fibroblasts,” Biophysical Journal, vol. 88, no. 6, pp. 3924–3935, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Biernacka and N. G. Frangogiannis, “Aging and cardiac fibrosis,” Aging and Disease, vol. 2, no. 2, pp. 158–173, 2011. View at Google Scholar
  39. C. H. Conrad, W. W. Brooks, J. A. Hayes, S. Sen, K. G. Robinson, and O. H. L. Bing, “Myocardial fibrosis and stiffness with hypertrophy and heart failure in the spontaneously hypertensive rat,” Circulation, vol. 91, no. 1, pp. 161–170, 1995. View at Google Scholar · View at Scopus
  40. M. F. Berry, A. J. Engler, Y. J. Woo et al., “Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 290, no. 6, pp. H2196–H2203, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Zabel, B. S. Koller, F. Sachs, and M. R. Franz, “Stretch-induced voltage changes in the isolated beating heart: importance of the timing of stretch and implications for stretch-activated ion channels,” Cardiovascular Research, vol. 32, no. 1, pp. 120–130, 1996. View at Publisher · View at Google Scholar · View at Scopus
  42. M. R. Franz and F. Bode, “Mechano-electrical feedback underlying arrhythmias: the atrial fibrillation case,” Progress in Biophysics and Molecular Biology, vol. 82, no. 1–3, pp. 163–174, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. F. Bode, F. Sachs, and M. R. Franz, “Tarantula peptide inhibits atrial fibrillation,” Nature, vol. 409, no. 6816, pp. 35–36, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. R. M. Shaw and Y. Rudy, “Electrophysiologic effects of acute myocardial ischemia: a mechanistic investigation of action potential conduction and conduction failure,” Circulation Research, vol. 80, no. 1, pp. 124–138, 1997. View at Google Scholar · View at Scopus
  45. V. Jacquemet and C. S. Henriquez, “Modelling cardiac fibroblasts: interactions with myocytes and their impact on impulse propagation,” Europace, vol. 9, pp. 29–37, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. S. A. Niederer, P. J. Hunter, and N. P. Smith, “A quantitative analysis of cardiac myocyte relaxation: a simulation study,” Biophysical Journal, vol. 90, no. 5, pp. 1697–1722, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Pellman, R. C. Lyon, and F. Sheikh, “Extracellular matrix remodeling in atrial fibrosis: mechanisms and implications in atrial fibrillation,” Journal of Molecular and Cellular Cardiology, vol. 48, no. 3, pp. 461–467, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. R. G. Assomull, S. K. Prasad, J. Lyne et al., “Cardiovascular magnetic resonance, fibrosis, and prognosis in dilated cardiomyopathy,” Journal of the American College of Cardiology, vol. 48, no. 10, pp. 1977–1985, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. B. T. John, B. K. Tamarappoo, J. L. Titus, W. D. Edwards, W.-K. Shen, and S. S. Chugh, “Global remodeling of the ventricular interstitium in idiopathic myocardial fibrosis and sudden cardiac death,” Heart Rhythm, vol. 1, no. 2, pp. 141–149, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. M. L. Antoni, S. A. Mollema, V. Delgado et al., “Prognostic importance of strain and strain rate after acute myocardial infarction,” European Heart Journal, vol. 31, no. 13, pp. 1640–1647, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. P. Kohl, P. Camelliti, F. L. Burton, and G. L. Smith, “Electrical coupling of fibroblasts and myocytes: relevance for cardiac propagation,” Journal of Electrocardiology, vol. 38, no. 4, supplement, pp. 45–50, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. M. B. Rook, A. C. G. Van Ginneken, B. De Jonge, A. El Aoumari, D. Gros, and H. J. Jongsma, “Differences in gap junction channels between cardiac myocytes, fibroblasts, and heterologous pairs,” American Journal of Physiology. Cell Physiology, vol. 263, no. 5, pp. C959–C977, 1992. View at Google Scholar · View at Scopus
  53. P. Kohl, A. G. Kamkin, I. S. Kiseleva, and D. Noble, “Mechanosensitive fibroblasts in the sino-atrial node region of rat heart: interaction with cardiomyocytes and possible role,” Experimental Physiology, vol. 79, no. 6, pp. 943–956, 1994. View at Google Scholar · View at Scopus