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A Three-dimensional Continuum Model of Active Contraction in Single Cardiomyocytes

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Modeling the Heart and the Circulatory System

Part of the book series: MS&A ((MS&A,volume 14))

Abstract

We investigate the interaction of intracellular calcium spatio-temporal variations with the self-sustained contractions in cardiac myocytes. A 3D continuum mathematical model is presented based on a hyperelastic description of the passive mechanical properties of the cell, combined with an active-strain framework to describe the active shortening of myocytes and its coupling with cytosolic and sarcoplasmic calcium dynamics. Some numerical tests of combined boundary conditions and ionic activations illustrate the ability of our model in reproducing key experimentally established features. Potential applications of the study for predicting pathological subcellular mechanisms affecting e.g. cardiac repolarization are discussed.

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References

  1. Berry, M.F., Engler, A.J., Woo, Y.J., Pirolli, T.J., Bish, L.T., Jayasankar, V., Morine, K.J., Gardner, T.J., Discher, D.E., Sweeney, H.L.: Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am. J. Physio. Heart. Circ. Physiol. 290, H2196–2203 (2006)

    Article  Google Scholar 

  2. Bers, D.M.: Cardiac excitation—contraction coupling. Nature 415, 198–205 (2002)

    Article  Google Scholar 

  3. Bloom, S.: Spontaneous rhythmic contraction of separated heart muscle cells. Science 167(3926), 1727–1729 (1970)

    Article  Google Scholar 

  4. Cherry, E.M., Fenton, F.H.: Visualization of spiral and scroll waves in simulated and experimental cardiac tissue. New J. Phys. 10, 125016 (2008)

    Article  Google Scholar 

  5. Bueno-Orovio, A., Cherry, E.M., Fenton, F.H.: Minimal model for human ventricular action potentials in tissue. J. Theor. Biol. 253, 544–560 (2008)

    Article  MathSciNet  Google Scholar 

  6. Capogrossi, M.C., Suarez-Isla, B.A., Lakatta, E.G.: The interaction of electrically stimulated twitches and spontaneous contractile waves in single cardiac myocytes. J. Gen. Physiol., 88, 615–633 (1986)

    Article  Google Scholar 

  7. Cherubini, C., Filippi, S., Gizzi, A.: Electroelastic unpinning of rotating vortices in biological excitable media. Phys. Rev. E, 85, 031915 (2012)

    Article  Google Scholar 

  8. Cherubini, C., Filippi, S., Nardinocchi, P., Teresi, L.: An electromechanical model of cardiac tissue: Constitutive issues and electrophysiological effects.Prog. Biophys. Mol. Biol., 97, 562–573 (2008)

    Article  Google Scholar 

  9. Delbridge, L.M.D., Roos, K.P.: Optical methods to evaluate the contractile function of unloaded isolated cardiac myocytes. J. Molec. Cell Cardiol., 29, 11–25 (1997)

    Article  Google Scholar 

  10. Deshpande, V.S., McMeeking, R.M., Evans, A.G.: A bio-chemo-mechanical model for cell contractility, PNAS, 103, 14015–14020 (2006)

    Article  Google Scholar 

  11. Deshpande, V.S., Mrksich, M., McMeeking, R.M., Evans, A.G.:A bio-mechanical model for coupling cell contractility with focal adhesion formation, J. Mech. Phys. Sol., 56, 1484–1510 (2008)

    Article  MATH  Google Scholar 

  12. Fabiato, A.: Appraisal of the physiological relevance of two hypothesis for the mechanism of calcium release from the mammalian cardiac sarcoplasmic reticulum: calcium-induced release versus charge-coupled release, Mol. Cell. Biochem., 89, 135–140 (1989).

    Article  Google Scholar 

  13. Fabiato, A., Fabiato, F.: Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J. Physiol. 249(3), 469–495 (1975)

    Article  Google Scholar 

  14. Fenton, F.H., Cherry, E.M.: Models of cardiac cells, Scholarpedia 3, 1868 (2008)

    Article  Google Scholar 

  15. Fenton, F.H., Gizzi, A., Cherubini, C., Pomella, N., Filippi, S.: Role of temperature on nonlinear cardiac dynamics, Phys. Rev. E Stat. Nonlin. Soft. Matter. Phys., 87, 042709 (2013)

    Article  Google Scholar 

  16. Geuzaine, C., Remacle, J.F.: Gmsh: a three-dimensional finite element mesh generator with built-in pre- and post-processing facilities. Int. J. Numer. Meth. Engrg., 79, 1309–1331 (2009)

    Article  MATH  MathSciNet  Google Scholar 

  17. Gizzi, A., Cherubini, C., Filippi, S., Pandolfi, A.: Theoretical and Numerical Modeling of Nonlinear Electromechanics with applications to Biological Active Media, Commun. Comput. Phys. 17(1), 93–126 (2015)

    Article  Google Scholar 

  18. Göktepe, S., Abilez, O.J., Kuhl, E.: A generic approach towards finite growth with examples of athletes heart, cardiac dilation, and cardiac wall thickening. J. Mech. Phys. Sol., 58, 1661–1680 (2010)

    Article  MATH  Google Scholar 

  19. Goldbeter, A., Dupont, G., Berridge, M.J.: Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein phosphorylation. Proc. Natl. Acad. Sci. USA, 87, 1461–1465 (1990)

    Article  Google Scholar 

  20. Goldmann, W.H. Mechanotransduction in cells. Cell. Biol. Int. 36, 567–70 (2012)

    Article  Google Scholar 

  21. Grosberg, A., Kuo, P.L., Guo, C.L., Geisse, N.A., Bray, M.A., Adams, W.J., Sheehy, S.P., Parker, K.K.: Self-organization of muscle cell structure and function. PLoS Comp. Biol., 7, e1001088 (2011)

    Article  Google Scholar 

  22. Hatano, A., Okada, J., Washio, T., Hisada, T., Sugiura, S.: A three-dimensional simulation model of cardiomyocyte integrating excitation-contraction coupling and metabolism. Biophys. J., 101, 2601–2610 (2011)

    Article  Google Scholar 

  23. Holzapfel, G.A., Ogden, R.W.: Constitutive modelling of passive myocardium: a structurally based framework for material characterization. Phil. Trans. R. Soc. Lond. A, 367, 3445–3475 (2009)

    Article  MATH  MathSciNet  Google Scholar 

  24. Humphrey, J.D.: Stress, strain, and mechanotransduction in cells. J. Biomech. Eng. 123, 638–641 (2001)

    Article  Google Scholar 

  25. Iribe, G., Helmes, M., Kohl, P.: Force-length relations in isolated intact cardiomyocytes subjected to dynamic changes in mechanical load. Am. J. Physiol. Heart Circ. Physiol., 292, H1487–H1497 (2007)

    Article  Google Scholar 

  26. Iribe, G., Ward, C.W., Camelliti, P., Bollensdorff, C., Mason, F., Burton, R.A.B., Garny, A., Morphew, M., Hoenger, A., Lederer, W.J., Kohl, P.: Axial stretch of rat single ventricular cardiomyocytes causes an acute and transient increase in Ca2+ spark rate. Circ. Res., 104, 787–795 (2009)

    Article  Google Scholar 

  27. Iyer, V., Mazhari, R., Winslow, R.L.: A computational model of the human left ventricular epicardial myocyte. Biophys. J., 87, 1507–1525 (2004)

    Article  Google Scholar 

  28. Kamgoué, A., Ohayon, J., Usson, Y., Riou, L., Tracqui, P.: Quantification of cardiomyocyte contraction based on image correlation analysis. Cytometry Part A 75, 298–308 (2009)

    Article  Google Scholar 

  29. Keener, J., Sneyd, J.: Mathematical physiology, Springer-Verlag, New York (1998)

    MATH  Google Scholar 

  30. Kockskåmper, J., von Lewinski, D., Khafaga, M., Elgner, A., Grimm, M., Eschenhagen, T., Gottlieb, P.A., Sachs, F., Pieske, B.: The slow force response to stretch in atrial and ventricular myocardium from human heart: functional relevance and subcellular mechanisms. Prog. Biophys. Mol. Biol., 97, 250–267 (2008)

    Article  Google Scholar 

  31. Laadhari, A., Ruiz-Baier, R., Quarteroni, A.: Fully Eulerian finite element approximation of a fluid-structure interaction problem in cardiac cells. Int. J. Numer. Meth. Engrg., 96, 712–738 (2013)

    Article  MathSciNet  Google Scholar 

  32. Lubarda, V.A.: Constitutive theories based on the multiplicative decomposition of deformation gradient: Thermoelasticity, elastoplasticity, and biomechanics. Appl. Mech. Rev., 57, 95–108 (2004)

    Article  Google Scholar 

  33. Li, J., Patel, V.V., Radice, G.L.: Dysregulation of cell adhesion proteins and cardiac arrhythmogenesis, Clin. Med. Res., 4, 42–52 (2006)

    Article  Google Scholar 

  34. Li, W., Gurev, V., McCulloch, A.D., Trayanova, N.A.: The role of mechanoelectric feedback in vulnerability to electric shock, Prog. Biophys. Mol. Biol., 97, 461–478 (2008)

    Article  Google Scholar 

  35. Louch, W.E., Stokke, M.K., Sjaastad, I., Christensen, G., Sejersted, O.M.: No rest for the weary: diastolic calcium homeostasis in the normal and failing myocardium, Physiology, 27, 308–323 (2008)

    Article  Google Scholar 

  36. Marshall, K.L., Lumpkin, E.A.: The molecular basis of mechanosensory transduction. Adv. Exp. Med. Biol., 739, 142–55 (2012)

    Article  Google Scholar 

  37. McCain, M.L., Lee, H.L., Aratyn-Schaus, Y., Kléber, A.G., Parker, K.K. Cooperative coupling of cell-matrix and cell-cell adhesions in cardiac muscle. PNAS, 109, 9881–9886 (2012)

    Article  Google Scholar 

  38. Nardinocchi, P., Teresi, L.: Electromechanical modeling of anisotropic cardiac tissues. Math. Mech. Solids, 18, 576–591 (2013)

    Article  MathSciNet  Google Scholar 

  39. Nobile, F., Quarteroni, A., Ruiz-Baier, R.: An active strain electromechanical model for cardiac tissue. Int. J. Numer. Meth. Biomed. Engrg., 28, 52–71 (2012)

    Article  MATH  MathSciNet  Google Scholar 

  40. Novak, I.L., Slepchenko, B.M., Mogilner, A., Loew, L.M.: Cooperativity between cell contractility and adhesion. Phys. Rev. Lett., 93, 268109 (2004)

    Article  Google Scholar 

  41. Nishimura, S., Seo, K., Nagasaki, M., Hosoya, Y., Yamashita, H., Fujita, H., Nagai, R., Sugiura, S.: Responses of single-ventricular myocytesto dynamic axial stretching. Prog. Biophys. Mol. Biol., 97, 282–297 (2008)

    Article  Google Scholar 

  42. Ortiz, M., Stainier, L.: The variational formulation of viscoplastic constitutive updates. Comp. Meth. Appl. Mech. Eng., 171, 419–444 (1999)

    Article  MATH  MathSciNet  Google Scholar 

  43. Ortiz, M., Pandolfi, A.: A variational Cam-clay theory of plasticity. Comp. Meth. Appl. Mech. Eng., 193, 2645–2666 (2004).

    Article  MATH  Google Scholar 

  44. Pandolfi, A., Conti, S., Ortiz, M.: A recursive-faulting model of distributed damage in confined brittle materials. J. Mech. Phys. Sol., 54, 1972–2003 (2006)

    Article  MATH  MathSciNet  Google Scholar 

  45. Parker, K.K., Tan, J., Chen, C.S., Tung, L.: Myofibrillar architecture in engineered cardiac myocytes. Circ. Res., 103, 340–342 (2008)

    Article  Google Scholar 

  46. Pullan, A.J., Buist, M.L., Cheng, L.K.: Mathematically Modeling the Electrical Activity of the Heart: From Cell to Body Surface and Back, World Scientific, Singapore (2005)

    Book  Google Scholar 

  47. Pumir, A., Sinha, S., Sridhar, S., Argentina, M., Horning, M., Filippi, S., Cherubini, C., Luther, S., Krinsky, V.: Wave-train-induced termination of weakly anchored vortices in excitable media. Phys. Rev. E, 82, 010901(R) (2010)

    Article  Google Scholar 

  48. Rice, J.J., Wang, F., Bers, D.M., de Tombe, P.P. Approximate model of cooperative activation and crossbridge cycling in cardiac muscle using ordinary differential equations. Biophys. J., 95, 2368–2390 (2008)

    Article  Google Scholar 

  49. Ronan, W., Deshpande, V.S., McMeeking, R.M., McGarry, J.P.: Numerical investigation of the active role of the actin cytoskeleton in the compression resistance of cells. J. Mech. Behav. Biomed. Mat., 14, 143–157 (2012)

    Article  Google Scholar 

  50. Rossi, S., Lassila, T., Ruiz-Baier, R., Sequeira, A., Quarteroni, A.: Thermodynamically consistent orthotropic activation model capturing ventricular systolic wall thickening in cardiac electromechanics. Eur. J. Mech. A/Solids 48, 129–142 (2014)

    Article  MathSciNet  Google Scholar 

  51. Ruiz-Baier, R., Gizzi, A., Rossi, S., Cherubini, C., Laadhari, A., Filippi, S., Quarteroni, A.: Mathematical modelling of active contraction in isolated cardiomyocytes, Math. Med. Biol. 31, 259–283 (2014)

    Article  MATH  MathSciNet  Google Scholar 

  52. Seol, C.A., Kim, W.T., Ha, J.M., Choe, H., Jang, Y.J., Youm, J.B., Earm, Y.E., Leem, C.H.: Stretch-activated currents in cardiomyocytes isolated from rabbit pulmonary veins. Prog. Biophys. Mol. Biol., 97, 217–231 (2008)

    Article  Google Scholar 

  53. Sheehy, S.P., Grosberg, A., Parker, K.K.: The contribution of cellular mechanotransduction to cardiomyocyte form and function. Biomech. Model. Mechanobiol. 11, 1227–1239 (2012)

    Article  Google Scholar 

  54. Sneyd, J., Ed.: Tutorials in Mathematical Biosciences II: Mathematical Modeling of Calcium Dynamics and Signal Transduction, Springer, ISBN 978-3-540-25439-3 (2005)

    Google Scholar 

  55. Stålhand, J., Klarbring, A., Holzapfel, G.A.: A mechanochemical 3D continuum model for smooth muscle contraction under finite strains. J. Theoret. Biol., 268, 120–130 (2011).

    Article  MathSciNet  Google Scholar 

  56. Stern, M.D.: Theory of excitation-contraction coupling in cardiac muscle. Biophys. J., 63, 497–517 (1992)

    Article  Google Scholar 

  57. Subramanian, S., Viatchenko-Karpinski, S., Lukyanenko, V., Györk, S., Wiesner, T.F. Underlying mechanisms of symmetric calcium wave propagation in rat ventricular myocytes. Biophys. J., 80, 1–11 (2001)

    Article  Google Scholar 

  58. Taber, L.A.: Biomechanics of cardiovascular development. Annu. Rev. Biomed. Eng., 3, 1–25 (2001)

    Article  Google Scholar 

  59. Takamatsu, T., Wier, W.G.: Calcium waves in mammalian heart: quantification of origin, magnitude, waveform and velocity. Fed. Am. Soc. Exp. Biol., 4, 1519–1525 (1990)

    Google Scholar 

  60. Ter Keurs, H.E.D.J., Boyden, P.A.: Calcium and arrhythmogenesis. Physiol. Rev. 87(2), 457–506 (2007)

    Article  Google Scholar 

  61. Tracqui, P., Ohayon, J.: An integrated formulation of anisotropic force-calcium relations driving spatio-temporal contractions of cardiac myocytes. Phil. Trans. Royal Soc. London A, 367, 4887–4905 (2009)

    Article  MATH  Google Scholar 

  62. Tveito, A., Lines, G.T., Edwards, A.G., Maleckar, M.M., Michailova, A., Hake, J., McCulloch, A.D.: Slow Calcium-Depolarization-Calcium waves may initiate fast local depolarization waves in ventricular tissue. Prog. Biophys. Molec. Biol., 110, 295–304 (2012)

    Article  Google Scholar 

  63. Vogel, F., Bustamante, R., Steinmann, P.: On some mixed variational principles in electro-elastostatics. Int. J. Nonlin. Mech., 47, 341–354 (2012)

    Article  Google Scholar 

  64. Washio, T., Okada, J. Sugiura, S., Hisada, T.: Approximation for cooperative interactions of a spatially-detailed cardiac sarcomere model. Cell. Mol. Bioeng., 5, 113–126 (2012)

    Article  Google Scholar 

  65. Ward, M.L., Williams, I.A., Chu, Y., Cooper, P.J., Ju, Y.K., Allen, D.G.: Stretch-activated channels in the heart: contributions to length-dependence and to cardiomyopathy.Prog. Biophys. Mol. Biol., 97, 232–249 (2008)

    Article  Google Scholar 

  66. Zhang, Y., Sekar, R.B., McCulloch, A.D., Tung, L.: Cell cultures as models of cardiac mechanoelectric feedback. Prog. Biophys. Mol. Biol., 97, 367–382 (2008)

    Article  Google Scholar 

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Gizzi, A., Ruiz-Baier, R., Rossi, S., Laadhari, A., Cherubini, C., Filippi, S. (2015). A Three-dimensional Continuum Model of Active Contraction in Single Cardiomyocytes. In: Quarteroni, A. (eds) Modeling the Heart and the Circulatory System. MS&A, vol 14. Springer, Cham. https://doi.org/10.1007/978-3-319-05230-4_6

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