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A Cross-Bridge Model Describing the Mechanoenergetics of Actomyosin Interaction

  • Mari Kalda
  • Pearu Peterson
  • Jüri EngelbrechtEmail author
  • Marko Vendelin

Abstract

In order to study the mechanical contraction and energy consumption by the cardiomyocytes we further developed an actomyosin model of Vendelin et al. (Ann. Biomed. Eng. 28:629–640, 2000). The model is of a self-consistent Huxley-type and is based on Hill formalism linking the free energy profile of reactions and mechanical force. In several experimental studies it has been shown that the dependency between oxygen consumption and stress-strain area is linear and is the same for isometric and shortening contractions. We analyzed the free energy profiles of actomyosin interaction by changing free energies of intermediate states and activation of different reactions. The model is able to replicate the linear dependence between oxygen consumption and stress-strain area together with other important mechanical properties of a cardiac muscle.

Keywords

Isometric Contraction Myosin Head Biochemical State Mechanical Contraction Free Energy Profile 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This research was supported by the European Union through the European Regional Development Fund and by the Estonian Science Foundation (Grant nr. 7344).

References

  1. Boudina S, Laclau M, Tariosse L, Daret D, Gouverneur G, Bonoron-Adèle S, Saks V, Santos PD (2002) Alteration of mitochondrial function in a model of chronic ischemia in vivo in rat heart. Am J Physiol, Heart Circ Physiol 282:821–831 Google Scholar
  2. Brutsaert DL, Clerck NMD, Goethals MA, Housmans PR (1978) Relaxation of ventricular cardiac muscle. J Physiol (Lond) 283:469–480 Google Scholar
  3. Cooke R, Pate E (1985) The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J 48:789–798 CrossRefGoogle Scholar
  4. Delhaas T, Arts T, Prinzen FW, Reneman RS (1994) Regional fibre stress-fibre strain area as an estimate of regional blood flow and oxygen demand in the canine heart. J Physiol (Lond) 477:481–496 Google Scholar
  5. Eisenberg E, Hill TL, Chen Y (1980) Cross-bridge model of muscle contraction. Quantitative analysis. Biophys J 29:195–227 CrossRefGoogle Scholar
  6. Gibbs CL, Barclay CJ (1995) Cardiac efficiency. Cardiovasc Res 30:627–634 Google Scholar
  7. Hill TL (1974) Theoretical formalism for the sliding filament model of contraction of striated muscle. Part I. Prog Biophys Mol Biol 28:267–340 CrossRefGoogle Scholar
  8. Hisano R, Cooper G (1987) Correlation of force-length area with oxygen consumption in ferret papillary muscle. Circ Res 61:318–328 CrossRefGoogle Scholar
  9. Janssen PM, Hunter WC (1995) Force, not sarcomere length, correlates with prolongation of isosarcometric contraction. Am J Physiol 269:676–685 Google Scholar
  10. Jepihhina N, Beraud N, Sepp M, Birkedal R, Vendelin M (2011) Permeabilized rat cardiomyocyte response demonstrates intracellular origin of diffusion obstacles. Biophys J 101:2112–2121 CrossRefGoogle Scholar
  11. Jewell BR (1977) A reexamination of the influence of muscle length on myocardial performance. Circ Res 40:221–230 CrossRefGoogle Scholar
  12. Kaasik A, Veksler V, Boehm E, Novotova M, Minajeva A, Ventura-Clapier R (2001) Energetic crosstalk between organelles: architectural integration of energy production and utilization. Circ Res 89:153–159 CrossRefGoogle Scholar
  13. Kay L, Saks VA, Rossi A (1997) Early alteration of the control of mitochondrial function in myocardial ischemia. J Mol Cell Cardiol 29:3399–3411 CrossRefGoogle Scholar
  14. Landesberg A, Sideman S (2000) Force-velocity relationship and biochemical-to-mechanical energy conversion by the sarcomere. Am J Physiol, Heart Circ Physiol 278:1274–1284 Google Scholar
  15. Månsson A (2010) Actomyosin-ADP states, interhead cooperativity, and the force-velocity relation of skeletal muscle. Biophys J 98:1237–1246 CrossRefGoogle Scholar
  16. Pate E, Cooke R (1989) A model of crossbridge action: the effects of ATP, ADP and Pi. J Muscle Res Cell Motil 29:181–196 CrossRefGoogle Scholar
  17. Ramay H, Vendelin M (2009) Diffusion restrictions surrounding mitochondria: a mathematical model of heart muscle fibers. Biophys J 97:443–452 CrossRefGoogle Scholar
  18. Saks V, Kuznetsov A, Andrienko T, Usson Y, Appaix F, Guerrero K, Kaambre T, Sikk P, Lemba M, Vendelin M (2003) Heterogeneity of ADP diffusion and regulation of respiration in cardiac cells. Biophys J 84:3436–3456 CrossRefGoogle Scholar
  19. Sepp M, Vendelin M, Vija H, Birkedal R (2010) ADP compartmentation analysis reveals coupling between pyruvate kinase and ATPases in heart muscle. Biophys J 98:2785–2793 CrossRefGoogle Scholar
  20. Suga H (1990) Ventricular energetics. Physiol Rev 70:247–277 Google Scholar
  21. Taylor TW, Goto Y, Hata K, Takasago T, Saeki A, Nishioka T, Suga H (1993a) Comparison of the cardiac force-time integral with energetics using a cardiac muscle model. J Biomech 26:1217–1225 CrossRefGoogle Scholar
  22. Taylor TW, Goto Y, Suga H (1993b) Variable cross-bridge cycling-ATP coupling accounts for cardiac mechanoenergetics. Am J Physiol 264:994–1004 Google Scholar
  23. Tobacman LS, Sawyer D (1990) Calcium binds cooperatively to the regulatory sites of the cardiac thin filament. J Biol Chem 265:931–939 Google Scholar
  24. Tran K, Smith N, Loiselle D, Crampin E (2010) A metabolite-sensitive, thermodynamically constrained model of cardiac cross-bridge cycling: implications for force development during ischemia. Biophys J 98:267–276 CrossRefGoogle Scholar
  25. Velden JV, Moorman AF, Stienen GJ (1998) Age-dependent changes in myosin composition correlate with enhanced economy of contraction in guinea-pig hearts. J Physiol (Lond) 507:497–510 CrossRefGoogle Scholar
  26. Vendelin M, Birkedal R (2008) Anisotropic diffusion of fluorescently labeled ATP in rat cardiomyocytes determined by raster image correlation spectroscopy. Am J Physiol, Cell Physiol 295:1302–1315 CrossRefGoogle Scholar
  27. Vendelin M, Bovendeerd PHM, Arts T, Engelbrecht J, van Campen DH (2000) Cardiac mechanoenergetics replicated by cross-bridge model. Ann Biomed Eng 28:629–640 CrossRefGoogle Scholar
  28. Vendelin M, Bovendeerd PHM, Engelbrecht J, Arts T (2002) Optimizing ventricular fibers: uniform strain or stress, but not ATP consumption, leads to high efficiency. Am J Physiol, Heart Circ Physiol 283:H1072–H1081 Google Scholar
  29. Vendelin M, Eimre M, Seppet E, Peet N, Andrienko T, Lemba M, Engelbrecht J, Seppet E, Saks V (2004). Intracellular diffusion of adenosine phosphates is locally restricted in cardiac muscle. Mol Cell Biochem 256–257:229–241 CrossRefGoogle Scholar
  30. Vendelin M, Hoerter J, Mateo P, Soboll S, Gillet B, Mazet J (2010). Modulation of energy transfer pathways between mitochondria and myofibrils by changes in performance of perfused heart. J Biol Chem 285:37240–37250 CrossRefGoogle Scholar
  31. Ventura-Clapier R, Mekhfi H, Vassort G (1987) Role of creatine kinase in force development in chemically skinned rat cardiac muscle. J Gen Physiol 89:815–837 CrossRefGoogle Scholar
  32. Zahalak GI, Ma SP (1990) Muscle activation and contraction: constitutive relations based directly on cross-bridge kinetics. J Biomech Eng 112:52–62 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Mari Kalda
    • 1
  • Pearu Peterson
    • 1
  • Jüri Engelbrecht
    • 2
    Email author
  • Marko Vendelin
    • 1
  1. 1.Laboratory of Systems Biology, Institute of CyberneticsTallinn University of TechnologyTallinnEstonia
  2. 2.Centre for Nonlinear Studies, Institute of CyberneticsTallinn University of TechnologyTallinnEstonia

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