Advertisement

Bioenergetics—Conversion of Biochemical to Mechanical Energy in the Cardiac Muscle

  • Samuel Sideman
  • Amir Landesberg

Abstract

Life is sustained by the continuous conversion of biochemical energy to mechanical energy, which is required to maintain the various functions of living organisms. This wide range of energetic activities depends on rotary and linear molecular (protein) motors of nanometer scale, which propel (bacteria, sperms), transport (messengers in neural network, cell division) generate high-energy metabolites (ATPsynthase) and perpetuate motion (muscle shortening).

This study relates to the linear molecular motor, myosin, which is energized by ATP (adenosine triphosphate) hydrolysis, and actuates muscle filament contraction. The actin-myosin filaments make up the intracellular contractile apparatus, the sarcomeres, and their relative motion, sliding one over the other, determines the functional characteristics of the contracting heart muscle.

The study explores the relationship between the biochemical energy consumption and the mechanical output of the motor units of the heart muscle. The analysis is based on coupling motor unit dynamics with free calcium binding kinetics, which regulates the motor unit activity. The calcium binds to the regulatory proteins of the contractile filaments and regulates the number of activated myosin motor units. The analysis quantifies the conversion efficiency and the determinants of the muscle’s economy. The intracellular interplay between efficiency and economy determines the adaptability of the heart muscle to the prevailing loading conditions. The analysis highlights the intracellular mechanisms and the adaptive processes that allow the heart to optimize its function under various loading conditions.

Whereas the thermodynamic efficiency of the overall metabolic transformation from biochemical energy to mechanical energy of the whole organ is 25–35%, the efficiency of energy transduction from ATP to mechanical energy ranges between 50 to 70%. This high efficiency of energy conversion reflects the extremely high efficiency of the myosin motor unit, wherein the ATPase enzyme is instrumental in ATP hydrolysis ATP + H2O ↔ ADP+P reaction and the production of mechanical energy. Finally, we discuss the notion that man is challenged by nature’s functional design in his pursuit of new horizons.

Keywords

Molecular motors crossbridge sarcomere energy conversion control cooperativity feedback mechanism contraction efficiency economy nanotechnology 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Woledge R.C., Reilly P.J. Molar Enthalpy Change to Hydrolysis of Phosphocreatine under Conditions in Muscle Cell. Biophys. J. 1988; 54: 97–104.CrossRefGoogle Scholar
  2. 2.
    Wang H., Oster G. Energy Tranduction in the F, Motor of ATP Synthase. Nature 1998; 396: 279–282.CrossRefGoogle Scholar
  3. 3.
    Oster G., Wang H. ATP Synthase: Two Motors, Two Fuels. Structure 1999; 7 (4): 67–72.CrossRefGoogle Scholar
  4. 4.
    Fisher M.E., Kolomeisky A.B. The Force Exerted by a Molecular Motor. Proc. Nat. Acad. Sci. USA. 96:6597–6602, 1999.CrossRefGoogle Scholar
  5. 5.
    Eisenberg E., Hill T.L. Muscle Contraction and Free Energy Transduction in Biological System. Science. 1985; 227: 999–1006.CrossRefGoogle Scholar
  6. 6.
    Landesberg A. End Systolic Pressure-Volume Relation Based on the Intracellular Control of Contraction. Am J Physiol. 1996; 270 (Heart Circ. Physiol. 39):H338–H349.Google Scholar
  7. 7.
    Landesberg A. Intracellular Mechanism in Control of Myocardial Mechanics and Energetics. In Analytical and Quantitative Cardiology: From Genetics to Function. S. Sideman and R. Beyar, eds.NY Plenum. 1997; 430: 75–87.CrossRefGoogle Scholar
  8. 8.
    Landesberg A., Sideman S. Coupling Calcium Binding to Troponin-C and Xb Cycling Kinetics in Skinned Cardiac Cells. Am J. Physiol. 1994; 266 (Heart Circ. Physiol. 35): H1261–H1271.Google Scholar
  9. 9.
    Landesberg A., Sideman S. Mechanical Regulation in the Cardiac Muscle by Coupling Calcium Binding to Troponin-C and Xb Cycling. A Dynamic Model. Am. J. Physiol. 1994; 267 (Heart Circ Physiol 36): H779–H795.Google Scholar
  10. 10.
    Landesberg A., Sideman S. Regulation of Energy Consumption in the Cardiac Muscle: Analysis of Isometric Contractions. A Dynamic Model. Am. J. Phsyiol. 1999; 276: H998–H1011.Google Scholar
  11. 11.
    Landesberg A., Sideman S. Force Velocity Relationship and Biochemical to Mechanical Energy Conversion by the Sarcomere. Am. J. Physiol., in press, 2000.Google Scholar
  12. 12.
    Landesberg A., ter Keurs HED.T. Regulation of Force Output by the Velocity of Sarcomere Shortening in Rat Cardiac Trabecular Circulation. 1997; 96 (8): 2906.Google Scholar
  13. 13.
    Landesberg A., ter Keurs HEDJ. Crossbridge Dynamics during Shortening is Determined by Two Kinetic Components. J. Mol. Cell. Cardiol. 1998; 30: A171.Google Scholar
  14. 14.
    Landesberg A., Liu P., Lichtenstein O., Shofti R., Beyar R., Sideman S. Effect of Ejection Velocity on Pressure Generation in the Heart. In situ canine studies. VIII Mediterranean Conf. on Medical and Biological Engineering and Computing, Limassol, Cyprus, pp. 1–5, 1998.Google Scholar
  15. 15.
    Beyar R., Sideman S. A Computer Study of the Left Ventricular Performance Based on Fiber Structure, Sarcomere Dynamics, and Transmural Electrical Propagation Velocity. Circ. Res. 1984; 55: 358–75.CrossRefGoogle Scholar
  16. 16.
    Campbell K.B., Shroff S.G., Kirkpatrick R.D. Short Time Scale Left Ventricle Systolic Dynamics. Circ. Res. 1991; 68:1532–48.CrossRefGoogle Scholar
  17. 17.
    Sagawa K., Maughan L., Suga H., Sunagawa K. Cardiac Contraction and the Pressure-Volume Relationship. London, UK: Oxford Univ Press, 1988.Google Scholar
  18. 18.
    Suga H. Ventricular Energetics. Physiol. Rev. 1990; 70:247–277.Google Scholar
  19. 19.
    Hisano G., Cooper IV. Correlation of Force-Length Area with Oxygen Consumption in Ferret Papillary Muscle. Circ. Res. 1987; 61:318–28.CrossRefGoogle Scholar
  20. 20.
    Landesberg A., Zhang Y.M., ter Keurs HEDJ. Regulation of Tension-Length Free Calcium Relationship in the Skinned Rat Trabeculae. J. Biophysics, in press 2000.Google Scholar
  21. 21.
    Peterson J.N., Hunber W.C., Berman M.R. Estimated Time Course of Calcium Bound to Troponin-c during Relaxation in Isolated Cardiac Muscle. Am. J. Cardiol. 1977; 40: 748–53.CrossRefGoogle Scholar
  22. 22.
    Landesberg A., Sideman S. Calcium Kinetics and Mechanical Regulation of Cardiac Muscle. In Interactive Phenomena in the Cardiac System. Sideman S., Beyar R., eds. Plenum Publishing Corp., NY, 1993; 59–77.CrossRefGoogle Scholar
  23. 23.
    Landesberg A. Intracellular Mechanism in Control of Myocardial Mechanics and Energetics. In Analytical and Quantitative Cardiology: From Genetics to Function, S. Sideman and R. Beyar. eds. New York Plenum, 1997; 430: 75–87.CrossRefGoogle Scholar
  24. 24.
    Allen D.G., Kentish J.C. The Cellular Basis of the Length Tension Regulation in Cardiac Muscle. J. Mol. Cellulal Biol., 1985; 17:821–40.Google Scholar
  25. 25.
    Eisenberg E., Hill T.L. Muscle Contraction and Free Energy Transduction in Biological System. Science. 1985; 227: 999–1006.CrossRefGoogle Scholar
  26. 26.
    Fozzard H.A., Haber E., Jennings R.B., Katz A.M., Morgan H.E. The Heart and Cardiovascular System. Scientific Foundations. Second Edition. NY: Raven Press, 1991: 1281–95.Google Scholar
  27. 27.
    Hill A.V. The Heat of Shortening and Dynamic Constants of Shortening. Proc. Royal Soc. London (Biol) 1938; 126: 136–195.Google Scholar
  28. 28.
    Landesberg A., Livshitz L., ter Keurs HEDJ. The Effect of Sarcomere Shortening Velocity on Force Generation, Analysis of and Verification of Models for Crossbridge Dynamics. W. Herzog, ed. John Wiley and Sons, in press 2000.Google Scholar
  29. 29.
    Mulieri L.A., Luhr G., Tvefry J., Alpert N.R. Metal-Film Thermopiles for Use with Rabbit Right Ventricular Papillary Muscle. Am. J. Physiol. 1977; 233:C146–C156.Google Scholar
  30. 30.
    Cooper G.N. Load and Length Regulation of Cardiac Energetics. Annu. Rev. Physiol. 1990; 52: 505–522.CrossRefGoogle Scholar
  31. 31.
    Alpert N.R., Mulieri L.A., Hasenfuss G., Holubarsch C. Optimization of Myocardial Function. In Myocardial Optimization and Efficiency: Evolutionary Aspects and Philosophy of Science Considerations. D. Burkhoff, J. Schaefer, K. Schaffne, D.T. Yue, eds. Springer-Verlag: NY, 1994; 29–41.Google Scholar
  32. 32.
    Alpert N.R., Mulieri L.A., Hasenfuss G. Myocardial Chemo-Mechanical Energy Transduction. In: The Heart and Cardiovascular System, 2nd Ed; HA Fozzard et al eds. Raven Press, NY, 1992; 111–128.Google Scholar
  33. 33.
    Alpert N.R., Mullieri L.A. Human Heart Failure: Determinants of Ventricular Dysfunction. In Analytical and Quantitative Cardiology, S. Sideman and R. Beyar, eds.Plenum Press, NY.1997; 97–108.CrossRefGoogle Scholar
  34. 34.
    Hasenfuss G., Mullieri L.A., Blanchard E.M., Holubarsch C.H., Leavitt B.J., Ittleman F., Alpert N.R. Energetic of Isometric Force Development in Control and Volume Overload Human Myocardium: Comparison with Animal Species. Cir. Res. 1991; 68: 836–846.CrossRefGoogle Scholar
  35. 35.
    Suga H., Goto Y., Kawaguchi O., Hata K., Takasago T., Sachi A., Taylor T.W. Ventricular Perspective of Efficiency. In Myocardial Optimization and Efficiency, Evolutionary Aspects and Philosphy of Science Consideration. D. Burkhoff, J. Schaefer, K. Schaffner, D.T. Yue (eds.) Basic Res. Cardiol., Springer-Verlag, NY. 1993; 88: 43–65.Google Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Samuel Sideman
    • 1
  • Amir Landesberg
    • 1
  1. 1.Technion-Israel Institute of TechnologyHaifaIsrael

Personalised recommendations