Journal of Muscle Research & Cell Motility

, Volume 19, Issue 8, pp 909–921 | Cite as

Regulatory roles of MgADP and calcium in tension development of skinned cardiac muscle

  • Norio Fukuda
  • Hideaki Fujita
  • Takashi Fujita
  • Shin'ichi Ishiwata
Article

Abstract

We investigated the regulatory roles of MgADP and free Ca2+ in isometric tension development in skinned bovine cardiac muscle. We found that, in the relaxed state without free Ca2+, MgADP elicited a sigmoidal increase in active tension, as is the case in skeletal muscle (ADP-contraction). The critical MgADP concentration, at which the tension increment became half-maximal, increased in proportion to MgATP concentration, with a slope of approximately 1 for cardiac and 4 for skeletal muscle. Raising the free Ca2+ concentration decreased the critical MgADP concentration in proportion to the free Ca2+ concentration. In addition, the apparent Ca2+ sensitivity of tension development increased with MgADP, while decreasing with inorganic phosphate (Pi); MgADP suppressed the Ca2+- desensitizing effect of Pi in a concentration-dependent manner. These activating effects of MgADP were quantitatively assessed by means of a model based upon the kinetic scheme of actomyosin ATPase. These experimental results and model simulation suggest that the state of thin filaments is synergistically regulated by both the binding of Ca2+ to troponin and the formation of the actomyosin–ADP complex.

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References

  1. ALLEN, D. G., MORRIS, P. G., ORCHARD, C. H. & PIROLO, J. S. (1985) A nuclear magnetic resonance study of metabolism in the ferret heart during hypoxia and inhibition of glycolysis. J. Physiol. (Lond.) 361, 185–204.Google Scholar
  2. ALLEN, D. G. & ORCHARD, C. H. (1987) Myocardial contractile function during ischaemia and hypoxia. Circ. Res. 60, 153–68.Google Scholar
  3. ASHLEY, C. C., MULLIGAN, I. P. & LEA, T. J. (1991) Ca2+and activation mechanisms in skeletal muscle. Quart. Rev. Biophys. 24, 1–73.Google Scholar
  4. BEST, P. M., DONALDSON, S. K. & KERRICK, W. G. L. (1977) Tension in mechanically disrupted mammalian cardiac cells: effects of magnesium adenosine triphosphate. J. Physiol. (Lond.) 265, 1–17.Google Scholar
  5. BRANDT, P. W., REUBEN, J. P. & GRUNDFEST, H. (1972) Regulation of tension in the skinned crayfish muscle fiber. J. Gen. Physiol. 59, 305–17.Google Scholar
  6. BREMEL, R. D. & WEBER, A. (1972) Cooperation within actin filament in vertebrate skeletal muscle. Nature (New Biol.) 238, 97–101.Google Scholar
  7. BROZOVICH, F. V., YATES, L. D. & GORDON, A. M. (1988) Muscle force and stiffness during activation and relaxation. Implications for the actomyosin ATPase. J. Gen. Physiol. 91, 399–420.Google Scholar
  8. CHALOVICH, J. M. & EISENBERG, E. (1982) Inhibition of actomyosin ATPase activity by troponin-tropomyosin without blocking the binding of myosin to actin. J. Biol. Chem. 257, 2432–7.Google Scholar
  9. COOKE. R. & PATE, E. (1985) The effects of ADP and phosphate on the contraction of muscle fibers. Biophys. J. 48, 789–98.Google Scholar
  10. EBASHI, S. & ENDO, M. (1968) Calcium ions and muscle contraction. Prog. Biophys. Mol. Biol. 18, 123–83.Google Scholar
  11. FUJITA, H. & ISHIWATA, S. (1998) Spontaneous oscillatory contraction without regulatory proteins in actin filament-reconstituted fibers. Biophys. J. 75, 1439–45.Google Scholar
  12. FUKUDA, N., FUJITA, T. & ISHIWATA, S. (1991) Effects of ADP, inorganic phosphate and calcium on spontaneous tension oscillation of glycerinated cardiac muscle. J. Muscle Res. Cell Motil. 12, 304.Google Scholar
  13. FUKUDA, N., FUJITA, H., FUJITA, T. & ISHIWATA, S. (1996) Spontaneous tension oscillation in skinned bovine cardiac muscle. Pflügers Arch. 433, 1–8.Google Scholar
  14. GEEVES, M. A. (1991) The dynamics of actin and myosin association and the crossbridge model of muscle contraction. Biochem. J. 274, 1–14.Google Scholar
  15. GODT, R. E. (1974) Calcium-activated tension of skinned muscle fibers of the frog. J. Gen. Physiol. 63, 722–39.Google Scholar
  16. GODT, R. E. & NOSEK, T. M. (1989) Changes of intracellular milieu with fatigue or hypoxia depress contraction of skinned rabbit skeletal and cardiac muscle. J. Physiol. (Lond.) 412, 155–80.Google Scholar
  17. GOLDMAN, Y. E. (1987) Kinetics of the actomyosin ATPase in muscle fibers. Ann. Rev. Physiol. 49, 637–54.Google Scholar
  18. GOLDMAN, Y. E. & BRENNER, B. (1987) Special topic: molecular mechanism of muscle contraction. Ann. Rev. Physiol. 49, 629–36.Google Scholar
  19. GÜTH, K. & POTTER, J. D. (1987) Effect of rigor and cycling cross-bridges on the structure of troponin C and on the Ca2+affinity of the Ca2+-specific regulatory sites in skinned rabbit psoas fibers. J. Biol. Chem. 262, 13627–35.Google Scholar
  20. HIBBERD, M. G., DANTZIG, J. A., TRENTHAM, D. R. & GOLDMAN, Y. E. (1985) Phosphate release and force generation in skeletal muscle fibers. Science 228, 1317–9.Google Scholar
  21. HOAR, P. E., MAHONEY, C. W., KERRICK, W. G. L. & MONTAGUE, D. (1987) MgADP increases maximum tension and Ca2+sensitivity in skinned rabbit soleus fibers. Pfügers Arch. 410, 30–36.Google Scholar
  22. HORIUTI, K. (1986) Some properties of the contractile system and sarcoplasmic reticulum of skinned slow fibres from Xenopus muscle. J. Physiol. (Lond.) 373, 1–23.Google Scholar
  23. ISHIWATA, S. & YASUDA, K. (1993) Mechano-chemical coupling in spontaneous oscillatory contraction of muscle. Phase Transitions 45, 105–36.Google Scholar
  24. JOHNSON, R. E. & ADAMS, P. H. (1984) ADP binds similarly to rigor muscle myofibrils and to actomyosin-subfragment one. FEBS Lett. 174, 11–14.Google Scholar
  25. KAMMERMEIER, H., SCHMIDT, P. & JUNGLING, E. (1982) Free energy change of ATP-hydrolysis: a causal factor of early hypoxic failure of the myocardium? J. Mol. Cell. Cardiol. 14, 267–77.Google Scholar
  26. KENTISH, J. C. (1986) The effects of inorganic phosphate and creatine phosphate on force production in skinned muscles from rat ventricles. J. Physiol. (Lond.) 412, 155–80.Google Scholar
  27. KUSUOKA, H., WEISFELDT, M. L., ZWEIER, J., JACOBUS, W. E. & MARBAN, E. (1986) Mechanisms of early contractile failure during hypoxia in intact ferret heart: evidence for modulation of maximal Ca2+-activated force by inorganic phosphate. Circ. Res. 59, 270–82.Google Scholar
  28. LEHRER, S. S. & GEEVES, M. A. (1998) The muscle thin filament as a classical cooperative/allosteric regulatory system. J. Mol. Biol. 277, 1081–9.Google Scholar
  29. LEHRER, S. S. & MORRIS, E. P. (1982) Dual effects of tropomyosin and troponin-tropomyosin on actomyosin subfragment 1 ATPase. J. Biol. Chem. 257, 8073–80.Google Scholar
  30. LIENHARD, G. E. & SECEMSKI, I. I. (1973) P1, P5-di(adenosine-5′) pentaphosphate, a potent multisubstrate inhibitor of adenylate kinase. J. Biol. Chem. 248, 1121–3.Google Scholar
  31. LU, Z., MOSS, R. L. & WALKER, J. W. (1993) Tension transients initiated by photogeneration of MgADP in skinned skeletal muscle fibers. J. Gen. Physiol. 101, 867–88.Google Scholar
  32. MARBAN, E. & KUSUOKA, H. (1987) Maximal Ca2+-activated force and myofilament sensitivity in intact mammalian hearts. J. Gen. Physiol. 90, 609–23.Google Scholar
  33. McKILLOP, D. F. A. & GEEVES, M. A. (1993) Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament. Biophys. J. 65, 693–701.Google Scholar
  34. METZGER, J. M. (1995) Myosin binding-induced cooperative activation of the thin filament in cardiac myocytes and skeletal muscle fibers. Biophys. J. 68, 1430–42.Google Scholar
  35. NAGASHIMA, H. & ASAKURA, S. (1982) Studies on cooperative properties of tropomyosin-actin and tropomyosin-troponin-actin complexes by the use of N-ethylmaleimide-treated and untreated species of myosin subfragment 1. J. Mol. Biol. 155, 409–28.Google Scholar
  36. PALMER, S. & KENTISH, J. C. (1994) The role of troponin C in modulating the Ca2+sensitivity of mammalian skinned cardiac and skeletal muscle fibres. J. Physiol. (Lond.) 480, 45–60.Google Scholar
  37. RUFF, R. L. & WEISSMAN, J. (1991) Iodoacetate-induced contracture in rat skeletal muscle: possible role of ADP. Am. J. Physiol. 261, C828–36.Google Scholar
  38. SEOW, C. Y. & FORD, L. E. (1997) Exchange of ATP for ADP on high-force cross-bridges of skinned rabbit muscle fibers. Biophys. J. 72, 2719–35.Google Scholar
  39. SHIMIZU, H., FUJITA, T. & ISHIWATA, S. (1992) Regulation of tension development by MgADP and Pi without Ca2+. Role in spontaneous tension oscillation of skeletal muscle. Biophys. J. 61, 1087–98.Google Scholar
  40. SIEMANKOWSKI, R. F. & WHITE, H. D. (1984) Kinetics of the interaction between actin, ADP, and cardiac myosin-S1. J. Biol. Chem. 259, 5045–53.Google Scholar
  41. SIEMANKOWSKI, R. F., WISEMAN, M. O. & WHITE, H. D. (1985) ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle. Proc. Natl Acad. Sci. USA 82, 658–62.Google Scholar
  42. SWARTZ, D. R. & MOSS, R. L. (1992) Influence of a strongbinding myosin analogue on calcium-sensitive mechanical properties of skinned skeletal muscle fibers. J. Biol. Chem. 267, 20497–506.Google Scholar
  43. SWARTZ, D. R., MOSS, R. L. & GREASER, M. L. (1996) Calcium alone does not fully activate the thin filament for S1 binding to rigor myofibrils. Biophys. J. 71, 1891–1904.Google Scholar
  44. SWEITZER, N. K. & MOSS, R. L. (1990) The effect of altered temperature on Ca2+-sensitive force in permeabilized myocardium and skeletal muscle. Evidence for force dependence of thin filament activation. J. Gen. Physiol. 96, 1221–45.Google Scholar
  45. WEBER, A. & MURRAY, J. M. (1973) Molecular control mechanisms in muscle contraction. Physiol. Rev. 53, 612–73.Google Scholar
  46. WILLIAMS, D. L., GREENE, L. E. & EISENBERG, E. (1988) Cooperative turning on of myosin subfragment 1 adenosinetriphosphatase activity by the troponin-tropomyosin-actin complex. Biochemistry 27, 6987–93.Google Scholar
  47. YAMASHITA, H., SATA, M., SUGIURA, S., MOMOMURA, S., SERIZAWA, T. & IIZUKA, M. (1994) ADP inhibits the sliding velocity of fluorescent actin filament on cardiac and skeletal myosins. Circ. Res. 74, 1027–33.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Norio Fukuda
  • Hideaki Fujita
  • Takashi Fujita
  • Shin'ichi Ishiwata

There are no affiliations available

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