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Sodium nitroprusside, a NO donor, modifies Ca2+ transport and mechanical properties in frog skeletal muscle

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Abstract

Recently it has been hypothesized that, in skeletal muscle, NO produced directly by high-frequency stimulation could produce contraction through reactions with thiol groups on the sarcoplasmic reticulum (SR). However, a possible cGMP-mediated relaxing effect, similar to that seen in smooth muscle, has also been demonstrated. We used purified SR preparations and single fibres from frog fast muscles incubated with different concentrations of sodium nitroprusside (SNP) in this study. The results obtained from a long low-frequency stimulation, together with those from a study on Ca2+ transport regulation, showed that the presence of NO precursor induced: an acceleration of the onset of fatigue in single fibres; a decreased vesicular Ca2+ content due to increased Ca2+ release; a shift to open status in SR Ca2+ channels; an increase in SR Ca2+ pump activity. The data presented in this paper seem to indicate that the increased NO in the muscle fibres can influence muscle activity in different ways, perhaps depending on the metabolic status of the muscle and target (filaments, sarcolemma, SR) with which the NO (or its derivatives) acts.

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References

  • BALON, T. W. & NADLER, J. L. (1994) Nitric oxide release is present from incubated skeletal muscle preparation. Appl. Physiol. 77, 2519–21.

    Google Scholar 

  • BREDT, D. S. & SNYDER, S. W. H. (1990) Isolation of nitric oxide synthase, a calmodulin-requiring enzyme. Proc. Natl Acad. Sci. USA 87, 682–5.

    Google Scholar 

  • BRIGGS, F. N., POLAND, J. L. & SOLARO, R. J. (1977) Relative capabilities of sarcoplasmic reticulum in fast and slow mammalian skeletal muscle. J. Physiol. 266, 587–94.

    Google Scholar 

  • FANÒ, G., BELIA, S., FULLE, S., ANGELELLA, P., PANARA, F., MARSILI, V. & PASCOLINI, R. (1989) Functional aspects of calcium transport in sarcoplasmic reticulum vesicles derived from frog skeletal muscle treated with saponin. J. Muscle Res. Cell Motil. 10, 326–30.

    Google Scholar 

  • FANÒ, G., MARSILI, V., PROTASI, F., MARIGGIÒ, M. A., FULLE, S., CECCHINI, E. & MENCHETTI, G. (1992) Relationship between an endogenous calcium binding protein (S-100ab) and Ca2+transport in frog skeletal muscle. Basic and Applied Myology 2, 309–16.

    Google Scholar 

  • FANÒ, G., MENCHETTI, G., DELLA TORRE, G., VOLPI, L., SECCA, T. & ORLACCHIO, A. (1982) Cyclic adenosine monophosphate and cyclic guanosine monophosphate variations during isometric tetanus in frog sartorius muscle. Can. J. Physiol. Pharmacol. 60, 79–83.

    Google Scholar 

  • FANÒ, G., TIJSKENS, P., COSCIA, F., CUCCURULLO, F. & MENCHETTI, G. (1997) The intricate story of nitric oxide as regulator of skeletal muscle activity: a brief report. Current Topics in Pharmacology 3, 247–53.

    Google Scholar 

  • FEELISH, M. & NOACK, E. A. (1987) Correlation between nitric oxide formation during degradation of organic nitrates and activation of guanylate cyclase. Eur. J. Pharmacol. 139, 19–30.

    Google Scholar 

  • FITTS, R. H., WINDER, W. W., BROOKE, M. H., KAISER, K. K. & HOLLOSZY, J. O. (1980) Contractile, biochemical and histochemical properties of thyrotoxic rat soleus muscle. Am. J. Physiol. 238, C15-C20.

    Google Scholar 

  • FORSTERMANN, U. (1994) Biochemistry and molecular biology of nitric oxide synthases. Arzneim.-Forsch./Drug Res. 44, 402–7.

    Google Scholar 

  • GARBERS, D. L. & MURAD, F. (1979) Guanylate cyclase assay methods. Adv. Cyclic Nucleotide Res. 10, 5867.

    Google Scholar 

  • GOPALAKRISHNA, R., CHEN, Z. H. & GUNDIMEDA, U. (1993) Nitric oxide and nitric oxide-generating agents induce a reversible inactivation of protein kinase C activity and phorbol ester binding. J. Biol. Chem. 268, 27180–85.

    Google Scholar 

  • GROZDANOVIC, Z., NAKOS, G., DAHRMANN, G., MAYER, B. & GOSSRAU, R. (1995) Species-independent expression of nitric oxide synthase in the sarcolemma region of visceral and somatic striated muscle fibers. Cell Tissue Res. 281, 493–9.

    Google Scholar 

  • KARAKI, H., OZAKI, H., HORI, M., MITSUI-SAITO, M., HARADA, K., MIYAMOTO, S., NAKAZAWA, H., WON, K. J. & SATO, K. (1997) Calcium movements, distribution and function in smooth muscle. Pharmacol. Rev. 49, 157230.

    Google Scholar 

  • KOBZIK, L., REID, M. B., BREDT, D. S. & STAMLER, J. S. (1994) Nitric oxide in skeletal muscle. Nature 372, 546–8.

    Google Scholar 

  • KOBZIK, L., STRINGER, B., BALLIGAND, J. L., REID, M. B. & STAMLER, J. S. (1995) Endothelial type nitric oxide synthase in skeletal muscle fibers: mitochondrial relationship. Biochem. Biophys. Res. Commun. 211, 375–81.

    Google Scholar 

  • LOMBARDI, V. & MENCHETTI, G. (1984) The maximum velocity of shortening during the early phases of the contraction in frog single muscle fibres. J. Muscle Res. Cell Motil. 5, 503–13.

    Google Scholar 

  • LORENZON, P., GIOVANNELLI, A., RAGOZZINO, D., EUSEBI, F. & RUZZIER, F. (1997) Spontaneous and repetitive calcium transient in C2C12 mouse myotubes during ''in vitro'' myogenesis. Europ. J. Neurosci. 9, 800–809.

    Google Scholar 

  • MANCINELLI, L., FANÒ, G., FERRONI, L., SECCA, T. & DOLCINI, B. M. (1983) Evidence for an inotropic positive action of cGMP during excitation-contraction coupling in frog sartorius muscle. Can. J. Physiol. Pharmacol. 61, 590–94.

    Google Scholar 

  • MARAGOS, C. M., WANG, J. M., HRABIE, J. A., OPPENHEIM, J. J. & KEEFER, K. (1993) Nitric oxide/nucleophile complexes inhibit the in vitro proliferation of A375 melanoma cells via nitric oxide release. Cancer Res. 53, 564–8.

    Google Scholar 

  • MARSILI, V., MANCINELLI, L., MENCHETTI, G., FULLE, S. & FANÒ, G. (1992) S-100ab increases calcium release in purified sarcoplasmic reticulum vesicles of frog skeletal muscle. J. Muscle Res. Cell Motil. 13, 511–15.

    Google Scholar 

  • MCGREW, S. G., WOLLEBEN, C., SIEGEL, P., INOUI, M. & FLEISCHER, S. (1989) Positive cooperativity of ryanodine binding to the calcium release channel of sarcoplasmic reticulum from the heart and skeletal muscle. Biochemistry 28, 168691.

    Google Scholar 

  • MOHAN, P., BRUSAERT, D. L., PAULUS, W. J. & SYS, S. U. (1996) Myocardial contractile response to nitric oxide and cGMP. Circulation 93, 1223–9.

    Google Scholar 

  • MURAD, F., ISHII, K., FORSTERMANN, U., GORSKY, L., KERWIN, J. F., POLLOCK, J. & HELLER, M. (1990) EDRF is an intracellular second messenger and autacoid to regulate cyclic GMP synthesis in many cells. In The Biology and Medicine of Signal Transduction(edited by NISHIZUKA, Y., et al.), pp. 143–64. New York: Raven Press.

    Google Scholar 

  • MURPHY, S., SIMMONS, M. L., AGULLO, L., GARCIA, A., FEINSTEIN, D. L., GALEA, E., REIS, D. J., MINCGOLOMB, D. & SCHWARTZ, J. P. (1993) Synthesis of nitric oxide in CNS glial cells. TINS 16, 323–8.

    Google Scholar 

  • MURRANT, C. L. & BARCLAY, J. K. A.D. (1995) Endothelial cell products alter mammalian skeletal muscle function in vitro. Can. J. Physiol. Pharmacol. 73, 736–41.

    Google Scholar 

  • MURRANT, C. L., WOODLEY, N. E. & BARCLAY, J. K. A.D. (1994) Effect of nitroprusside and endothelium-derived products on slow-twitch skeletal muscle function in vitro. Can. J. Physiol. Pharmacol. 72, 1089–93.

    Google Scholar 

  • NAKANE, M., SCHMIDT, H. H. H. W., POLLOCK, J., FORSTERMANN, U. & MURAD, F. (1983) Cloned human brain nitric oxide synthase is highly expressed in skeletal muscle. FEBS Lett. 316, 175–80.

    Google Scholar 

  • NELSON, M. T., CHENG, H. & RUBART, M. (1995) Relaxation of arterial smooth muscle by calcium sparks. Nature 270, 633–7.

    Google Scholar 

  • PALMER, R. M. J., FERRIGE, A. G. & MONCADA, S. (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327, 5246.

    Google Scholar 

  • REGNIER, M., LORENZ, R. R. & SIECK, G. C. (1992) Effects of oxygen radical scavengers on force production in single living frog skeletal muscle fibers (abstract). FASEB J. 6, A819.

    Google Scholar 

  • REID, M. B., KHAWLI, F. A. & MOODY, M. R. (1993) Reactive oxygen in skeletal muscle: III. Contractility of unfatigued muscle. J. Applied Physiol. 75, 1081–7.

    Google Scholar 

  • SCHATZMANN, H. J. (1973) Dependence on calcium concentration and stoichiometry of the calcium pump in human red cells. J. Physiol. 235, 551–69.

    Google Scholar 

  • SCHERER-SINGLER, U., VINCENT, S. R., KIMURA, H. & MCGEER, E. G. (1983) Demonstration of a unique population of neurons with NADPH diaphorase histochemistry. J. Neurosci. Meth. 9, 229–34.

    Google Scholar 

  • SCHMIDT, H. H. H. W., LOHMANN, S. M. & WALTER, U. (1993) The nitric oxide and cGMP signal transduction system: regulation and mechanism of action. Biochim. Biophys. Acta 1178, 153–75.

    Google Scholar 

  • STOYANOVSKY, D., MURPHY, T., ANNO, P. R., KIM, Y.-M. & SALAMA, G. (1997) Nitric oxide activates skeletal and cardiac ryanodine receptors. Cell Calcium 21, 19–29.

    Google Scholar 

  • STUART, J., PESSAH, I. N., FAVER, T. G. & ASCBRAMSON, J. J. (1992) Photooxidation of skeletal muscle sarcoplasmic reticulum induces rapid calcium release. Archiv. Biochem. Biophys. 292, 512–21.

    Google Scholar 

  • XIONG, H., BUCK, E., STUART, J., PESSAH, I. N., SALAMA, G. & ABRAMSON, J. J. (1992) Rose bengal activates the Ca2+release channel from skeletal muscle sarcoplasmic reticulum. Archiv. Biochem. Biophys. 292, 522–8.

    Google Scholar 

  • WESTERBLAD, H. & ALLEN, D. G. (1993) The contribution of (Ca2+)ito the slowing of relaxation in fatigued single fibres from mouse skeletal muscle. J. Physiol. 468, 729–40.

    Google Scholar 

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Authors
  1. S. Belia
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  2. T. Pietrangelo
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  3. S. Fulle
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  4. G. Menchetti
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  5. E. Cecchini
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  6. M. Felaco
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  7. J. Vecchiet
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  8. G. Fanò
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Belia, S., Pietrangelo, T., Fulle, S. et al. Sodium nitroprusside, a NO donor, modifies Ca2+ transport and mechanical properties in frog skeletal muscle. J Muscle Res Cell Motil 19, 865–876 (1998). https://doi.org/10.1023/A:1005499606155

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