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Action of perchlorate on the voltage dependent inactivation of excitation–contraction coupling in frog skeletal muscle fibres

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Abstract

Perchlorate is an agonist of excitation–contraction coupling (ECC) in skeletal muscle displacing charge movement and release activation towards more negative voltages. Contradictory effects of this compound on the voltage dependent inactivation (VDI) of ECC ranging from no effect to a negative shift have been previously reported. In this study we report the effect of the extracellular application of 8 mM perchlorate to cut frog fibres on: (1) the charge movement that activates release (Q1), (2) the charge movement measured in fibres inactivated by depolarization (Q2) and (3) on the steady state VDI of Q1 and Ca2+ release. Our findings were: (1) The central voltage of Q1 was negatively displaced by perchlorate from −29.0 ± 1.6 to −38.4 ± 1.7 mV (n = 4). The maximum Q1 was not significantly affected while the slope of the Q1 vs. V was increased by perchlorate. (2) The central voltage of Q2 was shifted from −91.6 ± 1.4 to −102.3 ± 1.5 mV (n = 4). (3) The central voltage of the steady state inactivation curve of Q1 went from −39.3 ± 1.8 to −48.6 ± 1.2 mV (mean ± SEM, n = 6). Perchlorate had a paradoxical effect on Ca2+ release, while potentiated the release flux in fibres held at −90 mV (peak release flux increased from 3.9 ± 1.1 to 6.8 ± 1.9 μM/ms, n = 5) it had an inhibitory effect when applied to fibres at a depolarized holding potential (peak release flux decreased from 3.9 ± 0.9 to 2.0 ± 0.5 μM/ms, n = 9). The above findings suggest that the effect on the steady state inactivation is a direct consequence of the negative shift in Q1 activation. The negative shift in the steady state inactivation of Q1 correlated well with the effect on Ca2+ release.

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References

  • Brum G, Rios E (1987) Intramembrane charge movement in frog skeletal muscle fibres. Properties of charge 2. J Physiol 387:489–517

    PubMed  CAS  Google Scholar 

  • Brum G, Fitts R, Pizarro G, Rios E (1988a) Voltage sensors of the frog skeletal muscle membrane require calcium to function in excitation–contraction coupling. J Physiol 398:475–505

    PubMed  CAS  Google Scholar 

  • Brum G, Ríos E, Stefani E (1988b) Effects of extracellular calcium on calcium movements of excitation–contraction coupling in frog skeletal muscle fibres. J Physiol 398:441–473

    PubMed  CAS  Google Scholar 

  • Brum G, Píriz N, De Armas R, Rios R, Stern M, Pizarro G (2003) Differential effects of voltage-dependent inactivation and local anesthetics on kinetic phases of Ca release in frog skeletal muscle. Biophys J 85:245–254

    PubMed  CAS  Google Scholar 

  • Chawla S, Skepper JN, Huang CL (2002) Differential effects of sarcoplasmic reticular Ca(2+)-ATPase inhibition on charge movements and calcium transients in intact amphibian skeletal muscle fibres. J Physiol 539:869–882

    Article  PubMed  CAS  Google Scholar 

  • De Armas R, González S, Brum G, Pizarro G (1998) Effects of 2,3-butanedione monoxime on excitation–contraction coupling in frog twitch fibres. J Muscle Res Cell Motil 19:961–977

    PubMed  Google Scholar 

  • Dulhunty AF, Zhu PH, Patterson MF, Ahern G (1992) Actions of perchlorate ions on rat soleus muscle fibres. J Physiol 448:99–119

    PubMed  CAS  Google Scholar 

  • Fill M, J Copello (2002) Ryanodine receptors calcium channels. Physiol Rev 82:893–922

    PubMed  CAS  Google Scholar 

  • Foulks JG, Perry FA (1979) The effects of temperature, local anaesthetics, pH, divalent cations, and group-specific reagents on repriming and repolarization-induced contractures in frog skeletal muscle. Can J Physiol Pharmacol 57:619–630

    PubMed  CAS  Google Scholar 

  • Foulks JG, Miller JA, Perry FA (1973) Repolarization-induced reactivation of contracture tension in frog skeletal muscle. Can J Physiol Pharmacol 51:324–334

    PubMed  CAS  Google Scholar 

  • Francini F, Stefani E (1989) Decay of calcium current in twitch fibres of the frog is influenced by intracellular EGTA. J Gen Physiol 94:953–969

    Article  PubMed  CAS  Google Scholar 

  • Gallant EM, Taus NS, Fletcher TF, Lentz LR, Louis CF, Mickelson JR (1993) Perchlorate potentiation of excitation–contraction coupling in mammalian skeletal muscles. Am J Physiol 264:C559–C567

    PubMed  CAS  Google Scholar 

  • García J, Pizarro G, Ríos E, Stefani E (1991) Effect of the calcium buffer EGTA on the “hump” component of charge movement in skeletal muscle. J Gen Physiol 97:885–996

    Article  PubMed  Google Scholar 

  • Gomolla M, Gottschalk G, Luttgau HC (1983) Perchlorate-induced alterations in electrical and mechanical parameters of frog skeletal muscle fibres. J Physiol 343:197–214

    PubMed  CAS  Google Scholar 

  • González A, Ríos E (1993) Perchlorate enhances transmission in skeletal muscle excitation–contraction coupling. J Gen Physiol 102:373–421

    Article  PubMed  Google Scholar 

  • Huang CL (1982) Pharmacological separation of charge movement components in frog skeletal muscle. J Physiol 324:375–387

    PubMed  CAS  Google Scholar 

  • Huang CL (1998) The influence of perchlorate ions on complex charging transients in amphibian striated muscle. J Physiol 506:699–714

    Article  PubMed  CAS  Google Scholar 

  • Hui CS, Chandler WK (1991) Q beta and Q gamma components of intramembranous charge movement in frog cut twitch fibres. J Gen Physiol 98:429–464

    Article  PubMed  CAS  Google Scholar 

  • Jong DS, Pape PC, Chandler WK (1995) Effect of sarcoplasmic reticulum calcium depletion on intramembranous charge movement in frog cut muscle fibres. J Gen Physiol 106:659–704

    Article  PubMed  CAS  Google Scholar 

  • Kovacs L, Ríos E, Schneider MF (1983) Measurement and modification of free calcium transients in frog skeletal muscle fibres by metallochromic indicator dye. J Physiol 343:161–196

    PubMed  CAS  Google Scholar 

  • Luttgau HC, Gottschalk G, Kovacs L, Fuxreiter M (1983) How perchlorate improves excitation–contraction coupling in skeletal muscle fibres. Biophys J 43(2):247–249

    PubMed  CAS  Google Scholar 

  • Ma J, Anderson K, Shirokov R, Levis R, Gonzalez A, Karhanek M, Hosey MM, Meissner G, Rios E (1993) Effects of perchlorate on the molecules of excitation–contraction coupling of skeletal and cardiac muscle. J Gen Physiol 102(3):423–448

    Article  PubMed  CAS  Google Scholar 

  • Martell AE, Smith RM (1982) Critical stability constants, vol 4. Plenum Press, New York

    Google Scholar 

  • Melzer W, Ríos E, Schneider MF (1984) Time course of calcium release and removal in skeletal muscle fibres. Biophys J 45:637–641

    PubMed  CAS  Google Scholar 

  • Oba T (1997) Niflumic acid differentially modulates two types of skeletal ryanodine-sensitive Ca2+-release channels. Am J Physiol 273:C1588–C1595

    PubMed  CAS  Google Scholar 

  • Pape PC, Jong DS, Chandler WK (1996) A slow component of intramembranous charge movement during sarcoplasmic reticulum calcium release in frog cut muscle fibres. J Gen Physiol 107:79–101

    Article  PubMed  CAS  Google Scholar 

  • Percival AL, Williams AJ, Kenyon JL, Grinsell MM, Airey JA, Sutko JL (1994) Chicken skeletal muscle ryanodine receptor isoforms: ion channel properties. Biophys J 67(5):1834–1850

    Article  PubMed  CAS  Google Scholar 

  • Piriz N, Brum G, Pizarro G (2006) Differential sensitivity to perchlorate and caffeine of tetracaine-resistant Ca2+ release in frog skeletal muscle. J Muscle Res Cell Motil 27:221–234

    Article  PubMed  CAS  Google Scholar 

  • Pizarro G, Csernoch L, Uribe I, Rodríguez M, Ríos E (1991) The relationship between Q gamma and Ca release from the sarcoplasmic reticulum in skeletal muscle. J Gen Physiol 97:913–947

    Article  PubMed  CAS  Google Scholar 

  • Protasi F, Paolini C, Nakai J, Beam KG, Franzini-Armstrong C, Allen PD (2002) Multiple regions of RyR1 mediate functional and structural interactions with alfa(1S)-dihydropyridine receptors in skeletal muscle. Biophys J 83:3230–3244

    PubMed  CAS  Google Scholar 

  • Rios E, Pizarro G (1991) Voltage sensor of excitation–contraction coupling in skeletal muscle. Physiol Rev 71:849–908

    PubMed  CAS  Google Scholar 

  • Rios E, Karhanek M, Ma J, Gonzalez A (1993) An allosteric model of the molecular interactions of excitation–contraction coupling in skeletal muscle. J Gen Physiol 102:449–481

    Article  PubMed  CAS  Google Scholar 

  • Schneider MF, Simon BJ, Szucs G (1987) Depletion of calcium from the sarcoplasmic reticulum during calcium release in frog skeletal muscle. J Physiol 392:167–192

    PubMed  CAS  Google Scholar 

  • Shirokova N, García J, Pizarro G, Ríos E (1996) Ca2+ release from the sarcoplasmic reticulum compared in amphibian and mammalian skeletal muscle. J Gen Physiol 107:1–18

    Article  PubMed  CAS  Google Scholar 

  • Squecco R, Bencini C, Piperio C, Francini F (2004) L-type Ca2+ channel and ryanodine receptor cross-talk in frog skeletal muscle. J Physiol 555:137–152

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was funded by a grant from CSIC to GP. We want to thank Mr. F. Olivera for his help in some of the experiments.

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  1. Departamento de Biofísica, Facultad de Medicina, Universidad de la República, Gral. Flores 2125, Montevideo, Uruguay

    Nazira Píriz & Gonzalo Pizarro

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  1. Nazira Píriz
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  2. Gonzalo Pizarro
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Correspondence to Gonzalo Pizarro.

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Píriz, N., Pizarro, G. Action of perchlorate on the voltage dependent inactivation of excitation–contraction coupling in frog skeletal muscle fibres. J Muscle Res Cell Motil 28, 315–328 (2007). https://doi.org/10.1007/s10974-008-9126-0

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  • DOI: https://doi.org/10.1007/s10974-008-9126-0

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