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Effect of activation of protein kinase C on excitation-contraction coupling in frog twitch muscle fibres

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Abstract

Intracellular Ca2+ transients were recorded from frog twitch muscle fibres in response to voltage-clamp depolarizing pulses, using arsenazo III as an intracellular Ca2+ indicator. The effect of the activation of protein kinase C (PKC) on the Ca2+ transients was studied. With 1 μM phorbol 12,13-dibutyrate (PDBu), a PKC activator, the peak of the Ca2+ transients increased to about 120% of control during the first 0.5 h, and then decreased gradually to a plateau of 44% of control within the following 2 h. This effect of PDBu could be alleviated significantly by PKC inhibitors, 10 μM polymyxin B (PMB) or 30 μM 1-(5-isoquinolinylsulphonyl)-2-methyl-piperazine (H-7). Moreover, PDBu caused an upward shift of the strength/duration curve. In Li+-loaded muscle fibres the Ca2+ transients could not fully recover after 80 mM K+ exposure for 15 min, while the post-K+ Ca2+ transients could be completely restored in the fibres not loaded with Li+. In the presence of 10 μM PMB or 30 μM H-7, a full restoration of the post-K+ Ca2+ transients was seen in Li+-loaded fibres. PMB supplemented after high-K+ exposure also could result in a complete recovery of the post-K+ Ca2+ transients in Li+-loaded fibres. The role of PKC in modulating excitation-contraction coupling in frog twitch muscle fibres is clearly indicated, but the mechanism(s) and physiological significance remain to be established.

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References

  1. 1.

    Ashley CC, Mulligan IP, Lea TJ (1991) Ca2+ and activation mechanism in skeletal muscle. Q Rev Biophys 24:1–73

  2. 2.

    Baba K, Baron CB, Coburn RF (1989) Phorbol ester effects on coupling mechanisms during cholinergic contraction of swine tracheal smooth muscle. J Physiol (Lond) 412:23–42

  3. 3.

    Berridge MJ (1987) Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu Rev Biochem 56:159–193

  4. 4.

    Chang CF, Gutierrez LM, Mundina-Weilenmann C, Hosey MM (1991) Dihydropyridine-sensitive calcium channels from skeletal muscle. II. Functional effects of differential phosphorylation of channel subunits. J Biol Chem 266:16 395–16 400

  5. 5.

    Chilvers ER, Nahorski SR (1990) Phosphoinositide metabolism in airway smooth muscle. Am Rev Respir Dis 141: S137-S140

  6. 6.

    Cleland PJF, Appleby GJ, Rattigan S, Clark MG (1989) Exercise-induced translocation of protein kinase C and production of diacylglycerol and phosphatidic acid in rat skeletal muscle in vivo. J Biol Chem 264:17 704–17 711

  7. 7.

    Dong Z, Zhu PH (1994) Effect of protein kinase C modulators on phosphoinositide metabolism in frog skeletal muscle. Neurosci Lett [Suppl] (in press)

  8. 8.

    Drammond AH, Raeburn CA (1984) The interaction of lithium with thyrotropin-releasing hormone-stimulated lipid metabolism in GH3 pituitary tumour cells. Enhancement of stimulated 1,2-diacylglycerol formation. Biochem J 224:129–136

  9. 9.

    Dulhunty AF (1992) The voltage-activation of contraction in skeletal muscle. Prog Biophys Mol Biol 57:181–223

  10. 10.

    Ferris CD, Huganir RL, Bredt DS, Cameron AM, Snyder SH (1991) Inositol trisphosphate receptor: Phosphorylation by protein kinase C and calcium calmodulin-dependent kinases in reconstituted lipid vesicles. Proc Natl Acad Sci USA 88:2232–2235

  11. 11.

    Fu DX, Zhu PH (1993) Depression of calcium transients after exposure to high K+ solution in Li+ loaded frog twitch muscle fibres. Sci China B 36:204–213

  12. 12.

    Godfrey PP (1989) Potentiation by lithium of CMP-phosphatidate formation in carbachol-stimulated rat cerebral-cortical slices and its reversal by myo-inositol. Biochem J 258:621–624

  13. 13.

    Jaimovich E (1991) Chemical transmission at the triad: InsP3? J Muscle Res Cell Motil 12:316–320

  14. 14.

    Ma J, Gutierrez LM, Hosey MM, Rios E (1992) Dihydropyridine-sensitive skeletal muscle Ca channels in polarized planar bilayers. 3. Effect of phosphorylation by protein kinase C. Biophys J 63:639–647

  15. 15.

    Miledi R, Parker I, Zhu PH (1982) Calcium transients evoked by action potentials in frog twitch muscle fibres. J Physiol (Lond) 333:655–679

  16. 16.

    Miledi R, Parker I, Zhu PH (1983) Calcium transients studied under voltage-clamp control in frog twitch muscle fibres. J Physiol (Lond) 340:649–680

  17. 17.

    Nishizuka Y, Shearman MS, Oda T, Berry N, Shinomura T, Asaoka Y, Ogita K, Koide H, Kikkawa U, Kishimoto A, Kose A, Saito N, Tanaka C (1991) Protein kinase C family and nervous function. In: Gispen WH, Routtenberg A (eds) Progress in brain research, vol 89. Elsevier Science, Amsterdam, pp 125–141

  18. 18.

    Numann RE, Hauschka SD, Scheuer T, Catterall WA (1992) Modulation of skeletal muscle Na channel by protein kinase C. Biophys J 61:112a

  19. 19.

    Rios E, Ma J, Gonzalez A (1991) The mechanical hypothesis of excitation-contraction (EC) coupling in skeletal muscle. J Muscle Res Cell Motil 12:127–135

  20. 20.

    Sabbadini RA, Salviati G, Dahms AS, Paolini PJ, Cunnigham HB, Ryan M (1991) The involvement of protein kinase C, phorbol esters and diacylglycerols in the modulation of striated muscle calcium release. Biophys J 59:10a

  21. 21.

    Salviati G, Cunningham B, Jachec-Schmidt C, Kang JJ, Dahms AS, Sabbadini R (1990) Localization of protein kinase C in junctional transverse tubule membranes. Biophys J 57:343a

  22. 22.

    Stephenson EW, Lerner SS (1987) Exogenous diacylglycerol and sphingosine modulate excitation-contraction coupling in skinned muscle fibers. J Gen Physiol 90:39a

  23. 23.

    Stephenson EW, Lerner SS (1988) Protein kinase C (PKC) modulators influence E-C coupling steps in skinned muscle fibers. Biophys J 53:468a

  24. 24.

    Timerman AP, Chadwick CC, Fleischer S (1990) Phosphorylation states of skeletal muscle ryanodine receptor and smooth muscle inositol 1,4,5-trisphosphate receptor (IP3Rec). Biophys J 57:286a

  25. 25.

    Wang XF, Hajizadeh S, Xu ZM, Yang LP, Zhang XD, Xie RY, Zhu PH (1992) Effect of bapta-AM loading on myoplasmic resting free calcium and calcium transients in frogh twitch muscle fibres. Chin J Physiol Sci 8:291–299

  26. 26.

    Woods NM, Cuthbertson KSR, Cobbold PH (1987) Phorbolester-induced alterations of free calcium ion transients in single rat hepatocytes. Biochem J 246:619–623

  27. 27.

    Zhu PH (1988) Effect of calcium free solution or gallopamil (D600) on excitation-contraction coupling in frog twitch muscle fibres. Chin J Physiol Sci 4:295–309

  28. 28.

    Zhu PH, Fu DX (1990) Effect of prolonged in vitro lithium treatment on calcium transients in frog twitch muscle fibres and its reversal by exogenous myo-inositol. Neuroscience 39:271–278

  29. 29.

    Zhu PH, Wang XF, Fu DX, Xu ZM (1993) Effect of lithium ions on basal free calcium and calcium transients of frog twitch muscle fibers. In: Birch NJ, Padgham C, Hughes MS (eds) Lithium in medicine and biology. Marius, Carnforth, pp 233–244

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Correspondence to P. H. Zhu.

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Wang, X.F., Zhu, P.H. Effect of activation of protein kinase C on excitation-contraction coupling in frog twitch muscle fibres. Pflügers Arch. 428, 224–231 (1994). https://doi.org/10.1007/BF00724501

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Key words

  • Skeletal muscle
  • Excitation-contraction coupling
  • Protein kinase C