Abstract
The effects of adrenaline and the β-adrenergic agonist isoprenaline on K+-evoked tension (K+-contracture) and Ba2+ current were investigated in chicken slow (anterior latissimus dorsi (ald)) muscle using isometric-tension measurements and current recording. Addition of adrenaline (10−7–10−5M) or isoprenaline (10−6–10−5 M) to the bath reduced the amplitude of the K+-contractures. These effects were blocked by the β-antagonist propranolol (5 × 10−6 M). External application of a cAMP analogue (8-bromo cyclic AMP; 1 × 10−4 M) also decreased the amplitude of the K+-contractures. To analyze the possible relationship between the induced tension reduction and effects on sarcolemmal Ca2+ channels, a slow action potential and a slow inward membrane current were studied in intact ald chicken muscle fibres. When the ald muscle was immersed in a Na+- and Cl−-free solution containing Ba2+ and depolarizing pulses were delivered from a −80 mV holding potential, the muscle fibres exhibited a small, slow Ba2+-dependent potential (observed at about −26 mV, peak amplitude, around −10 mV). The response was blocked by the addition of Co2+ (5 mM) or Cd2+ (2 mM). Using the three-microelectrode voltage-clamp technique, a slow inward membrane current underlying the Ba2+ potential could be discerned. The current had a mean threshold of −60 mV, reached maximum at about −5 mV and ranged from ca. 9 to 19 μA/cm2 (depending on the external Ba2+ concentration). It had a mean reversal potential of +45 mV. The Ba2+ inward current was diminished when adrenaline or isoprenaline was added to the bath (1 × 10−5 M); however, this decrease did not occur when propranolol was present (5 × 10−6 M). These results suggest that the decreases in the tension of K+-contractures induced by adrenaline and isoprenaline may occur through β-adrenergic effects on sarcolemmal Ca2+ channels in ald chicken slow muscle fibres.
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References
Adrian RH, Chandler WK and Hodgkin AL (1970) Voltage clamp experiments in striated muscle fibres. J Physiol (Lond ) 208: 607–644.
Arreola J, Calvo J, Garcia MC and Sanchez JA (1987) Modulation of calcium channels of twitch skeletal muscle fibres of the frog by adrenaline and cyclic adenosine monophosphate. J Physiol (Lond) 393: 307–330.
Bean BP (1989) Classes of calcium channels in vertebrate cells. Ann Rev Physiol 51: 367–384.
Beaty G and Stefani E (1976) Calcium dependent electrical activity in twitch muscle fibres of the frog. Proc Roy Soc B 194: 141–150.
Bowman WC (1980) Effects of adrenergic activators and inhibitors on the skeletal muscles. In: Szekeres L (ed) Handbook of Experimental Pharmacology. pp. 47–128 Springer Verlag, Berlin.
Cairns SP and Dulhunty A (1993) The effects of ?-adrenoceptor activation on contraction in isolated fast-and slow-twitch skeletal muscle fibres of the rat. Br J Pharmacol 110: 1133–1141.
Catterall WA (1998) Structure and function of voltage-sensitive ion channels. Science 242: 50–61.
Dolphin AC, Wootton JF, Scott RH and Trentham DR (1988) Photoactivation of intracellular guanosine triphosphate analogues reduces the amplitude and slows the kinetics of voltage-activated calcium channel currents in sensory neurons. Pflugers Arch 411(6): 628–636.
Fabiato A and Fabiato A (1979) Cyclic AMP-induced enhancement of calcium accumulation by the sarcoplasmic reticulum with no modification of the sensitivity of the myofilaments to calcium in skinned fibres from a fast skeletal muscle. Biochim Biophys Acta 539: 253–260.
Garcia MC and Escamilla-Sanchez J (1994) Positive inotropic effect of adrenaline on potassium contractures in tonic skeletal muscle fibres of the frog. Can J Physiol Pharm 72(12): 1580–1585.
Gilly WF and Hui S (1980) Membrane electrical properties of frog slow muscle fibres. J Physiol (Lond) 301: 157–173.
Ginsborg BL (1960) Some properties of avian skeletal muscle fibres with multiple neuromuscular junctions. J Physiol (Lond) 154: 581–598.
Glossman HD, Ferry R and Rombusch M (1984) Molecular pharmacology of the calcium channel: evidence for subtypes, multiple drug-receptor sites, channel subunits, and development of a radiiodinated 1,4,dihydropyridine calcium channel label, [125] iodipine. J Cardiovasc Pharmacol 6: 608–621.
Gonzalez-Serratos H, Hill L and Valle-Aguilera R (1981) Effects of catecholamines and cyclic AMP on excitation-contraction coupling in isolated skeletal muscle fibres of the frog. J Physiol (Lond) 315: 267–282.
Hagiwara S and Byerly L (1981) Membrane biophysics of calcium currents. Fed Proc 40: 2220–2225.
Hess A (1970). Vertebrate slow muscle fibres. Physiol Rev 50: 40–63.
Hoffman, BB and Lefkowitz RJ (1996) Catecholamines, sympathomimetic drugs, and adrenergic receptor antagonists. In: Goodman-Gilman A (ed) The pharmacological Basis of Therapeutics. (9th edn, CAP. 10. pp. 199–248) McGraw-Hill, WA.
Huerta M and Stefani E (1981) Potassium and caffeine contractures in fast and slow muscles of the chicken. J Physiol (Lond) 318: 181–189.
Huerta M and Stefani E (1986) Calcium action potentials and calcium currents in tonic muscle fibres of the frog (Rana pipiens). J Physiol (Lond) 372: 293–301.
Huerta M, Muñiz J, Trujillo X and Lomelí J (1991) Adrenergic modulation of the K+ contractures in tonic skeletal muscle fibres of the frog. Jpn J Physiol 41: 851–860.
Huerta M, Trujillo X and Vásquez C (1997) ß-adrenergic modulation of Ba2+ currents and K+ contractures in frog slow skeletal muscle fibres. Am J Physiol Cell Physiol 272: C77–C81.
Hullin R, Biel M, Flockerzi V and Hoffmann F (1993) Tissue-specific expression of calcium channels. Trends in Cardiovasc Med 3: 48–53.
Kano M (1975) Development of excitability in embryonic chick skeletal muscle cells. J Cell Physiol 86: 503–510.
Kano M, Wakuta K and Satoh R (1987) Calcium channel components of action potential in chick skeletal muscle cells developing in culture. Brain Res 429: 233–240.
Kano M, Wakuta K and Satoh R (1989) Two components of calcium channel current in embryonic chick skeletal muscle cells developing in culture. Dev Brain Res 47: 101–112.
Kikuchi T and Schmidt H (1983) Changes in resting and contractile properties of chicken muscle following denervation. Biom Res 4: 303–314.
Lalli MJ, Shimizu S, Sutli. RL, Kranias EG and Paul RJ (1999) [Ca2+]i homeostasis and cyclic nucleotide relaxation in aorta of phospholamban-deficient mice. Am J Physiol 277(3): H963–970.
Lamb GD and Walsh T (1987) Calcium currents, charge movement and dihydropyridine binding in fast-and slow-twitch muscles of rat and rabbit. J Physiol (Lond) 393: 595–617.
Oota I and Nagai T (1977) Effects of catecholamines on excitation-contraction coupling in frog single twitch fiber. Jpn J Physiol 27(2): 195–213.
Page SG (1969) Structure and some contractile properties of fast and slow muscles of the chicken. J Physiol (Lond) 205: 131–145.
Sanchez JA and Stefani E (1978) Inward calcium current in twitch muscle fibres of the frog. J Physiol (Lond) 283: 197–209.
Satoh R, Nakabayashi Y and Kano M (1991) Pharmacological properties of two types of calcium channel in embryonic chick skeletal muscle cells in culture. Neurosci Lett 122: 233–236.
Schmid A, Renaud JF and Lazdunski M (1985) Short term and long term effects of beta-adrenergic effectors and cyclic AMP on nitrendipine-sensitive voltage-dependent Ca2+ channels of skeletal muscle. J Biol Chem 260: 13041–13046.
Schwartz A, Entman ML, Kaniike,K, Lane LK, Van Winkle WB and Borner EP (1976) The rate of calcium uptake into sarcoplasmic reticulum of cardiac muscle and skeletal muscle. Effects of cyclic AMP-dependent protein kinase and phosphorylase b kinase. Biochim Biophys Acta 426: 57–72.
Somasundaram B and Tregear RT (1993) Isoproterenol and GTP gamma S inhibit L-type calcium channels of differentiating rat skeletal muscle cells. J Muscle Res Cell Motil 14(3): 341–346.
Somlyo AP and Somlyo AV (1969) Pharmacology of excitation-contraction coupling in vascular smooth muscle and in avian slow muscle. Fed Proc 28(5): 1634–1642.
Standen NB and Standfield PR (1982) A binding-site model for calcium channel inactivation that depends on calcium entry. Proc Roy Soc B 217: 101–110.
Stull JT, Blumenthal DK and Cooke R (1980) Regulation of contraction by myosin phosphorylation. A comparison between smooth and skeletal muscles. Biochem Pharmacol 29(19): 2537–2543.
Tashiro N (1973) Effects of isoprenaline on contractions of directly stimulated fast and slow skeletal muscles of the guinea-pig. Br J Pharmacol 48(1): 121–131.
Tomita T (1975) Action of catecholamines on skeletal muscle. In: Greep RO and Astwood EB (eds) Handbook of Physiology, Section 7: Endocrinology. (pp. 537–552) American Physiological Society, Washington, DC.
Vásquez C, Huerta M, Trujillo X, Marín JL, Andrade F and Trujillo-Hernández B (2001) Measurement of Ca2+ currents in intact slow skeletal muscle fibers of the frog by the three-microelectrode technique. Br Res Protocols 8(3): 208–211.
Welling A, Kwan YW, Boose E, Flockerzi V, Hoffmann F and Kass RS (1993) Subunit-dependent modulation of recombinant L-type calcium channels. Molecular basis for dihydropyridine tissue selectivity. Circ Res 73: 974–980.
Williams JH and Barnes WS (1989) The positive effect of adrenaline on skeletal muscle: a brief review. Muscle and Nerve 12: 968–975.
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Trujillo, X., Huerta, M., Vásquez, C. et al. Adrenaline diminishes K+ contractures and Ba2+-current in chicken slow skeletal muscle fibres. J Muscle Res Cell Motil 23, 157–165 (2002). https://doi.org/10.1023/A:1020295702288
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DOI: https://doi.org/10.1023/A:1020295702288