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Dependence of intracellular free calcium and tension on membrane potential and intracellular pH in single crayfish muscle fibres

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Abstract

The dependence of intracellular free calcium ([Ca2+]i) and tension on membrane potential and intracellular pH (pHi) was studied in single isolated fibres of the crayfish claw-opener muscle using ion-selective microelectrodes. Tension (T) was quantified as a percentage of the maximum force, or as force per cross-sectional area (N/cm2). In resting fibres, pHi had a mean value of 7.06. Contractions evoked by an increase extracellular potassium ([K+]0) produced a fall in pHi of 0.01–0.05 units. The lowest measured levels of resting [Ca2+]i corresponded to a pCai (= −log [Ca2+]i) of 6.8. Intracellular Ca2+ transients recorded during K+-induced contractions did not reveal any distinct threshold for force development. Both the resting [Ca2+]i and resting tension were decreased by an intracellular alkalosis and increased by an acidosis. The sensitivity of resting tension to a change in pHi (quantified as −dT/ dpHi) showed a progressive increase during a fall in pHi within the range examined (pHi 6.2–7.5). The pHi/[Ca2+]i and pHi/tension relationships were monotonic throughout the multiphasic pHi change caused by NH4Cl. A fall of 0.5–0.6 units in pHi did not produce a detectable shift in the pCai/tension relationship at low levels of force development. The results indicate that resting [Ca2+]i is slightly higher than the level required for contractile activation. They also show that the dependence of tension on pHi in crayfish muscle fibres is attributable to a direct H+ and Ca2+ interaction at the level of Ca2+ sequestration and/or transport. Finally, the results suggest that in situ, the effect of pH on the Ca2+ sensitivity of the myofibrillar system is not as large as could be expected on the basis of previous work on skinned crustacean muscle fibres.

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References

  • Allen DG, Orchard CH (1983) The effects of changes of pH on intracellular calcium transients in mammalian cardiac muscle. J Physiol (Lond) 333: 555–567

    Google Scholar 

  • Allen DG, Eisner DA, Orchard CH (1984) Factors influencing intracellular calcium concentration in quiescent ferret ventricular muscle. J Physiol (Lond) 350: 615–630

    Google Scholar 

  • Alvarez-Leefmans FJ, Rink TJ, Tsien RY (1981) Free calcium ions in neurones of Helix aspersa measured with ion-selective microelectrodes. J Physiol (Lond) 315: 531–548

    Google Scholar 

  • Ashley CC (1978) Calcium ion regulation in barnacle muscle fibers and its relation to force development. Ann NY Acad Sci 307: 308–329

    PubMed  Google Scholar 

  • Ashley CC, Moisescu DG (1977) Effect of changing the composition of the bathing solution upon the isometric tension-pCa relationship in bundles of crustacean myofibrils. J Physiol (Lond) 270: 627–652

    Google Scholar 

  • Ashley CC, Ridgway EB (1970) On the relationships between membrane potential, calcium transient and tension in single barnacle muscle fibres. J Physiol (Lond) 209: 105–130

    Google Scholar 

  • Ashley CC, Rink TJ, Tsien RY (1978) Changes in free Ca during muscle contraction, measured with an intracellular Ca-selective electrode. J Physiol (Lond) 280: 27P

  • Atwood HL, Hoyle G, Smyth T Jr, (1965) Mechanical and electrical responses of single innervated crab-muscle fibres. J Physiol (Lond) 180: 449–482.

    Google Scholar 

  • Bers DM, Ellis D (1982) Intracellular calcium and sodium activity in sheep heart Purkinje fibres. Effect of changes of external sodium and intracellular pH. Pflügers Arch 393: 171–178

    Google Scholar 

  • Blanchard EM, Solaro RJ (1984) Inhibition of the activation and troponin calcium binding of dog cardiac myofibrils by acidic pH. Circ Res 55: 382–391

    PubMed  Google Scholar 

  • Blinks JR, Rüdel R, Taylor SR (1978) Calcium transients in isolated amphibian skeletal muscle fibres: detection with aequorin. J Physiol (Lond) 277: 291–323

    Google Scholar 

  • Bountra C, Kaila K, Vaughan-Jones RD (1988a) Effect of repetitive activity upon intracellular pH, sodium and contraction in sheep cardiac Purkinje fibres. J Physiol (Lond) 398: 341–360

    Google Scholar 

  • Bountra C, Kaila K, Vaughan-Jones RD (1988b) Mechanism of rate-dependent pH changes in the sheep cardiac Purkinje fibre. J Physiol (Lond) 406: 483–501

    Google Scholar 

  • Chih CP, Ellington WR (1985) Metabolic correlates of intracellular pH change during rapid contractile activity in a molluscan muscle. J Exp Zool 236: 27–34

    Google Scholar 

  • Cooke R, Franks K, Luciani GB, Pate E (1988) The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate. J Physiol (Lond) 395: 77–97

    Google Scholar 

  • Dawson MJ, Gadian DG, Wilkie DR (1977) Contraction and recovery of living muscles studied by 31P nuclear magnetic resonance. J Physiol (Lond) 267: 703–735

    Google Scholar 

  • DiPolo R, Beaugé L (1982) The effect of pH on Ca2+ extrusion mechanisms in dialyzed squid axons. Biochim Biophys Acta 688: 237–245

    Google Scholar 

  • Dudel J, Rüdel R (1969) Voltage controlled contractions and current voltage relations of crayfish muscle fibres in chloride-free solutions. flügers Arch 308: 291–314

    Google Scholar 

  • Dudel J, Morad M, Rüdel R (1968) Contractions of single crayfish muscle fibres induced by controlled changes of membrane potential. Pflügers Arch 299: 38–51

    Google Scholar 

  • Fabiato A, Fabiato F (1978) Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiac and skeletal muscles. J Physiol (Lond) 276: 233–255

    Google Scholar 

  • Fry CH, Poole-Wilson PA (1981) Effects of acid-base changes on excitation and contraction coupling in guinea-pig and rabbit cardiac ventricular muscle. J Physiol (Lond) 313: 141–160

    Google Scholar 

  • Galler S, Moser H (1986) The ionic mechanism of intracellular pH regulation in crayfish muscle fibres. J Physiol (Lond) 374: 137–151

    Google Scholar 

  • Girardier L, Reuben JP, Brandt PW, Grundfest H (1963) Evidence for anion-permselective membrane in crayfish muscle fibers and its possible role in excitation-contraction coupling. J Gen Physiol 47: 189–214

    Google Scholar 

  • Hammelsbeck M, Rathmayer W (1989) Intracellular Na+, K+ and Cl− activity in tonic and phasic muscle fibers of the crab Eriphia. Pflügers Arch 413: 487–492

    Google Scholar 

  • Harvey DJ, Godber JF, Timmerman MP, Castell LM, Ashley CC (1985) Measurement of free Ca2+ changes and total Ca2+ release in a single striated muscle fibre using the fluorescent indicator quin 2. Biochem Biophys Res Commun 128: 1180–1189

    PubMed  Google Scholar 

  • Hoyle G (1968) Resting tension, “negative” contraction and “break” contraction in specialised crustacean muscle fibres. J Exp Zool 167: 551–566

    Google Scholar 

  • IUPAC (1976) Recommendations for nomenclature of ion-selective electrodes. Pure Appl Chem 48: 127–132

    Google Scholar 

  • Kaila K, Vaughan-Jones RD (1987) Influence of sodium-hydrogen exchange on intracellular pH, sodium and tension in sheep cardiac Purkinje fibres. J Physiol (Lond) 390: 93–118

    Google Scholar 

  • Kaila K, Voipio J (1985) A simple method for dry bevelling of micropipettes used in the construction of ion-selective microelectrodes. J Physiol (Lond) 369: 8P

  • Kaila K, Vaughan-Jones RD, Bountra C (1987) Regulation of intra-cellular pH in sheep cardiac Purkinje fibre: interactions among Na+, H+ and Ca2+. Can J Physiol Pharmacol 65: 963–969

    PubMed  Google Scholar 

  • Kaila K, Mattsson K, Voipio J (1989) Fall in intracellular pH and increase in resting tension induced by a mitochondrial uncoupling agent in crayfish muscle. J Physiol (Lond) 408: 271–293

    Google Scholar 

  • Kim D, Smith TW (1988) Cellular mechanisms underlying calcium-proton interactions in cultured chick ventricular muscle cells. J Physiol (Lond) 398: 391–410

    Google Scholar 

  • Lännergren J, Westerblad H (1989) Maximum tension and force-velocity properties of fatigued, single Xenopus muscle fibres studied by caffeine and high K+. J Physiol (Lond) 409: 473–490

    Google Scholar 

  • Lea TJ, Ashley CC (1978) Increase in free Ca2+ in muscle after exposure to CO2. Nature 275: 236–238

    PubMed  Google Scholar 

  • Lea TJ, Ashley CC (1981) Carbon dioxide or bicarbonate ions release Ca2+ from internal stores in crustacean myofibrillar bundles. J Membr Biol 61: 115–125

    PubMed  Google Scholar 

  • Lee CO, Uhm DY, Dresdner K (1980) Sodium-calcium exchange in rabbit heart muscle cells: direct measurement of sarcoplasmic Ca2+ activity. Science 209: 699–701

    Google Scholar 

  • López JR, Alamo L, Caputo C, DiPolo R, Vergara J (1983) Determination of ionic calcium in frog skeletal muscle fibers. Biophys J 43: 1–4

    Google Scholar 

  • Mainwood GW, Renaud JM, Mason MJ (1987) The pH dependence of the contractile response of fatigued skeletal muscle. Can J Physiol Pharmacol 65: 648–658

    Google Scholar 

  • Marban E, Rink TJ, Tsien RW, Tsien RY (1980) Free calcium in heart muscle at rest and during contraction measured with Ca2+-sensitive microelectrodes. Nature 286: 845–850

    PubMed  Google Scholar 

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

    Google Scholar 

  • Moss RL, Swinford AE, Greaser ML (1983) Alterations in the Ca2+ sensitivity of tension development by single skeletal muscle fibres at stretched lengths. Biophys J 43: 115–119

    Google Scholar 

  • Nosek TM, Fender KY, Godt RE (1987) It is diprotonated inorganic phosphate that depresses force in skinned skeletal muscle fibers. Science 236: 191–193

    Google Scholar 

  • Oehme M, Kessler M, Simon W (1976) Neutral carrier Ca2+-microelectrode. Chimia (Aarau) 30: 204–206

    Google Scholar 

  • Podolsky RJ, Schoenberg M (1983) Force and shortening in skeletal muscle. In: Peachey LD (ed) Handbook of physiology, section 10, Skeletal muscle. The American Physiological Society, Bethesda, pp 173–187

    Google Scholar 

  • Renaud JM, Allard Y, Mainwood GW (1986) Is the change in intracellular pH during fatigue large enough to be the main cause of fatigue? Can J Physiol Pharmacol 64: 764–767

    PubMed  Google Scholar 

  • Roos A, Boron WF (1981) Intracellular pH. Physiol Rev 61: 296–433

    Google Scholar 

  • Seo YK, Yoshizaki K, Morimoto T (1983) A 1H-nuclear magnetic resonance study on lactate and intracellular pH in frog muscle. Jpn J Physiol 33: 721–731

    Google Scholar 

  • Sharp AP, Thomas RC (1981) The effects of cloride substitution on intracellular pH in crab muscle. J Physiol (Lond) 312: 71–80

    Google Scholar 

  • Sheu S-S, Fozzard HA (1982) Transmembrane Na+ and Ca2+ electrochemical gradients in cardiac muscle and their relationship to force development. J Gen Physiol 80: 325–351

    Google Scholar 

  • Stephenson DG, Williams DA (1980) Activation of skinned arthropod muscle fibres by Ca2+ and Sr2+. J Muscle Res Cell Motil 1: 73–87

    PubMed  Google Scholar 

  • Taylor PS, Thomas RC (1984) The effect of leakage on microelectrode measurements of intracellular sodium activity in crab muscle fibres. J Physiol (Lond) 352: 539–550

    Google Scholar 

  • Tsien RY (1983) Intracellular measurements of ion activities. Annu Rev Biophys Bioeng 12: 91–116

    Article  Google Scholar 

  • Tsien RY, Rink TJ (1981) Ca2+-selective electrodes: a novel PVC-gelled neutral carrier mixture compared with other currently available sensors. J Neurosci Methods 4: 73–86

    PubMed  Google Scholar 

  • Vaughan-Jones RD, Eisner DA, Lederer WJ (1987) Effects of changes of intracellular pH on contraction in sheep cardiac Purkinje fibres. J Gen Physiol 89: 1015–1032

    Article  PubMed  Google Scholar 

  • Weast RC (ed) (1988) CRC handbook of chemistry and physics, 69th edn. CRC Press, Boca Raton

    Google Scholar 

  • Weingart R, Hess P (1984) Free calcium in sheep cardiac tissue and frog skeletal muscle measured with Ca2+-selective microelectrodes. Pflügers Arch 402: 1–9

    Google Scholar 

  • Westerblad H, Lännergren J (1988) The relation between force and intracellular pH in fatigued, single Xenopus muscle fibres. Acta Physiol Scand 133: 83–89

    PubMed  Google Scholar 

  • Zachar J, Zacharová D (1966) Potassium contractures in single muscle fibres of the crayfish. J Physiol (Lond) 186: 596–618

    Google Scholar 

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  1. Department of Zoology, Division of Physiology, University of Helsinki, Arkadiankatu 7, SF-00100, Helsinki, Finland

    K. Kaila & J. Voipio

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  1. K. Kaila
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  2. J. Voipio
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Kaila, K., Voipio, J. Dependence of intracellular free calcium and tension on membrane potential and intracellular pH in single crayfish muscle fibres. Pflügers Arch. 416, 501–511 (1990). https://doi.org/10.1007/BF00382682

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