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Mechanical characteristics of skinned and intact muscle fibres from the giant barnacle,Balanus nubilus

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Abstract

Intact muscle fibres fromBalanus nubilus develop tensions of up to 600 kN sd m−2 during electrical stimulation. The rise of tension occurs with a half-time (177 ms at 12° C) about fivefold longer than that of tetanised frog muscle at the same temperature. The response of myofibrillar bundles to a rapid stretch resembles that of frog muscle but has a yo value (i.e. the size of an instantaneous release necessary to just discharge tension) which is ca. 2.5 times smaller, and phase 2 of the tension transient (the “quick phase”) occurs at a rate comparable to that of frog muscle. In contrast, the ATPase activity (0.018 mmoles · kg wet weight−1 · s−1) of this preparation and its maximum shortening velocity (0.15–0.16 muscle lengths · s−1) are both at least fivefold slower than frog muscle. These findings can be accounted for by a cross-bridge cycle in barnacle muscle in which events prior and subsequent to the tension generating step(s) occur at a rate at least fivefold slower than comparable steps in frog muscle, but the step(s) associated with tension development occur at similar rates in the two preparations. Since the rate of mechanical relaxation in barnacle muscle is modified in the presence of intracellular calcium buffers and by depolarisation-induced elevation of the free calcium during the relaxation phase, it is proposed that the time course of relaxation is not determined exclusively by the kinetics of the cross-bridge cycle, but is also dependent on the free calcium concentration during relaxation.

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References

  • Ashley CC, Griffiths PJ (1983) The effects of injection of paralbumins into single muscle fibres from the barnacleBalanus nubilus. J Physiol (Lond) 345:105P

    Google Scholar 

  • Ashley CC, Lea TJ (19878) Calcium fluxes in single muscle fibres measured with a glass scintillator probe. J Physiol (Lond) 282:307–331

    Google Scholar 

  • Ashley CC, Lignon J (1981) Aequorin responses during relaxation of tension of single muscle fibres stimulated by voltage clamp. J Physiol (Lond) 318:10–11P

    Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Ashley CC, Griffiths PJ, Moisescu DG, Rose RM (1974) A method for injecting aequorin into large muscle fibres using a micropipette. J Physiol (Lond) 245:11–12P

    Google Scholar 

  • Ashley CC, Barsotti RJ, Ferenczi MA, Lea TJ, Mulligan IP (1987a) Fast activation of skinned muscle fibres from the frog by photolysis of caged calcium. J Physiol (Lond) 394:24

    Google Scholar 

  • Ashley CC, Kerrick WG, Lea TJ, Khalil R, Potter JD (1987b) Reconstitution of the calcium regulatory responses in TnC depleted skinned muscle fibres from the rabbit and barnacleBalanus nubilus. Biophys J 51:327a

    Google Scholar 

  • Ashley CC, Griffiths PJ, Potter JD (1988a) The mobility of TnCDANZ following injection into barnacle muscle fibres. J Physiol (Lond) 399:20P

    Google Scholar 

  • Ashley CC, Griffiths PJ, Hodgson S (1988b) Weakly attached states in myofibrillar bundles fromBalanus nubilus. J Physiol (Lond) 407:77P

    Google Scholar 

  • Brenner B, Schoenberg M, Chalovich JM, Greene LE, Eisenberg E (1982) Evidence for cross-bridge attachment in relaxed muscle at low ionic strength. Proc Natl Acad Sci USA 79:7288–7291

    Article  PubMed  CAS  Google Scholar 

  • Caldwell PC, Walster G (1963) Studies on the micro-injection of various substances into crab muscle fibres. J Physiol (Lond) 169:353–372

    CAS  Google Scholar 

  • Cannell MB (1982) Intracellular calcium during relaxation in frog single muscle fibres. J Physiol (Lond) 326:70P

    Google Scholar 

  • Cannell MB, Allen DG (1986) Model of calcium movements during activation in the sarcomere of frog skeletal muscle. Biophys J 45:913–925

    Google Scholar 

  • Carslaw HS, Jaeger JC (1959) Conduction of heat in solids, 2nd edn. Oxford University Press, pp 330

  • Cecchi G, Colomo F, Lombardi V (1976) A loudspeaker servo system for determination of mechanical characteristics of isolated muscle fibres. Boll Soc Ital Biol Sper 52:733–736

    PubMed  CAS  Google Scholar 

  • Cecchi G, Lombardi V, Colomo F (1978) Force-velocity relation in normal and nitrate-treated frog single muscle fibres during the rise of tension in an isometric tetanus. J Physiol (Lond) 285:257–273

    CAS  Google Scholar 

  • Cooke R, Pate E (1985) The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J 48:789–798

    PubMed  CAS  Google Scholar 

  • Edman KAP, Flitney FW (1978) Laser diffraction studies of sarcomere dynamics during “isometric” relaxation in isolated muscle fibres of the frog. J Physiol (Lond) 329:1–20

    Google Scholar 

  • Fatt P, Katz B (1953) The electrical properties of crustacean muscle fibres. J Physiol (Lond) 120:171–204

    CAS  Google Scholar 

  • Ford LE, Huxley AF, Simmons RM (1977) Tension responses to sudden length changes in stimulated frog muscle fibres near slack length. J Physiol (Lond) 269:441–515

    CAS  Google Scholar 

  • Goldman YE, Simmons RM (1984) Control of sarcomere length in skinned muscle fibres ofRana temporaria during mechanical transients. J Physiol (Lond) 350:497–518

    CAS  Google Scholar 

  • Goldman YE, Simmons RM (1986) The stiffness of frog skinned muscle fibres at altered lateral filament spacing. J Physiol (Lond) 378:175–194

    CAS  Google Scholar 

  • Griffiths PJ, Kuhn JH, Güth K, Rüegg JC (1979) Rate of isometric tension development in relation to calcium binding of skinned muscle fibres. Pflügers Arch 382:165–170

    PubMed  CAS  Google Scholar 

  • Griffiths PJ, Güth K, Kuhn HJ, Rüegg JC (1982) ATPase activity in rapidly activated skinned muscle fibres. Pflügers Arch 387:167–173

    Article  Google Scholar 

  • Griffiths PJ, Potter JD, Coles B, Strang P, Ashley CC (1984) Fluorescence changes from single muscle fibres injected with labelled troponin C (TnCDANZ). FEBS Lett 176:144–150

    Article  PubMed  CAS  Google Scholar 

  • Griffiths PJ, Potter JD, Maeda Y, Ashley CC (1988) Transient kinetics and time-resolved X-ray diffraction studies in isolated single muscle fibres. Adv Exp Med Biol 226:113–129

    PubMed  CAS  Google Scholar 

  • Hagiwara S, Naka K (1964) The initiation of spike potential in barnacle muscle fibers under low intracellular Ca2+. J Gen Physiol 48:141–162

    Article  PubMed  CAS  Google Scholar 

  • Hasselbach W (1966) Structural and enzymatic properties of the calcium transporting membranes of the sarcoplasmic reticulum. Ann NY Acad Sci 137:1041–1048

    Article  PubMed  CAS  Google Scholar 

  • Hill AV (1938) The heat of shortening and the dynamic constants of muscle. Proc R Soc Bl 26:136–195

    Google Scholar 

  • Hill TL (1989) Free energy transduction and biochemical cycle kinetics. Springer, Berlin, Heidelberg, New York

    Google Scholar 

  • Hodgkin AL, Keynes RD (1956) Experiments on the injection of substances into squid giant axons by means of a microsyringe. J Physiol (Lond) 131:592–616

    CAS  Google Scholar 

  • Hoyle G, Abbott BC (1967) Dynamic properties of giant muscle fibres of the barnacle. Am Zool 7:611

    Google Scholar 

  • Hoyle G, McNeill PA, Selverston AI (1973) Ultrastructure of barnacle giant muscle fibers. J Cell Biol 56:74–91

    Article  PubMed  CAS  Google Scholar 

  • Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Mol Biol 7:255–318

    CAS  Google Scholar 

  • Huxley AF, Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233:533–538

    Article  PubMed  CAS  Google Scholar 

  • Julian FJ, Rome LC, Stephenson DG, Striz S (1986) The maximum speed of shortening in living and skinned frog muscle fibres. J Physiol (Lond) 370:181–200

    CAS  Google Scholar 

  • Kawai M, Brandt PW, Orentlicher M (1977) Dependence of energy transduction in intact skeletal muscles on the time in tension. Biophys J 18:161–172

    PubMed  CAS  Google Scholar 

  • Kawai M, Güth K, Winnikes K, Haist C, Rüegg JC (1987) The effect of inorganic phosphate on the ATP hydrolysis rate and the tension transients in chemically skinned rabbit psoas fibres. Pflügers Arch 408:1–9

    Article  PubMed  CAS  Google Scholar 

  • Keynes RD, Rojas E, Taylor RE, Vergara J (1973) Calcium and potassium systems of a giant barnacle muscle fibre under membrane potential control. J Physiol (Lond) 229:409–455

    CAS  Google Scholar 

  • Kushmerick MJ, Podolsky RJ (1969) Ionic mobility in cells. Science 166:1297–1298

    Article  PubMed  CAS  Google Scholar 

  • Landolt-Borstein (1969) Zahlenwerte und Funktionen, vol 5a. Springer, Berlin Heidelberg New York, p 624

    Google Scholar 

  • Levy RM, Umazume Y, Kushmerick MJ (1976) Ca2+ dependence of tension and ADP production in segments of chemically skinned muscle fibres. Biochim Biophys Acta 430:352–365

    Article  PubMed  CAS  Google Scholar 

  • Loxdale HD (1976) A merthod for the continuous assay of picomole quantities of ADP released from glycerol-extracted skeletal muscle fibres on MgATP activation. J Physiol (Lond) 260:4–5P

    Google Scholar 

  • Matsubara I, Elliott GF (1972) X-ray diffraction studies on skinned single fibres of frog skeletal muscle. J Mol Biol 72:657–669

    Article  PubMed  CAS  Google Scholar 

  • Mulligan IP, Griffiths PJ, Ashley CC (1987) Laser flash photolysis of caged ATP in skinned muscle fibres fromBalanus nubilus. Biophys J 51:470a

    Google Scholar 

  • Pybus J, Tregear RT (1975) The relationship of adenosine triphosphate activity to tension and power output of insect flight muscle. J Physiol (Lond) 247:71–89

    CAS  Google Scholar 

  • Ridgway EB, Gordon AM (1984) Muscle calcium transient. Effect of post-stimulus length changes in single fibers. J Gen Physiol 83:75–103

    Article  PubMed  CAS  Google Scholar 

  • Stephenson DG, Stewart AW, Wilson GJ (1989) Dissociation of force from myofibrillar MgATPase and stiffness at short sarcomere lengths in rat and toad skeletal muscle. J Physiol (Lond) 410:351–367

    CAS  Google Scholar 

  • Taylor SR, Lopez JR, Griffiths PJ, Trube G, Cecchi G (1982) Calcium in excitation-contraction coupling of frog skeletal muscle. Can J Physiol Pharmacol 60:489–502

    PubMed  CAS  Google Scholar 

  • Timmerman MP, Ashley CC (1986) Fura-2 diffusion and its use as an indicator of transient free calcium changes in single striated muscle cells. FEBS Lett 209:1–8

    Article  PubMed  CAS  Google Scholar 

  • Woledge RW, Curtin NA, Homsher E (1985) Energetic aspect of muscle contraction. Monogr Physiol Soc, vol 41. Academic Press, London

    Google Scholar 

  • Yoshizaki K, Yoshiteru S, Hiroyasu N, Morimoto T (1982) Application of pulsed-gradient31P NMR on frog muscle to measure the diffusion rates of phosphorus compounds in cells. Biophys J 38:209–211

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

Download references

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Griffiths, P.J., Duchateau, J.J., Maeda, Y. et al. Mechanical characteristics of skinned and intact muscle fibres from the giant barnacle,Balanus nubilus . Pflugers Arch. 415, 554–565 (1990). https://doi.org/10.1007/BF02583506

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