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Parvalbumins and muscle relaxation: a computer simulation study

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Summary

The distribution of Ca2+ and Mg2+ among the ‘regulatory’ cation binding sites of troponin (T-sites) and the strong, Ca2+-Mg2+ binding sites of troponin and parvalbumins (P-sites) in the sarcoplasm of a muscle was calculated. At rest, 60% of the T-sites were metal free, while 92% of the P-sites were loaded with Mg2+.

In response to a Ca2+ pulse, troponin-calcium (T-Ca) complexes were rapidly formed, while the binding of Ca2+ to P-sites was limited by the slow rate of dissociation of the parvalbumin-magnesium (P-Mg) complexes. Muscle activation was not prevented by a high content of parvalbumins.

Parvalbumin and the sarcoplasmic reticulum (SR) pump were complementary relaxing factors that removed Ca2+ from the cytosol and from the T-sites. Parvalbumins dominated the first part of relaxation, while the action of the SR was essential to ensure the return to a very low level of free Ca2+ ion and of T-Ca. After relaxation, a large fraction of the Ca2+ pulse was still bound to parvalbumins and returned slowly to the SR during the recovery.

When the SR activity was reduced, the presence of parvalbumins preserved a fast rate of relaxation, at least for a few contractions. This may have a high adaptive value in cold-blooded animals.

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References

  • ASHLEY, C. C. & CAMPBELL, A. K. (1979)Detection and Measurement of Free Ca 2+ in Cells. Amsterdam: Elsevier/North Holland.

    Google Scholar 

  • ASHLEY, C. C., CALDWELL, P. C., LOWE, A. G., RICHARDS, C. D. & SCHIRMER, M. (1965) The amount of injected EGTA needed to suppress the contractile responses of single Maia muscle fibres and its relation to the amount of calcium released during contraction.J. Physiol. 179, 32–3P.

    Google Scholar 

  • ASHLEY, C. C., MOISESCU, D. G. & ROSE, R. M. (1974) Kinetics of calcium during contraction: myofibrillar and SR fluxes during a single response of a skeletal muscle fibre. InCalcium Binding Proteins (edited by DRABIKOWSKI, W., STRZELECKA-GOLASZEWSKA, M. and CARAFOLI, E.), pp. 609–642. Amsterdam: Elsevier.

    Google Scholar 

  • ASHLEY, C. C. & RIDGEWAY, E. B. (1970) On the relationships between membrane potential, calcium transient and tension in single barnacle muscle fibres.J. Physiol. 209, 105–30.

    Google Scholar 

  • BARON, G., DEMAILLE, J. & DUTRUGE, M. (1975) The distribution of parvalbumins in muscle and other tissues.FEBS Lett. 56, 156–60.

    Google Scholar 

  • BHUSHANA RAO, K. S. P. & GERDAY, C. (1973) Low molecular weight proteins of pike (Esox minus) white muscles. I. Extraction and purification-polymorphism.Comp. Biochem. Physiol. 44B, 931–7.

    Google Scholar 

  • BLINKS, J. R. (1973) Calcium transients in striated muscle cells.Eur. J. Cardiol. 1, 135–42.

    Google Scholar 

  • BLINKS, J. R., RÜDEL, R. & TAYLOR, S. R. (1977) Calcium transients in isolated amphibian skeletal muscle fibres: detection with aequorin.J. Physiol. 277, 291–323.

    Google Scholar 

  • BLUM, H. E., LEHKY, P., KOHLER, L., STEIN, E. A. & FISHER, E. H. (1977) Comparative properties of vertebrate parvalbumins.J. biol. Chem. 252, 2834–8.

    Google Scholar 

  • BLUM, H. E., POCINWONG, S. & FISHER, E. H. (1974) A phosphate acceptor protein related to parvalbumins in dogfish skeletal muscle.Proc. natn. Acad. Sci. 71, 2198–202.

    Google Scholar 

  • BONE, Q. (1966) On the function of the two types of myotomal muscle fibre in elasmobranch fish.J. mar. Biol. Ass. U.K. 46, 321–49.

    Google Scholar 

  • BRIGGS, N. (1975) Identification of the soluble relaxing factor as a parvalbumin.Fed. Proc. 34, 540.

    Google Scholar 

  • CAMPBELL, A. K., LEA, T. J. & ASHLEY, C. C. (1979) Coelenterate photoproteins. InDetection and Measurement of Free Ca 2+ in Cells (edited by ASHLEY, C. C. and CAMPBELL, A. K.), pp. 13–72. Amsterdam: Elsevier.

    Google Scholar 

  • COHEN, S. M. & TYLER-BURT, C. (1977)31P nuclear magnetic relaxation studies of phosphocreatine in intact muscle: Determination of intracellular free magnesium.Proc. natn. Acad. Sci. 74, 4271–5.

    Google Scholar 

  • COX, J. A., WNUK, W. & STEIN, E. A. (1977) Regulation of calcium binding by magnesium. InCalcium-binding Proteins and Calcium Function (edited by WASSERMAN, R. H., CORRADINO, R. A., CARAFOLI, E., KRETZINGER, R. H., MACHENNAN, D. H. and SIEGEL, F. L.), pp. 266–269. New York: North-Holland.

    Google Scholar 

  • CURTIN, N. A. & WOLEDGE, R. C. (1978) Energy changes and muscular contraction.Physiol. Rev. 58, 690–761.

    Google Scholar 

  • DEMAILLE, J., DUTRUGE, E., CAPONY, J.-P. & PECHÈRE, J.-F. (1974a) Muscular parvalbumins: A family of homologous calcium-binding proteins. Their relation to the calcium-binding troponin component. InCalcium Binding Proteins (edited by DRABIKOWSKI, W., STRZELECKA-GOLASZEWSKA, M. and CARAFOLI, E.), pp. 643–677. Amsterdam: Elsevier.

    Google Scholar 

  • DEMAILLE, J., DUTRUGE, E., EISENBERG, G., CAPONY, J. P. & PECHÈRE, J. F. (1974b) Troponins C from reptile and fish muscles and their relation to muscular parvalbumins.FEBS Lett. 42, 173–8.

    Google Scholar 

  • DEMAILLE, J., DUTRUGE, E., BARON, G., PECHÈRE, J.-F. & FISCHER, E. H. (1975) A reappraisal of the relationship of phosphate-acceptor protein to parvalbumin.Biochem. biophys. Res. Commun. 67, 1034–40.

    Google Scholar 

  • DIEBLER, H., EIGEN, M., ILGENFRITZ, G., MAASS, G. & WINKLER, R. (1969) Kinetics and mechanism of reactions of main group metal ions with biological carriers.Pure. Appl. Chem. 20, 93–115.

    Google Scholar 

  • EBASHI, S., ENDO, M. & OHTSUKI, I. (1969) Control of muscle contraction.Q. Rev. Biophys. 2, 351–84.

    Google Scholar 

  • ENDO, M. (1977) Calcium release from the sarcoplasmic reticulum.Physiol. Rev. 57, 71–108.

    Google Scholar 

  • GEAR, C. W. (1971)Numerical Initial Value Problems in Ordinary Differential Equations. pp. 158–166. Englewood Cliffs, New Jersey: Prentice-Hall.

    Google Scholar 

  • GERDAY, C., & GILLIS, J. M. (1976) The possible role of parvalbumins in the control of contraction.J. Physiol., Lond. 258, 96P.

    Google Scholar 

  • GILLIS, J. M. & GERDAY, C. (1977) Calcium movement between myofibrils, parvalbumins and sarcoplasmic reticulum in muscle. InCalcium-binding Proteins and Calcium Function (edited by WASSERMAN, R. M., CORRADINO, R. A., CARAFOLI, E., KRETZINGER, R. H., MACLENNAN, D. H. and SIEGEL, F. L.), pp. 193–196. New York: North Holland.

    Google Scholar 

  • GILLIS, J. M., PIRONT, A. & GOSSELIN-REY, C. (1979) Parvalbumins: distribution and physical state inside the muscle cell.Biochim. biophys. Acta 585, 444–50.

    Google Scholar 

  • GILLIS, J. M. (1980) The biological significance of muscle parvalbumins. InCalcium Binding Proteins: Structure and Function (edited by SIEGEL, F. L., CARAFOLI, E., KRETZINGER, R. H., MACLENNAN, D. H. and WASSERMAN, R. H.), pp. 309–311, Amsterdam: Elsevier/North-Holland.

    Google Scholar 

  • GOSSELIN-REY, C. & GERDAY, C. (1977) Parvalbumins from frog skeletal muscle (Rana temporaria). Isolation and characterization, structural modifications associated with calcium binding.Biochim. biophys. Acta 492, 53–63.

    Google Scholar 

  • HAMOIR, G. (1968) The comparative biochemistry of fish sarcoplasmic proteins.Acta Zool. Path. Antver. 46, 69–76.

    Google Scholar 

  • HAMOIR, G. (1974) Earlier and recent work on parvalbumins.Symp. Biol. Hung. 17, 17–33.

    Google Scholar 

  • HAMOIR, G., GERARDIN-OTTHIERS, N. & FOCANT, B. (1980) Protein differentiation of the superfast swimbladder muscle of the toadfishOpsanus tau.J. molec. Biol. 143, 155–60.

    Google Scholar 

  • HEIZMANN, G. W., HAUPTLE, M. T. & EPPENBERGER, H. M. (1977) The purification, characterization and localization of a parvalbumin-like protein from chicken-leg muscle.Eur. J. Biochem. 80, 433–41.

    Google Scholar 

  • HITCHCOCK, S. E. & KENDRICK-JONES, J. (1975) Myosin light chains, carp calcium binding protein, and troponin components: Do they interact to form functional complexes? InCalcium Transport in Contraction and Secretion (edited by CARAFOLI, E., CLEMENTI, F., DRABIKOWSKI, W. and MARGRETH, A.), pp. 447–458. Amsterdam: North-Holland.

    Google Scholar 

  • HOMSHER, E. & KEAN, C. J. (1978) Skeletal muscle energetics and metabolism.Ann. Rev. Physiol. 40, 93–131.

    Google Scholar 

  • INESI, G. & SCARPA, A. (1972) Fast kinetics of adenosine triphosphate dependent Ca2+ uptake by fragmented sarcoplasmic reticulum.Biochemistry 11, 356–9.

    Google Scholar 

  • INESI, G. & WATANABE, S. (1967) Temperature dependence of ATP hydrolysis and calcium uptake by fragmented sarcoplasmic membranes.Archs Biochem. Biophys. 121, 665–71.

    Google Scholar 

  • JOHNSON, J. D., CHARLTON, S. C. & POTTER, J. D. (1979) A fluorescence stopped-flow analysis of Ca2+ exchange with troponin-C.J. biol. Chem. 254, 3497–502.

    Google Scholar 

  • MCCRAKEN, D. D. & DORN, W. S. (1966)Numerical Methods and Fortran Programming. New York: John Wiley.

    Google Scholar 

  • PEACHEY, L. D. (1965) The sarcoplasmic reticulum and transverse tubule of the frog's sartorius.J. Cell Biol. 25, 209–31.

    Google Scholar 

  • PECHÈRE, J. F. & FOCANT, B. (1965) Carp myogens of white and red muscles. Gross isolation on Sephadex columns of the low molecular weight components and examination of their participation in anaerobic glycogenolysis.Biochem. J. 96, 113–8.

    Google Scholar 

  • PECHÈRE, J. F., CAPONY, J. P. & RYDEN, L. (1971) The primary structure of the major parvalbumin from hake muscle: Isolation and general properties of the protein.Eur. J. Biochem. 23, 421–8.

    Google Scholar 

  • PECHÈRE, J. F., DEMAILLE, J., DUTURGE, E., CAPONY, J. P., BARON, G. & PINA, C. (1975) Muscular parvalbumins. Some explorations into their possible biological significance. InCalcium Transport in Contraction and Secretion (edited by CARAFOLI, E., CLEMENTI, F., DRABIKOWSKI, W. and MARGRETH, A.), pp. 459–468. Amsterdam: North Holland.

    Google Scholar 

  • PECHÈRE, J. F., DERANCOURT, J. & HAIECH, J. (1977) The participation of parvalbumins in the activation-relaxation cycle of vertebrate fast skeletal muscle.FEBS Lett. 75, 111–4.

    Google Scholar 

  • POTTER, J. D. & GERGELY, J. (1975) The calcium and magnesium binding sites of troponin and their role in the regulation of myofibrillar adenosine triphosphatase.J. biol. Chem. 250, 4628–33.

    Google Scholar 

  • POTTER, J. D., JOHNSON, J. D. & MANDEL, F. (1978) Fluorescence stopped flow measurements of Ca2+ and Mg2+ binding to parvalbumins.Fed. Proc. 37, 1608.

    Google Scholar 

  • POTTER, J. D., JOHNSON, J. D., DEDMAN, J. R., SCHREIBER, W. E., MANDEL, F., JACKSON, R. L. & MEANS, A. R. (1977) InCalcium-binding Proteins and Calcium Function (edited by WASSERMAN, R. H., CORRADINO, R. A., CARAFOLI, E., KRETZINGER, R. H., MacLENNAN, D. H. and SIEGEL, F. L.), pp. 239–250. New York: North Holland.

    Google Scholar 

  • POTTER, J. D., ROBERTSON, S. P., COLLINS, J. H. & JOHNSON, J. D. (1980) The role of the Ca2+ and Mg2+ binding sites on troponin and other myofibrillar proteins in the regulation of muscle contraction. InCalcium Binding Proteins: Stucture and Function (edited by SIEGEL, F. L., CARAFOLI, E., KRETZINGER, R. H., MacLENNAN, D. H. and WASSERMAN, R. M.), pp. 279–288. Amsterdam: Elsevier/North-Holland.

    Google Scholar 

  • RALSTON, A. & RABINOWITZ, P. (1978)A First Course in Numerical Analysis. 2nd edn. New York: McGraw-Hill.

    Google Scholar 

  • ROBERTSON, S. P., JOHNSON, J. D. & POTTER, J. D. (1981) The time-course of Ca2+ exchange with calmodulin, troponin, parvalbumin, and myosin in response to transient increases in Ca2+.Biophys. J. 34, 559–69.

    Google Scholar 

  • SHAMPINE, L. F. & GEAR, C. W. (1979) A user's view of solving stiff ordinary differential equations.SIAM Rev. 21, 1–17.

    Google Scholar 

  • SOMLYO, A. V., GONZALEZ-SERRATOS, H., SCHUMAN, H., MCCLEILAN, G. & SOMLYO, A. P. (1981) Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: an electron probe study.J. Cell Biol. 90, 577–94.

    Google Scholar 

  • WEBER, A. M., HERZ, R. & REISS, I. (1966) Studies of the kinetics of calcium transport by isolated fragmented sarcoplasmic reticulum.Biochem. Z. 345, 329–41.

    Google Scholar 

  • WINEGRAD, S. (1968) Intracellular calcium movements of frog skeletal muscle during recovery from tetanus.J. gen. Physiol. 51, 65–83.

    Google Scholar 

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Author notes

  1. D. Thomason

    Present address: Department of Physiology and Biophysics, University of California, 92717, Irvine, California, USA

Authors and Affiliations

  1. Département de Physiologie, Université Catholique de Louvain, B-1200, Bruxelles, Belgium

    J. M. Gillis & J. Lefèvre

  2. Department of Biology, University of Virginia, 22901, Charlottesville, Virginia, USA

    D. Thomason & R. H. Kretsinger

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  1. J. M. Gillis
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Ed. notation: Free calcium ion (free Ca2+); bound calcium ion (bound Ca2+).

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Gillis, J.M., Thomason, D., Lefèvre, J. et al. Parvalbumins and muscle relaxation: a computer simulation study. J Muscle Res Cell Motil 3, 377–398 (1982). https://doi.org/10.1007/BF00712090

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