Order-disorder structural transitions in synthetic filaments of fast and slow skeletal muscle myosins under relaxing and activating conditions.

• Authors: Zoya A Podlubnaya , Sergey L Malyshev , Krzysztof Nieznański , Dariusz Stępkowski
• Languages of publication: EN

Abstracts

EN

In the previous study (Podlubnaya et al., 1999, J. Struc. Biol. 127, 1-15) Ca2+-induced reversible structural transitions in synthetic filaments of pure fast skeletal and cardiac muscle myosins were observed under rigor conditions (-Ca2+/+ Ca2+). In the present work these studies have been extended to new more order-producing conditions (presence of ATP in the absence of Ca2+) aimed at arresting the relaxed structure in synthetic filaments of both fast and slow skeletal muscle myosin. Filaments were formed from column-purified myosins (rabbit fast skeletal muscle and rabbit slow skeletal semimebranosus proprius muscle). In the presence of 0.1 mM free Ca2+, 3 mM Mg2+ and 2 mM ATP (activating conditions) these filaments had a spread structure with a random arrangement of myosin heads and subfragments 2 protruding from the filament backbone. Such a structure is indistinguishable from the filament structures observed previously for fast skeletal, cardiac (see reference cited above) and smooth (Podlubnaya et al., 1999, J. Muscle Res. Cell Motil. 20, 547-554) muscle myosins in the presence of 0.1 mM free Ca2+. In the absence of Ca2+ and in the presence of ATP (relaxing conditions) the filaments of both studied myosins revealed a compact ordered structure. The fast skeletal muscle myosin filaments exhibited an axial periodicity of about 14.5 nm and which was much more pronounced than under rigor conditions in the absence of Ca2+ (see the first reference cited). The slow skeletal muscle myosin filaments differ slightly in their appearance from those of fast muscle as they exhibit mainly an axial repeat of about 43 nm while the 14.5 nm repeat is visible only in some regions. This may be a result of a slightly different structural properties of slow skeletal muscle myosin. We conclude that, like other filaments of vertebrate myosins, slow skeletal muscle myosin filaments also undergo the Ca2+-induced structural order-disorder transitions. It is very likely that all vertebrate muscle myosins possess such a property.

Keywords

EN

method of slow skeletal muscle myosin preparation.; Ca2+-induced structural transitions; myosin filaments; fast and slow skeletal muscle myosin

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2000
• Volume: 47
• Issue: 4
• Pages: 1007-1017

Dates

published

2000

received

2000-09-26

revised

2000-11-7

accepted

2000-11-9

Contributors

author

Zoya A Podlubnaya

• Institute of Experimental and Theoretical Biophysics, Russian Academy of Sciences, 142290, Pushchino, Moscow Region, Russia

author

Sergey L Malyshev

• Institute of Experimental and Theoretical Biophysics, Russian Academy of Sciences, 142290, Pushchino, Moscow Region, Russia

author

Krzysztof Nieznański

• Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warszawa, Poland

author

Dariusz Stępkowski

• Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warszawa, Poland

References

• Bacou, F., Rouanet, P., Barjot, C., Janmot, C., Vigneron, P. & d'Albis, A. (1996) Expression of myosin isoforms in denervated, cross-reinnervated, and electrically stimulated rabbit muscles. Eur. J. Biochem. 236, 539-547.
• Borejdo, J. & Weber, M.M. (1982) Binding of calcium and magnesium to myosin in skeletal muscle myofibrils. Biochemistry 21, 549-555.
• Dawson, M.J., Gadian, D.G. & Wilkie, D.R. (1978) Muscular fatigue investigated by phosphorus nuclear magnetic resonance. Nature 274, 861-866.
• Donaldson, S.K., Best, P.M. & Kerrick, G.L. (1978) Characterization of the effects of Mg2+ on Ca2+- and Sr2+-activated tension generation of skinned rat cardiac fibers. J. Gen. Physiol. 71, 645-655.
• Fiske, C.H. & SubbaRow, Y. (1925) The colorimetric determination of phosphorus. J. Biol. Chem. 66, 375-400.
• Frado, L.L. & Craig, R. (1989) Structural changes induced in Ca2+-regulated myosin filaments by Ca2+ and ATP. J. Cell Biol. 109, 529-538.
• Herrmann, C., Sleep, J., Chaussepied, P., Travers, F. & Barman, T. (1993) A structural and kinetic study on myofibrils prevented from shortening by chemical cross-linking. Biochemistry 32, 7255-7263.
• Holroyde, M.J., Potter, J.D. & Solaro, R.J. (1979) The calcium binding properties of phosphorylated and unphosphorylated cardiac and skeletal myosins. J. Biol. Chem. 254, 6478-6482.
• Kerrick, W.G.L. & Donaldson, S.K. (1975) The comparative effects of (Ca2+) and (Mg2+) on tension generation in the fibers of skinned frog skeletal muscle and mechanically disrupted rat ventricular cardiac muscle. Pflugers Arch. 358, 195-201.
• Kurihara, S. (1994) Regulation of cardiac muscle contraction by intracellular Ca2+. Jpn. J. Physiol. 44, 591-611.
• Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
• Levine, R.J., Kensler, R.W., Yang, Z., Stull, J.T. & Sweeney, H.L. (1996) Myosin light chain phosphorylation affects the structure of rabbit skeletal muscle thick filaments. Biophys. J. 71, 898-907.
• Malyshev, S.L., Udaltsov, S.N., Stępkowski, D. & Podlubnaya, Z.A. (2000) Structural transitions in synthetic filaments of myosin from fast skeletal muscle under relaxing and activating conditions. 29th European Muscle Conference, September 8-13, 2000, Berlin, Germany, abs.7-127.
• Martin, H. & Barsotti, R.J. (1994) Activation of skinned trabeculae of the guinea pig induced by laser photolysis of caged ATP. Biophys. J. 67, 1933-1941.
• Ménétret, J.F., Schröder, R.R. & Hofmann, W. (1990) Cryo-electron microscopic studies of relaxed striated muscle thick filaments. J. Muscle Res. Cell Motil. 11, 1-11.
• Metzger, J.M. & Moss, R.L. (1990) Calcium-sensitive cross-bridge transitions in mammalian fast and slow skeletal muscle fibers. Science 247, 1088-1090.
• Moss, L.R. (1992) Ca2+ regulation of mechanical properties of striated muscle. Circ. Res. 70, 865-884.
• Pinset-Härström, I. & Truffy, J. (1979) Effects of adenosine triphosphate, inorganic phosphate and divalent cations on the size and structure of synthetic myosin filaments. An electron microscopic study. J. Mol. Biol. 134, 173-188.
• Podlubnaya, Z., Kąkol, I., Moczarska, A., Stępkowski, D. & Udaltsov, S. (1999a) Calcium-induced structural changes in synthetic myosin filaments of vertebrate striated muscles. J. Struct. Biol. 127, 1-15.
• Podlubnaya, Z., Kulikova, N. & Dąbrowska, R. (1999b) The effect of Ca2+ on the structure of synthetic filaments of smooth muscle myosin. J. Muscle Res. Cell Motil. 20, 547-554.
• Podlubnaya, Z.A., Kąkol, I., Moczarska, A., Stępkowski, D. & Udaltsov, S. (2000) Truncation of vertebrate striated muscle myosin light chains disturbs calcium-induced structural transitions in synthetic myosin filaments. J. Struct Biol. 131, 225-233.
• Reisler, E., Liu, J. & Cheung, P. (1983) Role of magnesium binding to myosin in controlling the state of cross-bridges in skeletal rabbit muscle. Biochemistry 22, 4954-4960.
• Stępkowski, D., Szczęsna, D., Wrotek, M. & Kąkol, I. (1985) Factors influencing interaction of phosphorylated and dephosphorylated myosin with actin. Biochim. Biophys. Acta 831, 321- 329.
• Stępkowski, D., Efimova, N., Paczyńska, A., Moczarska, A., Nieznańska, H. & Kąkol, I. (1997) The possible role of myosin A1 light chain in the weakening of actin-myosin interaction. Biochim. Biophys. Acta. 1340, 105- 114.
• Strzelecka-Gołaszewska, H., Jakubiak, M. & Drabikowski, W. (1975) Changes in the state of actin during superprecipitation of actomyosin. Eur. J. Biochem. 55, 221-230.
• Tartakowski, A.D. (1978) Methods of isolation and characterization of skeletal striated muscle myosin and its subunits; in Biophysical and Biochemical Methods of Investigation of Muscle Proteins (Pinaev, G.P., ed.) pp. 55-76, Nauka, Leningrad (in Russian).