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The chicken muscle thick filament: temperature and the relaxed cross-bridge arrangement

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Summary

Although chicken myosin S1 has recently been crystallized and its structure analysed, the relaxed periodic arrangement of myosin heads on the chicken thick filament has not been determined. We report here that the cross-bridge array of chicken filaments is temperature sensitive, and the myosin heads become disordered at temperatures near 4° C. At 25° C, however, thick filaments from chicken pectoralis muscle can be isolated with a well ordered, near-helical, arrangement of cross-bridges as seen in negatively stained preparations. This periodicity is confirmed by optical diffraction and computed transforms of images of the filaments. These show a strong series of layer lines near the orders of a 43 nm near-helical periodicity as expected from X-ray diffraction. Both analysis of phases on the first layer line, and computer filtered images of the filaments, are consistent with a three-stranded arrangement of the myosin heads on the filament.

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References

  • ASHTON, F. T., WEISEL, J. & PEPE, A. (1992) The myosin filament XIV. Backbone structure. Biophys. J. 61, 1513–28.

    Google Scholar 

  • BAHLER, M., WALLIMAN, T. & EPPENBERGER, H. M. (1985) Myofibrillar M-band proteins represent constituents of native thick filaments, frayed filaments and bare zone assemblages. J. Muscle Res. Cell Motil. 6, 783–800.

    Google Scholar 

  • BENNETT, P., CRAIG, R., STARR, R. & OFFER, G. (1986). The ultrastructural location of C-protein, X-protein and H-protein in rabbit muscle. J. Muscle Res. Cell Motil. 7, 550–67.

    Google Scholar 

  • BRENNER, B. (1987) Mechanical and structural approaches to correlation of crossbridge action with actomyosin ATPase in solution. Ann. Rev. Physiol. 49, 655–72.

    Google Scholar 

  • BRENNER, B. (1989) Muscle mechanics and biochemical kinetics. In Molecular Mechanisms in Muscular Contraction (edited by SQUIRE, J. M.) pp. 77–149. Boca Raton: CRC Press.

    Google Scholar 

  • CANTINO, M. & SQUIRE, J. (1986) Resting myosin crossbridge configuration in frog muscle thick filaments. J. Cell Biol. 102, 610–18.

    Google Scholar 

  • CRAIG, R. & OFFER, G. (1976) The location of C-protein in rabbit-skeletal muscle. Proc. R. Soc. Lond. B192, 451–61.

    Google Scholar 

  • CRAIG, R., PADRON, T. & KENDRICK-JONES, J. (1987) Structural changes accompanying phosphorylation of tarantula thick filaments. J. Cell Biol. 105, 1319–27.

    Google Scholar 

  • CRAIG, R., ALAMO, L. & PADRON, R. (1992) Structure of the myosin filaments of relaxed and rigor vertebrate striated myscle studied by rapid freezing electron microscopy. J. Mol. Biol. 228, 474–87.

    Google Scholar 

  • DAVIES, R. E. (1963) A molecular theory of muscle contractions: calcium dependent contractions with hydrogen bond formation plus ATP-dependent extensions of part of the myosin-actin crossbridges. Nature 199, 1068–74.

    Google Scholar 

  • DENNIS, J., SHIMIZU, T., REINACH, F. & FISCHMAN, D. (1984) Localization of C-protein isoforms in chicken skeletal muscle: ultrastructural detection using monoclonal antibodies. J. Cell Biol. 98, 1514–22.

    Google Scholar 

  • EVERETT, A. W. & SPARROW, M. P. (1987) Transient appearance of a fast myosin heavy chain epitope in slow-type muscle fibres during stretch hypertropy of the anterior latissimus dorsi muscle in the adult chicken. J. Muscle Res. Cell Motil. 8, 220–8.

    Google Scholar 

  • GOLDFINE, S. M., EINHEBER, S. & FISCHMAN, D. A. (1991) Cell-free incorporation of newly synthesized myosin subunits into thick myofilaments. J. Muscle Res. Cell Motil. 12, 161–70.

    Google Scholar 

  • HARFORD, J. & SQUIRE, J. (1986) “Crystalline” myosin crossbridge array in relaxed bony fish muscle. Low angle X-ray diffraction from plaice fin muscle and its interpretation. Biophys. J. 50, 145–55.

    Google Scholar 

  • HASELGROVE, J. C. (1975) X-ray evidence for conformational changes in the myosin filaments of vertebrate striated muscle. J. Miol. Biol. 92, 113–43.

    Google Scholar 

  • HASELGROVE, J. C. (1980) T model of myosin crossbridge structure consistent with the low-angle X-ray diffraction pattern of vertebrate muscle. J. Muscle Res. Cell Motil. 1, 177–91.

    Google Scholar 

  • HASELGROVE, J. C. & RODGER, C. D. (1980) The interpretation of X-ray diffraction patterns from vertebrate striated muscle. J. Muscle Res. Cell Motil. 1, 371–90.

    Google Scholar 

  • HOLMES, K. C., POPP, D., GEBHARD, W. & KABASCH, W. (1990a) Atomic model of the actin filament. Nature 347, 44–9.

    Google Scholar 

  • HOLMES, K. C., POPP, D., GEBHARD, W. & KABASCH, W. (1990b) The structure of F-actin calculated from X-ray diffraction diagrams and the 0.6 nm crystal structure. In Molecular Mechanisms in Muscular Contraction (edited by SQUIRE, J. M.) pp. 65–75. Boca Raton: CRC Press.

    Google Scholar 

  • HUXLEY, A. F. (1957) Muscle structure and theories of contraction. Prog. Biophys. 7, 255–313.

    Google Scholar 

  • HUXLEY, H. E. (1963) Electron microscope studies of the structure of natural and synthetic protein filaments from muscle. J. Mol. Biol. 7, 281–308.

    Google Scholar 

  • HUXLEY, H. E. (1969) The mechanism of muscle contraction. Science 164, 1356–66.

    Google Scholar 

  • HUXLEY, H. E. & HANSON, J. (1954). Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173, 973–6.

    Google Scholar 

  • HUXLEY, A. F. & NIEDERGERKE, R. (1954) Structural changes in muscle during contraction. Interference microscopy of living muscle fibers. Nature 173, 971–2.

    Google Scholar 

  • HUXLEY, H. E. & BROWN, W. (1967) The low angle X-ray diagram of vertebrate striated muscle and its behavior during contraction and rigor. J. Mol. Biol. 30, 383–434.

    Google Scholar 

  • HUXLEY, A. F. & SIMMONS, R. M. (1971) Proposed mechanism of force generation in striated muscle. Nature 233, 533–8.

    Google Scholar 

  • HUXLEY, H. E. & FARUQI, A. R. (1983) Time resolved X-ray diffraction studies on vertebrate striated muscle. Ann. Rev. Biophys. Bioeng. 12, 381–417.

    Google Scholar 

  • HUXLEY, H. E., FARUQI, A. R., BORDAS, J., KOCH, M. H. J. & MULCH, J. R. (1980) The use of synchrotron radiation in time-resolved X-ray diffraction studies of myosin layerline reflections during muscle contraction. Nature 284, 140–3.

    Google Scholar 

  • HUXLEY, H. E., FARUQI, A. R., KROSS, M., BORDAS, J. & KOCH, M. H. J. (1982) Time resolved X-ray diffraction studies of the myosin layer-line reflections during muscle contraction. J. Mol. Biol. 158, 637–84.

    Google Scholar 

  • IP, W. & HEUSER, J. (1983) Direct visualization of the myosin crossbridge helices on relaxed rabbit psoas thick filaments. J. Mol. Biol. 171, 105–9.

    Google Scholar 

  • ISHIJIMA, A., DOI, T., SAKURADA, K. & YANAGIDA, T. (1991) Sub-piconewton force fluctuations of acto-myosin in vitro. Nature 352, 301.

    Google Scholar 

  • KENSLER, R. W. & LEVINE, R. J. C. (1982) Determination of the handedness of the crossbridge helix of Limulus thick filaments. J. Muscle Res. Cell Motil. 3, 349–61.

    Google Scholar 

  • KENSLER, R. W. & STEWART, M. (1983) Forg skeletal muscle thick filaments are three-stranded. J. Cell Biol. 96, 1797–802.

    Google Scholar 

  • KENSLER, R. W. & STEWART, M. (1986) An ultrastructural study of crossbridge arrangement in the frog thigh muscle thick filament. Biophys. J. 49, 343–51.

    Google Scholar 

  • KENSLER, R. W. & STEWART, M. (1989) An ultrastructural study of crossbridge arrangement in the fish skeletal muscle thick filament. J. Cell Sci. 94, 391–401.

    Google Scholar 

  • KENSLER, R. W. & STEWART, M. (1993) The relaxed crossbridge pattern in isolated rabbit psoas muscle thick filaments. J. Cell Sci. 105, 841–8.

    Google Scholar 

  • KENSLER, R. W., LEVINE, R. J. C. & STEWART, M. (1985) An electron microscope and optical diffraction analysis of the structure of scorpion muscle thick filaments. J. Cell Biol. 101, 395–401.

    Google Scholar 

  • KENSLER, R. W., PETERSON, S. & NORBERG, M. (1994) The effects of changes in temperature or ionic strength on isolated rabbit and fish skeletal muscle thick filaments. J. Muscle Res. Cell Motil. 15, 69–79.

    Google Scholar 

  • KILBY, K. & DHOOT, G. K. (1988) Identification of some developmental isoforms of myosin heavy chains in avian muscle fibres. J. Muscle Res. Cell Motil. 9, 516–24.

    Google Scholar 

  • KLUG, A., CRICK, F. H. C. & WYKOFF, W. W. (1958) Diffraction by helical structures. Acta Crystallogr. 11, 199–213.

    Google Scholar 

  • LEVINE, R. J. C. (1993) Evidence for overlapping myosin heads on relaxed thick filaments of fish, frog, and scallop striated muscles. J. Struct. Biol. 110, 99–110.

    Google Scholar 

  • LEVINE, R. J. C., CHANTLER, P. D., KENSLER, R. W. & WOODHEAD, J. L. (1991) Effects of phosphorylation by light-chain kinase on the structure of Limulus thick filaments. J. Cell Biol. 113, 563–72.

    Google Scholar 

  • LEVINE, R. J. C., KENSLER, R. W., SWEENEY, H. L. & YANG, Z. (1992) Phosphorylation of myosin light chain produces changes in thick filaments from rabbit skeletal muscle. Mol. Biol. Cell 3, 363a (abstract).

    Google Scholar 

  • LOWEY, S. & HOLT, J. C. (1973) An immunochemical approach to the interaction of light and heavy chains in myosin. cold Spring Harbor Symposium 37, 19–28.

    Google Scholar 

  • LOWEY, J., POPP, D. & STEWART, A. A. (1991) X-ray studies of order-disorder transitions in the myosin heads of skinned rabbit psoas muslces. Biophys. J. 60, 812–24.

    Google Scholar 

  • LOWEY, S., SILBERSTEIN, L., GAUTHIER, G. F. & HOLT, J. C. (1979) Isolation and distribution of myosin isozymes. In Motility in Cell Function: Proceedings of the First John M. Marshall Symposium in Cell Biology (edited by PEPE, F. A., SANGER, J. W. & NACHMIAS, V. T.) pp. 53–67. New York: Academic Press.

    Google Scholar 

  • MENETRET, J. F., SCHRODER, R. R. & HOFMANN, W. (1990) Cryo-electron microscopic studies of relaxed striated muscle thick filaments. J. Muscle Res. Cell Motil. 11, 1–11.

    Google Scholar 

  • MILLMAN, B. (1979) X-ray diffraction from chicken skeletal Muscle. In Motility in Cell Function: Proceedings of the First John M. Marshall Symposium in Cell Biology (edited by PEPE, F. A., SANGER, J. W. & NACHMIAS, V. T.) pp. 351–4. New York: Academic Press.

    Google Scholar 

  • MOODY, M. F. (1967) Structure of the sheath of bacteriophage T4. I. Structure of the contracted sheath and polysheath. J. Mol. Biol. 25, 167–200.

    Google Scholar 

  • PADRON, R. & HUXLEY, H. E. (1984) The effect of the ATP analogue AMP.PNP on the structure of crossbridges in vertebrate skeletal muscles: X-ray diffraction and mechanical studies. J. Muscle Res. Cell Motil. 6, 613–55.

    Google Scholar 

  • PEPE, F. A. (1972) The myosin filament: immunochemical and ultrastructural approaches to molecular organization. Cold Spring Harbor Symposium 37, 92–108.

    Google Scholar 

  • PEPE, F. A. (1979) The myosin filament: molecular structure. In Motility in Cell Function: Proceedings of the First John M. Marshall Symposium in Cell Biology (edited by PEPE, F. A., SANGER, J. W. & NACHMIAS, V. T.) pp. 103–16. New York: Academic Press.

    Google Scholar 

  • BAYMENT, I., RYPNIEWSKI, W. R., SCHMIDT-BASE, K., SMITH, R., TOMCHICK, D. R., BENNING, M. M., WINKELMANN, D. A., WESENBERG, G. & HOLDEN, H. (1993a) Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261, 50–8.

    Google Scholar 

  • RAYMENT, I., HOLDEN, H. M., WHITTAKER, M., YOHN, C. B., LORENTZ, M., HOLMES, K. & MILLIGAN, R. (1993b) Structure of the actin-myosin complex and its implications for muscle contraction. Science 261, 58–65.

    Google Scholar 

  • REEDY, M. K., HOLMES, K. C. & TREGEAR, R. T. (1965) Induced changes in orientation of the crossbridges of glycerinated insect flight muscle. Nature 207, 1276–80.

    Google Scholar 

  • REINACH, F., MASAKI, T. & FISCHMAN, D. (1983) Characterization of the C-protein from posterior latissimus dorsi muscle of the adult chicken: heterogeneity within a single sarcomere. J. Cell Biol. 96, 297–300.

    Google Scholar 

  • ROME, E. (1972) Relaxation of glycerinated muscle: low angle X-ray diffraction studies. J. Mol. Biol. 65, 331–45.

    Google Scholar 

  • SAAD, A., PARDEE, J. & FISCHMAN, D. (1986) Dynamic exchange of myosin molecules between thick filaments. Proc. Natl. Acad. Sci. USA 83, 9483–7.

    Google Scholar 

  • SCHOENBERG, M. (1988) Characterization of the myosin adenosine triphosphate (M.ATP) crossbridge in rabbit and frog skeletal muscle fibres. Biophys. J. 54, 135–48.

    Google Scholar 

  • SCHRÖDER, R. R., HOFMANN, W., MILLER, U. C., MENETRET, J. F. & WRAY, J. S. (1990) Electron microscopy of thick filaments from rabbit skeletal muscle. J. Muscle Res. Cell Motil. 11, 67–68 (abstract).

    Google Scholar 

  • SHELTON, G. D. & BANDMAN, E. (1985) Unusual fast myosin isozyme pattern in the lateral gastrocnemius of the chicken. J. Muscle Res. Cell Motil. 6, 435–46.

    Google Scholar 

  • SQUIRE, J. M. (1981) The Structural Basis of Molecular Contraction. New York: Plenum Press.

    Google Scholar 

  • SQUIRE, J. M., HARFORD, J. J., EDMAN, A. C. & SJOSTROM, M. (1982) Fine structure of the A-band in cryo-sections. III. Crossbridge distribution and the axial structure of the human C-zone. J. Mol. Biol. 155, 467–94.

    Google Scholar 

  • STARR, R., ALMOND, R. & OFFER, G. (1985) Location of C-protein, H-protein, and X-protein in rabbit skeletal muscle fibre types. J. Muscle Res. Cell Motil. 6, 227–56.

    Google Scholar 

  • STEWART, M. (1988) Computer image processing of electron micrographs of biological structures with helical symmetry. J. Electron Microscopy Technique 9, 325–58.

    Google Scholar 

  • STEWART, M. & KENSLER, R. W. (1986) Arrangement of heads in relaxed thick filaments from frog skeletal muscle. J. Mol. Biol. 192, 831–51.

    Google Scholar 

  • STEWART, M., KENSLER, R. W. & LEVINE, R. J. C. (1985) Three-dimensional reconstruction of thick filaments from Limulus and scorpion muscle. J. Cell Biol. 101, 402–11.

    Google Scholar 

  • STREHLER, E. E., CARLSSON, E., EPPENBERGER, H. M. & THORNELL, L. E. (1983) Ultrastructural localization of M-band proteins in chicken breast muscle as revealed by combined immunocytochemistry and ultramicrotomy. J. Mol. Biol. 166, 141–58.

    Google Scholar 

  • SWEENEY, H. L. & STULL, J. (1986) Phosphorylation of myosin in permeabilized mammalian cardiac and skeletal muscle cells. Am. J. Physiol. 250, 657–60.

    Google Scholar 

  • TRINICK, J. & ELLIOTT, A. (1979) Electron microscopic studies of thick filaments from vertebrate skeletal muscle. J. Mol. Biol. 131, 133–6.

    Google Scholar 

  • UYEDA, T. Q. P., WARRICK, H. M., KRON, S. J. & SPUDICH, J. A. (1991) Quantized velocities at low myosin densities in an in vitro motility assay. Nature 352, 307.

    Google Scholar 

  • VARIANO-MARSTON, E., FRANZINI-ARMSTRONG, C. & HASELGROVE, J. C. (1984) The structure and deposition of crossbridges in deep-etched fish muscle. J. Muscle Res. Cell Motil. 5, 363–86.

    Google Scholar 

  • WAKABAYSHI, T., AKIBA, T., HIROSE, K., TOMIOKA, A., TOKUNAGA, M., SUZUKI, M., TOYOSHIMA, C., SUTOH, K., YAMAMOTO, K., MATSUMOTO, T., SAEKI, K. & AMEMIYA, Y. (1988) Temperature-induced change of thick filament and location of the functional sites of myosin. Adv. Exp. Med. Biol. 226, 39–48.

    Google Scholar 

  • WINKELMANN, D. A., LOWEY, S. & PRESS, J. L. (1983) Monoclonal antibodies localize changes on myosin heavy chain isozymes during avian myogenesis. Cell 34, 295–306.

    Google Scholar 

  • WOODHEAD, J. L. & LOWEY, S. (1982) Size and shape of skeletal muscle M-Protein. J. Mol. Biol. 157, 149–54.

    Google Scholar 

  • WOODHEAD, J. L. & LOWEY, S. (1983) An in vitro study of the interactions of skeletal muscle M-protein and creatine kinase with myosin and its subfragments. J. Mol. Biol. 168, 831–46.

    Google Scholar 

  • WRAY, J. S. (1982) Organization of myosin in invertebrate thick filaments. In Basic Biology of Muscle: A Comparative Approach (edited by TWAROG, B. M., LEVINE, R. S. C. & DEWEY, M.) pp. 29–36. New York: Raven Press.

    Google Scholar 

  • WRAY, J. S. (1987) Structure of relaxed myosin filaments in relation to nucleotide state in vertebrate skeletal muscle. J. Muscle Res. Cell Motil. 8 62 (abstract).

    Google Scholar 

  • WRIGLEY, N. G. (1968) The lattice spacing of crystalline catalase as an internal standard of length in electron microscopy. J. Ultrastruc. Res. 24, 454–64.

    Google Scholar 

  • YAGI, W., O'BRIEN, E. J. & MATSUBARA, I. (1981) Changes of thick filament structure during contraction of frog striated muscle. Biophys. J. 33, 121–38.

    Google Scholar 

  • YANAGIDA, T., ARATA, T. & OOSAWA, F. (1985) Sliding distance of actin filament induced by a myosin crossbridge during one ATP hydrolysis cycle. Nature 316, 366–9.

    Google Scholar 

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Kensler, R.W., Woodhead, J.L. The chicken muscle thick filament: temperature and the relaxed cross-bridge arrangement. J Muscle Res Cell Motil 16, 79–90 (1995). https://doi.org/10.1007/BF00125312

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