Abstract
THE uniform angle and conformation of myosin subfragment 1 (S1) bound to actin filaments (F-actin) attest to the precise alignment and stereospecificity of the binding of these two contractile proteins1,2. Because actin filaments are polar3, myosin heads must swing or rotate about the head–tail junction in order to bind. Electron microscopy of isolated thick filaments4 and of myosin molecules5 suggests that the molecules are flexible, but myosin fragments and crossbridges have been reported not to interact with inappropriately oriented actin filaments6,7. Here we describe myofibrillar defects engendered by a site-directed mutation within the flight-muscle-specific actin gene of the fruitfly Drosophila. The mutation apparently retards sarcomere assembly: peripheral thick and thin filaments are misregistered and not incorporated into the Z-line. Therefore, a myosin filament encounters thin filaments with the 'wrong' polarity. We show that myosin heads tethered in a single thick filament can bind with opposite rigor crossbridge angles to flanking thin filaments, which are apparently of opposite polarities. Preservation of identical actomyosin interfaces requires that sets of heads originating from opposite sides of the thick filament swivel 180° relative to each other, implying that myosin crossbridges are as flexible as isolated molecules.
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References
Amos, L. A., Huxley, H. E., Holmes, K. C., Goody, R. S. & Taylor, K. A. Nature 299, 467–469 (1982).
Milligan, R. A. & Flicker, P. F. J. Cell. Biol. 105, 29–39 (1987).
Huxley, H. E. J. molec. Biol. 7, 2381–308 (1963).
Knight, P. & Trinick, J. J. molec. Biol. 177, 461–482 (1984).
Winkelmann, D. A. & Lowey, S. J. molec. Biol. 188, 595–612 (1986).
Sheetz, M. & Spudich, J. Nature 303, 31–35 (1983).
Trombitas, K. & Tigyi-Seges, A. Nature 309, 168–170 (1984).
Fyrberg, E. A. Oxford Surv. Eukaryotic Genes 1, 61–86 (1984).
Ball, E. et al. Cell 51, 221–228 (1987).
Hiromi, Y., Okamoto, H., Gehring, W. J. & Hotta, Y. Cell 44, 293–301 (1986).
Okamoto, H. et al. EMBO J. 5, 589–596 (1986).
Reedy, M. K. & Reedy, M. C. J. molec. Biol. 185, 145–176 (1985).
Taylor, K. A., Reedy, M. C., Cordova, L. & Reedy, M. K. Nature 310, 285–291 (1984).
Trombitas, K., Baatsen, P. & Pollack, G. J. ultrastruct. molec. Str. Res. 97, 39–49 (1986).
Walker, M. & Trinick, J. J. molec. Biol. 192, 661–667 (1986).
Walker, M. & Trinick, J. J. Muscle Res. Cell Motil. 9, 359–366 (1988).
Mendelson, R. A., Morales, M. F. & Botts, J. Biochemistry 12, 2250–2255 (1973).
Thomas, D. D., Seidel, J. C., Hyde, J. S. & Gergely, J. Proc. natn. Acad. Sci. U.S.A. 72, 1729–1733 (1975).
Spradling, A. C. & Rubin, G. M. Science 218, 341–347 (1982).
Nakamaye, K. L. & Eckstein, F. Nucleic Acids Res. 14, 9679–9698.
Maxam, A. & Gilbert, W. Meth. Enzym. 65, 499–460 (1980).
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Reedy, M., Beall, C. & Fyrberg, E. Formation of reverse rigor chevrons by myosin heads. Nature 339, 481–483 (1989). https://doi.org/10.1038/339481a0
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DOI: https://doi.org/10.1038/339481a0
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