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2002 | 49 | 4 | 841-853
Article title

The vertebrate skeletal muscle thick filaments are not three-stranded. Reinterpretation of some experimental data*

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Computer simulation of mass distribution within the model and Fourier transforms of images depicting mass distribution are explored for verification of two alternative modes of the myosin molecule arrangement within the vertebrate skeletal muscle thick filaments. The model well depicting the complete bipolar structure of the thick filament and revealing a true threefold-rotational symmetry is a tube covered by two helices with a pitch of 2 × 43 nm due to arrangement of the myosin tails along a helical path and grouping of all myosin heads in the crowns rotated by 240° and each containing three cross-bridges separated by 0°, 120°, and 180°. The cross-bridge crown parameters are verified by EM images as well as by optical and low-angle X-ray diffraction patterns found in the literature. The myosin tail arrangement, at which the C-terminus of about 43-nm length is near-parallel to the filament axis and the rest of the tail is quite strongly twisted around, is verified by the high-angle X-ray diffraction patterns. A consequence of the new packing is a new way of movement of the myosin cross-bridges, namely, not by bending in the hinge domains, but by unwrapping from the thick filament surface towards the thin filaments along a helical path.
Physical description
  • Ashton FT, Weisel J, Pepe FA. (1992) The myosin filament. XIV. Backbone structure. Biophys J.; 61: 1513-28.
  • Bennett PM. (1981) The structure of spindle-shaped paracrystals of light meromyosin. J Mol Biol.; 146: 201-21.
  • Bordas J, Diakun GP, Diaz FG, Harries JE, Lewis RA, Lowy J, Mant GR, Towns-Andrews E. (1993) Two-dimensional time-resolved X-ray diffraction studies of live isometrically contracting frog sartorius muscle. J Muscle Res Cell Motil.; 14: 311-24.
  • Brenner B, Yu LC. (1991) Characterization of radial force and radial stiffness in Ca2+-activated skinned fibres of the rabbit psoas muscle. J Physiol.; 441: 703-18.
  • Cantino M, Squire JM. (1986) Resting myosin cross-bridge configuration in frog muscle thick filaments. J Cell Biol.; 102: 610-18.
  • Cantino ME, Brown LD, Chew M, Luther PK, Squire JM. (2000) A-band architecture in vertebrate skeletal muscle: polarity of the myosin head array. J Muscle Res Cell Motil.; 21: 681-90.
  • Cantino ME, Chew MW, Luther PK, Morris E, Squire JM. (2002) Structure and nucleotide- dependent changes of thick filaments in relaxed and rigor plaice fin muscle. J Struct Biol.; 137: 164-75.
  • Chew MWK, Squire JM. (1995) Packing of alpha-helical coiled-coil myosin rods in vertebrate muscle thick filaments. J Struct Biol.; 115: 233-49.
  • Cohen C, Holmes KC. (1963) X-ray diffraction evidence for alpha-helical coiled-coils in native muscle. J Mol Biol.; 6: 423-32.
  • Craig R, Alamo L, Padron R. (1992) Structure of the myosin filaments of relaxed and rigor vertebrate striated muscle studied by rapid freezing electron microscopy. J Mol Biol.; 228: 474-87.
  • Eakins F, AL-Khayat HA, Kensler RW, Morris EP, Squire JM. (2002) 3D structure of fish muscle myosin filaments. J Struct Biol.; 137: 154-63.
  • Elliott A, Lowy J, Parry DAD, Vibert PJ. (1968) Puzzle of the coiled coils in the alpha-protein paramyosin. Nature.; 218: 656-9.
  • Gonzalez RC, Wintz P. (1987) Image transforms. In Digital image processing. 61-137. Addison- Wesley Publishing Comp. Massachusetts.
  • Harrison RG, Lowey S, Cohen C. (1971) Assembly of myosin. J Mol Biol.; 59: 531-5.
  • Haselgrove JCR, Rodger CD. (1980) The interpretation of X-ray diffraction patterns from vertebrate striated muscle. J Muscle Res Cell Motil.; 1: 371-90.
  • Holmes KC. (1997) The swinging lever-arm hypothesis of muscle contraction. Curr Biol.; 7: R112-18.
  • Hudson L, Harford JJ, Denny RC, Squire JM. (1997) Myosin head configuration in relaxed fish muscle: resting state myosin heads must swing axially by up to 150 Å or turn upside down to reach rigor. J Mol Biol.; 273: 440-55.
  • Huxley AF. (1980) Reflection on muscle. Princeton University Press, Princeton, New Jersey.
  • Huxley HE. (1963) Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle. J Mol Biol.; 7: 281-308.
  • Huxley HE, Brown W. (1967) The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J Mol Biol.; 30: 383-434.
  • Ip W, Heuser J. (1983) Direct visualization of the myosin cross-bridge helices on relaxed rabbit psoas thick filaments. J Mol Biol.; 171: 105-9.
  • Kensler RW, Stewart M. (1983) Frog skeletal muscle thick filaments are three-stranded. J Cell Biol.; 96: 1797-802.
  • Kensler RW, Woodhead JL. (1995) The chicken muscle thick filament: temperature and the relaxed cross-bridge arrangement. J Muscle Res Cell Motil.; 16: 79-90.
  • Kensler RW, 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.
  • Klug A, Crick FHC, Wyckoff HW. (1958) Diffraction by helical structures. Acta Cryst.; 11: 199-212
  • Kowalczyk L, Skubiszak L. (1999) Algorithm for fast calculation of mass distribution. Biocyb Biomed Eng.; 19: 31-38.
  • Levine RJC. (1993) Evidence for overlapping myosin heads on relaxed thick filaments of fish, frog, and scallop striated muscles. J Struct Biol.; 110: 99-110.
  • Levine RJC. (1997) Differences in myosin head arrangement on relaxed thick filaments from Lethocerus and rabbit muscles. J Muscle Res Cell Motil.; 18: 529-43.
  • Linari M, Piazzesi G, Dobbie I, Koubassova N, Reconditi M, Narayanan T, Diat O, Irving M, Lombardi V. (2000) Interference fine structure and sarcomere length dependence of the axial X-ray pattern from active single muscle fibers. Proc Natl Acad Sci U S A.; 97: 7226-31.
  • Luther PK, Squire JM. (1980) Three-dimensional structure of the vertebrate muscle A-band. II. The myosin filament superlattice. J Mol Biol.; 141: 409-39.
  • Malinchik SB, Lednev VJ. (1992) Interpretation of the X-ray diffraction pattern from relaxed skeletal muscle and modelling of the thick filament structure. J Muscle Res Cell Motil.; 13: 406-19.
  • Malinchik SB, Xu S, Yu LC. (1997) Temperature-induced structural changes in the myosin thick filament of skinned rabbit psoas muscle. Biophys J.; 73: 2304-12.
  • Podlubnaya ZA, Kalamkarova MB, Nankina VP. (1969) Polymorphism of the light meromyosin crystallization. J Mol Biol.; 46: 591-2.
  • Rayment I, Rypniewski WR, Schmidt-Base K, Smith R, Tomchick DR, Benning MM, Winkelmann DA, Wessenberg G, Holden HM. (1993) Three-dimensional structure of myosin subfragment-1: A molecular motor. Science.; 261: 50-8.
  • Skubiszak L. (1993) Mechanism of muscle contraction. Technol Health Care.; 1: 133-42.
  • Skubiszak L, Kowalczyk L. (2001) Relation between the mechanical properties of muscles and their structure on the molecular level. Eng Trans.; 49: 191-212.
  • Skubiszak L, Kowalczyk L. (2002) Myosin molecule packing within the vertebrate skeletal muscle thick filaments. A complete bipolar model. Acta Biochim Polon.; 49: 829-40.
  • Squire JM. (1972) General model of myosin filament structure. 2. Myosin filaments and crossbridge interactions in vertebrate striated and insect flight muscles. J Mol Biol.; 72: 125-38.
  • Squire JM. (1973) General models of myosin filament structure. 3. Molecular packing arrangements in myosin filaments. J Mol Biol.; 77: 291-323.
  • Squire JM. (1997) Architecture and function in the muscle sarcomere. Curr Opin Struct Biol.; 7: 247-57.
  • Stewart M, Kensler R. (1986) Arrangement of myosin heads in relaxed thick filaments from frog skeletal muscle. J Mol Biol.; 192: 831-51.
  • Xu S, Malinchik S, Gilroy D, Kraft T, Brenner B, Yu LC. (1997) X-ray diffraction studies of cross-bridges weakly bound to actin in relaxed skinned fibers of rabbit psoas muscle. Biophys J.; 73: 2292-303.
  • Yagi N, Offer GW. (1981) X-ray diffraction and electron microscopy of a light meromyosin tactoid. J Mol Biol.; 151: 467-90.
  • Yagi N, O'Brien EJ, Matsubara I. (1981) Changes of thick filament structure during contraction of frog striated muscle. Biophys J.; 33: 121-38.
  • Yu LC, Brenner B. (1986) High-resolution equatorial X-ray diffraction from single skinned rabbit psoas fibers. Biophys J.; 49: 133-5.
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