Myosin molecule packing within the vertebrate skeletal muscle thick filaments. A complete bipolar model

• Autorzy: Skubiszak L. , Kowalczyk L.
• Języki publikacji: EN

Abstrakty

EN

Computer modelling related to the real dimensions of both the whole filament and the myosin molecule subfragments has revealed two alternative modes for myosin molecule packing which lead to the head disposition similar to that observed by EM on the surface of the cross-bridge zone of the relaxed vertebrate skeletal muscle thick fil­aments. One of the modes has been known for three decades and is usually incorpo­rated into the so-called three-stranded model. The new mode differs from the former one in two aspects: (1) myosin heads are grouped into asymmetrical cross-bridge crowns instead of symmetrical ones; (2) not the whole myosin tail, but only a 43-nm C-terminus of each of them is straightened and near-parallel to the filament axis, the rest of the tail is twisted. Concurrent exploration of these alternative modes has re­vealed their influence on the filament features. The parameter values for the filament models as well as for the building units depicting the myosin molecule subfragments are verified by experimental data found in the literature. On the basis of the new mode for myosin molecule packing a complete bipolar structure of the thick filament is cre­ated.

Słowa kluczowe

EN

thick filament; computer modelling; cross-bridge action; vertebrate; molecule; myosin; skeletal muscle

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2002
• Tom: 49
• Numer: 4
• Opis fizyczny: p.829-840,fig.

Twórcy

autor

Skubiszak L.

• Polish Academy of Sciences, Ks.Trojdena 4, 02-109 Warsaw, Poland

autor

Kowalczyk L.

Bibliografia

• Allakhverdov BL, Shpagina MD, Podlubnaya ZA. (1981) Study on structural elements of sarcomere: structure of thick filaments in muscle and after isolation. Acta Histochem Suppl.; 23: 83-7.
• Burke M, Harrington W. (1972) Geometry of the myosin dimer in high-salt media. II. Hydrodynamic studies on macromodels of myosin and its rod segments. Biochemistry.; 11: 1456-62.
• Cantino M, Squire JM. (1986) Resting myosin cross-bridge configuration in frog muscle thick filaments. J Cell Biol.; 102: 610-8.
• 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. (1977) Structure of A-segments from frog and rabbit skeletal muscle. J Mol Biol.; 109: 69-81.
• 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, Offer G. (1978) Shape and flexibility of the myosin molecule. J Mol Biol.; 123: 505-19. Elzinga M, Trus B. (1980) Methods in peptide and protein sequence analysis. Elsevier/ North-Holland, New York.
• Emes CH, Rowe A. (1978) Frictional properties and molecular weight of native and synthetic myosin filaments from vertebrate skeletal muscle. Biochim Biophys Acta.; 537: 125-44.
• Fraser RDB, MacRae TP. (1973) Conformation in fibrous proteins. Academic Press, New York.
• Geeves MA, Holmes KC. (1999) Structural mechanism of muscle contraction. Annu RevBiochem.; 68: 687-728.
• Harrison RG, Lowey S, Cohen C. (1971) Assembly of myosin. J Mol Biol.; 59: 531-5.
• 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 Â or turn upside down to reach rigor. J Mol Biol.; 273: 440-55.
• Huxley AF. (1980) Reflection on muscle. Princeton, Princeton University Press, 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.
• 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, Stewart M. (1986) An ultrastructural study of cross-bridge arrangement in the frog thigh muscle thick filament. Biophys J.; 49: 343-51.
• 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.
• Lamvik MK. (1978) Muscle thick filament mass measured by electron scattering. J Mol Biol.; 122: 55-68.
• Levine RJC. (1997) Differences in myosin head arrangement of relaxed thick filaments from Lethocerus and rabbit muscles. J Muscle Res Cell Motil.; 18: 529-43.
• Lowey S, Slayter H, Weeds A, Baker H. (1969) Substructure of the myosin molecule. 1. Subfragments of myosin by enzymic degradation. J Mol Biol.; 42: 1-29.
• 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.
• Molina MI, Kropp KE, Gulick J, Robbins J. (1987) The sequence of an embryonic myosin heavy chain gene and isolation of its corresponding cDNA. J Biol Chem.; 262: 6478-88.
• Morimoto K, Harrington WF. (1973) Isolation and composition of thick filaments from rabbit skeletal muscle. J Mol Biol.; 77: 165-75.
• Offer G. (1990) Skip residues correlate with bends in the myosin tail. J Mol Biol.; 216: 213-8.
• Pepe FA. (1967) The myosin filament. 1. Structural organization from antibody staining observed in electron microscopy. J Mol Biol.; 27: 203-25.
• Pepe FA, Drucker B. (1979) The myosin filament. 6. Myosin content. J Mol Biol.; 130: 379-93.
• 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.
• Sjostrom M, Squire JM. (1977) Fine structure of the A-band in cryo-sections. J Mol Biol.; 109: 49-68. Skubiszak L. (1990) Molecular organization in thick filament. Cell Biol.; 14: 207.
• Skubiszak L. (1992) New conception on muscle contraction mechanism: 1. Structural matching between the thick and thin filaments. J Muscle Res Cell Motil.; 13: 254.
• Skubiszak L. (1993) Force generation in muscle: 1. Molecular organization in the thick filament. Biocyb Biomed Eng.; 13: 75-96.
• Skubiszak L. (1996a) Structure and functional significance of the thick filament. Biofizika.; 41: 40-57.
• Skubiszak L. (1996b) Arrangement of myosin crossbridges on the surface of vertebrate skeletal muscle thick filament. Biophysics.; 41: 1167-74.
• Skubiszak L, Kowalczyk L. (1998). Computer system modelling muscle work. Technol Health Care.; 6: 139-49.
• Skubiszak L, Kowalczyk L. (2001) Relation between the mechanical properties of muscles and their structure on the molecular level. Engineering Transactions.; 49: 191-212.
• Skubiszak L, Kowalczyk L. (2002) The vertebrate skeletal muscle thick filaments are not three-stranded. Reinterpretation of some experimental data. Acta Biochim Polon.; 49: 841-853.
• 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. (1981) The structural basis of muscular contraction. Plenum Press, New York.
• Squire JM. (1992) Muscle filament lattice and stretch-activation: the match-mismatch model reassessed. J Muscle Res Cell Motil.; 13: 183-9.
• Squire JM. (1997) Architecture and function in the muscle sarcomere. Curr Opin Struct Biol.; 7: 247-57.
• Stewart M, Edwards P. (1984) Length of myosin rod and its proteolytic fragments determined by electron microscopy. FEBS Lett.; 168: 75-8.
• Stewart M, Kensler R. (1986) Arrangement of myosin heads in relaxed thick filaments from frog skeletal muscle. J Mol Biol.; 192: 831-51.
• Strehler EE, Strehler-Page MA, Perriard JC, Periasamy M, Nadal-Ginard B. (1986) Complete nucleotide and encoded amino acid sequence of a mammalian myosin heavy chain gene. Evidence against intron-dependent evolution of the rod. J Mol Biol.; 190: 291-317.
• Tregear RT, Squire JM. (1973) Myosin content and filament structure in smooth and striated muscles. J Mol Biol.; 77: 279-90.
• Trinick J, Elliott A. (1979) Electron microscope studies of thick filaments from vertebrate skeletal muscle. J Mol Biol.; 131: 133-6.
• Yu LC, Brenner B. (1986) High-resolution equatorial X-ray diffraction from single skinned rabbit psoas fibers. Biophys J.; 49: 133-5.
• Yu LC, Steven AC, Naylor GR, Gamble RC, Podolsky RJ. (1985) Distribution of mass in relaxed frog skeletal muscle and its redistribution upon activation. Biophys J.; 47: 311-21.