1887
Volume 2013, Issue 3
  • ISSN: 2305-7823
  • E-ISSN:

Abstract

High resolution information about the three-dimensional (3D) structure of myosin filaments has always been hard to obtain. Solving the 3D structure of myosin filaments is very important because mutations in human cardiac muscle myosin and its associated proteins (e.g. titin and myosin binding protein C) are known to be associated with a number of familial human cardiomyopathies (e.g. hypertrophic cardiomyopathy and dilated cardiomyopathy). In order to understand how normal heart muscle works and how it fails, as well as the effects of the known mutations on muscle contractility, it is essential to properly understand myosin filament 3D structure and properties in both healthy and diseased hearts.

The aim of this review is firstly to provide a general overview of the 3D structure of myosin thick filaments, as studied so far in both vertebrates and invertebrate striated muscles. Knowledge of this 3D structure is the starting point from which myosin filaments isolated from human cardiomyopathic samples, with known mutations in either myosin or its associated proteins (titin or C-protein), can be studied in detail. This should, in turn, enable us to relate the structure of myosin thick filament to its function and to understanding the disease process. A long term objective of this research would be to assist the design of possible therapeutic solutions to genetic myosin-related human cardiomyopathies.

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2014-01-01
2019-11-15
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References

  1. Huxley AF, Niedergerke R. Structural changes in muscle during contraction; interference microscopy of living muscle fibres. Nature. 1954; 173:4412:971973.
    [Google Scholar]
  2. Huxley HE, Hanson J. Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature. 1954; 173:4412:973976.
    [Google Scholar]
  3. Huxley HE. The mechanism of muscular contraction. Science. 1969; 164:3886:13561365.
    [Google Scholar]
  4. Rayment I, Rypniewski WR, Schmidt-Base K, Smith R, Tomchick DR, Benning MM, Winkelmann DA, Wesenberg G, Holden HM. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science. 1993; 261::5058.
    [Google Scholar]
  5. Dominguez R, Freyzon Y, Trybus KM, Cohen C. Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualization of the pre- power stroke state. Cell. 1998; 94::559571.
    [Google Scholar]
  6. AL-Khayat HA, Hudson L, Reedy MK, Irving TC, Squire JM. Myosin head configuration in relaxed insect flight muscle: X-ray modelled resting cross-bridges in a pre-powerstroke state are poised for actin binding. Biophys J. 2003; 85:2:10631079.
    [Google Scholar]
  7. Houdusse A, Szent-Gyorgyi AG, Cohen C. Three conformational states of scallop myosin S1. Proc Natl Acad Sci USA. 2000; 97::1123811243.
    [Google Scholar]
  8. Offer G, Moos C, Starr R. A new protein of the thick filaments of vertebrate skeletal myofibrils: extraction, purification and characterisation. J Mol Biol. 1973; 74:4:653676.
    [Google Scholar]
  9. Labeit S, Kolmerer B. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science. 1995; 270::293296.
    [Google Scholar]
  10. Trinick J. Cytoskeleton - titin as a scaffold and a spring. Curr Biol. 1996; 6::258260.
    [Google Scholar]
  11. Lehman W, Galinska-Rakoczy A, Hatch V, Tobacman LS, Craig R. Structural basis for the activation of muscle contraction by troponin and tropomyosin. J Mol Biol. 2009; 388:4:673681.
    [Google Scholar]
  12. Cammarato A, Craig R, Lehman W. Electron microscopy and three-dimensional reconstruction of native thin filaments reveal species-specific differences in regulatory strand densities. Biochem Biophys Res Commun. 2010; 391:1:193197.
    [Google Scholar]
  13. Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC. Atomic structure of the actin:DNase I complex. Nature. 1990; 347:6288:3744.
    [Google Scholar]
  14. Holmes KC, Popp D, Gebhard W, Kabsch W. Atomic model of the actin filament. Nature. 1990; 347:6288:4449.
    [Google Scholar]
  15. Oda T, Iwasa M, Aihara T, Maeda Y, Narita A. The nature of the globular- to fibrous-actin transition. Nature. 2009; 457::441445.
    [Google Scholar]
  16. Fujii T, Iwane AH, Yanagida T, Namba K. Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature. 2010; 467::724729.
    [Google Scholar]
  17. Li XE, Holmes KC, Lehman W, Jung H, Fischer S. The shape and flexibility of tropomyosin coiled coils: implications for actin filament assembly and regulation. J Mol Biol. 2010; 395:2:327329.
    [Google Scholar]
  18. Takeda S, Yamashita A, Maeda K, Maeda Y. Structure of the core domain of human cardiac troponin in the Ca2+-saturated form. Nature. 2003; 424::3541.
    [Google Scholar]
  19. Squire JM, AL-Khayat HA, Knupp C, Luther PK. 3D molecular architecture of muscle. Adv Protein Chem. 2005; 71::1787.
    [Google Scholar]
  20. Squire JM. Muscle myosin filaments: cores, crowns and couplings. Biophys Rev. 2009; 1::149160.
    [Google Scholar]
  21. Craig R. Isolation, electron microscopy and 3D reconstruction of invertebrate muscle myofilaments. Methods. 2012; 56::3343.
    [Google Scholar]
  22. AL-Khayat HA, Morris EP, Kensler RW, Squire JM. 3D structure of fish muscle myosin filaments by single particle analysis. J Struct Biol. 2006; 155::202217.
    [Google Scholar]
  23. AL-Khayat HA, Morris EP, Kensler RW, Squire JM. Myosin filament 3D structure in mammalian cardiac muscle. J Struct Biol. 2008; 163:2:117126.
    [Google Scholar]
  24. AL-Khayat HA, Kensler RW, Squire JM, Marston SB, Morris EP. Atomic model of the human cardiac myosin filament. Proc Natl Acad Sci USA. 2013; 110:1:318323.
    [Google Scholar]
  25. Zoghbi ME, Woodhead JL, Moss RL, Craig R. Three-dimensional structure of vertebrate cardiac muscle myosin filaments. Proc Natl Acad Sci USA. 2008; 105:7:23862390.
    [Google Scholar]
  26. Kensler RW. The mammalian cardiac muscle thick filament: crossbridge arrangement. J Struct Biol. 2005; 149:3:303331.
    [Google Scholar]
  27. Kensler RW, Stewart M. Frog skeletal muscle thick filaments are three-stranded. J Cell Biol. 1983; 96::17971802.
    [Google Scholar]
  28. Kensler RW, Stewart M. An ultrastructural study of cross-bridge arrangement in the frog thigh muscle thick filament. Biophys J. 1986; 49:1:343351.
    [Google Scholar]
  29. Kensler RW, Stewart M. An ultrastructural study of the cross-bridge arrangement in the fish skeletal muscle thick filament. J Cell Sci. 1989; 94::391401.
    [Google Scholar]
  30. Huxley HE, Brown W. The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J Mol Biol. 1967; 30::383434.
    [Google Scholar]
  31. Morris EP, Squire JM, Fuller GW. The 4-stranded helical arrangement of myosin heads on insect (Lethocerus) flight muscle thick filaments. J Struct Biol. 1991; 107::237249.
    [Google Scholar]
  32. Stewart M, Kensler RW, Levine RJ. Three-dimensional reconstruction of thick filaments from Limulus and scorpion muscle. J Cell Biol. 1985; 101::402411.
    [Google Scholar]
  33. Woodhead JL, Zhao F-Q, Craig R, Egelman EH, Alamo L, Padron R. Atomic model of a myosin filament in the relaxed state. Nature. 2005; 436::11951199.
    [Google Scholar]
  34. Alamo L, Wriggers W, Pinto A, Bartoli F, Salazar L, Zhao FQ, Craig R, Padron R. Three-dimensional reconstruction of tarantula myosin filaments suggests how phosphorylation may regulate myosin activity. J Mol Biol. 2008; 384:4:780797.
    [Google Scholar]
  35. Zhao F-Q, Craig R, Woodhead JL. Head-head interaction characterizes the relaxed state of Limulus muscle myosin filaments. J Mol Biol. 2009; 385::423431.
    [Google Scholar]
  36. Harrington WF, Rodgers ME. Myosin. Ann Rev Biochem. 1984; 53::3573.
    [Google Scholar]
  37. Squire JM, Luther PK, Morris EP. Organisation and properties of the striated muscle sarcomere. In: Squire JM, ed. Molecular Mechanisms in Muscular Contraction. Vol. 13. 1990;:148.
    [Google Scholar]
  38. Vibert P, Craig R. Electron microscopy and image analysis of myosin filaments from scallop striated muscles. J Mol Biol. 1983; 165:2:303320.
    [Google Scholar]
  39. Vibert P. Helical reconstruction of frozen-hydrated scallop myosin filaments. J Mol Biol. 1992; 223::661671.
    [Google Scholar]
  40. AL-Khayat HA, Morris EP, Squire JM. The 7-stranded structure of relaxed scallop muscle myosin filaments: support for a common theme of regulation in myosin-regulated muscles. J Struct Biol. 2009; 166:2:183194.
    [Google Scholar]
  41. Woodhead JL, Zhao F-Q, Craig R. Structural basis of the relaxed state of a Ca2+-regulated myosin filament and its evolutionary implications. Proc Natl Acad Sci USA. 2013; 110:21:85618566.
    [Google Scholar]
  42. Crowther RA, Padron R, Craig R. Arrangement of the heads of myosin in relaxed thick filaments from tarantula muscle. J Mol Biol. 1985; 184::429439.
    [Google Scholar]
  43. Offer G, Knight PJ, Burgess SA, Alamo L, Padron R. A new model for the surface arrangement of myosin molecules in tarantula thick filaments. J Mol Biol. 2000; 298::239260.
    [Google Scholar]
  44. Houdusse A, Kalabokis VN, Himmel D, Szent-Gyorgyi AG, Cohen C. Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell. 1999; 97::459470.
    [Google Scholar]
  45. Houdusse A, Sweeney HL. Myosin motors: missing structures and hidden springs. Curr Opin Struc Biol. 2001; 11::182194.
    [Google Scholar]
  46. Irving M, Allen TS, Sabidodavid C, Craik JS, Brandmeier B, Kendrick- Jones J, Corrie JET, Trentham DR, Goldman YE. Tilting of the light chain region of myosin during step length changes and active force generation in skeletal muscle. Nature. 1995; 375::688691.
    [Google Scholar]
  47. Uyeda T, Abramson PD, Spudich JA. The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc Natl Sci USA. 1996; 93:9:44594464.
    [Google Scholar]
  48. Holmes KC. The swinging lever-arm hypothesis of muscle contraction. Curr Biol. 1997; 7::R112R188.
    [Google Scholar]
  49. Geeves MA, Holmes KC. The molecular mechanism of muscle contraction. Adv Protein Chem. 2005; 71::161193.
    [Google Scholar]
  50. Kensler RW, Stewart M. The relaxed crossbridge pattern in isolated rabbit psoas muscle thick filaments. J Cell Sci. 1993; 105::841848.
    [Google Scholar]
  51. Stewart M, Kensler RW. Arrangement of myosin heads in relaxed thick filaments from frog skeletal muscle. J Mol Biol. 1986; 192::831851.
    [Google Scholar]
  52. Kensler RW, Woodhead JL. The chicken muscle thick filament: temperature and the relaxed crossbridge arrangement. J Musc Res Cell Motil. 1995; 16::7990.
    [Google Scholar]
  53. Eakins F, AL-Khayat HA, Morris EP, Kensler RW, Squire JM. 3D structure of fish muscle myosin filaments. J Struct Biol. 2002; 137::154163.
    [Google Scholar]
  54. Kensler RW, Harris SP. The structure of isolated cardiac myosin thick filaments from cardiac myosin binding protein-C knockout mice. Biophys J. 2008; 94::17971802.
    [Google Scholar]
  55. AL-Khayat HA, Morris EP, Squire JM. Single Particle Analysis: a new approach to solving the 3D structure of Myosin Filaments. Rev J Musc Res Cell Motil. 2004; 25:8:635644.
    [Google Scholar]
  56. AL-Khayat HA, Kensler RW, Morris EP, Squire JM. Three-Dimensional structure of the M-region (barezone) of vertebrate striated muscle myosin filaments by single particle analysis. J Mol Biol. 2010; 403:5:763776.
    [Google Scholar]
  57. AL-Khayat HA, Kensler RW, Squire JM, Marston SB, Morris EP. Three-dimensional structure of human cardiac muscle myosin filaments by electron microscopy and single particle analysis. Biophys J. 2012; 102:3:149a150a.
    [Google Scholar]
  58. Watkins H, Rosenzweig A, Hwang D-S, Levi T, McKenna WJ, Seidman CE, Seidman JG. Characteristics and prognostic implications of myosin missense mutations in familial hypertrophic cardiomyopathy. N Engl J Med. 1992; 326::11081114.
    [Google Scholar]
  59. Watkins H, Conner D, Thierfelder L, Jarcho JA, MacRae C, McKenna WJ, Maron BJ, Seidman JG, Seidman CE. Mutations in the cardiac myosin binding protein-C gene on chromosome 11 cause familial hypertrophic cardiomyopathy. Nat Gene. 1995; 11::434437.
    [Google Scholar]
  60. Richard P, Charron P, Carrier L, Ledeuil C, Cheav T, Pichereau C, Benaiche A, Isnard R, Dubourg O, Burban M, Gueffet JP, Millaire A, Desnos M, Schwartz K, Hainque B, Komajda M. Hypertrophic cardiomyopathy distribution of disease genes, spectrum of mutations and implications for a molecular diagnosis strategy. Circulation. 2003; 107:17:22272232.
    [Google Scholar]
  61. Seidman JG, Seidman CE. The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell. 2001; 104::557567.
    [Google Scholar]
  62. Seidman CE, Seidman JG. Identifying sarcomere gene mutations in hypertrophic cardiomyopathy: a personal history. Circ Res. 2011; 108:6:743750.
    [Google Scholar]
  63. Tajsharghi H, Thornell LE, Lindberg C, Lindvall B, Henriksson KG, Oldfors A. Myosin storage myopathy associated with a heterozygous missense mutation in MYH7. Ann Neurol. 2003; 54::494500.
    [Google Scholar]
  64. Tajsharghi H. Thick and thin filament gene mutations in striated muscle diseases. Int J Mol Sci. 2008; 9::12591275.
    [Google Scholar]
  65. Morimoto S. Sarcomeric proteins and inherited cardiomyopathies. Cardiovasc Res. 2008; 77::659666.
    [Google Scholar]
  66. Marston S. How do mutations in contractile proteins cause the primary familial cardiomyopathies. J Cardiovasc Trans Res. 2011; 4::245255.
    [Google Scholar]
  67. Bennett P, Craig R, Starr R, Offer G. The ultrastructural location of C-protein, X-protein and H-protein in rabbit muscle. J Musc Res Cell Motil. 1986; 7:6:550567.
    [Google Scholar]
  68. LeWinter MM, Granzier H. Cardiac titin: a multifunctional giant. Circulation. 2010; 121:19:21372145.
    [Google Scholar]
  69. Liversage AD, Holmes D, Knight PJ, Tskhovrebova L, Trinick J. Titin and the sarcomere symmetry paradox. J Mol Biol. 2001; 305:3:401409.
    [Google Scholar]
  70. Tskhovrebova L, Trinick J. Roles of titin in the structure and elasticity of the sarcomere. J Biomed Biotechnol. 2010; article 612482.
    [Google Scholar]
  71. van Heel M, Gowen B, Matadeen R, Orlova EV, Finn R, Pape T, Cohen D, Stark H, Schmidt R, Schatz M, Patwardhan A. Single-particle electron cryo-microscopy: towards atomic resolution. Quart Rev Biophys. 2000; 33::307369.
    [Google Scholar]
  72. De Rosier DJ, Klug A. Reconstruction of three dimensional structures from electron micrographs. Nature. 1968; 217:5124:130134.
    [Google Scholar]
  73. AL-Khayat HA, Bhella D, Kenney JM, Roth J-F, Kingsman AJ, Martin-Rendon E, Saibil HR. Yeast Ty Retrotransposons assemble into virus-like particles whose T-numbers depend on the C-terminal length of the capsid protein. J Mol Biol. 1999; 292:1:6573.
    [Google Scholar]
  74. Wendt T, Taylor D, Trybus KM, Taylor K. Three-dimensional image reconstruction of dephosphorylated smooth muscle heavy meromyosin reveals asymmetry in the interaction between myosin heads and placement of subfragment 2. Proc Natl Acad Sci USA. 2001; 98::43614366.
    [Google Scholar]
  75. Malik F, Teerlik J, Escandon R, Clarke C, Wolfe A. The selective cardiac myosin activator, CK1827452, a calcium-independent inotrope, increases left ventricular systolic function by increasing ejection time rather than the velocity of contraction. Circulation. 2006; 114:18:441.
    [Google Scholar]
  76. Teerlink JR. A novel approach to improve cardiac performance: cardiac myosin activators. Heart Fail Rev. 2009; 14:4:289298.
    [Google Scholar]
  77. Zewail AH. Four-dimensional electron microscopy. Science. 2010; 238::187193.
    [Google Scholar]
  78. Flannigan DJ, Zewail AH. 4D electron microscopy: principles and applications. Acc Chem Res. 2012; 45::18281839.
    [Google Scholar]
  79. Lorenz UJ, Zewail AH. Biomechanics of DNA structures visualised by 4D electron microscopy. Proc Natl Acad Sci USA. 2013; 110::28222827.
    [Google Scholar]
  80. Harris SP, Lyons RG, Bezold KL. In the thick of it: HCM-causing mutations in myosin binding proteins of the thick filament. Circ Res. 2011;  108:6:751764. (url: http://www.ncbi.nlm.nih.gov/pubmed/21415409).
    [Google Scholar]
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