Advertisement

Introduction

  • David Aitchison Smith
Chapter

Abstract

Our current understanding of the molecular mechanism of muscle contraction is the product of two millennia of speculation, dissection and theorising, in which the sarcomeres, which constitute the one-dimensional periodic structure of striated muscle, slowly came to the fore. In 1953, A.F. Huxley and H.E. Huxley observed that each sarcomere was composed of two lattices of interdigitating filaments which slid into each other as the muscle contracted, overthrowing the paradigm that contraction was caused by shrinking filaments. The dominant theory of contraction is built around the ‘swinging-lever-arm’ model, in which each myosin motor is attached to its thick filament by a 10 nm heavy chain which acts as a lever-arm, causing sliding when the motor is bound to a thin filament made of actin. This introduction presents an overview of muscle structure, contractile behaviour and different theories of contractility, which form the background for the construction of quantitative theories.

Keywords

Contraction Myosin Actin Sarcomere Tetanus 

References

  1. Astumian RD (1997) Thermodynamics and kinetics of a Brownian motor. Science 276:917–922CrossRefGoogle Scholar
  2. Baker J, Thomas DD (2000) A thermodynamic muscle model and a chemical basis for A.V. Hill’s muscle equation. J Muscle Res Cell Motil 21:335–344CrossRefGoogle Scholar
  3. Carlson FD, Wilkie DR (1974) Muscle physiology. Prentice-Hall, Englewood CliffsGoogle Scholar
  4. Cooke R, Franks K (1980) All myosin heads form bonds with actin in rigor rabbit skeletal muscle. Biochemist 19:2265–2269CrossRefGoogle Scholar
  5. Credi A, Silvi S, Venturi M (2014) Molecular machines and motors, Topics in Current Chemistry, vol 354. Springer, BerlinGoogle Scholar
  6. Elliott GF, Worthington CR (2001) Muscle contraction: viscous-like frictional forces and the impulsive model. Int J Biol Macromol 29:213–218CrossRefGoogle Scholar
  7. Elliott GF, Lowy J, Millman BM (1965) X-ray diffraction from living striated muscle during contraction. Nature 206:1357–1358CrossRefGoogle Scholar
  8. Fajer PG, Fajer EA, Thomas DD (1998) Myosin heads have a broad orientational distribution during isometric muscle contraction: time-resolved EPR studies using caged ATP. Proc Natl Acad Sci USA 87:5538–5542CrossRefGoogle Scholar
  9. Finer JT, Simmons RM, Spudich JA (1994) Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368:113–119CrossRefGoogle Scholar
  10. Funatsu T, Harada Y, Tokunaga M, Saito K, Yanagida T (1995) Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution. Nature 374:555–559CrossRefGoogle Scholar
  11. Gordon AM, Huxley AF, Julian F (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol (London) 184:170–192CrossRefGoogle Scholar
  12. Goss CM (1968) On movement of muscles by Galen of Pergamon. Am J Anat 123:24–25CrossRefGoogle Scholar
  13. Haselgrove JC, Huxley HE (1972) X-ray evidence for a conformational change in the actin-containing filaments of vertebrate striated muscle. Cold Spring Harb Symp Quant Biol 37:341–352CrossRefGoogle Scholar
  14. Herzberg O, James MNG (1988) Refined crystal structure of troponin C from turkey skeletal muscle at 2.0Å resolution. J Mol Biol 203:761–779CrossRefGoogle Scholar
  15. Hill AV (1953) The mechanics of active muscle. Proc R Soc B141:104–117Google Scholar
  16. Hirose K, Wakabayashi T (1988) Thin filaments of rabbit skeletal muscle are in helical register. J Mol Biol 204:797–801CrossRefGoogle Scholar
  17. Hitchcock-DeGregori S, Irving T (2014) Hugh E. Huxley: the compleat biophysicist. Biophys J 107:1493–1501CrossRefGoogle Scholar
  18. Holmes KC, Popp D, Gebhard W, Kabsch W (1990) Atomic model of the actin filament. Nature 347:44–49CrossRefGoogle Scholar
  19. Howard J (2001) Mechanics of motor proteins and the cytoskeleton. Sinauer Assoc. Inc., SunderlandGoogle Scholar
  20. 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 150Å or turn upside down to reach rigor. J Mol Biol 273:440–455CrossRefGoogle Scholar
  21. Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:257–318CrossRefGoogle Scholar
  22. Huxley HE (1963) Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle. J Mol Biol 7:281–308CrossRefGoogle Scholar
  23. Huxley HE (2004) Fifty years of muscle and the sliding filament hypothesis. Eur J Biochem 271:1403–1415CrossRefGoogle Scholar
  24. Huxley HE, Hanson J (1954) Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173:973–976CrossRefGoogle Scholar
  25. Huxley AF, Niedegerke R (1954) Structural changes in muscle during contraction: interference microscopy of living muscle fibres. Nature 173:971–973CrossRefGoogle Scholar
  26. Huxley AF, Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233:533–538CrossRefGoogle Scholar
  27. Ingels NB (1979) The molecular basis of force development in muscle. Palo Alto Medical Research Foundation, Palo Alto, pp 147–162Google Scholar
  28. Iwazumi T (1970) A new field theory of muscle contraction. Ph.D. thesis, University of PennsylvaniaGoogle Scholar
  29. Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC (1990) Atomic structure of the actin: DNase I complex. Nature 347:37–44CrossRefGoogle Scholar
  30. Edman KAP (1979) The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J Physiol (London) 291:143–159CrossRefGoogle Scholar
  31. Katz B (1966) Nerve, muscle and synapse. McGraw Hill, Inc, New YorkGoogle Scholar
  32. Kitamura K, Tokunaga M, Iwane AH, Yanagida T (1999) A single myosin head moves along an actin filament with regular steps of 5.3 nanometres. Nature 397:120–134CrossRefGoogle Scholar
  33. Kron SJ, Spudich JA (1986) Fluorescent actin filaments move on myosin fixed to a glass surface. Proc Natl Acad Sci USA 83:6272–6276CrossRefGoogle Scholar
  34. Linari M, Piazessi G, Dobbie I, Koubassova N, Reconditi M, Narayanan T, Diat O, Irving M, Lombardi V (2000) Interference fine structure and sarcomeric length dependence of the axial x-ray pattern from active single muscle fibers. Proc Natl Acad Sci USA 97:7226–7231CrossRefGoogle Scholar
  35. Lombardi V, Piazzesi G (1992) Force response in steady lengthening of active single muscle fibres. In: Simmons RM (ed) Muscular contraction. Cambridge University Press, CambridgeGoogle Scholar
  36. Luther PK (2004) Evolution of the muscle lattice in the vertebrate kingdom. Microsc Anal, March: 9–11Google Scholar
  37. Luther PK, Squire J (1980) Three-dimensional structure of the vertebrate muscle A-band. J Mol Biol 141:409–439CrossRefGoogle Scholar
  38. Lymn RW, Taylor EW (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemist 10:4617–4624CrossRefGoogle Scholar
  39. MacIntosh BR, Gardner PF, McComas AJ (2006) Skeletal muscle, form and function. Human Kinetics, ChampaignGoogle Scholar
  40. Maquet P, Nayler M, Ziggelaar A, Croone W (2000) William Croone: on the reason of the movement of the muscles. Trans Am Philos Soc 90(1):130CrossRefGoogle Scholar
  41. Martonosi A (2000) Animal electricity, Ca2+ and muscle contraction. A brief history of muscle research. Acta Chim Pol 47:493–516Google Scholar
  42. Matsubara I, Goldman YE, Simmons RM (1984) Changes in the lateral filament spacing of skinned muscle fibres when cross-bridges attach. J Mol Biol 173:15–33CrossRefGoogle Scholar
  43. Miklos S, Kellermayer Z, Smith SB, Granzier HL, Bustamente C (1997) Folding-unfolding transitions in single titin molecules characterised with laser tweezers. Science 276:1112–1116CrossRefGoogle Scholar
  44. Moore PB, Huxley HE, DeRosier DJ (1970) Three-dimensional reconstruction of F-actin, thin filaments and decorated thin filaments. J Mol Biol 50:279–288CrossRefGoogle Scholar
  45. Needham DM (1971) Machina Carnis: the biochemistry of muscular contraction in its historical development. C.U.P., CambridgeCrossRefGoogle Scholar
  46. Offer G, Knight PJ, Burgess SA, Alamo L, Padron R (2000) A new model for the surface arrangement of myosin molecules in tarantula thick filaments. J Mol Biol 298:239–260CrossRefGoogle Scholar
  47. Oplatka A (1997) Critical review of the swinging crossbridge theory and of the cardinal active role of water in muscle contraction. Crit Rev Biochem Mol Biol 32:307–360CrossRefGoogle Scholar
  48. Peachey LD (1965) The sarcoplasmic reticulum and transverse tubules of the frog’s sartorius. J Cell Biol 25:209–231CrossRefGoogle Scholar
  49. Piazzesi G, Reconditi M, Linari M, Lucii L, Bianco P, Brunello E, Decostre V, Stewart A, Gore DB, Irving TC, Irving M, Lombardi V (2007) Skeletal muscle performance determined by modulation of number of myosin motors rather than motor force or stroke size. Cell 131:784–795CrossRefGoogle Scholar
  50. Rayment I, Rypniewski WR, Schmidt-Base K, Smith R, Tomchick DR, Benning MM, Winkelmann DA, Wesenberg G, Holden HM (1993) Three-dimensional structure of a myosin subfragment-1: a molecular motor. Science 261:50–65CrossRefGoogle Scholar
  51. Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276:1109–1112CrossRefGoogle Scholar
  52. Rome LC (2006) Design and function of superfast muscles: new insights into the physiology of skeletal muscle. Annu Rev Physiol 68:193–221CrossRefGoogle Scholar
  53. Ruegg JC (2017) Calcium in muscle activation; a comparative approach. Springer, BerlinGoogle Scholar
  54. Squire J (1981) The structural basis of muscle contraction. Plenum, New YorkCrossRefGoogle Scholar
  55. Stephenson DG, Stewart AW, Wilson GJ (1989) Dissociation of force from myofibrillar MgATPase and stiffness at short sarcomere lengths in rat and toad skeletal muscle. J Physiol (London) 410:351–366CrossRefGoogle Scholar
  56. Sundaralingam M, Bergstrom R, Strasburg G, Rao ST, Rowchowdhury P, Greaser M, Wang BC (1985) Molecular structure of troponin C from chicken skeletal muscle at 3-angstrom resolution. Science 227:945–948CrossRefGoogle Scholar
  57. Suzuki Y, Yasunaga T, Ohkura R, Wakabayashi T, Sutoh K (1998) Swing of the lever arm of a myosin motor at the isomerization and phosphate-release steps. Nature 396:380–383CrossRefGoogle Scholar
  58. Takeda S, Yamashita A, Maeda K, Maeda Y (2003) Structure of the core domain of human cardiac troponin in the Ca2+-saturated form. Nature 424:35–41CrossRefGoogle Scholar
  59. Tskhovrebova L, Trinick J, Sleep J, Simmons RM (1997) Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature 387:308–312CrossRefGoogle Scholar
  60. Vibert P, Craig R, Lehman W (1997) Steric model for activation of muscle thin filaments. J Mol Biol 266:8–14CrossRefGoogle Scholar
  61. Westerblad H, Allen DG, Lannergren J (2002) Muscle fatigue: lactic acid or inorganic phosphate the major cause? News Physiol Soc 17:17–21Google Scholar
  62. Yomosa S (1985) Solitary excitations in muscle proteins. Phys Rev A 32:1752–1758CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • David Aitchison Smith
    • 1
  1. 1.Department of Physiology, Anatomy and MicrobiologyLa Trobe UniversityMelbourneAustralia

Personalised recommendations