Mechanics and models of the myosin motor.
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Journal: 2000/September - Philosophical Transactions of the Royal Society B: Biological Sciences
ISSN: 0962-8436
Abstract:
In striated muscles, shortening comes about by the sliding movement of thick filaments, composed mostly of myosin, relative to thin filaments, composed mostly of actin. This is brought about by cyclic action of 'cross-bridges' composed of the heads of myosin molecules projecting from a thick filament, which attach to an adjacent thin filament, exert force for a limited time and detach, and then repeat this cycle further along the filament. The requisite energy is provided by the hydrolysis of a molecule of adenosine triphosphate to the diphosphate and inorganic phosphate, the steps of this reaction being coupled to mechanical events within the cross-bridge. The nature of these events is discussed. There is good evidence that one of them is a change in the angle of tilt of a 'lever arm' relative to the 'catalytic domain' of the myosin head which binds to the actin filament. It is suggested here that this event is superposed on a slower, temperature-sensitive change in the orientation of the catalytic domain on the actin filament. Many uncertainties remain.
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Philos Trans R Soc Lond B Biol Sci 355(1396): 433-440
PMID: 10836496

Mechanics and models of the myosin motor.

Abstract

In striated muscles, shortening comes about by the sliding movement of thick filaments, composed mostly of myosin, relative to thin filaments, composed mostly of actin. This is brought about by cyclic action of 'cross-bridges' composed of the heads of myosin molecules projecting from a thick filament, which attach to an adjacent thin filament, exert force for a limited time and detach, and then repeat this cycle further along the filament. The requisite energy is provided by the hydrolysis of a molecule of adenosine triphosphate to the diphosphate and inorganic phosphate, the steps of this reaction being coupled to mechanical events within the cross-bridge. The nature of these events is discussed. There is good evidence that one of them is a change in the angle of tilt of a 'lever arm' relative to the 'catalytic domain' of the myosin head which binds to the actin filament. It is suggested here that this event is superposed on a slower, temperature-sensitive change in the orientation of the catalytic domain on the actin filament. Many uncertainties remain.

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Selected References

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  • Barclay CJ. A weakly coupled version of the Huxley crossbridge model can simulate energetics of amphibian and mammalian skeletal muscle. J Muscle Res Cell Motil. 1999 Feb;20(2):163–176. [PubMed] [Google Scholar]
  • Bershitsky SYu, Tsaturyan AK. Effect of joule temperature jump on tension and stiffness of skinned rabbit muscle fibers. Biophys J. 1989 Nov;56(5):809–816.[PMC free article] [PubMed] [Google Scholar]
  • Bershitsky SY, Tsaturyan AK. Tension responses to joule temperature jump in skinned rabbit muscle fibres. J Physiol. 1992 Feb;447:425–448.[PMC free article] [PubMed] [Google Scholar]
  • Bershitsky SY, Tsaturyan AK, Bershitskaya ON, Mashanov GI, Brown P, Burns R, Ferenczi MA. Muscle force is generated by myosin heads stereospecifically attached to actin. Nature. 1997 Jul 10;388(6638):186–190. [PubMed] [Google Scholar]
  • Davis JS, Harrington WF. A single order-disorder transition generates tension during the Huxley-Simmons phase 2 in muscle. Biophys J. 1993 Nov;65(5):1886–1898.[PMC free article] [PubMed] [Google Scholar]
  • Díaz Baños FG, Bordas J, Lowy J, Svensson A. Small segmental rearrangements in the myosin head can explain force generation in muscle. Biophys J. 1996 Aug;71(2):576–589.[PMC free article] [PubMed] [Google Scholar]
  • 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 Sep 4;94(5):559–571. [PubMed] [Google Scholar]
  • Duke TA. Molecular model of muscle contraction. Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):2770–2775.[PMC free article] [PubMed] [Google Scholar]
  • Ford LE, Huxley AF, Simmons RM. Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol. 1977 Jul;269(2):441–515.[PMC free article] [PubMed] [Google Scholar]
  • Burmeister Getz E, Cooke R, Selvin PR. Luminescence resonance energy transfer measurements in myosin. Biophys J. 1998 May;74(5):2451–2458.[PMC free article] [PubMed] [Google Scholar]
  • Gordon AM, Huxley AF, Julian FJ. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol. 1966 May;184(1):170–192.[PMC free article] [PubMed] [Google Scholar]
  • HANSON J, HUXLEY HE. Structural basis of the cross-striations in muscle. Nature. 1953 Sep 19;172(4377):530–532. [PubMed] [Google Scholar]
  • Harrington WF. On the origin of the contractile force in skeletal muscle. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5066–5070.[PMC free article] [PubMed] [Google Scholar]
  • Higuchi H, Goldman YE. Sliding distance per ATP molecule hydrolyzed by myosin heads during isotonic shortening of skinned muscle fibers. Biophys J. 1995 Oct;69(4):1491–1507.[PMC free article] [PubMed] [Google Scholar]
  • HILL AV. THE EFFECT OF LOAD ON THE HEAT OF SHORTENING OF MUSCLE. Proc R Soc Lond B Biol Sci. 1964 Jan 14;159:297–318. [PubMed] [Google Scholar]
  • Holmes KC. The swinging lever-arm hypothesis of muscle contraction. Curr Biol. 1997 Feb 1;7(2):R112–R118. [PubMed] [Google Scholar]
  • HUXLEY AF. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed] [Google Scholar]
  • Huxley AF. A note suggesting that the cross-bridge attachment during muscle contraction may take place in two stages. Proc R Soc Lond B Biol Sci. 1973 Feb 27;183(1070):83–86. [PubMed] [Google Scholar]
  • Huxley AF. Muscular contraction. J Physiol. 1974 Nov;243(1):1–43.[PMC free article] [PubMed] [Google Scholar]
  • HUXLEY AF, NIEDERGERKE R. Structural changes in muscle during contraction; interference microscopy of living muscle fibres. Nature. 1954 May 22;173(4412):971–973. [PubMed] [Google Scholar]
  • Huxley AF, Simmons RM. Proposed mechanism of force generation in striated muscle. Nature. 1971 Oct 22;233(5321):533–538. [PubMed] [Google Scholar]
  • Huxley AF, Tideswell S. Filament compliance and tension transients in muscle. J Muscle Res Cell Motil. 1996 Aug;17(4):507–511. [PubMed] [Google Scholar]
  • Huxley AF, Tideswell S. Rapid regeneration of power stroke in contracting muscle by attachment of second myosin head. J Muscle Res Cell Motil. 1997 Feb;18(1):111–114. [PubMed] [Google Scholar]
  • HUXLEY HE. Electron microscope studies of the organisation of the filaments in striated muscle. Biochim Biophys Acta. 1953 Nov;12(3):387–394. [PubMed] [Google Scholar]
  • HUXLEY HE. The double array of filaments in cross-striated muscle. J Biophys Biochem Cytol. 1957 Sep 25;3(5):631–648.[PMC free article] [PubMed] [Google Scholar]
  • Huxley HE. The mechanism of muscular contraction. Science. 1969 Jun 20;164(3886):1356–1365. [PubMed] [Google Scholar]
  • HUXLEY H, HANSON J. Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature. 1954 May 22;173(4412):973–976. [PubMed] [Google Scholar]
  • Huxley HE, Faruqi AR, Kress M, Bordas J, Koch MH. Time-resolved X-ray diffraction studies of the myosin layer-line reflections during muscle contraction. J Mol Biol. 1982 Jul 15;158(4):637–684. [PubMed] [Google Scholar]
  • Kitamura K, Tokunaga M, Iwane AH, Yanagida T. A single myosin head moves along an actin filament with regular steps of 5.3 nanometres. Nature. 1999 Jan 14;397(6715):129–134. [PubMed] [Google Scholar]
  • Lombardi V, Piazzesi G, Linari M. Rapid regeneration of the actin-myosin power stroke in contracting muscle. Nature. 1992 Feb 13;355(6361):638–641. [PubMed] [Google Scholar]
  • NEEDHAM DM. Myosin and adenosinetriphosphate in relation to muscle contraction. Biochim Biophys Acta. 1950 Jan;4(1-3):42–49. [PubMed] [Google Scholar]
  • Piazzesi G, Lombardi V. A cross-bridge model that is able to explain mechanical and energetic properties of shortening muscle. Biophys J. 1995 May;68(5):1966–1979.[PMC free article] [PubMed] [Google Scholar]
  • Piazzesi G, Francini F, Linari M, Lombardi V. Tension transients during steady lengthening of tetanized muscle fibres of the frog. J Physiol. 1992 Jan;445:659–711.[PMC free article] [PubMed] [Google Scholar]
  • PODOLSKY RJ. Kinetics of muscular contraction: the approach to the steady state. Nature. 1960 Nov 19;188:666–668. [PubMed] [Google Scholar]
  • Rapp GJ, Davis JS. X-ray diffraction studies on thermally induced tension generation in rigor muscle. J Muscle Res Cell Motil. 1996 Dec;17(6):617–629. [PubMed] [Google Scholar]
  • Rayment I, Holden HM, Whittaker M, Yohn CB, Lorenz M, Holmes KC, Milligan RA. Structure of the actin-myosin complex and its implications for muscle contraction. Science. 1993 Jul 2;261(5117):58–65. [PubMed] [Google Scholar]
  • Reedy MK, Holmes KC, Tregear RT. Induced changes in orientation of the cross-bridges of glycerinated insect flight muscle. Nature. 1965 Sep 18;207(5003):1276–1280. [PubMed] [Google Scholar]
  • Schmitz H, Reedy MC, Reedy MK, Tregear RT, Taylor KA. Tomographic three-dimensional reconstruction of insect flight muscle partially relaxed by AMPPNP and ethylene glycol. J Cell Biol. 1997 Nov 3;139(3):695–707.[PMC free article] [PubMed] [Google Scholar]
  • Suzuki Y, Yasunaga T, Ohkura R, Wakabayashi T, Sutoh K. Swing of the lever arm of a myosin motor at the isomerization and phosphate-release steps. Nature. 1998 Nov 26;396(6709):380–383. [PubMed] [Google Scholar]
  • Taylor KA, Schmitz H, Reedy MC, Goldman YE, Franzini-Armstrong C, Sasaki H, Tregear RT, Poole K, Lucaveche C, Edwards RJ, et al. Tomographic 3D reconstruction of quick-frozen, Ca2+-activated contracting insect flight muscle. Cell. 1999 Nov 12;99(4):421–431. [PubMed] [Google Scholar]
  • Tsaturyan AK, Bershitsky SY, Burns R, Ferenczi MA. Structural changes in the actin-myosin cross-bridges associated with force generation induced by temperature jump in permeabilized frog muscle fibers. Biophys J. 1999 Jul;77(1):354–372.[PMC free article] [PubMed] [Google Scholar]
  • Veigel C, Coluccio LM, Jontes JD, Sparrow JC, Milligan RA, Molloy JE. The motor protein myosin-I produces its working stroke in two steps. Nature. 1999 Apr 8;398(6727):530–533. [PubMed] [Google Scholar]
Physiological Laboratory, University of Cambridge, UK.
Physiological Laboratory, University of Cambridge, UK.
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Abstract

In striated muscles, shortening comes about by the sliding movement of thick filaments, composed mostly of myosin, relative to thin filaments, composed mostly of actin. This is brought about by cyclic action of 'cross-bridges' composed of the heads of myosin molecules projecting from a thick filament, which attach to an adjacent thin filament, exert force for a limited time and detach, and then repeat this cycle further along the filament. The requisite energy is provided by the hydrolysis of a molecule of adenosine triphosphate to the diphosphate and inorganic phosphate, the steps of this reaction being coupled to mechanical events within the cross-bridge. The nature of these events is discussed. There is good evidence that one of them is a change in the angle of tilt of a 'lever arm' relative to the 'catalytic domain' of the myosin head which binds to the actin filament. It is suggested here that this event is superposed on a slower, temperature-sensitive change in the orientation of the catalytic domain on the actin filament. Many uncertainties remain.

Abstract
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