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Science 2 July 1993:
Vol. 261. no. 5117, pp. 58 - 65
DOI: 10.1126/science.8316858
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Articles

Science, Vol 261, Issue 5117, 58-65
Copyright © 1993 by American Association for the Advancement of Science

articles

Structure of the actin-myosin complex and its implications for muscle contraction

I Rayment, HM Holden, M Whittaker, CB Yohn, M Lorenz, KC Holmes, and RA Milligan

Department of Biochemistry, University of Wisconsin, Madison 53705.

Muscle contraction consists of a cyclical interaction between myosin and actin driven by the concomitant hydrolysis of adenosine triphosphate (ATP). A model for the rigor complex of F actin and the myosin head was obtained by combining the molecular structures of the individual proteins with the low-resolution electron density maps of the complex derived by cryo-electron microscopy and image analysis. The spatial relation between the ATP binding pocket on myosin and the major contact area on actin suggests a working hypothesis for the crossbridge cycle that is consistent with previous independent structural and biochemical studies.


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The Sliding Filament Model: 1972-2004.
R. Cooke (2004)
J. Gen. Physiol. 123, 643-656
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Molecular Dynamics Analysis of Structural Factors Influencing Back Door Pi Release in Myosin.
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The Myosin Cardiac Loop Participates Functionally in the Actomyosin Interaction.
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Myosin Regulatory Domain Orientation in Skeletal Muscle Fibers: Application of Novel Electron Paramagnetic Resonance Spectral Decomposition and Molecular Modeling Methods.
B. A. J. Baumann, H. Liang, K. Sale, B. D. Hambly, and P. G. Fajer (2004)
Biophys. J. 86, 3030-3041
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Bifunctional Rhodamine Probes of Myosin Regulatory Light Chain Orientation in Relaxed Skeletal Muscle Fibers.
A. S. Brack, B. D. Brandmeier, R. E. Ferguson, S. Criddle, R. E. Dale, and M. Irving (2004)
Biophys. J. 86, 2329-2341
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Stepwise Sliding of Single Actin and Myosin Filaments.
X. Liu and G. H. Pollack (2004)
Biophys. J. 86, 353-358
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Protein Fiber Linear Dichroism for Structure Determination and Kinetics in a Low-Volume, Low-Wavelength Couette Flow Cell.
T. R. Dafforn, J. Rajendra, D. J. Halsall, L. C. Serpell, and A. Rodger (2004)
Biophys. J. 86, 404-410
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Clinical and genetic characteristics of {alpha} cardiac actin gene mutations in hypertrophic cardiomyopathy.
J Mogensen, A Perrot, P S Andersen, O Havndrup, I C Klausen, M Christiansen, P Bross, H Egeblad, H Bundgaard, K J Osterziel, et al. (2004)
J. Med. Genet. 41, e10-10
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Static and Dynamic X-Ray Diffraction Recordings from Living Mammalian and Amphibian Skeletal Muscles.
H. Iwamoto, J.'i. Wakayama, T. Fujisawa, and N. Yagi (2003)
Biophys. J. 85, 2492-2506
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Rigor-Force Producing Cross-Bridges in Skeletal Muscle Fibers Activated by a Substoichiometric Amount of ATP.
T. Yamada, Y. Takezawa, H. Iwamoto, S. Suzuki, and K. Wakabayashi (2003)
Biophys. J. 85, 1741-1753
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Requirement of Domain-Domain Interaction for Conformational Change and Functional ATP Hydrolysis in Myosin.
K. Ito, T. Q. P. Uyeda, Y. Suzuki, K. Sutoh, and K. Yamamoto (2003)
J. Biol. Chem. 278, 31049-31057
   Abstract »    Full Text »    PDF »
Myosin Head Configuration in Relaxed Insect Flight Muscle: X-Ray Modeled Resting Cross-Bridges in a Pre-Powerstroke State Are Poised for Actin Binding.
H. A. AL-Khayat, L. Hudson, M. K. Reedy, T. C. Irving, and J. M. Squire (2003)
Biophys. J. 85, 1063-1079
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The Conformation of Myosin Head Domains in Rigor Muscle Determined by X-Ray Interference.
M. Reconditi, N. Koubassova, M. Linari, I. Dobbie, T. Narayanan, O. Diat, G. Piazzesi, V. Lombardi, and M. Irving (2003)
Biophys. J. 85, 1098-1110
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Effects of halogenated anaesthetics on diaphragmatic actin-myosin cross-bridge kinetics.
O. Langeron, B. Bouhemad, G. Orliaguet, P. Coriat, Y. Lecarpentier, and B. Riou (2003)
Br. J. Anaesth. 90, 759-765
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She4p/Dim1p Interacts with the Motor Domain of Unconventional Myosins in the Budding Yeast, Saccharomyces cerevisiae.
H. Toi, K. Fujimura-Kamada, K. Irie, Y. Takai, S. Todo, and K. Tanaka (2003)
Mol. Biol. Cell 14, 2237-2249
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Analysis of Myosin Heavy Chain Functionality in the Heart.
M. Krenz, A. Sanbe, F. Bouyer-Dalloz, J. Gulick, R. Klevitsky, T. E. Hewett, H. E. Osinska, J. N. Lorenz, C. Brosseau, A. Federico, et al. (2003)
J. Biol. Chem. 278, 17466-17474
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Suppression of Muscle Hypercontraction by Mutations in the Myosin Heavy Chain Gene of Drosophila melanogaster.
U. Nongthomba, M. Cummins, S. Clark, J. O. Vigoreaux, and J. C. Sparrow (2003)
Genetics 164, 209-222
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Myosin isoforms show unique conformations in the actin-bound state.
N. Volkmann, G. Ouyang, K. M. Trybus, D. J. DeRosier, S. Lowey, and D. Hanein (2003)
PNAS 100, 3227-3232
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Myo3A, One of Two Class III Myosin Genes Expressed in Vertebrate Retina, Is Localized to the Calycal Processes of Rod and Cone Photoreceptors and Is Expressed in the Sacculus.
A. C. Dose, D. W. Hillman, C. Wong, L. Sohlberg, J. Lin-Jones, and B. Burnside (2003)
Mol. Biol. Cell 14, 1058-1073
   Abstract »    Full Text »    PDF »
Molecular Motors: Force and Movement Generated by Single Myosin II Molecules.
C. Ruegg, C. Veigel, J. E. Molloy, S. Schmitz, J. C. Sparrow, and R. H. A. Fink (2002)
Physiology 17, 213-218
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Molecular Mechanisms of Inherited Cardiomyopathies.
D. Fatkin and R. M. Graham (2002)
Physiol Rev 82, 945-980
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Force Kinetics and Individual Sarcomere Dynamics in Cardiac Myofibrils after Rapid Ca2+ Changes.
R. Stehle, M. Kruger, and G. Pfitzer (2002)
Biophys. J. 83, 2152-2161
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Polarized Fluorescence Depletion Reports Orientation Distribution and Rotational Dynamics of Muscle Cross-Bridges.
M. G. Bell, R. E. Dale, U. A. van der Heide, and Y. E. Goldman (2002)
Biophys. J. 83, 1050-1073
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Direct Modeling of X-Ray Diffraction Pattern from Skeletal Muscle in Rigor.
N. A. Koubassova and A. K. Tsaturyan (2002)
Biophys. J. 83, 1082-1097
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Ca2+ activation and tension cost in myofilaments from mouse hearts ectopically expressing enteric gamma -actin.
A. F. Martin, R. M. Phillips, A. Kumar, K. Crawford, Z. Abbas, J. L. Lessard, P. de Tombe, and R. J. Solaro (2002)
Am J Physiol Heart Circ Physiol 283, H642-H649
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An Automated Two-Dimensional Optical Force Clamp for Single Molecule Studies.
M. J. Lang, C. L. Asbury, J. W. Shaevitz, and S. M. Block (2002)
Biophys. J. 83, 491-501
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Actin-induced Closure of the Actin-binding Cleft of Smooth Muscle Myosin.
C. M. Yengo, E. M. De La Cruz, L. R. Chrin, D. P. Gaffney II, and C. L. Berger (2002)
J. Biol. Chem. 277, 24114-24119
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Myosin Light Chain Mutation Causes Autosomal Recessive Cardiomyopathy With Mid-Cavitary Hypertrophy and Restrictive Physiology.
T. M. Olson, M. L. Karst, F. G. Whitby, and D. J. Driscoll (2002)
Circulation 105, 2337-2340
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Holding two heads together: Stability of the myosin II rod measured by resonance energy transfer between the heads.
T. Chakrabarty, M. Xiao, R. Cooke, and P. R. Selvin (2002)
PNAS 99, 6011-6016
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Mutation of the myosin converter domain alters cross-bridge elasticity.
J. Kohler, G. Winkler, I. Schulte, T. Scholz, W. McKenna, B. Brenner, and T. Kraft (2002)
PNAS 99, 3557-3562
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Myosin heavy chain IIa gene mutation E706K is pathogenic and its expression increases with age.
H. Tajsharghi, L.-E. Thornell, N. Darin, T. Martinsson, M. Kyllerman, J. Wahlstrom, and A. Oldfors (2002)
Neurology 58, 780-786
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A Gradient of Myosin Regulatory Light-chain Phosphorylation across the Ventricular Wall Supports Cardiac Torsion.
J.S. DAVIS, S. HASSANZADEH, S. WINITSKY, H. WEN, A. ALETRAS, and N.D. EPSTEIN (2002)
Cold Spring Harb Symp Quant Biol 67, 345-352
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Kinesin: switch I & II and the motor mechanism.
F. J. Kull and S. A. Endow (2002)
J. Cell Sci. 115, 15-23
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Myosin V exhibits a high duty cycle and large unitary displacement.
J. R. Moore, E. B. Krementsova, K. M. Trybus, and D. M. Warshaw (2001)
J. Cell Biol. 155, 625-636
   Abstract »    Full Text »    PDF »
ATP Reorients the Neck Linker of Kinesin in Two Sequential Steps.
S. S. Rosenfeld, G. M. Jefferson, and P. H. King (2001)
J. Biol. Chem. 276, 40167-40174
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Signal Transduction in Smooth Muscle: Selected Contribution: Time course and heterogeneity of contractile responses in cultured human airway smooth muscle cells.
B. Fabry, G. N. Maksym, S. A. Shore, P. E. Moore, R. A. Panettieri Jr., J. P. Butler, and J. J. Fredberg (2001)
J Appl Physiol 91, 986-994
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The Emergence of Electron Tomography as an Important Tool for Investigating Cellular Ultrastructure.
B. F. McEwen and M. Marko (2001)
J. Histochem. Cytochem. 49, 553-564
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G. C. Sieck and M. Regnier (2001)
J Appl Physiol 90, 1158-1164
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Molecular Machines: Putting the Pieces Together.
E. Nogales and N. Grigorieff (2001)
J. Cell Biol. 152, F1-F10
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Conditional Expression of a Truncated Fragment of Nonmuscle Myosin II-A Alters Cell Shape but Not Cytokinesis in HeLa Cells.
Q. Wei and R. S. Adelstein (2000)
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Myosin light chain replacement in the heart.
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Am J Physiol Heart Circ Physiol 279, H1355-H1364
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Regulation of Contraction in Striated Muscle.
A. M. Gordon, E. Homsher, and M. Regnier (2000)
Physiol Rev 80, 853-924
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Skeletal Muscle Function and Fibre Types: the Relationship Between Occlusal Function and the Phenotype of Jaw-closing Muscles in Human.
J. J. Sciote and T. J. Morris (2000)
J. Orthod. 27, 15-30
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Conformational Distributions and Proximity Relationships in the Rigor Complex of Actin and Myosin Subfragment-1.
M. Nyitrai, G. Hild, A. Lukacs, E. Bodis, and B. Somogyi (2000)
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Visualizing myosin's power stroke in muscle contraction.
M. Reedy (2000)
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X-ray Structures of the Dictyostelium discoideum Myosin Motor Domain with Six No