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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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Cryo-EM and Single Particles.
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Effect of temperature on the working stroke of muscle myosin.
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The structural basis of the increase in isometric force production with temperature in frog skeletal muscle.
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Age-Related Decline in Actomyosin Function.
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Role of the N-terminal negative charges of actin in force generation and cross-bridge kinetics in reconstituted bovine cardiac muscle fibres.
X. Lu, M. K Bryant, K. E Bryan, P. A Rubenstein, and M. Kawai (2005)
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The ATP hydrolysis and phosphate release steps control the time course of force development in rabbit skeletal muscle.
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Clinical and genetic characteristics of {alpha} cardiac actin gene mutations in hypertrophic cardiomyopathy.
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She4p/Dim1p Interacts with the Motor Domain of Unconventional Myosins in the Budding Yeast, Saccharomyces cerevisiae.
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Temperature dependence of the force-generating process in single fibres from frog skeletal muscle.
G Piazzesi, M Reconditi, N Koubassova, V Decostre, M Linari, L Lucii, and V Lombardi (2003)
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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)
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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)
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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)
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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)
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The size and the speed of the working stroke of muscle myosin and its dependence on the force.
G. Piazzesi, L. Lucii, and V. Lombardi (2002)
J. Physiol. 545, 145-151
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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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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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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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    PDF »
Kinesin: switch I & II and the motor mechanism.
F. J. Kull and S. A. Endow (2002)
J. Cell Sci. 115, 15-23
   Abstract »    Full Text »    PDF »
Identification and validation of selective upregulation of ventricular myosin light chain type 2 mRNA in idiopathic dilated cardiomyopathy.
D. Haase, M. H. Lehmann, M. M. Korner, R. Korfer, H. H. Sigusch, and H. R. Figulla (2002)
Eur J Heart Fail 4, 23-31
   Abstract »    Full Text »    PDF »
Effects of substituting uridine triphosphate for ATP on the crossbridge cycle of rabbit muscle.
C. Y Seow, H. D White, and L. E Ford (2001)
J. Physiol. 537, 907-921
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »
Plasticity in Skeletal, Cardiac, and Smooth Muscle: Invited Review: Plasticity and energetic demands of contraction in skeletal and cardiac muscle.
G. C. Sieck and M. Regnier (2001)
J Appl Physiol 90, 1158-1164
   Abstract »    Full Text »    PDF »
Effect of temperature on elementary steps of the cross-bridge cycle in rabbit soleus slow-twitch muscle fibres.
G. Wang and M. Kawai (2001)
J. Physiol. 531, 219-234
   Abstract »    Full Text »    PDF »
Molecular Machines: Putting the Pieces Together.
E. Nogales and N. Grigorieff (2001)
J. Cell Biol. 152, F1-F10
   Abstract »    Full Text »    PDF »
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)
Mol. Biol. Cell 11, 3617-3627
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Myosin light chain replacement in the heart.
A. Sanbe, J. Gulick, E. Hayes, D. Warshaw, H. Osinska, C.-B. Chan, R. Klevitsky, and J. Robbins (2000)
Am J Physiol Heart Circ Physiol 279, H1355-H1364
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A combined mechanical and X-ray diffraction study of stretch potentiation in single frog muscle fibres.
M Linari, L Lucii, M Reconditi, M E V. Casoni, H Amenitsch, S Bernstorff, G Piazzesi, and V Lombardi (2000)
J. Physiol. 526, 589-596
   Abstract »    Full Text »    PDF »
Regulation of Contraction in Striated Muscle.
A. M. Gordon, E. Homsher, and M. Regnier (2000)
Physiol Rev 80, 853-924
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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)
J. Biol. Chem. 275, 2404-2409
   Abstract »    Full Text »    PDF »
Visualizing myosin's power stroke in muscle contraction.
M. Reedy (2000)
J. Cell Sci. 113, 3551-3562
   Abstract »    PDF »
X-ray Structures of the Dictyostelium discoideum Myosin Motor Domain with Six Non-nucleotide Analogs.
A. M. Gulick, C. B. Bauer, J. B. Thoden, E. Pate, R. G. Yount, and I. Rayment (2000)
J. Biol. Chem. 275, 398-408
   Abstract »    Full Text »    PDF »
Kinetic equilibrium of forces and molecular events in muscle contraction.
E. W. Becker (2000)
PNAS 97, 157-161
   Abstract »    Full Text »    PDF »
Powerful Activation of Skeletal Muscle Actomyosin ATPase by Goniodomin A Is Highly Sensitive to Troponin/Tropomyosin Complex.
K. Matsunaga, K. Nakatani, M. Murakami, K. Yamaguchi, and Y. Ohizumi (1999)
J. Pharmacol. Exp. Ther. 291, 1121-1126
   Abstract »    Full Text »
Actin--myosin interaction.
S. Sugiura (1999)
Cardiovasc Res 44, 266-273
   Abstract »    Full Text »    PDF »
Actin Residue Glu93 Is Identified as an Amino Acid Affecting Myosin Binding.
A. Razzaq, S. Schmitz, C. Veigel, J. E. Molloy, M. A. Geeves, and J. C. Sparrow (1999)
J. Biol. Chem. 274, 28321-28328
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Myosin II Folding Is Mediated by a Molecular Chaperonin.
R. Srikakulam and D. A. Winkelmann (1999)
J. Biol. Chem. 274, 27265-27273
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Phosphorylation-dependent Structural Changes in the Regulatory Light Chain Domain of Smooth Muscle Heavy Meromyosin.
X. Wu, B. A. Clack, G. Zhi, J. T. Stull, and C. R. Cremo (1999)
J. Biol. Chem. 274, 20328-20335
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Size and Charge Requirements for Kinetic Modulation and Actin Binding by Alkali 1-type Myosin Essential Light Chains.
D. J. Timson, H. R. Trayer, K. J. Smith, and I. P. Trayer (1999)
J. Biol. Chem. 274, 18271-18277
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Cardiac myosin heavy chains lacking the light chain binding domain cause hypertrophic cardiomyopathy in mice.
R. E. Welikson, S. H. Buck, J. R. Patel, R. L. Moss, K. L. Vikstrom, S. M. Factor, S. Miyata, H. D. Weinberger, and L. A. Leinwand (1999)
Am J Physiol Heart Circ Physiol 276, H2148-H2158
   Abstract »    Full Text »    PDF »
Molecular model of muscle contraction.
T. A. J. Duke (1999)
PNAS 96, 2770-2775
   Abstract »    Full Text »    PDF »
Specific Myosin Heavy Chain Mutations Suppress Troponin I Defects in Drosophila Muscles.
W. A. Kronert, A. Acebes, A. Ferrus, and S. I. Bernstein (1999)
J. Cell Biol. 144, 989-1000
   Abstract »    Full Text »    PDF »
Observation of transient disorder during myosin subfragment-1 binding to actin by stopped-flow fluorescence and millisecond time resolution electron cryomicroscopy: Evidence that the start of the crossbridge power stroke in muscle has variable geometry.
M. Walker, X.-Z. Zhang, W. Jiang, J. Trinick, and H. D. White (1999)
PNAS 96, 465-470
   Abstract »    Full Text »    PDF »
Substitution of flight muscle-specific actin by human (beta)-cytoplasmic actin in the indirect flight muscle of Drosophila.
V Brault, M. Reedy, U Sauder, R. Kammerer, U Aebi, and C Schoenenberger (1999)
J. Cell Sci. 112, 3627-3639
   Abstract »    PDF »
Differential Epitope Tagging of Actin in Transformed Drosophila Produces Distinct Effects on Myofibril Assembly and Function of the Indirect Flight Muscle.
V. Brault, U. Sauder, M. C. Reedy, U. Aebi, and C.-A. Schoenenberger (1999)
Mol. Biol. Cell 10, 135-149
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Structural invariance of constitutively active and inactive mutants of Acanthamoeba myosin IC bound to F-actin in the rigor and ADP-bound states.
B. O. Carragher, N. Cheng, Z.-Y. Wang, E. D. Korn, A. Reilein, D. M. Belnap, J. A. Hammer III, and A. C. Steven (1998)
PNAS 95, 15206-15211
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Conformational changes between the active-site and regulatory light chain of myosin as determined by luminescence resonance energy transfer: The effect of nucleotides and actin.
M. Xiao, H. Li, G. E. Snyder, R. Cooke, R. G. Yount, and P. R. Selvin (1998)
PNAS 95, 15309-15314
   Abstract »    Full Text »    PDF »
Nexilin: A Novel Actin Filament-binding Protein Localized at Cell-Matrix Adherens Junction.
T. Ohtsuka, H. Nakanishi, W. Ikeda, A. Satoh, Y. Momose, H. Nishioka, and Y. Takai (1998)
J. Cell Biol. 143, 1227-1238
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Nucleotide-dependent conformational change near the fulcrum region in Dictyostelium myosin II.
W. Liang and J. A. Spudich (1998)
PNAS 95, 12844-12847
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Smooth muscle myosin mutants containing a single tryptophan reveal molecular interactions at the actin-binding interface.
C. M. Yengo, P. M. Fagnant, L. Chrin, A. S. Rovner, and C. L. Berger (1998)
PNAS 95, 12944-12949
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Troponin and Tropomyosin : Proteins That Switch on and Tune in the Activity of Cardiac Myofilaments.
R. J. Solaro and H. M. Rarick (1998)
Circ. Res. 83, 471-480
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Mechanics, energetics, and crossbridge kinetics of rabbit diaphragm during congestive heart failure.
Y. Lecarpentier, D. Chemla, F. X. Blanc, J. C. Pourny, T. Joseph, B. Riou, and C. Coirault (1998)
FASEB J 12, 981-989
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Adducin Is an In Vivo Substrate for Protein Kinase C: Phosphorylation in the MARCKS-related Domain Inhibits Activity in Promoting Spectrin-Actin Complexes and Occurs in Many Cells, Including Dendritic Spines of Neurons.
Y. Matsuoka, X. Li, and V. Bennett (1998)
J. Cell Biol. 142, 485-497
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Frabin, a Novel FGD1-related Actin Filament-binding Protein Capable of Changing Cell Shape and Activating c-Jun N-terminal Kinase.
H. Obaishi, H. Nakanishi, K. Mandai, K. Satoh, A. Satoh, K. Takahashi, M. Miyahara, H. Nishioka, K. Takaishi, and Y. Takai (1998)
J. Biol. Chem. 273, 18697-18700
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Myosin conformational states determined by single fluorophore polarization.
D. M. Warshaw, E. Hayes, D. Gaffney, A.-M. Lauzon, J. Wu, G. Kennedy, K. Trybus, S. Lowey, and C. Berger (1998)
PNAS 95, 8034-8039
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Lipid nanotubes as substrates for helical crystallization of macromolecules.
E. M. Wilson-Kubalek, R. E. Brown, H. Celia, and R. A. Milligan (1998)
PNAS 95, 8040-8045
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A new look at thin filament regulation in vertebrate skeletal muscle.
J. M. Squire and E. P. Morris (1998)
FASEB J 12, 761-771
   Abstract »    Full Text »
A Myosin III from Limulus Eyes Is a Clock-Regulated Phosphoprotein.
B.-A. Battelle, A. W. Andrews, B. G. Calman, J. R. Sellers, R. M. Greenberg, and W. C. Smith (1998)
J. Neurosci. 18, 4548-4559
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Functional transitions in myosin: Formation of a critical salt-bridge and transmission of effect to the sensitive tryptophan.
H. Onishi, S.-i. Kojima, K. Katoh, K. Fujiwara, H. M. Martinez, and M. F. Morales (1998)
PNAS 95, 6653-6658
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Effects of Total Replacement of Atrial Myosin Light Chain-2 With the Ventricular Isoform in Atrial Myocytes of Transgenic Mice.
C. M. Pawloski-Dahm, G. Song, D. L. Kirkpatrick, J. Palermo, J. Gulick, G. W. Dorn II, J. Robbins, and R. A. Walsh (1998)
Circulation 97, 1508-1513
   Abstract »    Full Text »    PDF »
Molecular Genetic Dissection of Mouse Unconventional Myosin-VA: Head Region Mutations.
J.-D. Huang, M. J. T. V. Cope, V. Mermall, M. C. Strobel, J. Kendrick-Jones, L. B. Russell, M. S. Mooseker, N. G. Copeland, and N. A. Jenkins (1998)
Genetics 148, 1951-1961
   Abstract »    Full Text »    PDF »
New angle on myosin.
R. Cooke (1998)
PNAS 95, 2720-2722
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