The myosin II coiled-coil domain atomic structure in its native environment
Abstract
Significance Myosin II is the molecule that produces force in muscle contraction. Unlike the myosin head, its molecular motor, no atomic resolution structure of the ∼1000-residue–long α-helical coiled-coil tail has been reported. Here, we describe the cryo-EM atomic structure of the myosin tail within a native muscle thick filament. Three differences with crystal structures of myosin tail segments were found. The myosin head arrangement apparently alters the beginning of the tail. Striated muscle myosins have four skip residues, amino acids inserted to improve the alignment of charged residue clusters. Skips 1 and 3 agree with the crystal structures. Skip 2, which is a novel structure, and Skip 4 do not. Functional consequences are suggested by the myosin tail packing.
- Authors:
-
[1];
[2];
[3];
[1];
[3];
[2];
[4];
[5];
[3]
- Institute of Molecular Biophysics, Florida State University, Tallahassee, FL 32306-4380,, Department of Physics, Florida State University, Tallahassee, FL 32306-4380,
- Department of Chemistry and Biochemistry, University of California San Diego, La Jolla, CA 92093,
- Institute of Molecular Biophysics, Florida State University, Tallahassee, FL 32306-4380,
- Department of Biological Sciences, Illinois Institute of Technology, Chicago, IL 60616,
- Department of Cell Biology, Duke University Medical Center, Durham, NC 27607
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1773201
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Published Article
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 118 Journal Issue: 14; Journal ID: ISSN 0027-8424
- Publisher:
- Proceedings of the National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Rahmani, Hamidreza, Ma, Wen, Hu, Zhongjun, Daneshparvar, Nadia, Taylor, Dianne W., McCammon, J. Andrew, Irving, Thomas C., Edwards, Robert J., and Taylor, Kenneth A. The myosin II coiled-coil domain atomic structure in its native environment. United States: N. p., 2021.
Web. doi:10.1073/pnas.2024151118.
Rahmani, Hamidreza, Ma, Wen, Hu, Zhongjun, Daneshparvar, Nadia, Taylor, Dianne W., McCammon, J. Andrew, Irving, Thomas C., Edwards, Robert J., & Taylor, Kenneth A. The myosin II coiled-coil domain atomic structure in its native environment. United States. https://doi.org/10.1073/pnas.2024151118
Rahmani, Hamidreza, Ma, Wen, Hu, Zhongjun, Daneshparvar, Nadia, Taylor, Dianne W., McCammon, J. Andrew, Irving, Thomas C., Edwards, Robert J., and Taylor, Kenneth A. Mon .
"The myosin II coiled-coil domain atomic structure in its native environment". United States. https://doi.org/10.1073/pnas.2024151118.
@article{osti_1773201,
title = {The myosin II coiled-coil domain atomic structure in its native environment},
author = {Rahmani, Hamidreza and Ma, Wen and Hu, Zhongjun and Daneshparvar, Nadia and Taylor, Dianne W. and McCammon, J. Andrew and Irving, Thomas C. and Edwards, Robert J. and Taylor, Kenneth A.},
abstractNote = {Significance Myosin II is the molecule that produces force in muscle contraction. Unlike the myosin head, its molecular motor, no atomic resolution structure of the ∼1000-residue–long α-helical coiled-coil tail has been reported. Here, we describe the cryo-EM atomic structure of the myosin tail within a native muscle thick filament. Three differences with crystal structures of myosin tail segments were found. The myosin head arrangement apparently alters the beginning of the tail. Striated muscle myosins have four skip residues, amino acids inserted to improve the alignment of charged residue clusters. Skips 1 and 3 agree with the crystal structures. Skip 2, which is a novel structure, and Skip 4 do not. Functional consequences are suggested by the myosin tail packing.},
doi = {10.1073/pnas.2024151118},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 14,
volume = 118,
place = {United States},
year = {Mon Mar 29 00:00:00 EDT 2021},
month = {Mon Mar 29 00:00:00 EDT 2021}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.2024151118
https://doi.org/10.1073/pnas.2024151118
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Structure of the backbone in myosin filaments of muscle
journal, January 1979
- Wray, John S.
- Nature, Vol. 277, Issue 5691
Atomic model of a myosin filament in the relaxed state
journal, August 2005
- Woodhead, John L.; Zhao, Fa-Qing; Craig, Roger
- Nature, Vol. 436, Issue 7054
The accommodation index measures the perturbation associated with insertions and deletions in coiled-coils: Application to understand signaling in histidine kinases: Accommodation Index for Insertions in Coiled-Coils
journal, February 2017
- Schmidt, Nathan W.; Grigoryan, Gevorg; DeGrado, William F.
- Protein Science, Vol. 26, Issue 3
Probing Designability via a Generalized Model of Helical Bundle Geometry
journal, January 2011
- Grigoryan, Gevorg; DeGrado, William F.
- Journal of Molecular Biology, Vol. 405, Issue 4
Myosin II sequences for Lethocerus indicus
journal, April 2017
- Fee, Lanette; Lin, Weili; Qiu, Feng
- Journal of Muscle Research and Cell Motility, Vol. 38, Issue 2
The Structure of Paramyosin Fibrils According to X-Ray Diffraction
journal, January 1956
- Bear, Richard S.; Selby, Cecily Cannan
- The Journal of Biophysical and Biochemical Cytology, Vol. 2, Issue 1
An invertebrate smooth muscle with striated muscle myosin filaments
journal, October 2015
- Sulbarán, Guidenn; Alamo, Lorenzo; Pinto, Antonio
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 42
The packing of α-helices: simple coiled-coils
journal, September 1953
- Crick, F. H. C.
- Acta Crystallographica, Vol. 6, Issue 8
Crystal structures of human cardiac beta-myosin II S2- provide insight into the functional role of the S2 subfragment
journal, November 2006
- Blankenfeldt, W.; Thoma, N. H.; Wray, J. S.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 47
Structure of myosin filaments from relaxed Lethocerus flight muscle by cryo-EM at 6 Å resolution
journal, September 2016
- Hu, Zhongjun; Taylor, Dianne W.; Reedy, Michael K.
- Science Advances, Vol. 2, Issue 9
cisTEM, user-friendly software for single-particle image processing
journal, March 2018
- Grant, Timothy; Rohou, Alexis; Grigorieff, Nikolaus
- eLife, Vol. 7
Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit Solvent Particle Mesh Ewald
journal, August 2013
- Salomon-Ferrer, Romelia; Götz, Andreas W.; Poole, Duncan
- Journal of Chemical Theory and Computation, Vol. 9, Issue 9
Myosin filament structure in vertebrate smooth muscle.
journal, July 1996
- Xu, J. Q.; Harder, B. A.; Uman, P.
- Journal of Cell Biology, Vol. 134, Issue 1
X-ray diffraction evidence for myosin-troponin connections and tropomyosin movement during stretch activation of insect flight muscle
journal, December 2010
- Perz-Edwards, Robert J.; Irving, Thomas C.; Baumann, Bruce A. J.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 1
Flightin Is Essential for Thick Filament Assembly and Sarcomere Stability in Drosophila Flight Muscles
journal, December 2000
- Reedy, Mary C.; Bullard, Belinda; Vigoreaux, Jim O.
- Journal of Cell Biology, Vol. 151, Issue 7
Atomic model of the human cardiac muscle myosin filament
journal, December 2012
- AL-Khayat, H. A.; Kensler, R. W.; Squire, J. M.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 1
Assembly of myosin
journal, August 1971
- Harrison, Richard G.; Lowey, Susan; Cohen, Carolyn
- Journal of Molecular Biology, Vol. 59, Issue 3
General model of myosin filament structure
journal, June 1973
- Squire, J. M.
- Journal of Molecular Biology, Vol. 77, Issue 2
The Requirement for Mechanical Coupling Between Head and S2 Domains in Smooth Muscle Myosin ATPase Regulation and its Implications for Dimeric Motor Function
journal, January 2005
- Tama, Florence; Feig, Michael; Liu, Jun
- Journal of Molecular Biology, Vol. 345, Issue 4
Paramyosin in invertebrate muscles. II. Content in relation to structure and function.
journal, October 1976
- Levine, R. J.; Elfvin, M.; Dewey, M. M.
- Journal of Cell Biology, Vol. 71, Issue 1
Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions
journal, June 2010
- Pintilie, Grigore D.; Zhang, Junjie; Goddard, Thomas D.
- Journal of Structural Biology, Vol. 170, Issue 3
Proteolytic degradation of myosin and the meromyosins by a water-insoluble polyanionic derivative of trypsin
journal, February 1967
- Lowey, Susan; Goldstein, Leon; Cohen, Carolyn
- Journal of Molecular Biology, Vol. 23, Issue 3
Skip residues correlate with bends in the myosin tail
journal, November 1990
- Offer, Gerald
- Journal of Molecular Biology, Vol. 216, Issue 2
Crystalline sheets of tropomyosin
journal, March 1984
- Stewart, Murray
- Journal of Molecular Biology, Vol. 174, Issue 1
MonoRes: Automatic and Accurate Estimation of Local Resolution for Electron Microscopy Maps
journal, February 2018
- Vilas, Jose Luis; Gómez-Blanco, Josué; Conesa, Pablo
- Structure, Vol. 26, Issue 2
The paramyosin of insect flight muscle
journal, April 1973
- Bullard, Belinda; Luke, Barbaea; Winkelman, Lowell
- Journal of Molecular Biology, Vol. 75, Issue 2
X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle
journal, December 1994
- Huxley, H. E.; Stewart, A.; Sosa, H.
- Biophysical Journal, Vol. 67, Issue 6
Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle
journal, September 1982
- McLachlan, Andrew D.; Karn, Jonathan
- Nature, Vol. 299, Issue 5880
Visualization of an unstable coiled coil from the scallop myosin rod
journal, July 2003
- Li, Yu; Brown, Jerry H.; Reshetnikova, Ludmilla
- Nature, Vol. 424, Issue 6946
X-ray diffraction evidence for α-helical coiled-coils in native muscle
journal, May 1963
- Cohen, Carolyn; Holmes, Kenneth C.
- Journal of Molecular Biology, Vol. 6, Issue 5
Automatic local resolution-based sharpening of cryo-EM maps
journal, August 2019
- Ramírez-Aportela, Erney; Vilas, Jose Luis; Glukhova, Alisa
- Bioinformatics
Electron microscopy and image analysis of myosin filaments from scallop striated muscle
journal, April 1983
- Vibert, Peter; Craig, Roger
- Journal of Molecular Biology, Vol. 165, Issue 2
The structural basis of muscle contraction
journal, April 2000
- Holmes, Kenneth C.; Geeves, Michael A.
- Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1396
Structures of Smooth Muscle Myosin and Heavy Meromyosin in the Folded, Shutdown State
journal, October 2007
- Burgess, Stan A.; Yu, Shuizi; Walker, Matt L.
- Journal of Molecular Biology, Vol. 372, Issue 5
Lethocerus Myosin II complete coiled-coil domain resolved in its native environment
text, January 2021
- Rahmani, H.; Hu, Z.; Daneshparvar, N.
- Worldwide Protein Data Bank
Force generation by skeletal muscle is controlled by mechanosensing in myosin filaments
journal, November 2015
- Linari, Marco; Brunello, Elisabetta; Reconditi, Massimo
- Nature, Vol. 528, Issue 7581
Amino-Acid Sequence of Rabbit Skeletal Tropomyosin and Its Coiled-Coil Structure
journal, December 1972
- Sodek, J.; Hodges, R. S.; Smillie, L. B.
- Proceedings of the National Academy of Sciences, Vol. 69, Issue 12, p. 3800-3804
Spare the rod, spoil the regulation: Necessity for a myosin rod
journal, January 1997
- Trybus, K. M.; Freyzon, Y.; Faust, L. Z.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 1
Coupling between myosin head conformation and the thick filament backbone structure
journal, December 2017
- Hu, Zhongjun; Taylor, Dianne W.; Edwards, Robert J.
- Journal of Structural Biology, Vol. 200, Issue 3
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB
journal, July 2015
- Maier, James A.; Martinez, Carmenza; Kasavajhala, Koushik
- Journal of Chemical Theory and Computation, Vol. 11, Issue 8
Assembly of smooth muscle myosin into side-polar filaments.
journal, December 1977
- Craig, R.; Megerman, J.
- Journal of Cell Biology, Vol. 75, Issue 3
An Unstable Head–Rod Junction May Promote Folding into the Compact Off-State Conformation of Regulated Myosins
journal, February 2008
- Brown, Jerry H.; Yang, Yuting; Reshetnikova, Ludmilla
- Journal of Molecular Biology, Vol. 375, Issue 5
CryoEM structure of Drosophila flight muscle thick filaments at 7 Å resolution
journal, July 2020
- Daneshparvar, Nadia; Taylor, Dianne W.; O’Leary, Thomas S.
- Life Science Alliance, Vol. 3, Issue 8
Skip residues modulate the structural properties of the myosin rod and guide thick filament assembly
journal, July 2015
- Taylor, Keenan C.; Buvoli, Massimo; Korkmaz, Elif Nihal
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 29
Structure of the cross-striated adductor muscle of the scallop
journal, May 1976
- Millmax, Barry M.; Bennett, Pauline M.
- Journal of Molecular Biology, Vol. 103, Issue 3
The myosin interacting-heads motif present in live tarantula muscle explains tetanic and posttetanic phosphorylation mechanisms
journal, May 2020
- Padrón, Raúl; Ma, Weikang; Duno-Miranda, Sebastian
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 22
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
Coiled-Coil Unwinding at the Smooth Muscle Myosin Head-Rod Junction Is Required for Optimal Mechanical Performance
journal, April 2001
- Lauzon, Anne-Marie; Fagnant, Patty M.; Warshaw, David M.
- Biophysical Journal, Vol. 80, Issue 4
Helical reconstruction in RELION
journal, June 2017
- He, Shaoda; Scheres, Sjors H. W.
- Journal of Structural Biology, Vol. 198, Issue 3
Coiled coils: new structures and new functions
journal, October 1996
- Lupas, A.
- Trends in Biochemical Sciences, Vol. 21, Issue 10
Dynamic behaviour of the head-tail junction of myosin
journal, January 1996
- Knight, Peter J.
- Journal of Molecular Biology, Vol. 255, Issue 2
Light meromyosin fraction I: A helical molecule from myosin
journal, August 1960
- Szent-Györgyi, Andrew G.; Cohen, Carolyn; Philpott, Delbert E.
- Journal of Molecular Biology, Vol. 2, Issue 3
Regulation of Contraction by the Thick Filaments in Skeletal Muscle
journal, December 2017
- Irving, Malcolm
- Biophysical Journal, Vol. 113, Issue 12
Three-dimensional image reconstruction of dephosphorylated smooth muscle heavy meromyosin reveals asymmetry in the interaction between myosin heads and placement of subfragment 2
journal, April 2001
- Wendt, T.; Taylor, D.; Trybus, K. M.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 8
A New Internal Mode in F-Actin Helps Explain the Remarkable Evolutionary Conservation of Actin's Sequence and Structure
journal, April 2002
- Galkin, Vitold E.; VanLoock, Margaret S.; Orlova, Albina
- Current Biology, Vol. 12, Issue 7
Angular measurements of the dynein ring reveal a stepping mechanism dependent on a flexible stalk
journal, May 2017
- Lippert, Lisa G.; Dadosh, Tali; Hadden, Jodi A.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 23
X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction
journal, December 1994
- Wakabayashi, K.; Sugimoto, Y.; Tanaka, H.
- Biophysical Journal, Vol. 67, Issue 6
Lower Cambrian vertebrates from south China
journal, November 1999
- Shu, D-G.; Luo, H-L.; Conway Morris, S.
- Nature, Vol. 402, Issue 6757
X-ray evidence for conformational changes in the myosin filaments of vertebrate striated muscle
journal, February 1975
- Haselgrove, J. C.
- Journal of Molecular Biology, Vol. 92, Issue 1
Paramyosin is necessary for determination of nematode thick filament length in vivo
journal, December 1980
- Mackenzie, John M.; Epstein, Henry F.
- Cell, Vol. 22, Issue 3
A composite approach towards a complete model of the myosin rod: A Composite Approach to the Myosin Rod
journal, December 2015
- Korkmaz, E. Nihal; Taylor, Keenan C.; Andreas, Michael P.
- Proteins: Structure, Function, and Bioinformatics, Vol. 84, Issue 1
In Vivo X-Ray Diffraction of Indirect Flight Muscle from Drosophila melanogaster
journal, May 2000
- Irving, T. C.; Maughan, D. W.
- Biophysical Journal, Vol. 78, Issue 5
Does titin regulate the length of muscle thick filaments?
journal, January 1989
- Whiting, A.; Wardale, J.; Trinick, J.
- Journal of Molecular Biology, Vol. 205, Issue 1