The 7-stranded structure of relaxed scallop muscle myosin filaments

Support for a common head configuration in myosin-regulated muscles

Hind A. AL-Khayat, Edward P. Morris, John M. Squire

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

Isolated relaxed myosin filaments from the myosin-regulated scallop striated adductor muscle have been reconstructed using electron microscopy and single particle analysis of negatively stained filaments. Three-dimensional reconstruction using 7-fold rotational symmetry but without imposed helical symmetry confirmed that the myosin head array is a 7-stranded, right-handed long-pitch 24/1 helix (or left-handed short-pitch 10/1 helix) with the whole structure having an axial repeat of 1440 Å. Reconstruction using the full helical symmetry revealed details of the myosin head density distribution within the head crowns in the relaxed scallop myosin filament. The resulting density distribution can best be explained by an arrangement in which the two heads from the same myosin molecule interact together within each crown in a compact parallel fashion along the filament axis. The configuration is consistent with the published configuration of the two heads within vertebrate smooth muscle myosin molecules observed in two-dimensional crystals of smooth muscle myosin and in the structure of tarantula myosin filaments. All these three muscle types are myosin-regulated, providing further support for a general motif of intramolecular interacting-heads structure in the relaxed state of myosin-regulated muscles as was proposed earlier by Woodhead et al. [Woodhead, J.L., Zhao, F.-Q., Craig, R., Egelman, E.H., Alamo, L., Padron, R.. 2005. Atomic model of a myosin filament in the relaxed state. Nature 436, 1195-1199]. However, the orientation of the Wendt structure is different from that found by Woodhead in that the outer head projects outwards and the inner head lies closer to the filament backbone, as in earlier work done on the insect flight muscle myosin filaments [AL-Khayat, H.A., Hudson, L., Reedy, M.K., Irving, T.C., Squire, J.M., 2003. Myosin head configuration in relaxed insect flight muscle: X-ray modelled resting crossbridges in a pre-powerstroke state are poised for actin binding. Biophys. J. 85, 1063-1079]. Possible species specific details that may differ between the scallop and the tarantula myosin filaments are also discussed.

Original languageEnglish
Pages (from-to)183-194
Number of pages12
JournalJournal of Structural Biology
Volume166
Issue number2
DOIs
Publication statusPublished - May 2009
Externally publishedYes

Fingerprint

Pectinidae
Myosins
Head
Muscles
Smooth Muscle Myosins
Crowns
Insects
Striated Muscle

Keywords

  • 3D reconstruction
  • Electron microscopy
  • Myosin filaments
  • Myosin-linked regulation
  • Scallop striated muscle
  • Single particle analysis

ASJC Scopus subject areas

  • Structural Biology

Cite this

The 7-stranded structure of relaxed scallop muscle myosin filaments : Support for a common head configuration in myosin-regulated muscles. / AL-Khayat, Hind A.; Morris, Edward P.; Squire, John M.

In: Journal of Structural Biology, Vol. 166, No. 2, 05.2009, p. 183-194.

Research output: Contribution to journalArticle

@article{cc27420ad57149a2afc9685f2dc6d812,
title = "The 7-stranded structure of relaxed scallop muscle myosin filaments: Support for a common head configuration in myosin-regulated muscles",
abstract = "Isolated relaxed myosin filaments from the myosin-regulated scallop striated adductor muscle have been reconstructed using electron microscopy and single particle analysis of negatively stained filaments. Three-dimensional reconstruction using 7-fold rotational symmetry but without imposed helical symmetry confirmed that the myosin head array is a 7-stranded, right-handed long-pitch 24/1 helix (or left-handed short-pitch 10/1 helix) with the whole structure having an axial repeat of 1440 {\AA}. Reconstruction using the full helical symmetry revealed details of the myosin head density distribution within the head crowns in the relaxed scallop myosin filament. The resulting density distribution can best be explained by an arrangement in which the two heads from the same myosin molecule interact together within each crown in a compact parallel fashion along the filament axis. The configuration is consistent with the published configuration of the two heads within vertebrate smooth muscle myosin molecules observed in two-dimensional crystals of smooth muscle myosin and in the structure of tarantula myosin filaments. All these three muscle types are myosin-regulated, providing further support for a general motif of intramolecular interacting-heads structure in the relaxed state of myosin-regulated muscles as was proposed earlier by Woodhead et al. [Woodhead, J.L., Zhao, F.-Q., Craig, R., Egelman, E.H., Alamo, L., Padron, R.. 2005. Atomic model of a myosin filament in the relaxed state. Nature 436, 1195-1199]. However, the orientation of the Wendt structure is different from that found by Woodhead in that the outer head projects outwards and the inner head lies closer to the filament backbone, as in earlier work done on the insect flight muscle myosin filaments [AL-Khayat, H.A., Hudson, L., Reedy, M.K., Irving, T.C., Squire, J.M., 2003. Myosin head configuration in relaxed insect flight muscle: X-ray modelled resting crossbridges in a pre-powerstroke state are poised for actin binding. Biophys. J. 85, 1063-1079]. Possible species specific details that may differ between the scallop and the tarantula myosin filaments are also discussed.",
keywords = "3D reconstruction, Electron microscopy, Myosin filaments, Myosin-linked regulation, Scallop striated muscle, Single particle analysis",
author = "AL-Khayat, {Hind A.} and Morris, {Edward P.} and Squire, {John M.}",
year = "2009",
month = "5",
doi = "10.1016/j.jsb.2009.02.006",
language = "English",
volume = "166",
pages = "183--194",
journal = "Journal of Structural Biology",
issn = "1047-8477",
publisher = "Academic Press Inc.",
number = "2",

}

TY - JOUR

T1 - The 7-stranded structure of relaxed scallop muscle myosin filaments

T2 - Support for a common head configuration in myosin-regulated muscles

AU - AL-Khayat, Hind A.

AU - Morris, Edward P.

AU - Squire, John M.

PY - 2009/5

Y1 - 2009/5

N2 - Isolated relaxed myosin filaments from the myosin-regulated scallop striated adductor muscle have been reconstructed using electron microscopy and single particle analysis of negatively stained filaments. Three-dimensional reconstruction using 7-fold rotational symmetry but without imposed helical symmetry confirmed that the myosin head array is a 7-stranded, right-handed long-pitch 24/1 helix (or left-handed short-pitch 10/1 helix) with the whole structure having an axial repeat of 1440 Å. Reconstruction using the full helical symmetry revealed details of the myosin head density distribution within the head crowns in the relaxed scallop myosin filament. The resulting density distribution can best be explained by an arrangement in which the two heads from the same myosin molecule interact together within each crown in a compact parallel fashion along the filament axis. The configuration is consistent with the published configuration of the two heads within vertebrate smooth muscle myosin molecules observed in two-dimensional crystals of smooth muscle myosin and in the structure of tarantula myosin filaments. All these three muscle types are myosin-regulated, providing further support for a general motif of intramolecular interacting-heads structure in the relaxed state of myosin-regulated muscles as was proposed earlier by Woodhead et al. [Woodhead, J.L., Zhao, F.-Q., Craig, R., Egelman, E.H., Alamo, L., Padron, R.. 2005. Atomic model of a myosin filament in the relaxed state. Nature 436, 1195-1199]. However, the orientation of the Wendt structure is different from that found by Woodhead in that the outer head projects outwards and the inner head lies closer to the filament backbone, as in earlier work done on the insect flight muscle myosin filaments [AL-Khayat, H.A., Hudson, L., Reedy, M.K., Irving, T.C., Squire, J.M., 2003. Myosin head configuration in relaxed insect flight muscle: X-ray modelled resting crossbridges in a pre-powerstroke state are poised for actin binding. Biophys. J. 85, 1063-1079]. Possible species specific details that may differ between the scallop and the tarantula myosin filaments are also discussed.

AB - Isolated relaxed myosin filaments from the myosin-regulated scallop striated adductor muscle have been reconstructed using electron microscopy and single particle analysis of negatively stained filaments. Three-dimensional reconstruction using 7-fold rotational symmetry but without imposed helical symmetry confirmed that the myosin head array is a 7-stranded, right-handed long-pitch 24/1 helix (or left-handed short-pitch 10/1 helix) with the whole structure having an axial repeat of 1440 Å. Reconstruction using the full helical symmetry revealed details of the myosin head density distribution within the head crowns in the relaxed scallop myosin filament. The resulting density distribution can best be explained by an arrangement in which the two heads from the same myosin molecule interact together within each crown in a compact parallel fashion along the filament axis. The configuration is consistent with the published configuration of the two heads within vertebrate smooth muscle myosin molecules observed in two-dimensional crystals of smooth muscle myosin and in the structure of tarantula myosin filaments. All these three muscle types are myosin-regulated, providing further support for a general motif of intramolecular interacting-heads structure in the relaxed state of myosin-regulated muscles as was proposed earlier by Woodhead et al. [Woodhead, J.L., Zhao, F.-Q., Craig, R., Egelman, E.H., Alamo, L., Padron, R.. 2005. Atomic model of a myosin filament in the relaxed state. Nature 436, 1195-1199]. However, the orientation of the Wendt structure is different from that found by Woodhead in that the outer head projects outwards and the inner head lies closer to the filament backbone, as in earlier work done on the insect flight muscle myosin filaments [AL-Khayat, H.A., Hudson, L., Reedy, M.K., Irving, T.C., Squire, J.M., 2003. Myosin head configuration in relaxed insect flight muscle: X-ray modelled resting crossbridges in a pre-powerstroke state are poised for actin binding. Biophys. J. 85, 1063-1079]. Possible species specific details that may differ between the scallop and the tarantula myosin filaments are also discussed.

KW - 3D reconstruction

KW - Electron microscopy

KW - Myosin filaments

KW - Myosin-linked regulation

KW - Scallop striated muscle

KW - Single particle analysis

UR - http://www.scopus.com/inward/record.url?scp=63949085530&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=63949085530&partnerID=8YFLogxK

U2 - 10.1016/j.jsb.2009.02.006

DO - 10.1016/j.jsb.2009.02.006

M3 - Article

VL - 166

SP - 183

EP - 194

JO - Journal of Structural Biology

JF - Journal of Structural Biology

SN - 1047-8477

IS - 2

ER -