Myosin head configuration in relaxed insect flight muscle: X-ray modeled resting cross-bridges in a pre-powerstroke state are poised for actin binding

Hind A. Al-Khayat, Liam Hudson, Michael K. Reedy, Thomas C. Irving, John M. Squire

Research output: Contribution to journalArticle

54 Citations (Scopus)

Abstract

Low-angle x-ray diffraction patterns from relaxed insect flight muscle recorded on the BioCAT beamline at the Argonne APS have been modeled to 6.5 nm resolution (R-factor 9.7%, 65 reflections) using the known myosin head atomic coordinates, a hinge between the motor (catalytic) domain and the light chain-binding (neck) region (lever arm), together with a simulated annealing procedure. The best head conformation angles around the hinge gave a head shape that was close to that typical of relaxed M·ADP·Pi heads, a head shape never before demonstrated in intact muscle. The best packing constrained the eight heads per crown within a compact crown shelf projecting at ∼90° to the filament axis. The two heads of each myosin molecule assume nonequivalent positions, one head projecting outward while the other curves round the thick filament surface to nose against the proximal neck of the projecting head of the neighboring molecule. The projecting heads immediately suggest a possible cross-bridge cycle. The relaxed projecting head, oriented almost as needed for actin attachment, will attach, then release Pi followed by ADP, as the lever arm with a purely axial change in tilt drives ∼10 nm of actin filament sliding on the way to the nucleotide-free limit of its working stroke. The overall arrangement appears well designed to support precision cycling for the myogenic oscillatory mode of contraction with its enhanced stretch-activation response used in flight by insects equipped with asynchronous fibrillar flight muscles.

Original languageEnglish
Pages (from-to)1063-1079
Number of pages17
JournalBiophysical Journal
Volume85
Issue number2
Publication statusPublished - 1 Aug 2003
Externally publishedYes

Fingerprint

Myosins
Insects
Actins
Head
X-Rays
Muscles
Crowns
R388
Actin Cytoskeleton
Nose
Adenosine Diphosphate
Catalytic Domain
Neck
Nucleotides
Stroke
Light

ASJC Scopus subject areas

  • Biophysics

Cite this

Myosin head configuration in relaxed insect flight muscle : X-ray modeled resting cross-bridges in a pre-powerstroke state are poised for actin binding. / Al-Khayat, Hind A.; Hudson, Liam; Reedy, Michael K.; Irving, Thomas C.; Squire, John M.

In: Biophysical Journal, Vol. 85, No. 2, 01.08.2003, p. 1063-1079.

Research output: Contribution to journalArticle

Al-Khayat, Hind A. ; Hudson, Liam ; Reedy, Michael K. ; Irving, Thomas C. ; Squire, John M. / Myosin head configuration in relaxed insect flight muscle : X-ray modeled resting cross-bridges in a pre-powerstroke state are poised for actin binding. In: Biophysical Journal. 2003 ; Vol. 85, No. 2. pp. 1063-1079.
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