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Open AccessArticle

The Interacting Head Motif Structure Does Not Explain the X-Ray Diffraction Patterns in Relaxed Vertebrate (Bony Fish) Skeletal Muscle and Insect (Lethocerus) Flight Muscle

1
School of Optometry and Vision Science, Cardiff University, Cardiff CF10 3NB, UK
2
Division of Structural Biology, Institute of Cancer Research, London SW7 3RP, UK
3
Muscle Contraction Group, School of Physiology, Pharmacology and Neuroscience, University of Bristol, Bristol BS8 1TD, UK
4
Computational and Systems Medicine, Faculty of Medicine, Imperial College, London SW7 2BZ, UK
*
Author to whom correspondence should be addressed.
Biology 2019, 8(3), 67; https://doi.org/10.3390/biology8030067
Received: 18 July 2019 / Revised: 31 August 2019 / Accepted: 10 September 2019 / Published: 14 September 2019
(This article belongs to the Special Issue Feature Papers 2019)
Unlike electron microscopy, which can achieve very high resolution but to date can only be used to study static structures, time-resolved X-ray diffraction from contracting muscles can, in principle, be used to follow the molecular movements involved in force generation on a millisecond timescale, albeit at moderate resolution. However, previous X-ray diffraction studies of resting muscles have come up with structures for the head arrangements in resting myosin filaments that are different from the apparently ubiquitous interacting head motif (IHM) structures found by single particle analysis of electron micrographs of isolated myosin filaments from a variety of muscle types. This head organization is supposed to represent the super-relaxed state of the myosin filaments where adenosine triphosphate (ATP) usage is minimized. Here we have tested whether the interacting head motif structures will satisfactorily explain the observed low-angle X-ray diffraction patterns from resting vertebrate (bony fish) and invertebrate (insect flight) muscles. We find that the interacting head motif does not, in fact, explain what is observed. Previous X-ray models fit the observations much better. We conclude that the X-ray diffraction evidence has been well interpreted in the past and that there is more than one ordered myosin head state in resting muscle. There is, therefore, no reason to question some of the previous X-ray diffraction results on myosin filaments; time-resolved X-ray diffraction should be a reliable way to follow crossbridge action in active muscle and may be one of the few ways to visualise the molecular changes in myosin heads on a millisecond timescale as force is actually produced. View Full-Text
Keywords: bony fish muscle; insect flight muscle; myosin filament structure; myosin crossbridge cycle; thick filament activation; interacting head motif bony fish muscle; insect flight muscle; myosin filament structure; myosin crossbridge cycle; thick filament activation; interacting head motif
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Knupp, C.; Morris, E.; Squire, J.M. The Interacting Head Motif Structure Does Not Explain the X-Ray Diffraction Patterns in Relaxed Vertebrate (Bony Fish) Skeletal Muscle and Insect (Lethocerus) Flight Muscle. Biology 2019, 8, 67.

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