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Structural changes in isometrically contracting insect flight muscle trapped following a mechanical perturbation.

Publication ,  Journal Article
Wu, S; Liu, J; Reedy, MC; Perz-Edwards, RJ; Tregear, RT; Winkler, H; Franzini-Armstrong, C; Sasaki, H; Lucaveche, C; Goldman, YE; Reedy, MK ...
Published in: PLoS One
2012

The application of rapidly applied length steps to actively contracting muscle is a classic method for synchronizing the response of myosin cross-bridges so that the average response of the ensemble can be measured. Alternatively, electron tomography (ET) is a technique that can report the structure of the individual members of the ensemble. We probed the structure of active myosin motors (cross-bridges) by applying 0.5% changes in length (either a stretch or a release) within 2 ms to isometrically contracting insect flight muscle (IFM) fibers followed after 5-6 ms by rapid freezing against a liquid helium cooled copper mirror. ET of freeze-substituted fibers, embedded and thin-sectioned, provides 3-D cross-bridge images, sorted by multivariate data analysis into ~40 classes, distinct in average structure, population size and lattice distribution. Individual actin subunits are resolved facilitating quasi-atomic modeling of each class average to determine its binding strength (weak or strong) to actin. ~98% of strong-binding acto-myosin attachments present after a length perturbation are confined to "target zones" of only two actin subunits located exactly midway between successive troponin complexes along each long-pitch helical repeat of actin. Significant changes in the types, distribution and structure of actin-myosin attachments occurred in a manner consistent with the mechanical transients. Most dramatic is near disappearance, after either length perturbation, of a class of weak-binding cross-bridges, attached within the target zone, that are highly likely to be precursors of strong-binding cross-bridges. These weak-binding cross-bridges were originally observed in isometrically contracting IFM. Their disappearance following a quick stretch or release can be explained by a recent kinetic model for muscle contraction, as behaviour consistent with their identification as precursors of strong-binding cross-bridges. The results provide a detailed model for contraction in IFM that may be applicable to contraction in other types of muscle.

Duke Scholars

Published In

PLoS One

DOI

EISSN

1932-6203

Publication Date

2012

Volume

7

Issue

6

Start / End Page

e39422

Location

United States

Related Subject Headings

  • Troponin
  • Muscle, Skeletal
  • Models, Biological
  • Isometric Contraction
  • Heteroptera
  • General Science & Technology
  • Flight, Animal
  • Animals
  • Actins
 

Citation

APA
Chicago
ICMJE
MLA
NLM
Wu, S., Liu, J., Reedy, M. C., Perz-Edwards, R. J., Tregear, R. T., Winkler, H., … Taylor, K. A. (2012). Structural changes in isometrically contracting insect flight muscle trapped following a mechanical perturbation. PLoS One, 7(6), e39422. https://doi.org/10.1371/journal.pone.0039422
Wu, Shenping, Jun Liu, Mary C. Reedy, Robert J. Perz-Edwards, Richard T. Tregear, Hanspeter Winkler, Clara Franzini-Armstrong, et al. “Structural changes in isometrically contracting insect flight muscle trapped following a mechanical perturbation.PLoS One 7, no. 6 (2012): e39422. https://doi.org/10.1371/journal.pone.0039422.
Wu S, Liu J, Reedy MC, Perz-Edwards RJ, Tregear RT, Winkler H, et al. Structural changes in isometrically contracting insect flight muscle trapped following a mechanical perturbation. PLoS One. 2012;7(6):e39422.
Wu, Shenping, et al. “Structural changes in isometrically contracting insect flight muscle trapped following a mechanical perturbation.PLoS One, vol. 7, no. 6, 2012, p. e39422. Pubmed, doi:10.1371/journal.pone.0039422.
Wu S, Liu J, Reedy MC, Perz-Edwards RJ, Tregear RT, Winkler H, Franzini-Armstrong C, Sasaki H, Lucaveche C, Goldman YE, Reedy MK, Taylor KA. Structural changes in isometrically contracting insect flight muscle trapped following a mechanical perturbation. PLoS One. 2012;7(6):e39422.

Published In

PLoS One

DOI

EISSN

1932-6203

Publication Date

2012

Volume

7

Issue

6

Start / End Page

e39422

Location

United States

Related Subject Headings

  • Troponin
  • Muscle, Skeletal
  • Models, Biological
  • Isometric Contraction
  • Heteroptera
  • General Science & Technology
  • Flight, Animal
  • Animals
  • Actins