X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle

H. E. Huxley, A. Stewart, Hernando J. Sosa, T. Irving

Research output: Contribution to journalArticle

361 Citations (Scopus)

Abstract

We have used a small angle scattering system assembled on the high flux multipole wiggler beam line at CHESS (Cornell) to make very accurate spacing measurements of certain meridional and layer-line reflections from contracting muscles. During isometric contraction, the actin 27.3 Å reflection increases in spacing from its resting value by approximately 0.3%, and other actin reflections, including the 59 and 51 Å off-meridional reflections, show corresponding changes in spacing. When tension is augmented or diminished by applying moderate speed length changes to a contracting muscle, changes in spacing in the range of 0.19-0.24% (when scaled to full isometric tension) can be seen. The larger difference between the resting and isometric spacings suggests either nonlinearity at low tension levels or the presence of a component related to activation itself. Myosin filaments also show similar increases in axial period during slow stretch, in addition to the well known larger change associated with activation. An actin spacing change of 0.25-0.3% can also be measured during a 2 ms time frame immediately after a quick release, showing that the elastic behavior is rapid. These observations of filament extensions totaling 2-3 nm per half-sarcomere may necessitate some significant revision of the interpretation of a number of mechanical experiments in muscle, in which it has usually been assumed that virtually all of the elasticity resides in the cross-bridges.

Original languageEnglish (US)
Pages (from-to)2411-2421
Number of pages11
JournalBiophysical Journal
Volume67
Issue number6
StatePublished - 1994
Externally publishedYes

Fingerprint

Myosins
Actin Cytoskeleton
X-Ray Diffraction
Actins
Muscles
Small Angle Scattering
Sarcomeres
Isometric Contraction
Elasticity

ASJC Scopus subject areas

  • Biophysics

Cite this

X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. / Huxley, H. E.; Stewart, A.; Sosa, Hernando J.; Irving, T.

In: Biophysical Journal, Vol. 67, No. 6, 1994, p. 2411-2421.

Research output: Contribution to journalArticle

@article{35e5597aa40f4b958d10ab2592d6fddc,
title = "X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle",
abstract = "We have used a small angle scattering system assembled on the high flux multipole wiggler beam line at CHESS (Cornell) to make very accurate spacing measurements of certain meridional and layer-line reflections from contracting muscles. During isometric contraction, the actin 27.3 {\AA} reflection increases in spacing from its resting value by approximately 0.3{\%}, and other actin reflections, including the 59 and 51 {\AA} off-meridional reflections, show corresponding changes in spacing. When tension is augmented or diminished by applying moderate speed length changes to a contracting muscle, changes in spacing in the range of 0.19-0.24{\%} (when scaled to full isometric tension) can be seen. The larger difference between the resting and isometric spacings suggests either nonlinearity at low tension levels or the presence of a component related to activation itself. Myosin filaments also show similar increases in axial period during slow stretch, in addition to the well known larger change associated with activation. An actin spacing change of 0.25-0.3{\%} can also be measured during a 2 ms time frame immediately after a quick release, showing that the elastic behavior is rapid. These observations of filament extensions totaling 2-3 nm per half-sarcomere may necessitate some significant revision of the interpretation of a number of mechanical experiments in muscle, in which it has usually been assumed that virtually all of the elasticity resides in the cross-bridges.",
author = "Huxley, {H. E.} and A. Stewart and Sosa, {Hernando J.} and T. Irving",
year = "1994",
language = "English (US)",
volume = "67",
pages = "2411--2421",
journal = "Biophysical Journal",
issn = "0006-3495",
publisher = "Biophysical Society",
number = "6",

}

TY - JOUR

T1 - X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle

AU - Huxley, H. E.

AU - Stewart, A.

AU - Sosa, Hernando J.

AU - Irving, T.

PY - 1994

Y1 - 1994

N2 - We have used a small angle scattering system assembled on the high flux multipole wiggler beam line at CHESS (Cornell) to make very accurate spacing measurements of certain meridional and layer-line reflections from contracting muscles. During isometric contraction, the actin 27.3 Å reflection increases in spacing from its resting value by approximately 0.3%, and other actin reflections, including the 59 and 51 Å off-meridional reflections, show corresponding changes in spacing. When tension is augmented or diminished by applying moderate speed length changes to a contracting muscle, changes in spacing in the range of 0.19-0.24% (when scaled to full isometric tension) can be seen. The larger difference between the resting and isometric spacings suggests either nonlinearity at low tension levels or the presence of a component related to activation itself. Myosin filaments also show similar increases in axial period during slow stretch, in addition to the well known larger change associated with activation. An actin spacing change of 0.25-0.3% can also be measured during a 2 ms time frame immediately after a quick release, showing that the elastic behavior is rapid. These observations of filament extensions totaling 2-3 nm per half-sarcomere may necessitate some significant revision of the interpretation of a number of mechanical experiments in muscle, in which it has usually been assumed that virtually all of the elasticity resides in the cross-bridges.

AB - We have used a small angle scattering system assembled on the high flux multipole wiggler beam line at CHESS (Cornell) to make very accurate spacing measurements of certain meridional and layer-line reflections from contracting muscles. During isometric contraction, the actin 27.3 Å reflection increases in spacing from its resting value by approximately 0.3%, and other actin reflections, including the 59 and 51 Å off-meridional reflections, show corresponding changes in spacing. When tension is augmented or diminished by applying moderate speed length changes to a contracting muscle, changes in spacing in the range of 0.19-0.24% (when scaled to full isometric tension) can be seen. The larger difference between the resting and isometric spacings suggests either nonlinearity at low tension levels or the presence of a component related to activation itself. Myosin filaments also show similar increases in axial period during slow stretch, in addition to the well known larger change associated with activation. An actin spacing change of 0.25-0.3% can also be measured during a 2 ms time frame immediately after a quick release, showing that the elastic behavior is rapid. These observations of filament extensions totaling 2-3 nm per half-sarcomere may necessitate some significant revision of the interpretation of a number of mechanical experiments in muscle, in which it has usually been assumed that virtually all of the elasticity resides in the cross-bridges.

UR - http://www.scopus.com/inward/record.url?scp=0028081493&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0028081493&partnerID=8YFLogxK

M3 - Article

VL - 67

SP - 2411

EP - 2421

JO - Biophysical Journal

JF - Biophysical Journal

SN - 0006-3495

IS - 6

ER -