skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Low temperature traps myosin motors of mammalian muscle in a refractory state that prevents activation

Abstract

The active force of mammalian skeletal muscle is reduced at low temperatures. Caremani et al. reveal that this is due to the rise of a population of myosin motors captured in a refractory state insensitive to muscle activation.

Authors:
 [1]; ORCiD logo [1]; ORCiD logo [2];  [3]; ORCiD logo [4];  [4]; ORCiD logo [1];  [3]; ORCiD logo [1]; ORCiD logo [2]
  1. PhysioLab, University of Florence, Florence, Italy
  2. PhysioLab, University of Florence, Florence, Italy; Consorzio Nazionale Interuniversitario per le Scienze Fisiche della Materia, Firenze, Italy
  3. Randall Centre for Cell and Molecular Biophysics, King’s College London, London, UK
  4. Center for Synchrotron Radiation Research and Instrumentation and Department of Biological Sciences, Illinois Institute of Technology, Chicago, IL
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
FOREIGN
OSTI Identifier:
1578235
Resource Type:
Journal Article
Journal Name:
Journal of General Physiology
Additional Journal Information:
Journal Volume: 151; Journal Issue: 11; Journal ID: ISSN 0022-1295
Country of Publication:
United States
Language:
ENGLISH

Citation Formats

Caremani, Marco, Brunello, Elisabetta, Linari, Marco, Fusi, Luca, Irving, Thomas C., Gore, David, Piazzesi, Gabriella, Irving, Malcolm, Lombardi, Vincenzo, and Reconditi, Massimo. Low temperature traps myosin motors of mammalian muscle in a refractory state that prevents activation. United States: N. p., 2019. Web. doi:10.1085/jgp.201912424.
Caremani, Marco, Brunello, Elisabetta, Linari, Marco, Fusi, Luca, Irving, Thomas C., Gore, David, Piazzesi, Gabriella, Irving, Malcolm, Lombardi, Vincenzo, & Reconditi, Massimo. Low temperature traps myosin motors of mammalian muscle in a refractory state that prevents activation. United States. doi:10.1085/jgp.201912424.
Caremani, Marco, Brunello, Elisabetta, Linari, Marco, Fusi, Luca, Irving, Thomas C., Gore, David, Piazzesi, Gabriella, Irving, Malcolm, Lombardi, Vincenzo, and Reconditi, Massimo. Wed . "Low temperature traps myosin motors of mammalian muscle in a refractory state that prevents activation". United States. doi:10.1085/jgp.201912424.
@article{osti_1578235,
title = {Low temperature traps myosin motors of mammalian muscle in a refractory state that prevents activation},
author = {Caremani, Marco and Brunello, Elisabetta and Linari, Marco and Fusi, Luca and Irving, Thomas C. and Gore, David and Piazzesi, Gabriella and Irving, Malcolm and Lombardi, Vincenzo and Reconditi, Massimo},
abstractNote = {The active force of mammalian skeletal muscle is reduced at low temperatures. Caremani et al. reveal that this is due to the rise of a population of myosin motors captured in a refractory state insensitive to muscle activation.},
doi = {10.1085/jgp.201912424},
journal = {Journal of General Physiology},
issn = {0022-1295},
number = 11,
volume = 151,
place = {United States},
year = {2019},
month = {9}
}

Works referenced in this record:

Power Output Is Increased After Phosphorylation of Myofibrillar Proteins in Rat Skinned Cardiac Myocytes
journal, December 2001

  • Herron, Todd J.; Korte, F. Steven; McDonald, Kerry S.
  • Circulation Research, Vol. 89, Issue 12
  • DOI: 10.1161/hh2401.101908

X-ray evidence for radial cross-bridge movement and for the sliding filament model in actively contracting skeletal muscle
journal, July 1973


Effect of temperature on the working stroke of muscle myosin
journal, September 2005

  • Decostre, V.; Bianco, P.; Lombardi, V.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 39
  • DOI: 10.1073/pnas.0506795102

Atomic model of a myosin filament in the relaxed state
journal, August 2005

  • Woodhead, John L.; Zhao, Fa-Qing; Craig, Roger
  • Nature, Vol. 436, Issue 7054
  • DOI: 10.1038/nature03920

Interacting-heads motif has been conserved as a mechanism of myosin II inhibition since before the origin of animals
journal, February 2018

  • Lee, Kyoung Hwan; Sulbarán, Guidenn; Yang, Shixin
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 9
  • DOI: 10.1073/pnas.1715247115

Changes in conformation of myosin heads during the development of isometric contraction and rapid shortening in single frog muscle fibres
journal, January 1999


All myosin heads form bonds with actin in rigor rabbit skeletal muscle
journal, May 1980


Temperature-dependent transitions in isometric contractions of rat muscle.
journal, June 1983


Time-resolved X-ray diffraction studies of the myosin layer-line reflections during muscle contraction
journal, July 1982


Tension responses to sudden length change in stimulated frog muscle fibres near slack length
journal, July 1977


Stiffness and Fraction of Myosin Motors Responsible for Active Force in Permeabilized Muscle Fibers from Rabbit Psoas
journal, April 2007


Temperature dependence of the force-generating process in single fibres from frog skeletal muscle
journal, May 2003


The binding of skeletal muscle C-protein to F-actin, and its relation to the interaction of actin with myosin subfragment-1
journal, October 1978


Characterization of radial force and radial stiffness in Ca(2+)-activated skinned fibres of the rabbit psoas muscle.
journal, September 1991


Myosin Head Configurations in Resting and Contracting Murine Skeletal Muscle
journal, September 2018

  • Ma, Weikang; Gong, Henry; Irving, Thomas
  • International Journal of Molecular Sciences, Vol. 19, Issue 9
  • DOI: 10.3390/ijms19092643

Mechanism of force generation by myosin heads in skeletal muscle
journal, February 2002

  • Piazzesi, Gabriella; Reconditi, Massimo; Linari, Marco
  • Nature, Vol. 415, Issue 6872
  • DOI: 10.1038/415659a

Atomic Structure of Scallop Myosin Subfragment S1 Complexed with MgADP
journal, May 1999


Interference fine structure and sarcomere length dependence of the axial x-ray pattern from active single muscle fibers
journal, June 2000

  • Linari, M.; Piazzesi, G.; Dobbie, I.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 13
  • DOI: 10.1073/pnas.97.13.7226

Direct Modeling of X-Ray Diffraction Pattern from Contracting Skeletal Muscle
journal, September 2008

  • Koubassova, Natalia A.; Bershitsky, Sergey Y.; Ferenczi, Michael A.
  • Biophysical Journal, Vol. 95, Issue 6
  • DOI: 10.1529/biophysj.107.120832

X-ray Diffraction Studies of the Thick Filament in Permeabilized Myocardium from Rabbit
journal, November 2006


Temperature-induced structural changes in the myosin thick filament of skinned rabbit psoas muscle
journal, November 1997


Muscle Structure and Theories of Contraction
journal, January 1957


A multipurpose instrument for time-resolved ultra-small-angle and coherent X-ray scattering
journal, October 2018

  • Narayanan, Theyencheri; Sztucki, Michael; Van Vaerenbergh, Pierre
  • Journal of Applied Crystallography, Vol. 51, Issue 6
  • DOI: 10.1107/S1600576718012748

Temperature dependency of force loss and Ca 2+ homeostasis in mouse EDL muscle after eccentric contractions
journal, April 2002

  • Warren, Gordon L.; Ingalls, Christopher P.; Armstrong, R. B.
  • American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 282, Issue 4
  • DOI: 10.1152/ajpregu.00671.2001

The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor
journal, December 1967


Temperature and Ligand Dependence of Conformation and Helical Order in Myosin Filaments
journal, January 2003


X-ray Interference Studies of Crossbridge Action in Muscle Contraction: Evidence from Quick Releases
journal, November 2006

  • Huxley, Hugh; Reconditi, Massimo; Stewart, Alex
  • Journal of Molecular Biology, Vol. 363, Issue 4
  • DOI: 10.1016/j.jmb.2006.08.075

Thick-Filament Extensibility in Intact Skeletal Muscle
journal, October 2018


Changes in the X-ray reflections from contracting muscle during rapid mechanical transients and their structural implications
journal, September 1983


Force generation by skeletal muscle is controlled by mechanosensing in myosin filaments
journal, November 2015

  • Linari, Marco; Brunello, Elisabetta; Reconditi, Massimo
  • Nature, Vol. 528, Issue 7581
  • DOI: 10.1038/nature15727

Dynamic properties of mammalian skeletal muscles.
journal, January 1972


Sarcomere-length dependence of myosin filament structure in skeletal muscle fibres of the frog: Myosin filament structure in skeletal muscle
journal, February 2014


X-ray diffraction study of fast and slow mammalian skeletal muscle in the live relaxed state
journal, September 1985


Interpretation of the X-ray diffraction pattern from relaxed skeletal muscle and modelling of the thick filament structure
journal, August 1992

  • Malinchik, S. B.; Lednev, V. V.
  • Journal of Muscle Research and Cell Motility, Vol. 13, Issue 4
  • DOI: 10.1007/BF01738036

Muscle force is generated by myosin heads stereospecifically attached to actin
journal, July 1997

  • Bershitsky, Sergey Y.; Tsaturyan, Andrey K.; Bershitskaya, Olga N.
  • Nature, Vol. 388, Issue 6638
  • DOI: 10.1038/40651

Control of muscle contraction
journal, November 1969

  • Ebashi, Setsuro; Endo, Makoto; Ohtsuki, Iwao
  • Quarterly Reviews of Biophysics, Vol. 2, Issue 4
  • DOI: 10.1017/S0033583500001190

Three-dimensional structure of vertebrate cardiac muscle myosin filaments
journal, February 2008

  • Zoghbi, M. E.; Woodhead, J. L.; Moss, R. L.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 7
  • DOI: 10.1073/pnas.0708912105

The myosin motor in muscle generates a smaller and slower working stroke at higher load
journal, April 2004

  • Reconditi, Massimo; Linari, Marco; Lucii, Leonardo
  • Nature, Vol. 428, Issue 6982
  • DOI: 10.1038/nature02380

Myosin light chain phosphorylation enhances contraction of heart muscle via structural changes in both thick and thin filaments
journal, May 2016

  • Kampourakis, Thomas; Sun, Yin-Biao; Irving, Malcolm
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 21
  • DOI: 10.1073/pnas.1602776113

Recent improvements in small angle x-ray diffraction for the study of muscle physiology
journal, September 2006


Diffraction by partially occupied helices
journal, May 2002

  • Tsaturyan, Andrey K.
  • Acta Crystallographica Section A Foundations of Crystallography, Vol. 58, Issue 3
  • DOI: 10.1107/S0108767302001307

Myosin binding protein-C phosphorylation is the principal mediator of protein kinase A effects on thick filament structure in myocardium
journal, November 2012

  • Colson, Brett A.; Patel, Jitandrakumar R.; Chen, Peter P.
  • Journal of Molecular and Cellular Cardiology, Vol. 53, Issue 5
  • DOI: 10.1016/j.yjmcc.2012.07.012

X-ray studies of order-disorder transitions in the myosin heads of skinned rabbit psoas muscles
journal, October 1991


Relationship between muscle fiber types and sizes and muscle architectural properties in the mouse hindlimb
journal, August 1994

  • Burkholder, Thomas J.; Fingado, Brian; Baron, Stephanie
  • Journal of Morphology, Vol. 221, Issue 2
  • DOI: 10.1002/jmor.1052210207

Regulation of Contraction by the Thick Filaments in Skeletal Muscle
journal, December 2017


Hypertrophic cardiomyopathy and the myosin mesa: viewing an old disease in a new light
journal, July 2017

  • Trivedi, Darshan V.; Adhikari, Arjun S.; Sarkar, Saswata S.
  • Biophysical Reviews, Vol. 10, Issue 1
  • DOI: 10.1007/s12551-017-0274-6

The M·ADP·Pi State Is Required for Helical Order in the Thick Filaments of Skeletal Muscle
journal, November 1999


Out Cold: Biochemical Regulation of Mammalian Hibernation – A Mini-Review
journal, January 2010


The BioCAT undulator beamline 18ID: a facility for biological non-crystalline diffraction and X-ray absorption spectroscopy at the Advanced Photon Source
journal, August 2004

  • Fischetti, R.; Stepanov, S.; Rosenbaum, G.
  • Journal of Synchrotron Radiation, Vol. 11, Issue 5
  • DOI: 10.1107/S0909049504016760

Regulation of Contraction in Striated Muscle
journal, January 2000


Myosin ATP turnover rate is a mechanism involved in thermogenesis in resting skeletal muscle fibers
journal, December 2009

  • Stewart, M. A.; Franks-Skiba, K.; Chen, S.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 1
  • DOI: 10.1073/pnas.0909468107

X-ray Interference Studies of Crossbridge Action in Muscle Contraction: Evidence from Muscles During Steady Shortening
journal, November 2006

  • Huxley, Hugh; Reconditi, Massimo; Stewart, Alex
  • Journal of Molecular Biology, Vol. 363, Issue 4
  • DOI: 10.1016/j.jmb.2006.08.055

Motion of myosin head domains during activation and force development in skeletal muscle
journal, April 2011

  • Reconditi, M.; Brunello, E.; Linari, M.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 17
  • DOI: 10.1073/pnas.1018330108

Myosin complexed with ADP and blebbistatin reversibly adopts a conformation resembling the start point of the working stroke
journal, March 2010

  • Takacs, B.; Billington, N.; Gyimesi, M.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 15
  • DOI: 10.1073/pnas.0907585107

Stabilization of Helical Order in the Thick Filaments by Blebbistatin: Further Evidence of Coexisting Multiple Conformations of Myosin
journal, May 2009


Detection of radial crossbridge force by lattice spacing changes in intact single muscle fibers
journal, December 1990


X-ray evidence for conformational changes in the myosin filaments of vertebrate striated muscle
journal, February 1975


Minimum number of myosin motors accounting for shortening velocity under zero load in skeletal muscle: Minimum number of motors for maximum shortening velocity
journal, December 2016

  • Fusi, Luca; Percario, Valentina; Brunello, Elisabetta
  • The Journal of Physiology, Vol. 595, Issue 4
  • DOI: 10.1113/JP273299

Fraction of myosin heads bound to thin filaments in rigor fibrils from insect flight and vertebrate muscles
journal, October 1981

  • Lovell, Stephen J.; Knight, Peter J.; Harrington, William F.
  • Nature, Vol. 293, Issue 5834
  • DOI: 10.1038/293664a0

Myosin filament activation in the heart is tuned to the mechanical task
journal, March 2017

  • Reconditi, Massimo; Caremani, Marco; Pinzauti, Francesca
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 12
  • DOI: 10.1073/pnas.1619484114

Axial and Radial Forces of Cross-Bridges Depend on Lattice Spacing
journal, December 2010


A New State of Cardiac Myosin with Very Slow ATP Turnover: A Potential Cardioprotective Mechanism in the Heart
journal, April 2011


FIT2D : a multi-purpose data reduction, analysis and visualization program
journal, March 2016


X-ray diffraction studies of cross-bridges weakly bound to actin in relaxed skinned fibers of rabbit psoas muscle
journal, November 1997