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

Caremani, Marco; Brunello, Elisabetta; Linari, Marco; Fusi, Luca; Irving, Thomas C.; Gore, David; Piazzesi, Gabriella; Irving, Malcolm; Lombardi, Vincenzo; Reconditi, Massimo

doi:10.1085/jgp.201912424

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

Abstract

Myosin motors in the thick filament of resting striated (skeletal and cardiac) muscle are trapped in an OFF state, in which the motors are packed in helical tracks on the filament surface, inhibiting their interactions with actin and utilization of ATP. To investigate the structural changes induced in the thick filament of mammalian skeletal muscle by changes in temperature, we collected x-ray diffraction patterns from the fast skeletal muscle extensor digitorum longus of the mouse in the temperature range from near physiological (35°C) to 10°C, in which the maximal isometric force (T₀) shows a threefold decrease. In resting muscle, x-ray reflections signaling the OFF state of the thick filament indicate that cooling produces a progressive disruption of the OFF state with motors moving away from the ordered helical tracks on the surface of the thick filament. We find that the number of myosin motors in the OFF state at 10°C is half of that at 35°C. At T₀, changes in the x-ray signals that report the fraction and conformation of actin-attached motors can be explained if the threefold decrease in force associated with lowering temperature is due not only to a decrease in the force-generating transition in the actin-attached motorsmore »« less

Authors:

Caremani, Marco;

;

; Fusi, Luca;

; Gore, David;

; Irving, Malcolm;

;

Publication Date:: Wed Sep 25 00:00:00 EDT 2019

Research Org.:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Org.:: USDOE Office of Science (SC)

OSTI Identifier:: 1566274

Alternate Identifier(s):: OSTI ID: 1578235

Grant/Contract Number:: AC02-06CH11357; RBFR08JAMZ; FG02-88ER25053

Resource Type:: Published Article

Journal Name:: Journal of General Physiology

Additional Journal Information:: Journal Name: Journal of General Physiology Journal Volume: 151 Journal Issue: 11; Journal ID: ISSN 0022-1295

Publisher:: Rockefeller University Press

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

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.

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                    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.  https://doi.org/10.1085/jgp.201912424

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                    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.  https://doi.org/10.1085/jgp.201912424.

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@article{osti_1566274,

  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 = {Myosin motors in the thick filament of resting striated (skeletal and cardiac) muscle are trapped in an OFF state, in which the motors are packed in helical tracks on the filament surface, inhibiting their interactions with actin and utilization of ATP. To investigate the structural changes induced in the thick filament of mammalian skeletal muscle by changes in temperature, we collected x-ray diffraction patterns from the fast skeletal muscle extensor digitorum longus of the mouse in the temperature range from near physiological (35°C) to 10°C, in which the maximal isometric force (T0) shows a threefold decrease. In resting muscle, x-ray reflections signaling the OFF state of the thick filament indicate that cooling produces a progressive disruption of the OFF state with motors moving away from the ordered helical tracks on the surface of the thick filament. We find that the number of myosin motors in the OFF state at 10°C is half of that at 35°C. At T0, changes in the x-ray signals that report the fraction and conformation of actin-attached motors can be explained if the threefold decrease in force associated with lowering temperature is due not only to a decrease in the force-generating transition in the actin-attached motors but also to a twofold decrease in the number of such motors. Thus, lowering the temperature reduces to the same extent the fraction of motors in the OFF state at rest and the fraction of motors attached to actin at T0, suggesting that motors that leave the OFF state accumulate in a disordered refractory state that makes them unavailable for interaction with actin upon stimulation. This regulatory effect of temperature on the thick filament of mammalian skeletal muscle could represent an energetically convenient mechanism for hibernating animals.},

  doi          = {10.1085/jgp.201912424},

  journal      = {Journal of General Physiology},

  number       = 11,

  volume       = 151,

  place        = {United States},

  year         = {Wed Sep 25 00:00:00 EDT 2019},

  month        = {Wed Sep 25 00:00:00 EDT 2019}

}

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Muscle protein analysis. II. Two-dimensional electrophoresis of normal and diseased human skeletal muscle

Journal Article Giometti, C S ; Barany, M ; Danon, M J ; ... - Clin. Chem.; (United States)

High-resolution two-dimensional electrophoresis was used to analyze the major proteins of normal and pathological human-muscle samples. The normal human-muscle pattern contains four myosin light chains: three that co-migrate with the myosin light chains from rabbit fast muscle (extensor digitorum longus), and one that co-migrates with the light chain 2 from rabbit slow muscle (soleus). Of seven Duchenne muscular dystrophy samples, four yielded patterns with decreased amounts of actin and myosin relative to normal muscle, while three samples gave patterns comparable to that for normal muscle. Six samples from patients with myotonic dystrophy also gave normal patterns. In nemaline rod myopathy,more »« less

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

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Citation Formats

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

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

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

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

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

Differential roles of regulatory light chain and myosin binding protein-C phosphorylations in the modulation of cardiac force development: X-ray studies of RLC phosphorylation in skinned murine cardiac muscle journal, March 2010

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

Resolution of Conformational States of Dictyostelium Myosin II Motor Domain Using Tryptophan (W501) Mutants: Implications for the Open-Closed Transition Identified by Crystallography † journal, December 2000

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

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

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

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

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

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

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

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

Kinetic Resolution of a Conformational Transition and the ATP Hydrolysis Step Using Relaxation Methods with a Dictyostelium Myosin II Mutant Containing a Single Tryptophan Residue † journal, October 2001

Structural Characterization of Weakly Attached Cross-Bridges in the A·M·ATP State in Permeabilized Rabbit Psoas Muscle journal, April 2002

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

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

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

Structural changes in myosin motors and filaments during relaxation of skeletal muscle: Structural changes in myosin during relaxation of skeletal muscle journal, September 2009

Control of muscle contraction journal, November 1969

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

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

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

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

The structural basis of the increase in isometric force production with temperature in frog skeletal muscle: Structural basis of increased muscle force at higher temperature journal, August 2005

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

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

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

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

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

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

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

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

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

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

Thick Filament Mechano-Sensing in Skeletal and Cardiac Muscles: A Common Mechanism Able to Adapt the Energetic Cost of the Contraction to the Task journal, June 2018

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

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

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

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

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

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

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

Differential roles of regulatory light chain and myosin binding protein-C phosphorylations in the modulation of cardiac force development: X-ray studies of RLC phosphorylation in skinned murine cardiac muscle
journal, March 2010

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

Resolution of Conformational States of Dictyostelium Myosin II Motor Domain Using Tryptophan (W501) Mutants: Implications for the Open-Closed Transition Identified by Crystallography ^†
journal, December 2000

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

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

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

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

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

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

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

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

Kinetic Resolution of a Conformational Transition and the ATP Hydrolysis Step Using Relaxation Methods with a Dictyostelium Myosin II Mutant Containing a Single Tryptophan Residue ^†
journal, October 2001

Structural Characterization of Weakly Attached Cross-Bridges in the A·M·ATP State in Permeabilized Rabbit Psoas Muscle
journal, April 2002

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

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

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

Structural changes in myosin motors and filaments during relaxation of skeletal muscle: Structural changes in myosin during relaxation of skeletal muscle
journal, September 2009

Control of muscle contraction
journal, November 1969

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

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

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

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

The structural basis of the increase in isometric force production with temperature in frog skeletal muscle: Structural basis of increased muscle force at higher temperature
journal, August 2005

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

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

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

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

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

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

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

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

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

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

Thick Filament Mechano-Sensing in Skeletal and Cardiac Muscles: A Common Mechanism Able to Adapt the Energetic Cost of the Contraction to the Task
journal, June 2018

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

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