Abstract
Actin-myosin (actomyosin) generates mechanical force by consuming ATP molecules. We apply the energy landscape perspective to address a controversial issue as to whether the myosin head moves with multiple steps after a single ATP hydrolysis or only a single mechanical event of the lever-arm swinging follows a single ATP hydrolysis. Here we propose a theoretical model in which the refolding of the partially unfolded actomyosin complex and the movement of the myosin head along the actin filament are coupled. A single ATP hydrolysis is followed by the formation of a high free-energy partially unfolded actomyosin complex, which then gradually refolds with a concomitant multiple stepping movement on the way to the lowest free-energy rigor state. The model quantitatively explains the single-molecular observation of the multiple stepping movement and is consistent with structural observations of the disorder in the actomyosin-binding process. The model also explains the observed variety in dwell time before each step, which is not accounted for by previous models, such as the lever-arm or ratchet models.
MeSH Terms
Actins/chemistry,physiology
Actomyosin/chemistry,physiology
Adenosine Triphosphate/metabolism
Animals
Binding Sites
Biomechanical Phenomena
Energy Metabolism
Hydrolysis
In Vitro Techniques
Macromolecular Substances
Models, Biological
Monte Carlo Method
Muscle Contraction/physiology
Myosins/chemistry,physiology
Protein Conformation
Thermodynamics
Chemicals
Actins
Macromolecular Substances
Adenosine Triphosphate
Actomyosin
Myosins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Terada Tomoki P
Graduate School of Human Informatics, Nagoya University, Nagoya 464-8601, Japan. terada@info.human.nagoya-u.ac.jp
Sasai Masaki
Yomo Tetsuya
References (30)
30 references, click to expand
-
Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head.
Cell. 1999 May 14;97(4):459-70
PMID: 10338210
-
The force exerted by a molecular motor.
Proc Natl Acad Sci U S A. 1999 Jun 8;96(12):6597-602
PMID: 10359757
-
Lever arm model of force generation by actin-myosin-ATP.
Biochemistry. 1999 Aug 3;38(31):9791-7
PMID: 10433684
-
Myosin VI is an actin-based motor that moves backwards.
Nature. 1999 Sep 30;401(6752):505-8
PMID: 10519557
-
The mechanochemistry of molecular motors.
Biophys J. 2000 Feb;78(2):541-56
PMID: 10653770
-
Actomyosin: law and order in motility.
Curr Opin Cell Biol. 2000 Feb;12(1):26-34
PMID: 10679363
-
Structural mechanism of muscle contraction.
Annu Rev Biochem. 1999;68:687-728
PMID: 10872464
-
Speeding molecular recognition by using the folding funnel: the fly-casting mechanism.
Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8868-73
PMID: 10908673
-
A large step for myosin.
Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9357-9
PMID: 10944206
-
Conformational selection during weak binding at the actin and myosin interface.
Biophys J. 2000 Sep;79(3):1498-510
PMID: 10969011
-
Evidence for cleft closure in actomyosin upon ADP release.
Nat Struct Biol. 2000 Dec;7(12):1147-55
PMID: 11101898
-
Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase.
Nature. 2001 Apr 19;410(6831):898-904
PMID: 11309608
-
Stretching the lever-arm theory.
Nature. 2002 Jan 10;415(6868):129-31
PMID: 11805818
-
A simple theory of motor protein kinetics and energetics.
Biophys Chem. 1997 Sep 1;67(1-3):263-7
PMID: 17029900
-
Protein motors and Maxwell's demons: does mechanochemical transduction involve a thermal ratchet?
Adv Biophys. 1990;26:97-134
PMID: 2150583
-
Thermodynamic analysis of muscle ATPase mechanisms.
Physiol Rev. 1985 Apr;65(2):467-551
PMID: 2580325
-
Protein Folding: A Perspective from Theory and Experiment.
Angew Chem Int Ed Engl. 1998 Apr 20;37(7):868-893
PMID: 29711488
-
Spin glasses and the statistical mechanics of protein folding.
Proc Natl Acad Sci U S A. 1987 Nov;84(21):7524-8
PMID: 3478708
-
Sliding distance of actin filament induced by a myosin crossbridge during one ATP hydrolysis cycle.
Nature. 1985 Jul 25-31;316(6026):366-9
PMID: 4022127
-
Movement of single myosin filaments and myosin step size on an actin filament suspended in solution by a laser trap.
Biophys J. 1994 Mar;66(3 Pt 1):769-77
PMID: 8011909
-
The swinging lever-arm hypothesis of muscle contraction.
Curr Biol. 1997 Feb 1;7(2):R112-8
PMID: 9081660
-
Thermodynamics and kinetics of a Brownian motor.
Science. 1997 May 9;276(5314):917-22
PMID: 9139648
-
Actomyosin interaction in striated muscle.
Physiol Rev. 1997 Jul;77(3):671-97
PMID: 9234962
-
Simultaneous observation of individual ATPase and mechanical events by a single myosin molecule during interaction with actin.
Cell. 1998 Jan 23;92(2):161-71
PMID: 9458041
-
A large and distinct rotation of the myosin light chain domain occurs upon muscle contraction.
Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):2944-9
PMID: 9501195
-
Myosin conformational states determined by single fluorophore polarization.
Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8034-9
PMID: 9653135
-
F1-ATPase is a highly efficient molecular motor that rotates with discrete 120 degree steps.
Cell. 1998 Jun 26;93(7):1117-24
PMID: 9657145
-
Microsecond rotational dynamics of spin-labeled myosin regulatory light chain induced by relaxation and contraction of scallop muscle.
Biochemistry. 1998 Oct 13;37(41):14428-36
PMID: 9772169
-
Observation of transient disorder during myosin subfragment-1 binding to actin by stopped-flow fluorescence and millisecond time resolution electron cryomicroscopy: evidence that the start of the crossbridge power stroke in muscle has variable geometry.
Proc Natl Acad Sci U S A. 1999 Jan 19;96(2):465-70
PMID: 9892656
-
A single myosin head moves along an actin filament with regular steps of 5.3 nanometres.
Nature. 1999 Jan 14;397(6715):129-34
PMID: 9923673