The Synergic Role of Actomyosin Architecture and Biased Detachment in Muscle Energetics: Insights in Cross Bridge Mechanism Beyond the Lever-Arm Swing

Autor: Toshio Yanagida, Mitsuhiro Iwaki, Lorenzo Marcucci, Hiroki Fukunaga
Jazyk: angličtina
Rok vydání: 2021
Předmět:
0301 basic medicine
Isometric exercise
Rotation
Quantitative Biology::Cell Behavior
Protein filament
0302 clinical medicine
Models
Myosin
Biology (General)
Spectroscopy
Physics
Adenosine Triphosphatases
Muscles
General Medicine
Mechanics
Actomyosin
Computer Science Applications
Chemistry
medicine.symptom
Monte Carlo Method
Muscle contraction
Muscle Contraction
muscle energetics
QH301-705.5
3D geometry
Thermal fluctuations
Models
Biological
Article
Catalysis
Inorganic Chemistry
Quantitative Biology::Subcellular Processes
03 medical and health sciences
medicine
Torque
Animals
Humans
Physical and Theoretical Chemistry
QD1-999
Molecular Biology
Mechanical energy
Monte Carlo simulation
Brownian ratchets
Organic Chemistry
Biological
Mechanism (engineering)
Kinetics
030104 developmental biology
DNA origami
Muscle energetics
030217 neurology & neurosurgery
Zdroj: International Journal of Molecular Sciences
Volume 22
Issue 13
International Journal of Molecular Sciences, Vol 22, Iss 7037, p 7037 (2021)
ISSN: 1422-0067
DOI: 10.3390/ijms22137037
Popis: Muscle energetics reflects the ability of myosin motors to convert chemical energy into mechanical energy. How this process takes place remains one of the most elusive questions in the field. Here we combined experimental measurements of in vitro sliding velocity based on DNA-origami built filaments carrying myosins with different lever arm length and simulations based on a Monte-Carlo model which accounts for three basic components: (i) the geometrical hindrance, (ii) the mechano-sensing mechanism, and (iii) the biased kinetics for stretched or compressed motors. The model simulations showed that the geometrical hindrance due to acto-myosin spatial mismatching and the preferential detachment of compressed motors are synergic in generating the rapid increase in the ATP-ase rate from isometric to moderate velocities of contraction, thus acting as an energy-conservation strategy in muscle contraction. The velocity measurements on a DNA-origami filament that preserves the motors’ distribution showed that geometrical hindrance and biased detachment generate a non-zero sliding velocity even without rotation of the myosin lever-arm, which is widely recognized as the basic event in muscle contraction. Because biased detachment is a mechanism for the rectification of thermal fluctuations, in the Brownian-ratchet framework, we predict that it requires a non-negligible amount of energy to preserve the second law of thermodynamics. Taken together, our theoretical and experimental results elucidate non-conventional components in the chemo-mechanical energy transduction in muscle.
Databáze: OpenAIRE
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