Stochastic force generation by small ensembles of myosin II motors.

Forces in the actin cytoskeleton are generated by small groups of nonprocessive myosin II motors for which stochastic effects are highly relevant. Using a cross-bridge model with the assumptions of fast power-stroke kinetics and equal load sharing between equivalent states, we derive a one-step master equation for the activity of a finite-sized ensemble of mechanically coupled myosin II motors. For constant external load, this approach yields analytical results for duty ratio and force-velocity relation as a function of ensemble size. We find that stochastic effects cannot be neglected for ensemble sizes below 15. The one-step master equation can be used also for efficient computer simulations with linear elastic external load and reveals the sequence of buildup of force and ensemble rupture that is characteristic for reconstituted actomyosin contractility.

[1]  Y. Kafri,et al.  Tug of war in motility assay experiments , 2009, Physical biology.

[2]  J. Prost,et al.  Spontaneous Oscillations of Collective Molecular Motors , 1996, cond-mat/9611204.

[3]  Spontaneous oscillations of a minimal actomyosin system under elastic loading. , 2009 .

[4]  N. Kampen,et al.  Stochastic processes in physics and chemistry , 1981 .

[5]  F. MacKintosh,et al.  Nonequilibrium Mechanics of Active Cytoskeletal Networks , 2007, Science.

[6]  G. Borisy,et al.  Non-sarcomeric mode of myosin II organization in the fibroblast lamellum , 1993, The Journal of cell biology.

[7]  S. Lowen.  The Biophysical Journal , 1960, Nature.

[8]  A. Huxley.  Muscle structure and theories of contraction. , 1957, Progress in biophysics and biophysical chemistry.

[9]  J. Spudich,et al.  Single myosin molecule mechanics: piconewton forces and nanometre steps , 1994, Nature.

[10]  O. Bagasra,et al.  Proceedings of the National Academy of Sciences , 1914, Science.

[11]  T. Duke,et al.  Molecular model of muscle contraction. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. Stewart,et al.  Skeletal Muscle Performance Determined by Modulation of Number of Myosin Motors Rather Than Motor Force or Stroke Size , 2007, Cell.

[13]  Fred C. MacKintosh,et al.  Active multistage coarsening of actin networks driven by myosin motors , 2011, Proceedings of the National Academy of Sciences.

[14]  William H Guilford,et al.  Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[15]  J. Patlak,et al.  Slip sliding away: load-dependence of velocity generated by skeletal muscle myosin molecules in the laser trap. , 2005, Biophysical journal.

[16]  R. Rosenfeld.  Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[17]  J. Joanny,et al.  Coordination and collective properties of molecular motors: theory. , 2010, Current opinion in cell biology.

[18]  Thomas Duke,et al.  Instabilities in the transient response of muscle. , 2003, Biophysical journal.

[19]  W. Ebeling.  Stochastic Processes in Physics and Chemistry , 1995 .

[20]  K. Tamura,et al.  Metabolic engineering of plant alkaloid biosynthesis. Proc Natl Acad Sci U S A , 2001 .

[21]  R. Lipowsky,et al.  Cooperative cargo transport by several molecular motors. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Justin E. Molloy,et al.  Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers , 2003, Nature Cell Biology.

[23]  October I.  Physical Review Letters , 2022 .

[24]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]／Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[25]  D. Gillespie.  A General Method for Numerically Simulating the Stochastic Time Evolution of Coupled Chemical Reactions , 1976 .

[26]  J. Howard,et al.  Molecular motors: structural adaptations to cellular functions , 1997, Nature.