Literature DB >> 35867749

Motor guidance by long-range communication on the microtubule highway.

Sithara S Wijeratne1,2, Shane A Fiorenza3, Alex E Neary2, Radhika Subramanian1,2, Meredith D Betterton3,4,5.   

Abstract

Coupling of motor proteins within arrays drives muscle contraction, flagellar beating, chromosome segregation, and other biological processes. Current models of motor coupling invoke either direct mechanical linkage or protein crowding, which rely on short-range motor-motor interactions. In contrast, coupling mechanisms that act at longer length scales remain largely unexplored. Here we report that microtubules can physically couple motor movement in the absence of detectable short-range interactions. The human kinesin-4 Kif4A changes the run length and velocity of other motors on the same microtubule in the dilute binding limit, when approximately 10-nm-sized motors are much farther apart than the motor size. This effect does not depend on specific motor-motor interactions because similar changes in Kif4A motility are induced by kinesin-1 motors. A micrometer-scale attractive interaction potential between motors is sufficient to recreate the experimental results in a biophysical model. Unexpectedly, our theory suggests that long-range microtubule-mediated coupling affects not only binding kinetics but also motor mechanochemistry. Therefore, the model predicts that motors can sense and respond to motors bound several micrometers away on a microtubule. Our results are consistent with a paradigm in which long-range motor interactions along the microtubule enable additional forms of collective motor behavior, possibly due to changes in the microtubule lattice.

Entities:  

Keywords:  cytoskeleton; kinesin; microtubules; motors

Mesh:

Substances:

Year:  2022        PMID: 35867749      PMCID: PMC9282251          DOI: 10.1073/pnas.2120193119

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   12.779


  58 in total

1.  Crowding of molecular motors determines microtubule depolymerization.

Authors:  Louis Reese; Anna Melbinger; Erwin Frey
Journal:  Biophys J       Date:  2011-11-01       Impact factor: 4.033

2.  Kinetics of nucleotide-dependent structural transitions in the kinesin-1 hydrolysis cycle.

Authors:  Keith J Mickolajczyk; Nathan C Deffenbaugh; Jaime Ortega Arroyo; Joanna Andrecka; Philipp Kukura; William O Hancock
Journal:  Proc Natl Acad Sci U S A       Date:  2015-12-16       Impact factor: 11.205

3.  Long-range cooperative binding of kinesin to a microtubule in the presence of ATP.

Authors:  Etsuko Muto; Hiroyuki Sakai; Kuniyoshi Kaseda
Journal:  J Cell Biol       Date:  2005-02-28       Impact factor: 10.539

4.  Understanding mechanochemical coupling in kinesins using first-passage-time processes.

Authors:  Anatoly B Kolomeisky; Evgeny B Stukalin; Alex A Popov
Journal:  Phys Rev E Stat Nonlin Soft Matter Phys       Date:  2005-03-08

5.  Molecular mechanisms for microtubule length regulation by kinesin-8 and XMAP215 proteins.

Authors:  Louis Reese; Anna Melbinger; Erwin Frey
Journal:  Interface Focus       Date:  2014-12-06       Impact factor: 3.906

Review 6.  The Kinesin-1 Chemomechanical Cycle: Stepping Toward a Consensus.

Authors:  William O Hancock
Journal:  Biophys J       Date:  2016-03-29       Impact factor: 4.033

7.  The low-angle x-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor.

Authors:  H E Huxley; W Brown
Journal:  J Mol Biol       Date:  1967-12-14       Impact factor: 5.469

8.  Modeling spatiotemporally varying protein-protein interactions in CyLaKS, the Cytoskeleton Lattice-based Kinetic Simulator.

Authors:  Shane A Fiorenza; Daniel G Steckhahn; Meredith D Betterton
Journal:  Eur Phys J E Soft Matter       Date:  2021-08-18       Impact factor: 1.890

9.  Biophysics of filament length regulation by molecular motors.

Authors:  Hui-Shun Kuan; M D Betterton
Journal:  Phys Biol       Date:  2013-04-16       Impact factor: 2.583

10.  Molecular Motors: Power Strokes Outperform Brownian Ratchets.

Authors:  Jason A Wagoner; Ken A Dill
Journal:  J Phys Chem B       Date:  2016-05-17       Impact factor: 2.991

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