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1. Deciphering the transport of elastic filaments by antagonistic motor proteins

Author

J. C. Dallon, Cécile Leduc, Stéphanie Portet, Sandrine Etienne-Manneville, University of Manitoba [Winnipeg], Polarité cellulaire, Migration et Cancer - Cell Polarity, Migration and Cancer, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Brigham Young University (BYU), S.P. was partly supported by an National Sciences and Engineering Research Concil of Canada (NSERC) Discovery Grant. S.E.-M. and C.L. were supported by the Centre National de Recherche Scientifique, La Ligue Contre le Cancer, and the Institut Pasteur., The authors would like to thank the Isaac Newton Institute for Mathematical Sciences for support and hospitality during the program 'Coupling Geometric PDE's with Physics for Cell Morphology, Motility and Pattern Formation' when the work on this paper was undertaken. S.P. would like to thank Institut Pasteur for support of her stay. S.P. would like to thank P. van den Driessche for discussions on similar matrices., Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), and ANR-16-CE13-0019,SiFi2Net,Filaments intermédiaires: du filament unique au réseau(2016)

Subjects
MESH: Biological Transport, Dynein, Intermediate Filaments, MESH: Molecular Motor Proteins, macromolecular substances, Models, Biological, 01 natural sciences, 010305 fluids & plasmas, Slow motion, Protein filament, Motor protein, 0103 physical sciences, Molecular motor, Elasticity (economics), 010306 general physics, Intermediate filament, Physics, MESH: Kinetics, Molecular Motor Proteins, MESH: Models, Biological, Biological Transport, Elasticity, Kinetics, MESH: Intermediate Filaments, Biophysics, MESH: Elasticity, Kinesin, [SDV.SPEE]Life Sciences [q-bio]/Santé publique et épidémiologie
Abstract

International audience; Intermediate filaments are long elastic fibers that are transported by the microtubule-associated motor proteins kinesin and dynein inside the cell. How elastic filaments are efficiently transported by antagonistic motors is not well understood and is difficult to measure with current experimental techniques. Adapting the tug-of-war paradigm for vesiclelike cargos, we develop a mathematical model to describe the motion of an elastic filament punctually bound to antagonistic motors. As observed in cells, up to three modes of transport are obtained; dynein-driven retrograde, kinesin-driven anterograde fast motions, and a slow motion. Motor properties and initial conditions that depend on intracellular context regulate the transport of filaments. Filament elasticity is found to affect both the mode and the efficiency of transport. We further show that the coordination of motors along the filament emerges from the interplay between intracellular context and elastic properties of filaments.

Published
2019
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2. Stochastic modeling reveals how motor protein and filament properties affect intermediate filament transport

Author

Sandrine Etienne-Manneville, Stéphanie Portet, Cécile Leduc, J. C. Dallon, Brigham Young University (BYU), Polarité cellulaire, Migration et Cancer - Cell Polarity, Migration and Cancer, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), University of Manitoba [Winnipeg], This work was supported by: EPSRC grant numbers EP/K032208/1 and EP/R014604/1 and by La Ligue contre le cancer and the Institut Pasteur., The authors would like to thank the Isaac Newton Institute for Mathematical Sciences for support and hospitality during the programme 'Coupling Geometric PDE’s with Physics for Cell Morphology, Motility and Pattern Formation' when the work on this paper was undertaken., Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), and ANR-16-CE13-0019,SiFi2Net,Filaments intermédiaires: du filament unique au réseau(2016)

Subjects
0301 basic medicine, Statistics and Probability, Materials science, [SDV]Life Sciences [q-bio], Dynein, Biological Transport, Active, Kinesins, Catch bond, macromolecular substances, [SDV.BC]Life Sciences [q-bio]/Cellular Biology, Microtubules, Models, Biological, General Biochemistry, Genetics and Molecular Biology, Quantitative Biology::Cell Behavior, Protein filament, Motor protein, Quantitative Biology::Subcellular Processes, 03 medical and health sciences, 0302 clinical medicine, Molecular motor, Vimentin, Intermediate filaments, Intermediate filament, Cytoskeleton, Stochastic Processes, General Immunology and Microbiology, Applied Mathematics, Dyneins, Molecular motors, General Medicine, Kinesin, Stochastic, 030104 developmental biology, Modeling and Simulation, Biophysics, General Agricultural and Biological Sciences, 030217 neurology & neurosurgery
Abstract

International audience; Intermediate filaments are a key component of the cytoskeleton. Their transport along microtubules plays an essential role in the control of the shape and structural organization of cells. To identify the key parameters responsible for the control of intermediate filament transport, we generated a model of elastic filament transport by microtubule-associated dynein and kinesin. The model is also applicable to the transport of any elastically-coupled cargoes. We investigate the effect of filament properties such as number of motor binding sites, length, and elasticity on motion of filaments. Additionally, we consider the effect of motor properties, i.e. off rates, on filament transport. When one motor has a catch bond off rate it dictates the motion, whereas when motors have the same type of off rate filaments can alternate between retrograde and anterograde motions. The elasticity of filaments optimizes the filament transport and the coordination of motors along the length of the filament.

Published
2019
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