Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins

Molecular motor proteins fulfill the critical function of transporting organelles and other building blocks along the biopolymer network of the cell’s cytoskeleton, but crowding effects are believed to crucially affect this motor-driven transport due to motor interactions. Physical transport models,...

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Main Authors: Daniël M. Miedema, Vandana S. Kushwaha, Dmitry V. Denisov, Seyda Acar, Bernard Nienhuis, Erwin J. G. Peterman, Peter Schall
Format: Article
Language:English
Published: American Physical Society 2017-11-01
Series:Physical Review X
Online Access:http://doi.org/10.1103/PhysRevX.7.041037
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spelling doaj-554dedee2a4e48d2ab76f18db312ff612020-11-24T22:05:24ZengAmerican Physical SocietyPhysical Review X2160-33082017-11-017404103710.1103/PhysRevX.7.041037Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor ProteinsDaniël M. MiedemaVandana S. KushwahaDmitry V. DenisovSeyda AcarBernard NienhuisErwin J. G. PetermanPeter SchallMolecular motor proteins fulfill the critical function of transporting organelles and other building blocks along the biopolymer network of the cell’s cytoskeleton, but crowding effects are believed to crucially affect this motor-driven transport due to motor interactions. Physical transport models, like the paradigmatic, totally asymmetric simple exclusion process (TASEP), have been used to predict these crowding effects based on simple exclusion interactions, but verifying them in experiments remains challenging. Here, we introduce a correlation imaging technique to precisely measure the motor density, velocity, and run length along filaments under crowding conditions, enabling us to elucidate the physical nature of crowding and test TASEP model predictions. Using the kinesin motor proteins kinesin-1 and OSM-3, we identify crowding effects in qualitative agreement with TASEP predictions, and we achieve excellent quantitative agreement by extending the model with motor-specific interaction ranges and crowding-dependent detachment probabilities. These results confirm the applicability of basic nonequilibrium models to the intracellular transport and highlight motor-specific strategies to deal with crowding.http://doi.org/10.1103/PhysRevX.7.041037
collection DOAJ
language English
format Article
sources DOAJ
author Daniël M. Miedema
Vandana S. Kushwaha
Dmitry V. Denisov
Seyda Acar
Bernard Nienhuis
Erwin J. G. Peterman
Peter Schall
spellingShingle Daniël M. Miedema
Vandana S. Kushwaha
Dmitry V. Denisov
Seyda Acar
Bernard Nienhuis
Erwin J. G. Peterman
Peter Schall
Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins
Physical Review X
author_facet Daniël M. Miedema
Vandana S. Kushwaha
Dmitry V. Denisov
Seyda Acar
Bernard Nienhuis
Erwin J. G. Peterman
Peter Schall
author_sort Daniël M. Miedema
title Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins
title_short Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins
title_full Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins
title_fullStr Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins
title_full_unstemmed Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins
title_sort correlation imaging reveals specific crowding dynamics of kinesin motor proteins
publisher American Physical Society
series Physical Review X
issn 2160-3308
publishDate 2017-11-01
description Molecular motor proteins fulfill the critical function of transporting organelles and other building blocks along the biopolymer network of the cell’s cytoskeleton, but crowding effects are believed to crucially affect this motor-driven transport due to motor interactions. Physical transport models, like the paradigmatic, totally asymmetric simple exclusion process (TASEP), have been used to predict these crowding effects based on simple exclusion interactions, but verifying them in experiments remains challenging. Here, we introduce a correlation imaging technique to precisely measure the motor density, velocity, and run length along filaments under crowding conditions, enabling us to elucidate the physical nature of crowding and test TASEP model predictions. Using the kinesin motor proteins kinesin-1 and OSM-3, we identify crowding effects in qualitative agreement with TASEP predictions, and we achieve excellent quantitative agreement by extending the model with motor-specific interaction ranges and crowding-dependent detachment probabilities. These results confirm the applicability of basic nonequilibrium models to the intracellular transport and highlight motor-specific strategies to deal with crowding.
url http://doi.org/10.1103/PhysRevX.7.041037
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