Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins

Daniel M. Miedema, Vandana S. Kushwaha, Dmitry V. Denisov, Seyda Acar, Bernard Nienhuis, Erwin J. G. Peterman, Peter Schall

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

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.
Original languageEnglish
Article number41037
JournalPhysical Review X
Volume7
Issue number4
DOIs
Publication statusPublished - 16 Nov 2017

Cite this

Miedema, D. M., Kushwaha, V. S., Denisov, D. V., Acar, S., Nienhuis, B., Peterman, E. J. G., & Schall, P. (2017). Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins. Physical Review X, 7(4), [41037]. https://doi.org/10.1103/PhysRevX.7.041037
Miedema, Daniel M. ; Kushwaha, Vandana S. ; Denisov, Dmitry V. ; Acar, Seyda ; Nienhuis, Bernard ; Peterman, Erwin J. G. ; Schall, Peter. / Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins. In: Physical Review X. 2017 ; Vol. 7, No. 4.
@article{db43a9e1fe964c14acd25e49bfbf74e2,
title = "Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins",
abstract = "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.",
author = "Miedema, {Daniel M.} and Kushwaha, {Vandana S.} and Denisov, {Dmitry V.} and Seyda Acar and Bernard Nienhuis and Peterman, {Erwin J. G.} and Peter Schall",
year = "2017",
month = "11",
day = "16",
doi = "10.1103/PhysRevX.7.041037",
language = "English",
volume = "7",
journal = "Physical Review X",
issn = "2160-3308",
publisher = "American Physical Society",
number = "4",

}

Miedema, DM, Kushwaha, VS, Denisov, DV, Acar, S, Nienhuis, B, Peterman, EJG & Schall, P 2017, 'Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins' Physical Review X, vol. 7, no. 4, 41037. https://doi.org/10.1103/PhysRevX.7.041037

Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins. / Miedema, Daniel M.; Kushwaha, Vandana S.; Denisov, Dmitry V.; Acar, Seyda; Nienhuis, Bernard; Peterman, Erwin J. G.; Schall, Peter.

In: Physical Review X, Vol. 7, No. 4, 41037, 16.11.2017.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - Correlation Imaging Reveals Specific Crowding Dynamics of Kinesin Motor Proteins

AU - Miedema, Daniel M.

AU - Kushwaha, Vandana S.

AU - Denisov, Dmitry V.

AU - Acar, Seyda

AU - Nienhuis, Bernard

AU - Peterman, Erwin J. G.

AU - Schall, Peter

PY - 2017/11/16

Y1 - 2017/11/16

N2 - 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.

AB - 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.

U2 - 10.1103/PhysRevX.7.041037

DO - 10.1103/PhysRevX.7.041037

M3 - Article

VL - 7

JO - Physical Review X

JF - Physical Review X

SN - 2160-3308

IS - 4

M1 - 41037

ER -