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Motor guidance by long-range communication on the microtubule highway
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...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9282251/ https://www.ncbi.nlm.nih.gov/pubmed/35867749 http://dx.doi.org/10.1073/pnas.2120193119 |
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author | Wijeratne, Sithara S. Fiorenza, Shane A. Neary, Alex E. Subramanian, Radhika Betterton, Meredith D. |
author_facet | Wijeratne, Sithara S. Fiorenza, Shane A. Neary, Alex E. Subramanian, Radhika Betterton, Meredith D. |
author_sort | Wijeratne, Sithara S. |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-9282251 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-92822512023-01-07 Motor guidance by long-range communication on the microtubule highway Wijeratne, Sithara S. Fiorenza, Shane A. Neary, Alex E. Subramanian, Radhika Betterton, Meredith D. Proc Natl Acad Sci U S A Physical Sciences 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. National Academy of Sciences 2022-07-07 2022-07-12 /pmc/articles/PMC9282251/ /pubmed/35867749 http://dx.doi.org/10.1073/pnas.2120193119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Physical Sciences Wijeratne, Sithara S. Fiorenza, Shane A. Neary, Alex E. Subramanian, Radhika Betterton, Meredith D. Motor guidance by long-range communication on the microtubule highway |
title | Motor guidance by long-range communication on the microtubule highway |
title_full | Motor guidance by long-range communication on the microtubule highway |
title_fullStr | Motor guidance by long-range communication on the microtubule highway |
title_full_unstemmed | Motor guidance by long-range communication on the microtubule highway |
title_short | Motor guidance by long-range communication on the microtubule highway |
title_sort | motor guidance by long-range communication on the microtubule highway |
topic | Physical Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9282251/ https://www.ncbi.nlm.nih.gov/pubmed/35867749 http://dx.doi.org/10.1073/pnas.2120193119 |
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