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Regulation of in vivo dynein force production by CDK5 and 14-3-3ε and KIAA0528

Single-molecule cytoplasmic dynein function is well understood, but there are major gaps in mechanistic understanding of cellular dynein regulation. We reported a mode of dynein regulation, force adaptation, where lipid droplets adapt to opposition to motion by increasing the duration and magnitude...

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Autores principales: Chapman, Dail E., Reddy, Babu J. N., Huy, Bunchhin, Bovyn, Matthew J., Cruz, Stephen John S., Al-Shammari, Zahraa M., Han, Han, Wang, Wenqi, Smith, Deanna S., Gross, Steven P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6335402/
https://www.ncbi.nlm.nih.gov/pubmed/30651536
http://dx.doi.org/10.1038/s41467-018-08110-z
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author Chapman, Dail E.
Reddy, Babu J. N.
Huy, Bunchhin
Bovyn, Matthew J.
Cruz, Stephen John S.
Al-Shammari, Zahraa M.
Han, Han
Wang, Wenqi
Smith, Deanna S.
Gross, Steven P.
author_facet Chapman, Dail E.
Reddy, Babu J. N.
Huy, Bunchhin
Bovyn, Matthew J.
Cruz, Stephen John S.
Al-Shammari, Zahraa M.
Han, Han
Wang, Wenqi
Smith, Deanna S.
Gross, Steven P.
author_sort Chapman, Dail E.
collection PubMed
description Single-molecule cytoplasmic dynein function is well understood, but there are major gaps in mechanistic understanding of cellular dynein regulation. We reported a mode of dynein regulation, force adaptation, where lipid droplets adapt to opposition to motion by increasing the duration and magnitude of force production, and found LIS1 and NudEL to be essential. Adaptation reflects increasing NudEL-LIS1 utilization; here, we hypothesize that such increasing utilization reflects CDK5-mediated NudEL phosphorylation, which increases the dynein-NudEL interaction, and makes force adaptation possible. We report that CDK5, 14-3-3ε, and CDK5 cofactor KIAA0528 together promote NudEL phosphorylation and are essential for force adaptation. By studying the process in COS-1 cells lacking Tau, we avoid confounding neuronal effects of CDK5 on microtubules. Finally, we extend this in vivo regulatory pathway to lysosomes and mitochondria. Ultimately, we show that dynein force adaptation can control the severity of lysosomal tug-of-wars among other intracellular transport functions involving high force.
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spelling pubmed-63354022019-01-18 Regulation of in vivo dynein force production by CDK5 and 14-3-3ε and KIAA0528 Chapman, Dail E. Reddy, Babu J. N. Huy, Bunchhin Bovyn, Matthew J. Cruz, Stephen John S. Al-Shammari, Zahraa M. Han, Han Wang, Wenqi Smith, Deanna S. Gross, Steven P. Nat Commun Article Single-molecule cytoplasmic dynein function is well understood, but there are major gaps in mechanistic understanding of cellular dynein regulation. We reported a mode of dynein regulation, force adaptation, where lipid droplets adapt to opposition to motion by increasing the duration and magnitude of force production, and found LIS1 and NudEL to be essential. Adaptation reflects increasing NudEL-LIS1 utilization; here, we hypothesize that such increasing utilization reflects CDK5-mediated NudEL phosphorylation, which increases the dynein-NudEL interaction, and makes force adaptation possible. We report that CDK5, 14-3-3ε, and CDK5 cofactor KIAA0528 together promote NudEL phosphorylation and are essential for force adaptation. By studying the process in COS-1 cells lacking Tau, we avoid confounding neuronal effects of CDK5 on microtubules. Finally, we extend this in vivo regulatory pathway to lysosomes and mitochondria. Ultimately, we show that dynein force adaptation can control the severity of lysosomal tug-of-wars among other intracellular transport functions involving high force. Nature Publishing Group UK 2019-01-16 /pmc/articles/PMC6335402/ /pubmed/30651536 http://dx.doi.org/10.1038/s41467-018-08110-z Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Chapman, Dail E.
Reddy, Babu J. N.
Huy, Bunchhin
Bovyn, Matthew J.
Cruz, Stephen John S.
Al-Shammari, Zahraa M.
Han, Han
Wang, Wenqi
Smith, Deanna S.
Gross, Steven P.
Regulation of in vivo dynein force production by CDK5 and 14-3-3ε and KIAA0528
title Regulation of in vivo dynein force production by CDK5 and 14-3-3ε and KIAA0528
title_full Regulation of in vivo dynein force production by CDK5 and 14-3-3ε and KIAA0528
title_fullStr Regulation of in vivo dynein force production by CDK5 and 14-3-3ε and KIAA0528
title_full_unstemmed Regulation of in vivo dynein force production by CDK5 and 14-3-3ε and KIAA0528
title_short Regulation of in vivo dynein force production by CDK5 and 14-3-3ε and KIAA0528
title_sort regulation of in vivo dynein force production by cdk5 and 14-3-3ε and kiaa0528
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6335402/
https://www.ncbi.nlm.nih.gov/pubmed/30651536
http://dx.doi.org/10.1038/s41467-018-08110-z
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