Cargando…

Local Monomer Levels and Established Filaments Potentiate Non-Muscle Myosin 2 Assembly

The ability to dynamically assemble contractile networks is required throughout cell physiology, yet the biophysical mechanisms regulating non-muscle myosin 2 filament assembly in living cells are lacking. Here we use a suite of dynamic, quantitative imaging approaches to identify deterministic fact...

Descripción completa

Detalles Bibliográficos
Autores principales: Quintanilla, Melissa A., Patel, Hiral, Wu, Huini, Sochacki, Kem A., Akamatsu, Matthew, Rotty, Jeremy D., Korobova, Farida, Bear, James E., Taraska, Justin W., Oakes, Patrick W., Beach, Jordan R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10168331/
https://www.ncbi.nlm.nih.gov/pubmed/37162845
http://dx.doi.org/10.1101/2023.04.26.538303
_version_ 1785038835849101312
author Quintanilla, Melissa A.
Patel, Hiral
Wu, Huini
Sochacki, Kem A.
Akamatsu, Matthew
Rotty, Jeremy D.
Korobova, Farida
Bear, James E.
Taraska, Justin W.
Oakes, Patrick W.
Beach, Jordan R.
author_facet Quintanilla, Melissa A.
Patel, Hiral
Wu, Huini
Sochacki, Kem A.
Akamatsu, Matthew
Rotty, Jeremy D.
Korobova, Farida
Bear, James E.
Taraska, Justin W.
Oakes, Patrick W.
Beach, Jordan R.
author_sort Quintanilla, Melissa A.
collection PubMed
description The ability to dynamically assemble contractile networks is required throughout cell physiology, yet the biophysical mechanisms regulating non-muscle myosin 2 filament assembly in living cells are lacking. Here we use a suite of dynamic, quantitative imaging approaches to identify deterministic factors that drive myosin filament appearance and amplification. We find that actin dynamics regulate myosin assembly, but that the actin architecture plays a minimal direct role. Instead, remodeling of actin networks modulates the local myosin monomer levels and facilitates assembly through myosin:myosin driven interactions. Using optogenetically controlled myosin, we demonstrate that locally concentrating myosin is sufficient to both form filaments and jump-start filament amplification and partitioning. By counting myosin monomers within filaments, we demonstrate a myosin-facilitated assembly process that establishes sub-resolution filament stacks prior to partitioning into clusters that feed higher-order networks. Together these findings establish the biophysical mechanisms regulating the assembly of non-muscle contractile structures that are ubiquitous throughout cell biology.
format Online
Article
Text
id pubmed-10168331
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Cold Spring Harbor Laboratory
record_format MEDLINE/PubMed
spelling pubmed-101683312023-05-10 Local Monomer Levels and Established Filaments Potentiate Non-Muscle Myosin 2 Assembly Quintanilla, Melissa A. Patel, Hiral Wu, Huini Sochacki, Kem A. Akamatsu, Matthew Rotty, Jeremy D. Korobova, Farida Bear, James E. Taraska, Justin W. Oakes, Patrick W. Beach, Jordan R. bioRxiv Article The ability to dynamically assemble contractile networks is required throughout cell physiology, yet the biophysical mechanisms regulating non-muscle myosin 2 filament assembly in living cells are lacking. Here we use a suite of dynamic, quantitative imaging approaches to identify deterministic factors that drive myosin filament appearance and amplification. We find that actin dynamics regulate myosin assembly, but that the actin architecture plays a minimal direct role. Instead, remodeling of actin networks modulates the local myosin monomer levels and facilitates assembly through myosin:myosin driven interactions. Using optogenetically controlled myosin, we demonstrate that locally concentrating myosin is sufficient to both form filaments and jump-start filament amplification and partitioning. By counting myosin monomers within filaments, we demonstrate a myosin-facilitated assembly process that establishes sub-resolution filament stacks prior to partitioning into clusters that feed higher-order networks. Together these findings establish the biophysical mechanisms regulating the assembly of non-muscle contractile structures that are ubiquitous throughout cell biology. Cold Spring Harbor Laboratory 2023-04-27 /pmc/articles/PMC10168331/ /pubmed/37162845 http://dx.doi.org/10.1101/2023.04.26.538303 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Quintanilla, Melissa A.
Patel, Hiral
Wu, Huini
Sochacki, Kem A.
Akamatsu, Matthew
Rotty, Jeremy D.
Korobova, Farida
Bear, James E.
Taraska, Justin W.
Oakes, Patrick W.
Beach, Jordan R.
Local Monomer Levels and Established Filaments Potentiate Non-Muscle Myosin 2 Assembly
title Local Monomer Levels and Established Filaments Potentiate Non-Muscle Myosin 2 Assembly
title_full Local Monomer Levels and Established Filaments Potentiate Non-Muscle Myosin 2 Assembly
title_fullStr Local Monomer Levels and Established Filaments Potentiate Non-Muscle Myosin 2 Assembly
title_full_unstemmed Local Monomer Levels and Established Filaments Potentiate Non-Muscle Myosin 2 Assembly
title_short Local Monomer Levels and Established Filaments Potentiate Non-Muscle Myosin 2 Assembly
title_sort local monomer levels and established filaments potentiate non-muscle myosin 2 assembly
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10168331/
https://www.ncbi.nlm.nih.gov/pubmed/37162845
http://dx.doi.org/10.1101/2023.04.26.538303
work_keys_str_mv AT quintanillamelissaa localmonomerlevelsandestablishedfilamentspotentiatenonmusclemyosin2assembly
AT patelhiral localmonomerlevelsandestablishedfilamentspotentiatenonmusclemyosin2assembly
AT wuhuini localmonomerlevelsandestablishedfilamentspotentiatenonmusclemyosin2assembly
AT sochackikema localmonomerlevelsandestablishedfilamentspotentiatenonmusclemyosin2assembly
AT akamatsumatthew localmonomerlevelsandestablishedfilamentspotentiatenonmusclemyosin2assembly
AT rottyjeremyd localmonomerlevelsandestablishedfilamentspotentiatenonmusclemyosin2assembly
AT korobovafarida localmonomerlevelsandestablishedfilamentspotentiatenonmusclemyosin2assembly
AT bearjamese localmonomerlevelsandestablishedfilamentspotentiatenonmusclemyosin2assembly
AT taraskajustinw localmonomerlevelsandestablishedfilamentspotentiatenonmusclemyosin2assembly
AT oakespatrickw localmonomerlevelsandestablishedfilamentspotentiatenonmusclemyosin2assembly
AT beachjordanr localmonomerlevelsandestablishedfilamentspotentiatenonmusclemyosin2assembly