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Plectin linkages are mechanosensitive and required for the nuclear piston mechanism of three-dimensional cell migration
Cells migrating through physiologically relevant three-dimensional (3D) substrates such as cell-derived matrix (CDM) use actomyosin and vimentin intermediate filaments to pull the nucleus forward and pressurize the front of the cell as part of the nuclear piston mechanism of 3D migration. In this st...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The American Society for Cell Biology
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9635290/ https://www.ncbi.nlm.nih.gov/pubmed/35857713 http://dx.doi.org/10.1091/mbc.E21-08-0414 |
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author | Marks, Pragati C. Hewitt, Breanne R. Baird, Michelle A. Wiche, Gerhard Petrie, Ryan J. |
author_facet | Marks, Pragati C. Hewitt, Breanne R. Baird, Michelle A. Wiche, Gerhard Petrie, Ryan J. |
author_sort | Marks, Pragati C. |
collection | PubMed |
description | Cells migrating through physiologically relevant three-dimensional (3D) substrates such as cell-derived matrix (CDM) use actomyosin and vimentin intermediate filaments to pull the nucleus forward and pressurize the front of the cell as part of the nuclear piston mechanism of 3D migration. In this study, we tested the role of the cytoskeleton cross-linking protein plectin in facilitating the movement of the nucleus through 3D matrices. We find that the interaction of F-actin and vimentin filaments in cells on 2D glass and in 3D CDM requires actomyosin contractility. Plectin also facilitated these interactions and interacts with vimentin in response to NMII contractility and substrate stiffness, suggesting that the association of plectin and vimentin is mechanosensitive. We find that this mechanosensitive plectin complex slows down 2D migration but is critical for pulling the nucleus forward and generating compartmentalized intracellular pressure in 3D CDM, as well as low-pressure lamellipodial migration in 3D collagen. Finally, plectin expression helped to polarize NMII to in front of the nucleus and to localize the vimentin network around the nucleus. Together, our data suggest that plectin cross-links vimentin and actomyosin filaments, organizes the vimentin network, and polarizes NMII to facilitate the nuclear piston mechanism of 3D cell migration. |
format | Online Article Text |
id | pubmed-9635290 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | The American Society for Cell Biology |
record_format | MEDLINE/PubMed |
spelling | pubmed-96352902022-12-07 Plectin linkages are mechanosensitive and required for the nuclear piston mechanism of three-dimensional cell migration Marks, Pragati C. Hewitt, Breanne R. Baird, Michelle A. Wiche, Gerhard Petrie, Ryan J. Mol Biol Cell Articles Cells migrating through physiologically relevant three-dimensional (3D) substrates such as cell-derived matrix (CDM) use actomyosin and vimentin intermediate filaments to pull the nucleus forward and pressurize the front of the cell as part of the nuclear piston mechanism of 3D migration. In this study, we tested the role of the cytoskeleton cross-linking protein plectin in facilitating the movement of the nucleus through 3D matrices. We find that the interaction of F-actin and vimentin filaments in cells on 2D glass and in 3D CDM requires actomyosin contractility. Plectin also facilitated these interactions and interacts with vimentin in response to NMII contractility and substrate stiffness, suggesting that the association of plectin and vimentin is mechanosensitive. We find that this mechanosensitive plectin complex slows down 2D migration but is critical for pulling the nucleus forward and generating compartmentalized intracellular pressure in 3D CDM, as well as low-pressure lamellipodial migration in 3D collagen. Finally, plectin expression helped to polarize NMII to in front of the nucleus and to localize the vimentin network around the nucleus. Together, our data suggest that plectin cross-links vimentin and actomyosin filaments, organizes the vimentin network, and polarizes NMII to facilitate the nuclear piston mechanism of 3D cell migration. The American Society for Cell Biology 2022-09-22 /pmc/articles/PMC9635290/ /pubmed/35857713 http://dx.doi.org/10.1091/mbc.E21-08-0414 Text en © 2022 Marks et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. https://creativecommons.org/licenses/by-nc-sa/3.0/This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial-Share Alike 4.0 International Creative Commons License. |
spellingShingle | Articles Marks, Pragati C. Hewitt, Breanne R. Baird, Michelle A. Wiche, Gerhard Petrie, Ryan J. Plectin linkages are mechanosensitive and required for the nuclear piston mechanism of three-dimensional cell migration |
title | Plectin linkages are mechanosensitive and required for the nuclear piston mechanism of three-dimensional cell migration |
title_full | Plectin linkages are mechanosensitive and required for the nuclear piston mechanism of three-dimensional cell migration |
title_fullStr | Plectin linkages are mechanosensitive and required for the nuclear piston mechanism of three-dimensional cell migration |
title_full_unstemmed | Plectin linkages are mechanosensitive and required for the nuclear piston mechanism of three-dimensional cell migration |
title_short | Plectin linkages are mechanosensitive and required for the nuclear piston mechanism of three-dimensional cell migration |
title_sort | plectin linkages are mechanosensitive and required for the nuclear piston mechanism of three-dimensional cell migration |
topic | Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9635290/ https://www.ncbi.nlm.nih.gov/pubmed/35857713 http://dx.doi.org/10.1091/mbc.E21-08-0414 |
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