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Vimentin Tail Segments Are Differentially Exposed at Distinct Cellular Locations and in Response to Stress

The intermediate filament protein vimentin plays a key role in cell signaling and stress sensing, as well as an integrator of cytoskeletal dynamics. The vimentin monomer consists of a central rod-like domain and intrinsically disordered head and tail domains. Although the organization of vimentin ol...

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Autores principales: Lois-Bermejo, Irene, González-Jiménez, Patricia, Duarte, Sofia, Pajares, María A., Pérez-Sala, Dolores
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9235546/
https://www.ncbi.nlm.nih.gov/pubmed/35769261
http://dx.doi.org/10.3389/fcell.2022.908263
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author Lois-Bermejo, Irene
González-Jiménez, Patricia
Duarte, Sofia
Pajares, María A.
Pérez-Sala, Dolores
author_facet Lois-Bermejo, Irene
González-Jiménez, Patricia
Duarte, Sofia
Pajares, María A.
Pérez-Sala, Dolores
author_sort Lois-Bermejo, Irene
collection PubMed
description The intermediate filament protein vimentin plays a key role in cell signaling and stress sensing, as well as an integrator of cytoskeletal dynamics. The vimentin monomer consists of a central rod-like domain and intrinsically disordered head and tail domains. Although the organization of vimentin oligomers in filaments is beginning to be understood, the precise disposition of the tail region remains to be elucidated. Here we observed that electrophilic stress-induced condensation shielded vimentin from recognition by antibodies against specific segments of the tail domain. A detailed characterization revealed that vimentin tail segments are differentially exposed at distinct subcellular locations, both in basal and stress conditions. The 411–423 segment appeared accessible in all cell areas, correlating with vimentin abundance. In contrast, the 419–438 segment was more scantily recognized in perinuclear vimentin and lipoxidative stress-induced bundles, and better detected in peripheral filaments, where it appeared to protrude further from the filament core. These differences persisted in mitotic cells. Interestingly, both tail segments showed closer accessibility in calyculin A-treated cells and phosphomimetic mutants of the C-terminal region. Our results lead us to hypothesize the presence of at least two distinct arrangements of vimentin tail in cells: an “extended” conformation (accessible 419–438 segment), preferentially detected in peripheral areas with looser filaments, and a “packed” conformation (shielded 419–438 segment), preferentially detected at the cell center in robust filaments and lipoxidative stress-induced bundles. These different arrangements could be putatively interconverted by posttranslational modifications, contributing to the versatility of vimentin functions and/or interactions.
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spelling pubmed-92355462022-06-28 Vimentin Tail Segments Are Differentially Exposed at Distinct Cellular Locations and in Response to Stress Lois-Bermejo, Irene González-Jiménez, Patricia Duarte, Sofia Pajares, María A. Pérez-Sala, Dolores Front Cell Dev Biol Cell and Developmental Biology The intermediate filament protein vimentin plays a key role in cell signaling and stress sensing, as well as an integrator of cytoskeletal dynamics. The vimentin monomer consists of a central rod-like domain and intrinsically disordered head and tail domains. Although the organization of vimentin oligomers in filaments is beginning to be understood, the precise disposition of the tail region remains to be elucidated. Here we observed that electrophilic stress-induced condensation shielded vimentin from recognition by antibodies against specific segments of the tail domain. A detailed characterization revealed that vimentin tail segments are differentially exposed at distinct subcellular locations, both in basal and stress conditions. The 411–423 segment appeared accessible in all cell areas, correlating with vimentin abundance. In contrast, the 419–438 segment was more scantily recognized in perinuclear vimentin and lipoxidative stress-induced bundles, and better detected in peripheral filaments, where it appeared to protrude further from the filament core. These differences persisted in mitotic cells. Interestingly, both tail segments showed closer accessibility in calyculin A-treated cells and phosphomimetic mutants of the C-terminal region. Our results lead us to hypothesize the presence of at least two distinct arrangements of vimentin tail in cells: an “extended” conformation (accessible 419–438 segment), preferentially detected in peripheral areas with looser filaments, and a “packed” conformation (shielded 419–438 segment), preferentially detected at the cell center in robust filaments and lipoxidative stress-induced bundles. These different arrangements could be putatively interconverted by posttranslational modifications, contributing to the versatility of vimentin functions and/or interactions. Frontiers Media S.A. 2022-06-08 /pmc/articles/PMC9235546/ /pubmed/35769261 http://dx.doi.org/10.3389/fcell.2022.908263 Text en Copyright © 2022 Lois-Bermejo, González-Jiménez, Duarte, Pajares and Pérez-Sala. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Lois-Bermejo, Irene
González-Jiménez, Patricia
Duarte, Sofia
Pajares, María A.
Pérez-Sala, Dolores
Vimentin Tail Segments Are Differentially Exposed at Distinct Cellular Locations and in Response to Stress
title Vimentin Tail Segments Are Differentially Exposed at Distinct Cellular Locations and in Response to Stress
title_full Vimentin Tail Segments Are Differentially Exposed at Distinct Cellular Locations and in Response to Stress
title_fullStr Vimentin Tail Segments Are Differentially Exposed at Distinct Cellular Locations and in Response to Stress
title_full_unstemmed Vimentin Tail Segments Are Differentially Exposed at Distinct Cellular Locations and in Response to Stress
title_short Vimentin Tail Segments Are Differentially Exposed at Distinct Cellular Locations and in Response to Stress
title_sort vimentin tail segments are differentially exposed at distinct cellular locations and in response to stress
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9235546/
https://www.ncbi.nlm.nih.gov/pubmed/35769261
http://dx.doi.org/10.3389/fcell.2022.908263
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