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Stress-induced phase separation of ERES components into Sec bodies precedes ER exit inhibition in mammalian cells

Phase separation of components of ER exit sites (ERES) into membraneless compartments, the Sec bodies, occurs in Drosophila cells upon exposure to specific cellular stressors, namely, salt stress and amino acid starvation, and their formation is linked to the early secretory pathway inhibition. Here...

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Autores principales: van Leeuwen, Wessel, Nguyen, Dan T. M., Grond, Rianne, Veenendaal, Tineke, Rabouille, Catherine, Farías, Ginny G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10112967/
https://www.ncbi.nlm.nih.gov/pubmed/36325988
http://dx.doi.org/10.1242/jcs.260294
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author van Leeuwen, Wessel
Nguyen, Dan T. M.
Grond, Rianne
Veenendaal, Tineke
Rabouille, Catherine
Farías, Ginny G.
author_facet van Leeuwen, Wessel
Nguyen, Dan T. M.
Grond, Rianne
Veenendaal, Tineke
Rabouille, Catherine
Farías, Ginny G.
author_sort van Leeuwen, Wessel
collection PubMed
description Phase separation of components of ER exit sites (ERES) into membraneless compartments, the Sec bodies, occurs in Drosophila cells upon exposure to specific cellular stressors, namely, salt stress and amino acid starvation, and their formation is linked to the early secretory pathway inhibition. Here, we show Sec bodies also form in secretory mammalian cells upon the same stress. These reversible and membraneless structures are positive for ERES components, including both Sec16A and Sec16B isoforms and COPII subunits. We find that Sec16A, but not Sec16B, is a driver for Sec body formation, and that the coalescence of ERES components into Sec bodies occurs by fusion. Finally, we show that the stress-induced coalescence of ERES components into Sec bodies precedes ER exit inhibition, leading to their progressive depletion from ERES that become non-functional. Stress relief causes an immediate dissolution of Sec bodies and the concomitant restoration of ER exit. We propose that the dynamic conversion between ERES and Sec body assembly, driven by Sec16A, regulates protein exit from the ER during stress and upon stress relief in mammalian cells, thus providing a conserved pro-survival mechanism in response to stress.
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spelling pubmed-101129672023-04-19 Stress-induced phase separation of ERES components into Sec bodies precedes ER exit inhibition in mammalian cells van Leeuwen, Wessel Nguyen, Dan T. M. Grond, Rianne Veenendaal, Tineke Rabouille, Catherine Farías, Ginny G. J Cell Sci Research Article Phase separation of components of ER exit sites (ERES) into membraneless compartments, the Sec bodies, occurs in Drosophila cells upon exposure to specific cellular stressors, namely, salt stress and amino acid starvation, and their formation is linked to the early secretory pathway inhibition. Here, we show Sec bodies also form in secretory mammalian cells upon the same stress. These reversible and membraneless structures are positive for ERES components, including both Sec16A and Sec16B isoforms and COPII subunits. We find that Sec16A, but not Sec16B, is a driver for Sec body formation, and that the coalescence of ERES components into Sec bodies occurs by fusion. Finally, we show that the stress-induced coalescence of ERES components into Sec bodies precedes ER exit inhibition, leading to their progressive depletion from ERES that become non-functional. Stress relief causes an immediate dissolution of Sec bodies and the concomitant restoration of ER exit. We propose that the dynamic conversion between ERES and Sec body assembly, driven by Sec16A, regulates protein exit from the ER during stress and upon stress relief in mammalian cells, thus providing a conserved pro-survival mechanism in response to stress. The Company of Biologists Ltd 2022-12-01 /pmc/articles/PMC10112967/ /pubmed/36325988 http://dx.doi.org/10.1242/jcs.260294 Text en © 2022. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
van Leeuwen, Wessel
Nguyen, Dan T. M.
Grond, Rianne
Veenendaal, Tineke
Rabouille, Catherine
Farías, Ginny G.
Stress-induced phase separation of ERES components into Sec bodies precedes ER exit inhibition in mammalian cells
title Stress-induced phase separation of ERES components into Sec bodies precedes ER exit inhibition in mammalian cells
title_full Stress-induced phase separation of ERES components into Sec bodies precedes ER exit inhibition in mammalian cells
title_fullStr Stress-induced phase separation of ERES components into Sec bodies precedes ER exit inhibition in mammalian cells
title_full_unstemmed Stress-induced phase separation of ERES components into Sec bodies precedes ER exit inhibition in mammalian cells
title_short Stress-induced phase separation of ERES components into Sec bodies precedes ER exit inhibition in mammalian cells
title_sort stress-induced phase separation of eres components into sec bodies precedes er exit inhibition in mammalian cells
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10112967/
https://www.ncbi.nlm.nih.gov/pubmed/36325988
http://dx.doi.org/10.1242/jcs.260294
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