Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades

Intermediate filament (IF) proteins, including nuclear lamins and cytoplasmic IF proteins, are essential cytoskeletal components of bilaterian cells. Despite their important role in protecting tissues against mechanical force, no cytoplasmic IF proteins have been convincingly identified in arthropod...

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Published in:eLife
Main Authors: Hering, Lars, Bouameur, Jamal-Eddine, Reichelt, Julian, Magin, Thomas M, Mayer, Georg
Other Authors: Deutsche Forschungsgemeinschaft
Format: Article in Journal/Newspaper
Language:English
Published: eLife Sciences Publications, Ltd 2016
Subjects:
Online Access:http://dx.doi.org/10.7554/elife.11117
https://cdn.elifesciences.org/articles/11117/elife-11117-v3.pdf
https://cdn.elifesciences.org/articles/11117/elife-11117-v3.xml
https://elifesciences.org/articles/11117
id crelifesciences:10.7554/elife.11117
record_format openpolar
spelling crelifesciences:10.7554/elife.11117 2024-09-15T18:41:38+00:00 Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades Hering, Lars Bouameur, Jamal-Eddine Reichelt, Julian Magin, Thomas M Mayer, Georg Deutsche Forschungsgemeinschaft Deutsche Forschungsgemeinschaft Deutsche Forschungsgemeinschaft 2016 http://dx.doi.org/10.7554/elife.11117 https://cdn.elifesciences.org/articles/11117/elife-11117-v3.pdf https://cdn.elifesciences.org/articles/11117/elife-11117-v3.xml https://elifesciences.org/articles/11117 en eng eLife Sciences Publications, Ltd http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ eLife volume 5 ISSN 2050-084X journal-article 2016 crelifesciences https://doi.org/10.7554/elife.11117 2024-08-13T04:19:43Z Intermediate filament (IF) proteins, including nuclear lamins and cytoplasmic IF proteins, are essential cytoskeletal components of bilaterian cells. Despite their important role in protecting tissues against mechanical force, no cytoplasmic IF proteins have been convincingly identified in arthropods. Here we show that the ancestral cytoplasmic IF protein gene was lost in the entire panarthropod (onychophoran + tardigrade + arthropod) rather than arthropod lineage and that nuclear, lamin-derived proteins instead acquired new cytoplasmic roles at least three times independently in collembolans, copepods, and tardigrades. Transcriptomic and genomic data revealed three IF protein genes in the tardigrade Hypsibius dujardini, one of which (cytotardin) occurs exclusively in the cytoplasm of epidermal and foregut epithelia, where it forms belt-like filaments around each epithelial cell. These results suggest that a lamin derivative has been co-opted to enhance tissue stability in tardigrades, a function otherwise served by cytoplasmic IF proteins in all other bilaterians. Article in Journal/Newspaper Copepods Tardigrade eLife eLife 5
institution Open Polar
collection eLife
op_collection_id crelifesciences
language English
description Intermediate filament (IF) proteins, including nuclear lamins and cytoplasmic IF proteins, are essential cytoskeletal components of bilaterian cells. Despite their important role in protecting tissues against mechanical force, no cytoplasmic IF proteins have been convincingly identified in arthropods. Here we show that the ancestral cytoplasmic IF protein gene was lost in the entire panarthropod (onychophoran + tardigrade + arthropod) rather than arthropod lineage and that nuclear, lamin-derived proteins instead acquired new cytoplasmic roles at least three times independently in collembolans, copepods, and tardigrades. Transcriptomic and genomic data revealed three IF protein genes in the tardigrade Hypsibius dujardini, one of which (cytotardin) occurs exclusively in the cytoplasm of epidermal and foregut epithelia, where it forms belt-like filaments around each epithelial cell. These results suggest that a lamin derivative has been co-opted to enhance tissue stability in tardigrades, a function otherwise served by cytoplasmic IF proteins in all other bilaterians.
author2 Deutsche Forschungsgemeinschaft
Deutsche Forschungsgemeinschaft
Deutsche Forschungsgemeinschaft
format Article in Journal/Newspaper
author Hering, Lars
Bouameur, Jamal-Eddine
Reichelt, Julian
Magin, Thomas M
Mayer, Georg
spellingShingle Hering, Lars
Bouameur, Jamal-Eddine
Reichelt, Julian
Magin, Thomas M
Mayer, Georg
Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades
author_facet Hering, Lars
Bouameur, Jamal-Eddine
Reichelt, Julian
Magin, Thomas M
Mayer, Georg
author_sort Hering, Lars
title Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades
title_short Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades
title_full Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades
title_fullStr Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades
title_full_unstemmed Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades
title_sort novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades
publisher eLife Sciences Publications, Ltd
publishDate 2016
url http://dx.doi.org/10.7554/elife.11117
https://cdn.elifesciences.org/articles/11117/elife-11117-v3.pdf
https://cdn.elifesciences.org/articles/11117/elife-11117-v3.xml
https://elifesciences.org/articles/11117
genre Copepods
Tardigrade
genre_facet Copepods
Tardigrade
op_source eLife
volume 5
ISSN 2050-084X
op_rights http://creativecommons.org/licenses/by/4.0/
http://creativecommons.org/licenses/by/4.0/
http://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.7554/elife.11117
container_title eLife
container_volume 5
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