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Intestinal intermediate filament polypeptides in C. elegans: Common and isotype-specific contributions to intestinal ultrastructure and function

Geisler, Florian; Coch, Richard A.; Richardson, Christine; Goldberg, Martin; Bevilacqua, Carlo; Prevede, Robert; Leube, Rudolf E.

Intestinal intermediate filament polypeptides in C. elegans: Common and isotype-specific contributions to intestinal ultrastructure and function Thumbnail


Authors

Florian Geisler

Richard A. Coch

Christine Richardson

Martin Goldberg

Carlo Bevilacqua

Robert Prevede

Rudolf E. Leube



Abstract

The abundance and diversity of intermediate filaments (IFs) in the C. elegans intestine indicate important contributions to intestinal function and organismal wellbeing. Fluorescent IF reporters localize below the actin-rich brush border and are highly enriched in the lumen-enveloping endotube, which is attached to the C. elegans apical junction. Mapping intestinal viscoelasticity by contact-free Brillouin microscopy reveals that the IF-rich endotube is positioned at the interface between the stiff brush border and soft cytoplasm suggesting a mechanical buffering function to deal with the frequent luminal distortions occurring during food intake and movement. In accordance, depletion of IFB-2, IFC-2 and IFD-2 leads to intestinal lumen dilation although depletion of IFC-1, IFD-1 and IFP-1 do not. Ultrastructural analyses of loss of function mutants further show that IFC-2 mutants have a rarefied endotube and IFB-2 mutants lack an endotube altogether. Remarkably, almost all IFB-2- and IFC-2-deficient animals develop to fertile adults. But developmental retardation, reduced brood size, altered survival and increased sensitivity to microbial toxin, osmotic and oxidative stress are seen in both mutants albeit to different degrees. Taken together, we propose that individual intestinal IF polypeptides contribute in different ways to endotube morphogenesis and cooperate to cope with changing environments.

Citation

Geisler, F., Coch, R. A., Richardson, C., Goldberg, M., Bevilacqua, C., Prevede, R., & Leube, R. E. (2020). Intestinal intermediate filament polypeptides in C. elegans: Common and isotype-specific contributions to intestinal ultrastructure and function. Scientific Reports, 10, Article 3142. https://doi.org/10.1038/s41598-020-59791-w

Journal Article Type Article
Acceptance Date Jan 17, 2020
Online Publication Date Feb 21, 2020
Publication Date 2020
Deposit Date Feb 21, 2020
Publicly Available Date Mar 28, 2024
Journal Scientific Reports
Publisher Nature Research
Peer Reviewed Peer Reviewed
Volume 10
Article Number 3142
DOI https://doi.org/10.1038/s41598-020-59791-w

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http://creativecommons.org/licenses/by/4.0/

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copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
© The Author(s) 2020




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