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

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

Research output: Contribution to journalArticlepeer-review

18 Scopus citations

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.
Original languageEnglish (US)
JournalSCIENTIFIC REPORTS
Volume10
Issue number1
DOIs
StatePublished - Feb 21 2020
Externally publishedYes

Bibliographical note

KAUST Repository Item: Exported on 2022-06-07
Acknowledgements: We thank Barbara Bonn, Janis Moeller and Sabine Eisner for excellent technical support. We also would like to thank Dr. Marco Felkl for providing purified recombinant IFC-2e and Dr. Olaf Bossinger for fruitful discussions. Wild-type N2 and strains RB1742, DP38 and BK36 were obtained from the Caenorhabditis Genetics Centre (University of Minnesota, Minneapolis, MN). We would like to thank Drs. Ronen Zaidel-Bar (Tel Aviv University, Israel), Matthew Buechner (University of Kansas, Lawrence, USA) and Monica Driscoll/Meghan Arnold (Rutgers, The State University of New Jersey; Arnold et al., manuscript in preparation) for generous sharing of strains, Dr. Christian Frøkjær-Jensen (King Abdullah University, Thuwal, Saudi-Arabia) for providing plasmid pCFJ104 and Dr. Raffi Aroian (UMASS Medical School, Worcester, MA) for Cry5B-expressing bacteria. Monoclonal antibody MH33 was obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by the University of Iowa, Department of Biology, Iowa City, IA. The work was supported by the German Research Council (LE566/14-1, 3) and the European Molecular Biology Laboratory.
This publication acknowledges KAUST support, but has no KAUST affiliated authors.

ASJC Scopus subject areas

  • General

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