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

Scientific Reports, vol. 10, pp. 3142

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.

Authors 5

1. Florian Geisler Aachen Institute of Molecular and Cellular Anatomy (MOCA)

   RWTH Aachen University

   Affiliation as printed

   Institute of Molecular and Cellular Anatomy, RWTH Aachen University, Aachen, Germany

2. Richard A. Coch Aachen Institute of Molecular and Cellular Anatomy (MOCA)

   RWTH Aachen University

   Affiliation as printed

   Institute of Molecular and Cellular Anatomy, RWTH Aachen University, Aachen, Germany

3. Carlo Bevilacqua

   Heidelberg University · European Molecular Biology Laboratory · European Molecular Biology Laboratory

   Affiliation as printed

   Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Collaboration for joint PhD degree between EMBL and Heidelberg University, Faculty of Biosciences, Heidelberg, Germany

4. Robert Prevedel

   European Molecular Biology Laboratory

   Affiliation as printed

   Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany

5. Rudolf E. Leube corresponding Aachen Institute of Molecular and Cellular Anatomy (MOCA)

   RWTH Aachen University

   Affiliation as printed

   Institute of Molecular and Cellular Anatomy, RWTH Aachen University, Aachen, Germany. rleube@ukaachen.de

   Institute of Molecular and Cellular Anatomy, RWTH Aachen University, Aachen, Germany