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

dc.contributor.authorGeisler, Florian
dc.contributor.authorCoch, Richard A.
dc.contributor.authorRichardson, Christine
dc.contributor.authorGoldberg, Martin
dc.contributor.authorBevilacqua, Carlo
dc.contributor.authorPrevedel, Robert
dc.contributor.authorLeube, Rudolf E.
dc.contributor.institutionInstitute of Molecular and Cellular Anatomy, RWTH Aachen University, Aachen, Germany
dc.contributor.institutionSchool of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom
dc.contributor.institutionCell Biology and Biophysics Unit, European Molecular Biology Laboratory, Collaboration for joint PhD degree between EMBL and Heidelberg University, Faculty of Biosciences, Heidelberg, Germany
dc.contributor.institutionCell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany
dc.date.accessioned2022-06-06T11:47:33Z
dc.date.available2022-06-06T11:47:33Z
dc.date.issued2020-02-21
dc.description.abstractThe 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.
dc.description.sponsorshipWe 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.
dc.identifier.citationGeisler, F., Coch, R. A., Richardson, C., Goldberg, M., Bevilacqua, C., Prevedel, 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(1). doi:10.1038/s41598-020-59791-w
dc.identifier.doi10.1038/s41598-020-59791-w
dc.identifier.eid2-s2.0-85079813962
dc.identifier.issn2045-2322
dc.identifier.issue1
dc.identifier.journalSCIENTIFIC REPORTS
dc.identifier.pmcidPMC7035338
dc.identifier.pmid32081918
dc.identifier.urihttp://hdl.handle.net/10754/678695
dc.identifier.volume10
dc.identifier.wosutWOS:000563083300007
dc.publisherSpringer Science and Business Media LLC
dc.relation.urlhttp://www.nature.com/articles/s41598-020-59791-w
dc.titleIntestinal intermediate filament polypeptides in C. elegans: Common and isotype-specific contributions to intestinal ultrastructure and function
dc.typeArticle
display.details.left<span><h5>Type</h5>Article<br><br><h5>Authors</h5><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.author=Geisler, Florian,equals">Geisler, Florian</a><br><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.author=Coch, Richard A.,equals">Coch, Richard A.</a><br><a href="https://repository.kaust.edu.sa/search?query=orcid.id:0000-0003-2622-2261&spc.sf=dc.date.issued&spc.sd=DESC">Richardson, Christine</a> <a href="https://orcid.org/0000-0003-2622-2261" target="_blank"><img src="https://repository.kaust.edu.sa/server/api/core/bitstreams/82a625b4-ed4b-40c8-865a-d6a5225a26a4/content" width="16" height="16"/></a><br><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.author=Goldberg, Martin,equals">Goldberg, Martin</a><br><a href="https://repository.kaust.edu.sa/search?query=orcid.id:0000-0001-9084-0641&spc.sf=dc.date.issued&spc.sd=DESC">Bevilacqua, Carlo</a> <a href="https://orcid.org/0000-0001-9084-0641" target="_blank"><img src="https://repository.kaust.edu.sa/server/api/core/bitstreams/82a625b4-ed4b-40c8-865a-d6a5225a26a4/content" width="16" height="16"/></a><br><a href="https://repository.kaust.edu.sa/search?query=orcid.id:0000-0003-3366-4703&spc.sf=dc.date.issued&spc.sd=DESC">Prevedel, Robert</a> <a href="https://orcid.org/0000-0003-3366-4703" target="_blank"><img src="https://repository.kaust.edu.sa/server/api/core/bitstreams/82a625b4-ed4b-40c8-865a-d6a5225a26a4/content" width="16" height="16"/></a><br><a href="https://repository.kaust.edu.sa/search?query=orcid.id:0000-0002-5519-7379&spc.sf=dc.date.issued&spc.sd=DESC">Leube, Rudolf E.</a> <a href="https://orcid.org/0000-0002-5519-7379" target="_blank"><img src="https://repository.kaust.edu.sa/server/api/core/bitstreams/82a625b4-ed4b-40c8-865a-d6a5225a26a4/content" width="16" height="16"/></a><br><br><h5>Date</h5>2020-02-21</span>
display.details.right<span><h5>Abstract</h5>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.<br><br><h5>Citation</h5>Geisler, F., Coch, R. A., Richardson, C., Goldberg, M., Bevilacqua, C., Prevedel, 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(1). doi:10.1038/s41598-020-59791-w<br><br><h5>Acknowledgements</h5>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.<br><br><h5>Publisher</h5><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.publisher=Springer Science and Business Media LLC,equals">Springer Science and Business Media LLC</a><br><br><h5>Journal</h5><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.journal=SCIENTIFIC REPORTS,equals">SCIENTIFIC REPORTS</a><br><br><h5>DOI</h5><a href="https://doi.org/10.1038/s41598-020-59791-w">10.1038/s41598-020-59791-w</a><br><br><h5>PubMed ID</h5><a href="https://www.ncbi.nlm.nih.gov/pubmed/32081918">32081918</a><br><br><h5>PubMed Central ID</h5><a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7035338">PMC7035338</a><br><br><h5>Additional Links</h5>http://www.nature.com/articles/s41598-020-59791-w</span>
orcid.authorGeisler, Florian
orcid.authorCoch, Richard A.
orcid.authorRichardson, Christine::0000-0003-2622-2261
orcid.authorGoldberg, Martin
orcid.authorBevilacqua, Carlo::0000-0001-9084-0641
orcid.authorPrevedel, Robert::0000-0003-3366-4703
orcid.authorLeube, Rudolf E.::0000-0002-5519-7379
orcid.id0000-0002-5519-7379
orcid.id0000-0003-3366-4703
orcid.id0000-0001-9084-0641
orcid.id0000-0003-2622-2261
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