A maternal-effect toxin affects epithelial differentiation and tissue mechanics in caenorhabditis elegans

  • Selfish genetic elements that act as post-segregation distorters cause lethality in non-carrier individuals after fertilization. Two post-segregation distorters have been previously identified in Caenorhabditis elegans, the peel-1/zeel-1 and the sup-35/pha-1 elements. These elements seem to act as modification-rescue systems, also called toxin/antidote pairs. Here we show that the maternal-effect toxin/zygotic antidote pair sup-35/pha-1 is required for proper expression of apical junction (AJ) components in epithelia and that sup-35 toxicity increases when pathways that establish and maintain basal epithelial characteristics, die-1, elt-1, lin-26, and vab-10, are compromised. We demonstrate that pha-1(e2123) embryos, which lack the antidote, are defective in epidermal morphogenesis and frequently fail to elongate. Moreover, seam cells are frequently misshaped and mispositioned and cell bond tension is reduced in pha-1(e2123) embryos, suggesting altered tissue material properties in the epidermis. Several aspects of this phenotype can also be induced in wild-type embryos by exerting mechanical stress through uniaxial loading. Seam cell shape, tissue mechanics, and elongation can be restored in pha-1(e2123) embryos if expression of the AJ molecule DLG-1/Discs large is reduced. Thus, our experiments suggest that maternal-effect toxicity disrupts proper development of the epidermis which involves distinct transcriptional regulators and AJ components.

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Author:Christina Lehmann, Christian PohlORCiDGND
URN:urn:nbn:de:hebis:30:3-633855
DOI:https://doi.org/10.3389/fcell.2021.743496
ISSN:2296-634X
Parent Title (English):Frontiers in cell and developmental biology
Publisher:Frontiers Media
Place of publication:Lausanne
Document Type:Article
Language:English
Date of Publication (online):2021/10/14
Date of first Publication:2021/10/14
Publishing Institution:Universitätsbibliothek Johann Christian Senckenberg
Release Date:2022/01/18
Tag:C. elegans; Discs large; apical junction; epidermis; morphogenesis; selfish genetic element; tissue mechanics
Volume:9
Issue:art. 743496
Page Number:15
First Page:1
Last Page:15
Note:
We acknowledged funding by Deutsche Forschungsgemeinschaft FOR 1756 (Functional dynamics of cell contacts in cellular assemblies and migratory cells) and EXC 115 (Cluster of Excellence Macromolecular Complexes in Action). Most of the strains used in this study were provided by the Caenorhabditis Genetics Center, which is funded by the National Institutes of Health Office of Research Infrastructure Programs (P40 OD010440).
HeBIS-PPN:491316496
Institutes:Fachübergreifende Einrichtungen
Medizin / Medizin
Dewey Decimal Classification:5 Naturwissenschaften und Mathematik / 57 Biowissenschaften; Biologie / 570 Biowissenschaften; Biologie
6 Technik, Medizin, angewandte Wissenschaften / 61 Medizin und Gesundheit / 610 Medizin und Gesundheit
Sammlungen:Universitätspublikationen
Open-Access-Publikationsfonds:Medizin
Licence (German):License LogoCreative Commons - Namensnennung 4.0