Zonula adherens formation in Caenorhabditis elegans requires dlg-1, the homologue of the Drosophila gene discs large
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The correct assembly of junction components, such as E-cadherin and beta-catenin, into the zonula adherens is fundamental for the function of epithelia, both in flies and in vertebrates. In C. elegans, however, the cadherin-catenin system is not essential for general adhesion, raising the question as to the genetic basis controlling junction morphogenesis in nematodes. Here we show that dlg-1, the C. elegans homologue of the Drosophila tumour-suppressor gene discs-large, plays a crucial role in epithelial development. DLG-1 is restricted to adherens junctions of all embryonic epithelia, which contrasts with the localisation of the Drosophila and vertebrate homologues in septate and tight junctions, respectively. Proper localisation of DLG-1 requires the basolateral LET-413 protein, but is independent of the cadherin-catenin system. Embryos in which dlg-1 activity was eliminated by RNA-mediated interference fail to form a continuous belt of junction-associated antigens and arrest development. Loss of dlg-1 activity differentially affects localisation of proteins normally enriched apically to the zonula adherens. While the distribution of an atypical protein kinase C (PKC-3) and other cytoplasmic proteins (PAR-3, PAR-6) is not affected in dlg-1 (RNAi) embryos, the transmembrane protein encoded by crb-1, the C. elegans homologue of Drosophila crumbs, is no longer concentrated in this domain. In contrast to Drosophila, however, crb-1 and a second crb-like gene are not essential for epithelial development in C. elegans. Together the data indicate that several aspects of the spatial organisation of epithelial cells and its genetic control differ between flies, worms, and vertebrates, while others are conserved. The molecular nature of DLG-1 makes it a likely candidate to participate in the organisation of a protein scaffold that controls the assembly of junction components into the zonula adherens.
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As in Drosophila, C. elegans Dlg-1 mutants share many of the same defects, and LET-413 is required for Dlg-1 localization.
“As in Drosophila, C. elegans Dlg-1 mutants share many of the same defects, and LET-413 is required for Dlg-1 localization (Bossinger et al., 2001; Köppen et al., 2001; McMahon et al., 2001; Mathew et al., 2002; Lockwood et al., 2008; Caria et al., 2018).”
From Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation (2019) · cites this paper as Bossinger et al., 2001
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“elegans Dlg-1 mutants share many of the same defects, and LET-413 is required for Dlg-1 localization (Bossinger et al., 2001; Köppen et al., 2001; McMahon et al., 2001; Mathew et al., 2002; Lockwood et al., 2008; Caria et al., 2018).”
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- Authors
- Bossinger, O., Klebes, A., Segbert, C., Theres, C., & Knust, E.
- Affiliations
- Heinrich Heine University Düsseldorf (DE)
- Corresponding author
- Bossinger, Olaf
- ORCID
- Knust, Elisabeth
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2001-02
- Volume
- 230
- Issue
- 1
- Pages
- 29-42
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W2139168014
- Cited by
- 161
- References
- 67
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 1 · 2023: 3 · 2022: 4 · 2021: 6 · 2020: 3 · 2019: 6 · 2018: 6 · 2017: 4 · 2016: 4 · 2015: 6 · 2014: 2 · 2013: 5 · 2012: 9
- FWCI
- 5.12
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- National Institutes of Health
- National Center for Research Resources
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Keywords
- adherens junctions, DLG1, Discs large, Caenorhabditis elegans, epithelial development, Crumbs, protein kinase C, Par3, Par6, protein scaffolds
- MeSH terms
- Amino Acid Sequence, Animals, Digestive System, Drosophila, Membrane Proteins, Molecular Sequence Data, Mutation, Species Specificity, Helminth Proteins, Caenorhabditis elegans, Genes, Helminth, Genes, Insect, Sequence Homology, Amino Acid, Gene Expression Regulation, Developmental, Insect Proteins, Tumor Suppressor Proteins, Drosophila Proteins
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