Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia

Mathias Köppen; Jeffrey S. Simske; Paul A. Sims; Bonnie L. Firestein; David H. Hall; Anthony D. Radice; Christopher Rongo; Jeffrey D. Hardin

doi:10.1038/ncb1101-983

Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia

Mathias Köppen
, Jeffrey S. Simske
, Paul A. Sims
, Bonnie L. Firestein
, David H. Hall
, Anthony D. Radice
, Christopher Rongo
, Jeffrey D. Hardin

Pharmacology and Nutritional Sciences

Research output: Contribution to journal › Article › peer-review

263 Citations (SciVal)

Abstract

The function of epithelial cell sheets depends on the integrity of specialized cell-cell junctions that connect neighbouring cells. We have characterized the novel coiled-coil protein AJM-1, which localizes to an apical junctional domain of Caenorhabditis elegans epithelia basal to the HMR-HMP (cadherin-catenin) complex. In the absence of AJM-1, the integrity of this domain is compromised. Proper AJM-1 localization requires LET-413 and DLG-1, homologues of the Drosophila tumour suppressors Scribble and Discs large, respectively. DLG-1 physically interacts with AJM-1 and is required for its normal apical distribution, and LET-413 mediates the rapid accumulation of both DLG-1 and AJM-1 in the apical domain. In the absence of both dlg-1 and let-413 function AJM-1 is almost completely lost from apical junctions in embryos, whereas HMP-1 (α-catenin) localization is only mildly affected. We conclude that LET-413 and DLG-1 cooperatively control AJM-1 localization and that AJM-1 controls the integrity of a distinct apical junctional domain in C. elegans.

Original language	English
Pages (from-to)	983-991
Number of pages	9
Journal	Nature Cell Biology
Volume	3
Issue number	11
DOIs	https://doi.org/10.1038/ncb1101-983
State	Published - 2001

Funding

ACKNOWLEDGEMENTS We thank members of the Hardin laboratory for helpful discussion and critical reading of the manuscript, J. Pawley for help with confocal microscopy, and the Wickens laboratory, in particular D. Bernstein, for technical assistance with two-hybrid experiments and the GST pull-down assay. This work was supported by NSF grant DBI97-24515 and NIH grant GM58038 awarded to J.D.H. The Bio-Rad MRC 1024 confocal microscope is supported by NSF grant 9724515. Correspondence and requests for materials should be addressed to J.D.H. The GenBank accession numbers for the C25A11.4 (ajm-1) sequence and the dlg-1 sequence are U39650 and AJ295228, respectively.

Funders	Funder number
National Institutes of Health
National Science Foundation	DBI97-24515, 9724515
National Institute of General Medical Sciences	R01GM058038
National Center for Research Resources	R24RR012596

ASJC Scopus subject areas

Cell Biology

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10.1038/ncb1101-983

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title = "Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia",

abstract = "The function of epithelial cell sheets depends on the integrity of specialized cell-cell junctions that connect neighbouring cells. We have characterized the novel coiled-coil protein AJM-1, which localizes to an apical junctional domain of Caenorhabditis elegans epithelia basal to the HMR-HMP (cadherin-catenin) complex. In the absence of AJM-1, the integrity of this domain is compromised. Proper AJM-1 localization requires LET-413 and DLG-1, homologues of the Drosophila tumour suppressors Scribble and Discs large, respectively. DLG-1 physically interacts with AJM-1 and is required for its normal apical distribution, and LET-413 mediates the rapid accumulation of both DLG-1 and AJM-1 in the apical domain. In the absence of both dlg-1 and let-413 function AJM-1 is almost completely lost from apical junctions in embryos, whereas HMP-1 (α-catenin) localization is only mildly affected. We conclude that LET-413 and DLG-1 cooperatively control AJM-1 localization and that AJM-1 controls the integrity of a distinct apical junctional domain in C. elegans.",

author = "Mathias K{\"o}ppen and Simske, \{Jeffrey S.\} and Sims, \{Paul A.\} and Firestein, \{Bonnie L.\} and Hall, \{David H.\} and Radice, \{Anthony D.\} and Christopher Rongo and Hardin, \{Jeffrey D.\}",

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AU - Köppen, Mathias

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AU - Firestein, Bonnie L.

AU - Hall, David H.

AU - Radice, Anthony D.

AU - Rongo, Christopher

AU - Hardin, Jeffrey D.

PY - 2001

Y1 - 2001

N2 - The function of epithelial cell sheets depends on the integrity of specialized cell-cell junctions that connect neighbouring cells. We have characterized the novel coiled-coil protein AJM-1, which localizes to an apical junctional domain of Caenorhabditis elegans epithelia basal to the HMR-HMP (cadherin-catenin) complex. In the absence of AJM-1, the integrity of this domain is compromised. Proper AJM-1 localization requires LET-413 and DLG-1, homologues of the Drosophila tumour suppressors Scribble and Discs large, respectively. DLG-1 physically interacts with AJM-1 and is required for its normal apical distribution, and LET-413 mediates the rapid accumulation of both DLG-1 and AJM-1 in the apical domain. In the absence of both dlg-1 and let-413 function AJM-1 is almost completely lost from apical junctions in embryos, whereas HMP-1 (α-catenin) localization is only mildly affected. We conclude that LET-413 and DLG-1 cooperatively control AJM-1 localization and that AJM-1 controls the integrity of a distinct apical junctional domain in C. elegans.

AB - The function of epithelial cell sheets depends on the integrity of specialized cell-cell junctions that connect neighbouring cells. We have characterized the novel coiled-coil protein AJM-1, which localizes to an apical junctional domain of Caenorhabditis elegans epithelia basal to the HMR-HMP (cadherin-catenin) complex. In the absence of AJM-1, the integrity of this domain is compromised. Proper AJM-1 localization requires LET-413 and DLG-1, homologues of the Drosophila tumour suppressors Scribble and Discs large, respectively. DLG-1 physically interacts with AJM-1 and is required for its normal apical distribution, and LET-413 mediates the rapid accumulation of both DLG-1 and AJM-1 in the apical domain. In the absence of both dlg-1 and let-413 function AJM-1 is almost completely lost from apical junctions in embryos, whereas HMP-1 (α-catenin) localization is only mildly affected. We conclude that LET-413 and DLG-1 cooperatively control AJM-1 localization and that AJM-1 controls the integrity of a distinct apical junctional domain in C. elegans.

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Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia

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