Localization of apical epithelial determinants by the basolateral PDZ protein Scribble
Abstract
The generation of membrane domains with distinct protein constituents is a hallmark of cell polarization. In epithelia, segregation of membrane proteins into apical and basolateral compartments is critical for cell morphology, tissue physiology and cell signalling. Drosophila proteins that confer apical membrane identity have been found, but the mechanisms that restrict these determinants to the apical cell surface are unknown. Here we show that a laterally localized protein is required for the apical confinement of polarity determinants. Mutations in Drosophila scribble (scrib), which encodes a multi-PDZ (PSD-95, Discs-large and ZO-1) and leucine-rich-repeat protein, cause aberrant cell shapes and loss of the monolayer organization of embryonic epithelia. Scrib is localized to the epithelial septate junction, the analogue of the vertebrate tight junction, at the boundary of the apical and basolateral cell surfaces. Loss of scrib function results in the misdistribution of apical proteins and adherens junctions to the basolateral cell surface, but basolateral protein localization remains intact. These phenotypes can be accounted for by mislocalization of the apical determinant Crumbs. Our results show that the lateral domain of epithelia, particularly the septate junction, functions in restricting apical membrane identity and correctly placing adherens junctions.
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Loss of SCRIB expression functions as a tumor suppressor in Drosophila and mammals.
“Loss of SCRIB that results in uncontrolled proliferation and tissue growth identifying it as tumor suppressor (1).”
From Mislocalization of the Cell Polarity Protein Scribble Promotes Mammary Tumorigenesis and Is Associated with Basal Breast Cancer (2014) · cites this paper as [1]
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Jarjour, A. A., Boyd, A., Dow, L. E., Holloway, R. K., Goebbels, S., Humbert, P. O., Williams, A., & ffrench-Constant, C. (2015) · PLOS Biology · doi:10.1371/journal.pbio.1002107 · Cited by 39 · see citing works
LET-413/Erbin acts as a RAB-5 effector to promote RAB-10 activation during endocytic recycling
Liu, H., Wang, S., Hang, W., Gao, J., Zhang, W., Cheng, Z., Yang, C., He, J., Zhou, J., Chen, J., et al. (2018) · Journal of Cell Biology · doi:10.1083/jcb.201705136 · Cited by 38 · see citing works
Rui, M., Qian, J., Liu, L., Cai, Y., Lv, H., Han, J., Jia, Z., & Xie, W. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.794040 · Cited by 37 · see citing works
Kharfallah, F., Guyot, M. C., El Hassan, A. R., Allache, R., Merello, E., De Marco, P., Di Cristo, G., Capra, V., & Kibar, Z. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx122 · Cited by 28 · see citing works
The polarity protein Scribble positions DLC3 at adherens junctions to regulate Rho signaling
Hendrick, J., Franz-Wachtel, M., Moeller, Y., Schmid, S., Macek, B., & Olayioye, M. A. (2016) · Journal of Cell Science · doi:10.1242/jcs.190074 · Cited by 32 · see citing works
Localization, Not Important in All Tumor-Suppressing Properties: A Lesson Learnt from Scribble
Elsum, I. A., & Humbert, P. O. (2013) · Cells Tissues Organs · doi:10.1159/000348423 · Cited by 27 · see citing works
Pichaud, F., & Desplan, C. (2002) · Nature · doi:10.1038/416139a · Cited by 15 · see citing works
Loss of Cell Adhesion Increases Tumorigenic Potential of Polarity Deficient Scribble Mutant Cells
Waghmare, I., & Kango-Singh, M. (2016) · PLOS ONE · doi:10.1371/journal.pone.0158081 · Cited by 14 · see citing works
- Authors
- Bilder, D., & Perrimon, N.
- Affiliations
- Harvard University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Bilder, David
- Venue
- Nature
- Published
- 2000-02
- Volume
- 403
- Issue
- 6770
- Pages
- 676-680
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1521774859
- Cited by
- 716
- References
- 31
- Citations by year
- 2026: 10 · 2025: 13 · 2024: 15 · 2023: 14 · 2022: 25 · 2021: 21 · 2020: 24 · 2019: 31 · 2018: 22 · 2017: 30 · 2016: 26 · 2015: 24 · 2014: 35 · 2013: 34 · 2012: 30
- FWCI
- 16.02
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hippo pathway signaling and YAP/TAZ
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- Scribble, cell polarity, epithelial polarity, PDZ domain proteins, septate junctions, tight junctions, Crumbs, adherens junctions, Drosophila, cell shape
- MeSH terms
- Amino Acid Sequence, Animals, Cloning, Molecular, Drosophila, Epithelial Cells, Intercellular Junctions, Membrane Proteins, Molecular Sequence Data, Mutation, Tissue Distribution, Open Reading Frames, Cell Polarity, Protein Structure, Tertiary, Drosophila Proteins
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