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Armadillo is required for adherens junction assembly, cell polarity, and morphogenesis during Drosophila embryogenesis.
Open accessAbstract
Morphological and biochemical analyses have identified a set of proteins which together form a structure known as the adherens junction. Elegant experiments in tissue culture support the idea that adherens junctions play a key role in cell-cell adhesion and in organizing cells into epithelia. During normal embryonic development, cells quickly organize epithelia; these epithelial cells participate in many of the key morphogenetic movements of gastrulation. This prompted the hypothesis that adherens junctions ought to be critical for normal embryonic development. Drosophila Armadillo, the homologue of vertebrate beta-catenin, is a core component of the adherens junction protein complex and has been hypothesized to be essential for adherens junction function in vivo. We have used an intermediate mutant allele of armadillo, armadilloXP33, to test these hypotheses in Drosophila embryos. Adherens junctions cannot assemble in the absence of Armadillo, leading to dramatic defects in cell-cell adhesion. The epithelial cells of the embryo lose adhesion to each other, round up, and apparently become mesenchymal. Mutant cells also lose their normal cell polarity. These disruptions in the integrity of epithelia block the appropriate morphogenetic movements of gastrulation. These results provide the first demonstration of the effect of loss of adherens junctions on Drosophila embryonic development.
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“Indeed, experiments in Drosophila have shown that mutations in junctional proteins not only affect junction formation but also disturb epithelial polarity, whereas polarity mutants have a profound effect on junction formation as well (Cox et al, 1996;Muller and Wieschaus, 1996;Tanentzapf et al, 2000).”
From E‐cadherin is essential for in vivo epidermal barrier function by regulating tight junctions (2005) · cites this paper as Cox et al, 1996
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“…at Chapel Hill, Chapel Hill, NC 27599-3280, USA 2Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-3280, USA 3Department of Biological Sciences, Carnegie Mellon University, Pittsburgh PA 15213, USA 4Curriculum in Genetics and Molecular…”
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BackgroundMultivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis
Perez-Vale, K. Z., Yow, K. D., Johnson, R. I., Byrnes, A. E., Finegan, T. M., Slep, K. C., & Peifer, M. A. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202104087 · Cited by 30
“Ecad, the catenins, and Baz are essential for AJ formation and stability; without these, embryos fall apart at gastrulation (Cox et al., 1996; Müller and Wieschaus, 1996; Sarpal et al., 2012).”
BackgroundSelf-citationChigita, S., Sugiura, T., Abe, M., Kobayashi, Y., Shimoda, M., Onoda, M., & Shirasuna, K. (2012) · International Journal of Oncology · doi:10.3892/ijo.2012.1671 · Cited by 25
“By sequestering β-catenin at the membrane, cadherins modulate the signalling properties of cytosolic β-catenin, creating a finely tuned balance between Wnt signalling and cell-cell adhesion (22-24).”
BackgroundZhang, W., Yan, S., Liu, M., Zhang, G., Yang, S., He, S., Bai, J.-F., Quan, L., Zhu, H.-X., Dong, Y., et al. (2010) · Cancer Letters · doi:10.1016/j.canlet.2010.04.001 · Cited by 25
Cleavage of Armadillo/beta-catenin by the caspase DrICE in Drosophila apoptotic epithelial cells
Kessler, T., & Müller, H. J. (2009) · BMC Developmental Biology · doi:10.1186/1471-213x-9-15 · Cited by 25
“DE-cadherin and Arm are essential to mediate cell adhesion during the establishment of cell junctions in early development [18-22].”
BackgroundThe cytoskeletal motor proteins Dynein and MyoV direct apical transport of Crumbs
Aguilar‐Aragon, M., Fletcher, G., & Thompson, B. J. (2019) · Developmental Biology · doi:10.1016/j.ydbio.2019.12.009 · Cited by 25
“The actin cytoskeleton is organized by the Rho GTPase and adherens junctions (Cox et al., 1996; Fox et al., 2005; Homem and Peifer, 2008; Muller and Wieschaus, 1996; Peifer et al., 1993) which are ultimately positioned between the core apical and basolateral polarity determinants.”
BackgroundBenchabane, H., Hughes, E. G., Takacs, C. M., Baird, J. R., & Ahmed, Y. F. (2008) · Development · doi:10.1242/dev.013805 · Cited by 21
“Arm functions not only as a transcriptional activator, but also as an essential component in the formation and maintenance of cadherin-based adherens junctions (Cox et al., 1996; Muller and Wieschaus, 1996).”
BackgroundDonmez, H., Demirezen, Ş., & Beksaç, M. (2016) · Tissue & Cell · doi:10.1016/j.tice.2016.04.001 · Cited by 22
CYFIP dependent Actin Remodeling controls specific aspects of Drosophila eye morphogenesis
Galy, A., Schenck, A., Şahin, H. B., Qurashi, A., Sahel, J., Diebold, C., & Giangrande, A. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.08.009 · Cited by 17
Pon, Y., & Wong, A. (2006) · Molecular Endocrinology · doi:10.1210/me.2006-0125 · Cited by 22
Knust, E., & Leptin, M. (1996) · Bioessays · doi:10.1002/bies.950180802 · Cited by 22
Dcas Supports Cell Polarization and Cell-Cell Adhesion Complexes in Development
Tikhmyanova, N., Tulin, A. V., Roegiers, F., & Golemis, E. A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012369 · Cited by 20
“Like arm2, these alleles express a truncated form of Armadillo [58,59], due to either amino acid replacements resulting in a stop codon (arm2 and arm3) or p-element insertion (arm8) within the arm repeats. arm3 is embryonic lethal typically at stage 16, and is characterized by segment polarity and DC defects, while ar…”
BackgroundCadherins and catenins, Wnts and SOXs: Embryonic patterning in Xenopus
Amand, A. L. S., & Klymkowsky, M. W. (2001) · International review of cytology · doi:10.1016/s0074-7696(01)03010-8 · Cited by 20
Weng, J., Yu, L., Chen, Z.-F., Su, H.-Y., Yu, S.-X., Zhang, Y., Lei, X., Chen, L.-X., Cui, Y., Huang, Q.-B., et al. (2019) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2018.12.012 · Cited by 20
Hilbig, D., Dietrich, N., Wandel, E., Gonsior, S., Sittig, D., Hamann, J., & Aust, G. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00182 · Cited by 20
“In adherens junctions it links the transmembrane receptor E-cadherin (Ecad), which mediates strong homotypic adhesion between neighboring cells, via connecting proteins to the actin cytoskeleton (5).”
BackgroundDifferential Regulation of Cadherins and Catenins During Axonal Reorganization in the Adult Rat CNS
Fasen, K., Beck, H., Elger, C., & Lie, A. (2002) · Journal of Neuropathology and Experimental Neurology · doi:10.1093/jnen/61.10.903 · Cited by 20
Kumar, J. P., Wilkie, G., Tekotte, H., Moses, K., & Davis, I. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0468 · Cited by 20
“Arm encodes a b-catenin that is localized to adherens junctions which maintain adhesion between cells in neuroepithelial sheets (Cox et al., 1996), but also functions separately in transducing the wingless”
BackgroundKo, C. S., Kalakuntla, P., & Martin, A. C. (2019) · bioRxiv · doi:10.1101/862821 · Cited by 19
“causing constitutively round cells that do not invaginate (Cox et al., 1996; Dawes-Hoang 163 et al., 2005).”
BackgroundBao, R., Fischer, T., Bolognesi, R., Brown, S. J., & Friedrich, M. (2012) · Molecular biology and evolution · doi:10.1093/molbev/msr219 · Cited by 19
Lilien, J., Balsamo, J., Hoffman, S., & Eisenberg, C. (1997) · Current Topics in Developmental Biology · doi:10.1016/s0070-2153(08)60259-8 · Cited by 19
The α-Catenin mechanosensing M region is required for cell adhesion during tissue morphogenesis
Sheppard, L., Green, D. G., Lerchbaumer, G., Rothenberg, K. E., Fernández‐González, R., & Tepaß, U. (2022) · The Journal of Cell Biology · doi:10.1083/jcb.202108091 · Cited by 30
“During cellularization, Cno recruitment is unaffected by the loss of Arm, and instead requires the small GTPase Rap1 (Sawyer et al., 2009).”
BackgroundInfluential
Metadata
- Authors
- Cox, R. T., Kirkpatrick, C., & Peifer, M.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Venue
- The Journal of cell biology
- Publisher
- Rockefeller University Press
- Published
- 1996-07-01
- Volume
- 134
- Issue
- 1
- Pages
- 133-148
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC2120919
- OpenAlex
- W2030945799
- Cited by
- 300
- References
- 58
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 4 · 2023: 2 · 2022: 7 · 2021: 6 · 2020: 8 · 2019: 9 · 2018: 6 · 2017: 7 · 2016: 4 · 2015: 3 · 2014: 3 · 2013: 10 · 2012: 7
- FWCI
- 7.46
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- National Institute of General Medical Sciences (T32GM007092, 5T32 GM-07092)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Keywords
- armadillos, β-catenin, cell-cell adhesion, epithelial morphogenesis, cell polarity, gastrulation, Drosophila embryogenesis, mesenchymal transition, epithelial barrier integrity
- MeSH terms
- Actins, Animals, Cell Adhesion, Cytoskeletal Proteins, DNA Mutational Analysis, Drosophila melanogaster, Epithelial Cells, Gastrula, Intercellular Junctions, Membrane Proteins, Actin Cytoskeleton, Microscopy, Electron, Scanning, Morphogenesis, Oogenesis, Proteins, Transcription Factors, Trans-Activators, Cell Adhesion Molecules, Cadherins, Cell Polarity, Drosophila Proteins, alpha Catenin, Armadillo Domain Proteins
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