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Role for a Cindr–Arf6 axis in patterning emerging epithelia

Patterning of the Drosophila pupal eye is characterized by precise cell movements. In this paper, we demonstrate that these movements require an Arf regulatory cycle that connects surface receptors to actin-based movement. dArf6 activity—regulated by the Arf GTPase–activating proteins (ArfGAPs) dAsa...

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Autores principales: Johnson, Ruth I., Sedgwick, Alanna, D'Souza-Schorey, Crislyn, Cagan, Ross L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3226471/
https://www.ncbi.nlm.nih.gov/pubmed/21976699
http://dx.doi.org/10.1091/mbc.E11-04-0305
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author Johnson, Ruth I.
Sedgwick, Alanna
D'Souza-Schorey, Crislyn
Cagan, Ross L.
author_facet Johnson, Ruth I.
Sedgwick, Alanna
D'Souza-Schorey, Crislyn
Cagan, Ross L.
author_sort Johnson, Ruth I.
collection PubMed
description Patterning of the Drosophila pupal eye is characterized by precise cell movements. In this paper, we demonstrate that these movements require an Arf regulatory cycle that connects surface receptors to actin-based movement. dArf6 activity—regulated by the Arf GTPase–activating proteins (ArfGAPs) dAsap and dArfGAP3 and the Arf GTP exchange factors Schizo and dPsd—promoted large cellular extensions; time-lapse microscopy indicated that these extensions presage cell rearrangements into correct epithelial niches. During this process, the Drosophila eye also requires interactions between surface Neph1/nephrin adhesion receptors Roughest and Hibris, which bind the adaptor protein Cindr (CD2AP). We provide evidence that Cindr forms a physical complex with dArfGAP3 and dAsap. Our data suggest this interaction sequesters ArfGAP function to liberate active dArf6 elsewhere in the cell. We propose that a Neph1/nephrin–Cindr/ArfGAP complex accumulates to limit local Arf6 activity and stabilize adherens junctions. Our model therefore links surface adhesion via an Arf6 regulatory cascade to dynamic modeling of the cytoskeleton, accounting for precise cell movements that organize the functional retinal field. Further, we demonstrate a similar relationship between the mammalian Cindr orthologue CD2AP and Arf6 activity in cell motility assays. We propose that this Cindr/CD2AP-mediated regulation of Arf6 is a widely used mechanism in emerging epithelia.
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spelling pubmed-32264712012-02-16 Role for a Cindr–Arf6 axis in patterning emerging epithelia Johnson, Ruth I. Sedgwick, Alanna D'Souza-Schorey, Crislyn Cagan, Ross L. Mol Biol Cell Articles Patterning of the Drosophila pupal eye is characterized by precise cell movements. In this paper, we demonstrate that these movements require an Arf regulatory cycle that connects surface receptors to actin-based movement. dArf6 activity—regulated by the Arf GTPase–activating proteins (ArfGAPs) dAsap and dArfGAP3 and the Arf GTP exchange factors Schizo and dPsd—promoted large cellular extensions; time-lapse microscopy indicated that these extensions presage cell rearrangements into correct epithelial niches. During this process, the Drosophila eye also requires interactions between surface Neph1/nephrin adhesion receptors Roughest and Hibris, which bind the adaptor protein Cindr (CD2AP). We provide evidence that Cindr forms a physical complex with dArfGAP3 and dAsap. Our data suggest this interaction sequesters ArfGAP function to liberate active dArf6 elsewhere in the cell. We propose that a Neph1/nephrin–Cindr/ArfGAP complex accumulates to limit local Arf6 activity and stabilize adherens junctions. Our model therefore links surface adhesion via an Arf6 regulatory cascade to dynamic modeling of the cytoskeleton, accounting for precise cell movements that organize the functional retinal field. Further, we demonstrate a similar relationship between the mammalian Cindr orthologue CD2AP and Arf6 activity in cell motility assays. We propose that this Cindr/CD2AP-mediated regulation of Arf6 is a widely used mechanism in emerging epithelia. The American Society for Cell Biology 2011-12-01 /pmc/articles/PMC3226471/ /pubmed/21976699 http://dx.doi.org/10.1091/mbc.E11-04-0305 Text en © 2011 Johnson et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society of Cell Biology.
spellingShingle Articles
Johnson, Ruth I.
Sedgwick, Alanna
D'Souza-Schorey, Crislyn
Cagan, Ross L.
Role for a Cindr–Arf6 axis in patterning emerging epithelia
title Role for a Cindr–Arf6 axis in patterning emerging epithelia
title_full Role for a Cindr–Arf6 axis in patterning emerging epithelia
title_fullStr Role for a Cindr–Arf6 axis in patterning emerging epithelia
title_full_unstemmed Role for a Cindr–Arf6 axis in patterning emerging epithelia
title_short Role for a Cindr–Arf6 axis in patterning emerging epithelia
title_sort role for a cindr–arf6 axis in patterning emerging epithelia
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3226471/
https://www.ncbi.nlm.nih.gov/pubmed/21976699
http://dx.doi.org/10.1091/mbc.E11-04-0305
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