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Deciphering the roles of cell shape and Fat and Dachsous planar polarity in arranging the Drosophila apical microtubule network through quantitative image analysis

Deciphering the roles of cell shape and Fat and Dachsous planar polarity in arranging the Drosophila apical microtubule network through quantitative image analysis
Deciphering the roles of cell shape and Fat and Dachsous planar polarity in arranging the Drosophila apical microtubule network through quantitative image analysis

In epithelial cells, planar polarization of subapical microtubule networks is thought to be important for both breaking cellular symmetry and maintaining the resulting cellular polarity. Studies in the Drosophila pupal wing and other tissues have suggested two alternative mechanisms for specifying network polarity. On one hand, mechanical strain and/or cell shape have been implicated as key determinants; on the other hand, the Fat-Dachsous planar polarity pathway has been suggested to be the primary polarizing cue. Using quantitative image analysis in the pupal wing, we reassess these models. We found that cell shape was a strong predictor of microtubule organization in the developing wing epithelium. Conversely, Fat-Dachsous polarity cues do not play any direct role in the organization of the subapical microtubule network, despite being able to weakly recruit the microtubule minus-end capping protein Patronin to cell boundaries. We conclude that any effect of Fat-Dachsous on microtubule polarity is likely to be indirect, via their known ability to regulate cell shape.

1059-1524
Moreno, Miguel Ramírez
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Hunton, Robert
d3ddabae-3ce5-473d-bed4-e1af234c7bec
Strutt, David
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Bulgakova, Natalia A
f01bab85-42b3-403b-926c-3b56b17de5dd
Moreno, Miguel Ramírez
22b64166-df15-46e0-b5a5-2e99ea81d0da
Hunton, Robert
d3ddabae-3ce5-473d-bed4-e1af234c7bec
Strutt, David
d949abec-6b0e-43e3-b684-c9af70cd5e5a
Bulgakova, Natalia A
f01bab85-42b3-403b-926c-3b56b17de5dd

Moreno, Miguel Ramírez, Hunton, Robert, Strutt, David and Bulgakova, Natalia A (2023) Deciphering the roles of cell shape and Fat and Dachsous planar polarity in arranging the Drosophila apical microtubule network through quantitative image analysis. Molecular Biology of the Cell, 34 (6), [ar55]. (doi:10.1091/mbc.E22-09-0442).

Record type: Article

Abstract

In epithelial cells, planar polarization of subapical microtubule networks is thought to be important for both breaking cellular symmetry and maintaining the resulting cellular polarity. Studies in the Drosophila pupal wing and other tissues have suggested two alternative mechanisms for specifying network polarity. On one hand, mechanical strain and/or cell shape have been implicated as key determinants; on the other hand, the Fat-Dachsous planar polarity pathway has been suggested to be the primary polarizing cue. Using quantitative image analysis in the pupal wing, we reassess these models. We found that cell shape was a strong predictor of microtubule organization in the developing wing epithelium. Conversely, Fat-Dachsous polarity cues do not play any direct role in the organization of the subapical microtubule network, despite being able to weakly recruit the microtubule minus-end capping protein Patronin to cell boundaries. We conclude that any effect of Fat-Dachsous on microtubule polarity is likely to be indirect, via their known ability to regulate cell shape.

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Accepted/In Press date: 26 January 2023
e-pub ahead of print date: 5 May 2023
Published date: 15 May 2023
Additional Information: Funding Information: We acknowledge the Bloomington Drosophila Stock Center for fly stocks and the Developmental Studies Hybridoma Bank for antibodies. We thank the technical staff of the Wolfson Light Microscopy Facility and the Drosophila Facility at the University of Sheffield. All imaging work was performed at the Wolfson Light Microscopy Facility, using the FV1000 Olympus and Airyscan Zeiss microscopes. This work was supported by a grant from the Biotechnology and Biological Sciences Research Council, UK Research and Innovation (BB/SOO7342/1) to D.S. and N.A.B. and a Wellcome Trust Senior Fellowship (210630/Z/18/Z) to D.S. Publisher Copyright: © 2023 Ramirez-Moreno et al.

Identifiers

Local EPrints ID: 477552
URI: http://eprints.soton.ac.uk/id/eprint/477552
ISSN: 1059-1524
PURE UUID: d27562be-018d-49a0-92fe-1bddcb8835d9
ORCID for Miguel Ramírez Moreno: ORCID iD orcid.org/0000-0003-1559-8976

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Date deposited: 08 Jun 2023 16:41
Last modified: 17 Mar 2024 04:15

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Contributors

Author: Miguel Ramírez Moreno ORCID iD
Author: Robert Hunton
Author: David Strutt
Author: Natalia A Bulgakova

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