A role for Myo-II zipper and spaghetti squash in Gliotactin-dependent Drosophila melanogaster wing hair planar cell polarity.

Planar cell polarity, polarization in the plane of an epithelium, is critical for tissue development. The Drosophila melanogaster wing epithelium is an important model system for planar cell polarity establishment and has greatly informed studies in vertebrates. The well-studied Frizzled-dependent a...

Full description

Saved in:
Bibliographic Details
Main Authors: Chase Holland, Natalya Cox, Hanna Dery, Mariah Williams, Gwendolyn Jones, Lindi Newton, Kristin Jurgensen, Han Chang, Alex Hord, Won Chang, Damon Montgomery, Hawkins Hochstedler, Amish Mishra, Jessica Baker
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0328970
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850063198543151104
author Chase Holland
Natalya Cox
Hanna Dery
Mariah Williams
Gwendolyn Jones
Lindi Newton
Kristin Jurgensen
Han Chang
Alex Hord
Won Chang
Damon Montgomery
Hawkins Hochstedler
Amish Mishra
Jessica Baker
author_facet Chase Holland
Natalya Cox
Hanna Dery
Mariah Williams
Gwendolyn Jones
Lindi Newton
Kristin Jurgensen
Han Chang
Alex Hord
Won Chang
Damon Montgomery
Hawkins Hochstedler
Amish Mishra
Jessica Baker
author_sort Chase Holland
collection DOAJ
description Planar cell polarity, polarization in the plane of an epithelium, is critical for tissue development. The Drosophila melanogaster wing epithelium is an important model system for planar cell polarity establishment and has greatly informed studies in vertebrates. The well-studied Frizzled-dependent and Fat - Dachsous - Four-jointed pathways establish proximal-to-distal polarity of wing hairs, while a Frizzled-independent mechanism mediated by septate junction proteins Gliotactin, Coracle, and Varicose is required for parallel alignment of neighboring hairs. In this study, we explore a requirement for the non-muscle myosin II proteins Spaghetti Squash and Zipper in wing hair planar cell polarity. We confirm a previously recognized role in hair initiation and demonstrate a second, novel Gliotactin-interacting requirement for spaghetti squash and zipper in parallel alignment. Immunolabeling experiments demonstrate that Spaghetti Squash and Zipper localize to the base of the developing hairs during the same time frame that septate junction proteins transiently relocalize to the apical cell surface. This localization is abrogated in Gliotactin loss-of-function genotypes. We propose that Gliotactin promotes Spaghetti Squash and Zipper accumulation at the cell apical surface during wing hair extension and that this apical Myosin-II complex stabilizes the developing hair base, maintaining parallel alignment of neighboring wing hairs.
format Article
id doaj-art-e3854386965e4912a69b8a4c64708932
institution DOAJ
issn 1932-6203
language English
publishDate 2025-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-e3854386965e4912a69b8a4c647089322025-08-20T02:49:43ZengPublic Library of Science (PLoS)PLoS ONE1932-62032025-01-01207e032897010.1371/journal.pone.0328970A role for Myo-II zipper and spaghetti squash in Gliotactin-dependent Drosophila melanogaster wing hair planar cell polarity.Chase HollandNatalya CoxHanna DeryMariah WilliamsGwendolyn JonesLindi NewtonKristin JurgensenHan ChangAlex HordWon ChangDamon MontgomeryHawkins HochstedlerAmish MishraJessica BakerPlanar cell polarity, polarization in the plane of an epithelium, is critical for tissue development. The Drosophila melanogaster wing epithelium is an important model system for planar cell polarity establishment and has greatly informed studies in vertebrates. The well-studied Frizzled-dependent and Fat - Dachsous - Four-jointed pathways establish proximal-to-distal polarity of wing hairs, while a Frizzled-independent mechanism mediated by septate junction proteins Gliotactin, Coracle, and Varicose is required for parallel alignment of neighboring hairs. In this study, we explore a requirement for the non-muscle myosin II proteins Spaghetti Squash and Zipper in wing hair planar cell polarity. We confirm a previously recognized role in hair initiation and demonstrate a second, novel Gliotactin-interacting requirement for spaghetti squash and zipper in parallel alignment. Immunolabeling experiments demonstrate that Spaghetti Squash and Zipper localize to the base of the developing hairs during the same time frame that septate junction proteins transiently relocalize to the apical cell surface. This localization is abrogated in Gliotactin loss-of-function genotypes. We propose that Gliotactin promotes Spaghetti Squash and Zipper accumulation at the cell apical surface during wing hair extension and that this apical Myosin-II complex stabilizes the developing hair base, maintaining parallel alignment of neighboring wing hairs.https://doi.org/10.1371/journal.pone.0328970
spellingShingle Chase Holland
Natalya Cox
Hanna Dery
Mariah Williams
Gwendolyn Jones
Lindi Newton
Kristin Jurgensen
Han Chang
Alex Hord
Won Chang
Damon Montgomery
Hawkins Hochstedler
Amish Mishra
Jessica Baker
A role for Myo-II zipper and spaghetti squash in Gliotactin-dependent Drosophila melanogaster wing hair planar cell polarity.
PLoS ONE
title A role for Myo-II zipper and spaghetti squash in Gliotactin-dependent Drosophila melanogaster wing hair planar cell polarity.
title_full A role for Myo-II zipper and spaghetti squash in Gliotactin-dependent Drosophila melanogaster wing hair planar cell polarity.
title_fullStr A role for Myo-II zipper and spaghetti squash in Gliotactin-dependent Drosophila melanogaster wing hair planar cell polarity.
title_full_unstemmed A role for Myo-II zipper and spaghetti squash in Gliotactin-dependent Drosophila melanogaster wing hair planar cell polarity.
title_short A role for Myo-II zipper and spaghetti squash in Gliotactin-dependent Drosophila melanogaster wing hair planar cell polarity.
title_sort role for myo ii zipper and spaghetti squash in gliotactin dependent drosophila melanogaster wing hair planar cell polarity
url https://doi.org/10.1371/journal.pone.0328970
work_keys_str_mv AT chaseholland aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT natalyacox aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT hannadery aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT mariahwilliams aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT gwendolynjones aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT lindinewton aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT kristinjurgensen aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT hanchang aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT alexhord aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT wonchang aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT damonmontgomery aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT hawkinshochstedler aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT amishmishra aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT jessicabaker aroleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT chaseholland roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT natalyacox roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT hannadery roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT mariahwilliams roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT gwendolynjones roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT lindinewton roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT kristinjurgensen roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT hanchang roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT alexhord roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT wonchang roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT damonmontgomery roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT hawkinshochstedler roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT amishmishra roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity
AT jessicabaker roleformyoiizipperandspaghettisquashingliotactindependentdrosophilamelanogasterwinghairplanarcellpolarity