Morphogenetic forces planar polarize LGN/Pins in the embryonic head during Drosophila gastrulation

Spindle orientation is often achieved by a complex of Partner of Inscuteable (Pins)/LGN, Mushroom Body Defect (Mud)/Nuclear Mitotic Apparatus (NuMa), Gαi, and Dynein, which interacts with astral microtubules to rotate the spindle. Cortical Pins/LGN recruitment serves as a critical step in this proce...

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Main Authors: Jaclyn Camuglia, Soline Chanet, Adam C Martin
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/78779
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author Jaclyn Camuglia
Soline Chanet
Adam C Martin
author_facet Jaclyn Camuglia
Soline Chanet
Adam C Martin
author_sort Jaclyn Camuglia
collection DOAJ
description Spindle orientation is often achieved by a complex of Partner of Inscuteable (Pins)/LGN, Mushroom Body Defect (Mud)/Nuclear Mitotic Apparatus (NuMa), Gαi, and Dynein, which interacts with astral microtubules to rotate the spindle. Cortical Pins/LGN recruitment serves as a critical step in this process. Here, we identify Pins-mediated planar cell polarized divisions in several of the mitotic domains of the early Drosophila embryo. We found that neither planar cell polarity pathways nor planar polarized myosin localization determined division orientation; instead, our findings strongly suggest that Pins planar polarity and force generated from mesoderm invagination are important. Disrupting Pins polarity via overexpression of a myristoylated version of Pins caused randomized division angles. We found that disrupting forces through chemical inhibitors, depletion of an adherens junction protein, or blocking mesoderm invagination disrupted Pins planar polarity and spindle orientation. Furthermore, directional ablations that separated mesoderm from mitotic domains disrupted spindle orientation, suggesting that forces transmitted from mesoderm to mitotic domains can polarize Pins and orient division during gastrulation. To our knowledge, this is the first in vivo example where mechanical force has been shown to polarize Pins to mediate division orientation.
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spelling doaj.art-6b61dd0e81344fb0a3cf1ca8b0cadad12022-12-22T03:50:43ZengeLife Sciences Publications LtdeLife2050-084X2022-07-011110.7554/eLife.78779Morphogenetic forces planar polarize LGN/Pins in the embryonic head during Drosophila gastrulationJaclyn Camuglia0https://orcid.org/0000-0001-9268-9471Soline Chanet1https://orcid.org/0000-0002-4065-9411Adam C Martin2https://orcid.org/0000-0001-8060-2607Biology Department, Massachusetts Institute of Technology, Cambridge, MA, United StatesCenter for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, Université PSL, Paris, FranceBiology Department, Massachusetts Institute of Technology, Cambridge, MA, United StatesSpindle orientation is often achieved by a complex of Partner of Inscuteable (Pins)/LGN, Mushroom Body Defect (Mud)/Nuclear Mitotic Apparatus (NuMa), Gαi, and Dynein, which interacts with astral microtubules to rotate the spindle. Cortical Pins/LGN recruitment serves as a critical step in this process. Here, we identify Pins-mediated planar cell polarized divisions in several of the mitotic domains of the early Drosophila embryo. We found that neither planar cell polarity pathways nor planar polarized myosin localization determined division orientation; instead, our findings strongly suggest that Pins planar polarity and force generated from mesoderm invagination are important. Disrupting Pins polarity via overexpression of a myristoylated version of Pins caused randomized division angles. We found that disrupting forces through chemical inhibitors, depletion of an adherens junction protein, or blocking mesoderm invagination disrupted Pins planar polarity and spindle orientation. Furthermore, directional ablations that separated mesoderm from mitotic domains disrupted spindle orientation, suggesting that forces transmitted from mesoderm to mitotic domains can polarize Pins and orient division during gastrulation. To our knowledge, this is the first in vivo example where mechanical force has been shown to polarize Pins to mediate division orientation.https://elifesciences.org/articles/78779spindle orientationmechanicsmorphogenesisadherens junctionsPins/LGNDrosophila
spellingShingle Jaclyn Camuglia
Soline Chanet
Adam C Martin
Morphogenetic forces planar polarize LGN/Pins in the embryonic head during Drosophila gastrulation
eLife
spindle orientation
mechanics
morphogenesis
adherens junctions
Pins/LGN
Drosophila
title Morphogenetic forces planar polarize LGN/Pins in the embryonic head during Drosophila gastrulation
title_full Morphogenetic forces planar polarize LGN/Pins in the embryonic head during Drosophila gastrulation
title_fullStr Morphogenetic forces planar polarize LGN/Pins in the embryonic head during Drosophila gastrulation
title_full_unstemmed Morphogenetic forces planar polarize LGN/Pins in the embryonic head during Drosophila gastrulation
title_short Morphogenetic forces planar polarize LGN/Pins in the embryonic head during Drosophila gastrulation
title_sort morphogenetic forces planar polarize lgn pins in the embryonic head during drosophila gastrulation
topic spindle orientation
mechanics
morphogenesis
adherens junctions
Pins/LGN
Drosophila
url https://elifesciences.org/articles/78779
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AT solinechanet morphogeneticforcesplanarpolarizelgnpinsintheembryonicheadduringdrosophilagastrulation
AT adamcmartin morphogeneticforcesplanarpolarizelgnpinsintheembryonicheadduringdrosophilagastrulation