The Drosophila Afadin and ZO-1 homologs Canoe and Polychaetoid act in parallel to maintain epithelial integrity when challenged by adherens junction remodeling

Manning, Lathiena; Perez-Vale, Kia Z.; Schaefer, Kristina N.; Sewell, Mycah T.; Peifer, Mark

doi:10.1101/609123

Cited by 2 publications

(2 citation statements)

References 84 publications

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“…We also provide direct evidence that large epithelial rupture can arise by intercellular detachment during cell division, which provides a weak spot primed for disruption upon increased mechanical stress. This is consistent with previous observations that reinforcement of junctional attachment to the cytoskeleton prevents detachment during cell division in the Drosophila embryonic epithelium and mammalian cell culture [68,69]. Dividing cells do not generate gaps upon aPKC inactivation in a mosaic tissue, showing that a direct effect in mitotic cells is not responsible for gap formation by itself.…”

Section: Discussionsupporting

confidence: 93%

Apical constriction induces tissue rupture in a proliferative epithelium

Osswald

Barros-Carvalho

Carmo

et al. 2022

Preprint

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Apical-basal polarity is an essential epithelial trait controlled by the evolutionarily conserved PAR-aPKC polarity network. Deregulation of polarity proteins disrupts tissue organization during development and in disease, but the underlying mechanisms are unclear due to the broad implications of polarity loss. Here, we uncovered how Drosophila aPKC maintains epithelial architecture by directly observing tissue disorganization after fast optogenetic inactivation in living adult flies and ovaries cultured ex vivo. We show that fast aPKC perturbation in the proliferative follicular epithelium produces large epithelial gaps that result from increased apical constriction, rather than loss of apical-basal polarity. Accordingly, we could modulate the incidence of epithelial gaps by increasing and decreasing actomyosin-driven contractility. We traced the origin of epithelial gaps to tissue rupture next to dividing cells. Live imaging shows that aPKC perturbation rapidly induces apical constriction in non-mitotic cells, producing pulling forces that ultimately detach dividing and neighbouring cells. We further demonstrate that epithelial rupture requires a global increase of apical constriction, since it was prevented by the presence of non-constricting cells. Conversely, a global induction of apical tension through light-induced recruitment of RhoGEF2 to the apical side was sufficient to produce tissue rupture. Hence, our work reveals that the roles of aPKC in polarity and actomyosin regulation are separable and provides the first in vivo evidence that excessive tissue stress can break the epithelial barrier during proliferation.

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Section: Discussionsupporting

confidence: 93%

Apical constriction induces tissue rupture in a proliferative epithelium

Osswald

Barros-Carvalho

Carmo

et al. 2022

Preprint

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“…Lmo7 has been reported to respond to the mechanical force (Hashimoto et al, 2019). Lmo7 binds Afadin that was implicated in force transmission at cell-cell junctions (Choi et al, 2016;Manning et al, 2019;Yu and Zallen, 2020). Supporting this hypothesis, we found that Lmo7 influences the distribution of Wtip, a sensor of mechanical tension (Chu et al, 2018).…”

Section: Discussionsupporting

confidence: 77%

Lmo7 recruits myosin II heavy chain to induce apical constriction in Xenopus ectoderm

Matsuda

Chu

Sokol

2021

Preprint

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The reduction of the apical domain, or apical constriction, is a process that occurs in a single cell or is coordinated in a group of cells in the epithelium. Coordinated apical constriction is particularly important when the epithelium is undergoing dynamic morphogenetic events such as furrow or tube formation. However, the underlying mechanisms remain incompletely understood. Here we show that Lim only protein 7 (Lmo7) is a novel activator of apical constriction in the Xenopus superficial ectoderm, which coordinates actomyosin contractility in a group of cells during epithelial morphogenesis. Like other apical constriction regulators, Lmo7 requires the activation of the Rho-Rock-Myosin II pathway to induce apical constriction. However, instead of increasing the phosphorylation of myosin light chain (MLC), Lmo7 binds muscle myosin II heavy chain A (NMIIA) and increases its association with actomyosin bundles at adherens junctions (AJs). Lmo7 overexpression modulates the subcellular distribution of Wtip, a tension marker at AJs, suggesting that Lmo7 generates mechanical forces at AJs. We propose that Lmo7 increases actomyosin contractility at AJs by promoting the formation of actomyosin bundles.

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The Drosophila Afadin and ZO-1 homologs Canoe and Polychaetoid act in parallel to maintain epithelial integrity when challenged by adherens junction remodeling

Cited by 2 publications

References 84 publications

Apical constriction induces tissue rupture in a proliferative epithelium

Apical constriction induces tissue rupture in a proliferative epithelium

Lmo7 recruits myosin II heavy chain to induce apical constriction in Xenopus ectoderm

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