A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding

Gillard, Ghislain; Girdler, Gemma; Röper, Katja

doi:10.1038/s41467-021-24332-0

Cited by 13 publications

(23 citation statements)

References 74 publications

(122 reference statements)

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“…The microtubule reorganization we observe differs from recent studies that have demonstrated an interplay between the two cytoskeletal systems in two ways: first, microtubule reorganization occurs in the apical plane rather than along the apicobasal axis; second, the consequences, of the perturbations tested, on actomyosin and microtubule cytoskeleton are also different (Booth et al, 2014;Ko et al, 2019;Gillard et al, 2021).…”

Section: The Importance Of Apical Microtubule Network Reorganization ...contrasting

confidence: 97%

The microtubule end-binding proteins EB1 and Patronin modulate the spatiotemporal dynamics of myosin and pattern pulsed apical constriction

et al. 2022

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Apical constriction powers amnioserosa contraction during Drosophila dorsal closure. The nucleation, movement and dispersal of apicomedial actomyosin complexes generates pulsed apical constrictions during early closure. Persistent apicomedial and circumapical actomyosin complexes drive unpulsed constrictions that follow. Here, we show that the microtubule end-binding proteins EB1 and Patronin pattern constriction dynamics and contraction kinetics by coordinating the balance of actomyosin forces in the apical plane. We find that microtubule growth from moving Patronin platforms governs the spatiotemporal dynamics of apicomedial myosin through the regulation of RhoGTPase signaling by transient EB1-RhoGEF2 interactions. We uncover the dynamic reorganization of a subset of short non-centrosomally nucleated apical microtubules that surround the coalescing apicomedial myosin complex, trail behind it as it moves and disperse as the complex dissolves. We demonstrate that apical microtubule reorganization is sensitive to Patronin levels. Microtubule depolymerization compromised apical myosin enrichment and altered constriction dynamics. Together, our findings uncover the importance of reorganization of an intact apical microtubule meshwork, by moving Patronin platforms and growing microtubule ends, in enabling the spatiotemporal modulation of actomyosin contractility and, through it, apical constriction.

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Section: The Importance Of Apical Microtubule Network Reorganization ...contrasting

confidence: 97%

The microtubule end-binding proteins EB1 and Patronin modulate the spatiotemporal dynamics of myosin and pattern pulsed apical constriction

et al. 2022

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“…The levels of apical-medial Patronin were still sufficient to capture microtubule-minus ends released by Katanin, thereby generating the non-centrosomal microtubules that will then form the longitudinal array as we showed previously (Gillard et al, 2021). These data illustrate that not only the longitudinal microtubule array but also apicalmedial b-H-Spectrin are both required to support apical-medial actomyosin assembly and function to drive apical constriction.…”

Section: B-h-spectrin Is Required For Apical Constriction and The Ass...supporting

confidence: 74%

β-H-Spectrin is a key component of an apical-medial hub of proteins during cell wedging in tube morphogenesis

Gillard,

Röper

2023

Preprint

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Coordinated cell shape changes are a major driver of tissue morphogenesis during development, with apical constriction or wedging of groups of epithelial cells for instance leading to tissue bending in folding or budding processes. During the budding of the tubes of the salivary glands in theDrosophilaembryo we previously identified a key interplay between the apical-medial actomyosin that drives apical constriction with the underlying longitudinal microtubule array. At this microtubule-actomyosin interface a hub of proteins accumulates: in addition to the microtubule-actin crosslinker Shot and the minus-end-binder Patronin, we identified two actin-crosslinkers, β-H-Spectrin and Filamin, and the multi-PDZ protein Big bang as components of this apical-medial hub. Tissue-specific degradation of β-H-Spectrin led to reduction of apical-medial Big bang, F-actin, Shot and Patronin and concomittant defects in apical constriction and tube morphogenesis. Residual Patronin still present in the apical-medial position was sufficient to assist microtubule reorganisation into the longitudinal array. In contrast to Patronin and Shot, neither β-H-Spectrin nor Big bang required microtubules for their localisation. β-H-Spectrin instead appeared to be recruited to the apical-medial domain via binding to phosphoinositides that accumulated here. Overexpression of a β-H-Spectrin fragment containing its PH domain displaced endogenous β-H-Spectrin from the apical-medial domain and led to strong morphogenetic defects. The interconnected hub therefore required the synergy of membrane-associated β-H-Spectrin and microtubules and their respective interactors for its assembly and function in sustaining the apical constriction during tube invagination.

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“…The disappearance of apical MTs is not driven by a shift of the centrosome position 33 (Supplementary Fig. 3k ), nor relocalisation of MTs or a change of MTs association with the centrosome 35 , or modulation of the localisation of the non-centrosomal MTs organisers Patronin and Shot 33 , 36 , 37 (Supplementary Fig. 3i, j ).…”

Section: Discussionmentioning

confidence: 97%

Microtubule disassembly by caspases is an important rate-limiting step of cell extrusion

2022

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The expulsion of dying epithelial cells requires well-orchestrated remodelling steps to maintain tissue sealing. This process, named cell extrusion, has been mostly analysed through the study of actomyosin regulation. Yet, the mechanistic relationship between caspase activation and cell extrusion is still poorly understood. Using the Drosophila pupal notum, a single layer epithelium where extrusions are caspase-dependent, we showed that the initiation of cell extrusion and apical constriction are surprisingly not associated with the modulation of actomyosin concentration and dynamics. Instead, cell apical constriction is initiated by the disassembly of a medio-apical mesh of microtubules which is driven by effector caspases. Importantly, the depletion of microtubules is sufficient to bypass the requirement of caspases for cell extrusion, while microtubule stabilisation strongly impairs cell extrusion. This study shows that microtubules disassembly by caspases is a key rate-limiting step of extrusion, and outlines a more general function of microtubules in epithelial cell shape stabilisation.

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A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding

Cited by 13 publications

References 74 publications

The microtubule end-binding proteins EB1 and Patronin modulate the spatiotemporal dynamics of myosin and pattern pulsed apical constriction

The microtubule end-binding proteins EB1 and Patronin modulate the spatiotemporal dynamics of myosin and pattern pulsed apical constriction

β-H-Spectrin is a key component of an apical-medial hub of proteins during cell wedging in tube morphogenesis

Microtubule disassembly by caspases is an important rate-limiting step of cell extrusion

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