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

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  • Ghislain Gillard

    (MRC-Laboratory of Molecular Biology)

  • Gemma Girdler

    (MRC-Laboratory of Molecular Biology
    University of Cambridge)

  • Katja Röper

    (MRC-Laboratory of Molecular Biology)

Abstract

Non-centrosomal microtubule arrays serve crucial functions in cells, yet the mechanisms of their generation are poorly understood. During budding of the epithelial tubes of the salivary glands in the Drosophila embryo, we previously demonstrated that the activity of pulsatile apical-medial actomyosin depends on a longitudinal non-centrosomal microtubule array. Here we uncover that the exit from the last embryonic division cycle of the epidermal cells of the salivary gland placode leads to one centrosome in the cells losing all microtubule-nucleation capacity. This restriction of nucleation activity to the second, Centrobin-enriched, centrosome is key for proper morphogenesis. Furthermore, the microtubule-severing protein Katanin and the minus-end-binding protein Patronin accumulate in an apical-medial position only in placodal cells. Loss of either in the placode prevents formation of the longitudinal microtubule array and leads to loss of apical-medial actomyosin and impaired apical constriction. We thus propose a mechanism whereby Katanin-severing at the single active centrosome releases microtubule minus-ends that are then anchored by apical-medial Patronin to promote formation of the longitudinal microtubule array crucial for apical constriction and tube formation.

Suggested Citation

  • Ghislain Gillard & Gemma Girdler & Katja Röper, 2021. "A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-24332-0
    DOI: 10.1038/s41467-021-24332-0
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    Cited by:

    1. Amrita Singh & Sameedha Thale & Tobias Leibner & Lucas Lamparter & Andrea Ricker & Harald Nüsse & Jürgen Klingauf & Milos Galic & Mario Ohlberger & Maja Matis, 2024. "Dynamic interplay of microtubule and actomyosin forces drive tissue extension," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Alexis Villars & Alexis Matamoro-Vidal & Florence Levillayer & Romain Levayer, 2022. "Microtubule disassembly by caspases is an important rate-limiting step of cell extrusion," Nature Communications, Nature, vol. 13(1), pages 1-18, December.

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