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Distinct molecular cues ensure a robust microtubule-dependent nuclear positioning in the Drosophila oocyte

Author

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  • Nicolas Tissot

    (Polarity and Morphogenesis Team, Institut Jacques Monod, CNRS UMR 7592, Université Paris-Diderot, Sorbonne sParis Cité)

  • Jean-Antoine Lepesant

    (Polarity and Morphogenesis Team, Institut Jacques Monod, CNRS UMR 7592, Université Paris-Diderot, Sorbonne sParis Cité)

  • Fred Bernard

    (Polarity and Morphogenesis Team, Institut Jacques Monod, CNRS UMR 7592, Université Paris-Diderot, Sorbonne sParis Cité)

  • Kevin Legent

    (Polarity and Morphogenesis Team, Institut Jacques Monod, CNRS UMR 7592, Université Paris-Diderot, Sorbonne sParis Cité)

  • Floris Bosveld

    (Polarity, Institut Curie, CNRS UMR 3215, INSERM U934)

  • Charlotte Martin

    (Polarity, Institut Curie, CNRS UMR 3215, INSERM U934)

  • Orestis Faklaris

    (Polarity and Morphogenesis Team, Institut Jacques Monod, CNRS UMR 7592, Université Paris-Diderot, Sorbonne sParis Cité)

  • Yohanns Bellaïche

    (Polarity, Institut Curie, CNRS UMR 3215, INSERM U934)

  • Maïté Coppey

    (Polarity and Morphogenesis Team, Institut Jacques Monod, CNRS UMR 7592, Université Paris-Diderot, Sorbonne sParis Cité)

  • Antoine Guichet

    (Polarity and Morphogenesis Team, Institut Jacques Monod, CNRS UMR 7592, Université Paris-Diderot, Sorbonne sParis Cité)

Abstract

Controlling nucleus localization is crucial for a variety of cellular functions. In the Drosophila oocyte, nuclear asymmetric positioning is essential for the reorganization of the microtubule (MT) network that controls the polarized transport of axis determinants. A combination of quantitative three-dimensional live imaging and laser ablation-mediated force analysis reveal that nuclear positioning is ensured with an unexpected level of robustness. We show that the nucleus is pushed to the oocyte antero-dorsal cortex by MTs and that its migration can proceed through distinct tracks. Centrosome-associated MTs favour one migratory route. In addition, the MT-associated protein Mud/NuMA that is asymmetrically localized in an Asp-dependent manner at the nuclear envelope hemisphere where MT nucleation is higher promotes a separate route. Our results demonstrate that centrosomes do not provide an obligatory driving force for nuclear movement, but together with Mud, contribute to the mechanisms that ensure the robustness of asymmetric nuclear positioning.

Suggested Citation

  • Nicolas Tissot & Jean-Antoine Lepesant & Fred Bernard & Kevin Legent & Floris Bosveld & Charlotte Martin & Orestis Faklaris & Yohanns Bellaïche & Maïté Coppey & Antoine Guichet, 2017. "Distinct molecular cues ensure a robust microtubule-dependent nuclear positioning in the Drosophila oocyte," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
  • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_ncomms15168
    DOI: 10.1038/ncomms15168
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    Cited by:

    1. 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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