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Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes

Author

Listed:
  • Xing Duan

    (Johns Hopkins University School of Medicine
    Johns Hopkins University)

  • Yizeng Li

    (Kennesaw State University
    Johns Hopkins University)

  • Kexi Yi

    (Stowers Institute for Medical Research)

  • Fengli Guo

    (Stowers Institute for Medical Research)

  • HaiYang Wang

    (Johns Hopkins University School of Medicine
    Johns Hopkins University)

  • Pei-Hsun Wu

    (Johns Hopkins University)

  • Jing Yang

    (Johns Hopkins University)

  • Devin B. Mair

    (Johns Hopkins University School of Medicine
    Johns Hopkins University
    Johns Hopkins University School of Medicine)

  • Edwin Angelo Morales

    (Johns Hopkins University School of Medicine)

  • Petr Kalab

    (Johns Hopkins University)

  • Denis Wirtz

    (Johns Hopkins University)

  • Sean X. Sun

    (Johns Hopkins University)

  • Rong Li

    (Johns Hopkins University School of Medicine
    Johns Hopkins University
    National University of Singapore)

Abstract

Migration of meiosis-I (MI) spindle from the cell center to a sub-cortical location is a critical step for mouse oocytes to undergo asymmetric meiotic cell division. In this study, we investigate the mechanism by which formin-2 (FMN2) orchestrates the initial movement of MI spindle. By defining protein domains responsible for targeting FMN2, we show that spindle-periphery localized FMN2 is required for spindle migration. The spindle-peripheral FMN2 nucleates short actin bundles from vesicles derived likely from the endoplasmic reticulum (ER) and concentrated in a layer outside the spindle. This layer is in turn surrounded by mitochondria. A model based on polymerizing actin filaments pushing against mitochondria, thus generating a counter force on the spindle, demonstrated an inherent ability of this system to break symmetry and evolve directional spindle motion. The model is further supported through experiments involving spatially biasing actin nucleation via optogenetics and disruption of mitochondrial distribution and dynamics.

Suggested Citation

  • Xing Duan & Yizeng Li & Kexi Yi & Fengli Guo & HaiYang Wang & Pei-Hsun Wu & Jing Yang & Devin B. Mair & Edwin Angelo Morales & Petr Kalab & Denis Wirtz & Sean X. Sun & Rong Li, 2020. "Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-019-14068-3
    DOI: 10.1038/s41467-019-14068-3
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    Cited by:

    1. Elena Kozgunova & Mari W. Yoshida & Ralf Reski & Gohta Goshima, 2022. "Spindle motility skews division site determination during asymmetric cell division in Physcomitrella," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

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