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

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 and Rong Li ()
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Xing Duan: Johns Hopkins University School of Medicine
Yizeng Li: Kennesaw State University
Kexi Yi: Stowers Institute for Medical Research
Fengli Guo: Stowers Institute for Medical Research
HaiYang Wang: Johns Hopkins University School of Medicine
Pei-Hsun Wu: Johns Hopkins University
Jing Yang: Johns Hopkins University
Devin B. Mair: 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

Nature Communications, 2020, vol. 11, issue 1, 1-15

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41467-019-14068-3

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