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

Xing Duan; Yizeng Li; Kexi Yi; Fengli Guo; Hai Yang Wang; Pei Hsun Wu; Jing Yang; Devin B. Mair; Edwin Angelo Morales; Petr Kalab; Denis Wirtz; Sean X. Sun; Rong Li

doi:10.1038/s41467-019-14068-3

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

Xing Duan, Yizeng Li, Kexi Yi, Fengli Guo, Hai Yang Wang, Pei Hsun Wu, Jing Yang, Devin B. Mair, Edwin Angelo Morales, Petr Kalab, Denis Wirtz, Sean X. Sun, Rong Li

Research output: Contribution to journal › Article › peer-review

11 Scopus citations

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.

Original language	English (US)
Article number	277
Journal	Nature communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-14068-3
State	Published - Dec 1 2020

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General
General Physics and Astronomy

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@article{aa11c25565aa4abd966ffa00881b093c,

title = "Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes",

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.",

author = "Xing Duan and Yizeng Li and Kexi Yi and Fengli Guo and Wang, {Hai Yang} and Wu, {Pei Hsun} and Jing Yang and Mair, {Devin B.} and Morales, {Edwin Angelo} and Petr Kalab and Denis Wirtz and Sun, {Sean X.} and Rong Li",

note = "Funding Information: We thank Marie-Helene Verlhac for providing the mCherry-myosin Vb tail plasmid, Melina Schuh for providing pGEMHE-mCherry-full length myosin Vb plasmid, Philip Leder for providing Fmn2-null mice, Jan Ellenberg for providing Fmn2-mCherry, Clare Waterman for providing Fmn2-EGFP. Petr Solc for providing pYX-RNA-eGFP plasmid, Takanari Inoue for providing miLID and mSSPBR73Q plasmid, and Tom Rapoport for providing the Sec61-β plasmid. We thank Brian Slaughter, Jay Unruh, and Boris Rubinstein for input in data analysis. We thank Jiten Narang and Christopher Lemmon for assistance with microfabrication. This work is supported by grant RO1-HD086577 from the National Institute of Health to RL. Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2020",

month = dec,

day = "1",

doi = "10.1038/s41467-019-14068-3",

language = "English (US)",

volume = "11",

journal = "Nature communications",

issn = "2041-1723",

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TY - JOUR

T1 - Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes

AU - Duan, Xing

AU - Li, Yizeng

AU - Yi, Kexi

AU - Guo, Fengli

AU - Wang, Hai Yang

AU - Wu, Pei Hsun

AU - Yang, Jing

AU - Mair, Devin B.

AU - Morales, Edwin Angelo

AU - Kalab, Petr

AU - Wirtz, Denis

AU - Sun, Sean X.

AU - Li, Rong

N1 - Funding Information: We thank Marie-Helene Verlhac for providing the mCherry-myosin Vb tail plasmid, Melina Schuh for providing pGEMHE-mCherry-full length myosin Vb plasmid, Philip Leder for providing Fmn2-null mice, Jan Ellenberg for providing Fmn2-mCherry, Clare Waterman for providing Fmn2-EGFP. Petr Solc for providing pYX-RNA-eGFP plasmid, Takanari Inoue for providing miLID and mSSPBR73Q plasmid, and Tom Rapoport for providing the Sec61-β plasmid. We thank Brian Slaughter, Jay Unruh, and Boris Rubinstein for input in data analysis. We thank Jiten Narang and Christopher Lemmon for assistance with microfabrication. This work is supported by grant RO1-HD086577 from the National Institute of Health to RL. Publisher Copyright: © 2020, The Author(s).

PY - 2020/12/1

Y1 - 2020/12/1

N2 - 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.

AB - 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.

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VL - 11

JO - Nature communications

JF - Nature communications

IS - 1

M1 - 277

ER -

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

Abstract

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