Cargando…

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

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 prot...

Descripción completa

Detalles Bibliográficos
Autores principales: Duan, Xing, Li, Yizeng, Yi, Kexi, Guo, Fengli, Wang, HaiYang, Wu, Pei-Hsun, Yang, Jing, Mair, Devin B., Morales, Edwin Angelo, Kalab, Petr, Wirtz, Denis, Sun, Sean X., Li, Rong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6959240/
https://www.ncbi.nlm.nih.gov/pubmed/31937754
http://dx.doi.org/10.1038/s41467-019-14068-3
_version_ 1783487553426423808
author Duan, Xing
Li, Yizeng
Yi, Kexi
Guo, Fengli
Wang, HaiYang
Wu, Pei-Hsun
Yang, Jing
Mair, Devin B.
Morales, Edwin Angelo
Kalab, Petr
Wirtz, Denis
Sun, Sean X.
Li, Rong
author_facet Duan, Xing
Li, Yizeng
Yi, Kexi
Guo, Fengli
Wang, HaiYang
Wu, Pei-Hsun
Yang, Jing
Mair, Devin B.
Morales, Edwin Angelo
Kalab, Petr
Wirtz, Denis
Sun, Sean X.
Li, Rong
author_sort Duan, Xing
collection PubMed
description 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.
format Online
Article
Text
id pubmed-6959240
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-69592402020-01-15 Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes Duan, Xing Li, Yizeng Yi, Kexi Guo, Fengli Wang, HaiYang Wu, Pei-Hsun Yang, Jing Mair, Devin B. Morales, Edwin Angelo Kalab, Petr Wirtz, Denis Sun, Sean X. Li, Rong Nat Commun Article 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. Nature Publishing Group UK 2020-01-14 /pmc/articles/PMC6959240/ /pubmed/31937754 http://dx.doi.org/10.1038/s41467-019-14068-3 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Duan, Xing
Li, Yizeng
Yi, Kexi
Guo, Fengli
Wang, HaiYang
Wu, Pei-Hsun
Yang, Jing
Mair, Devin B.
Morales, Edwin Angelo
Kalab, Petr
Wirtz, Denis
Sun, Sean X.
Li, Rong
Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes
title Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes
title_full Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes
title_fullStr Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes
title_full_unstemmed Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes
title_short Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes
title_sort dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6959240/
https://www.ncbi.nlm.nih.gov/pubmed/31937754
http://dx.doi.org/10.1038/s41467-019-14068-3
work_keys_str_mv AT duanxing dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT liyizeng dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT yikexi dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT guofengli dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT wanghaiyang dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT wupeihsun dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT yangjing dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT mairdevinb dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT moralesedwinangelo dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT kalabpetr dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT wirtzdenis dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT sunseanx dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes
AT lirong dynamicorganelledistributioninitiatesactinbasedspindlemigrationinmouseoocytes