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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...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2020
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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 |
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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 |
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