Cargando…

Syncytial germline architecture is actively maintained by contraction of an internal actomyosin corset

Syncytial architecture is an evolutionarily-conserved feature of the germline of many species and plays a crucial role in their fertility. However, the mechanism supporting syncytial organization is largely unknown. Here, we identify a corset-like actomyosin structure within the syncytial germline o...

Descripción completa

Detalles Bibliográficos
Autores principales: Priti, Agarwal, Ong, Hui Ting, Toyama, Yusuke, Padmanabhan, Anup, Dasgupta, Sabyasachi, Krajnc, Matej, Zaidel-Bar, Ronen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6224597/
https://www.ncbi.nlm.nih.gov/pubmed/30410005
http://dx.doi.org/10.1038/s41467-018-07149-2
_version_ 1783369629359407104
author Priti, Agarwal
Ong, Hui Ting
Toyama, Yusuke
Padmanabhan, Anup
Dasgupta, Sabyasachi
Krajnc, Matej
Zaidel-Bar, Ronen
author_facet Priti, Agarwal
Ong, Hui Ting
Toyama, Yusuke
Padmanabhan, Anup
Dasgupta, Sabyasachi
Krajnc, Matej
Zaidel-Bar, Ronen
author_sort Priti, Agarwal
collection PubMed
description Syncytial architecture is an evolutionarily-conserved feature of the germline of many species and plays a crucial role in their fertility. However, the mechanism supporting syncytial organization is largely unknown. Here, we identify a corset-like actomyosin structure within the syncytial germline of Caenorhabditis elegans, surrounding the common rachis. Using laser microsurgery, we demonstrate that actomyosin contractility within this structure generates tension both in the plane of the rachis surface and perpendicular to it, opposing membrane tension. Genetic and pharmacological perturbations, as well as mathematical modeling, reveal a balance of forces within the gonad and show how changing the tension within the actomyosin corset impinges on syncytial germline structure, leading, in extreme cases, to sterility. Thus, our work highlights a unique tissue-level cytoskeletal structure, and explains the critical role of actomyosin contractility in the preservation of a functional germline.
format Online
Article
Text
id pubmed-6224597
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-62245972018-11-13 Syncytial germline architecture is actively maintained by contraction of an internal actomyosin corset Priti, Agarwal Ong, Hui Ting Toyama, Yusuke Padmanabhan, Anup Dasgupta, Sabyasachi Krajnc, Matej Zaidel-Bar, Ronen Nat Commun Article Syncytial architecture is an evolutionarily-conserved feature of the germline of many species and plays a crucial role in their fertility. However, the mechanism supporting syncytial organization is largely unknown. Here, we identify a corset-like actomyosin structure within the syncytial germline of Caenorhabditis elegans, surrounding the common rachis. Using laser microsurgery, we demonstrate that actomyosin contractility within this structure generates tension both in the plane of the rachis surface and perpendicular to it, opposing membrane tension. Genetic and pharmacological perturbations, as well as mathematical modeling, reveal a balance of forces within the gonad and show how changing the tension within the actomyosin corset impinges on syncytial germline structure, leading, in extreme cases, to sterility. Thus, our work highlights a unique tissue-level cytoskeletal structure, and explains the critical role of actomyosin contractility in the preservation of a functional germline. Nature Publishing Group UK 2018-11-08 /pmc/articles/PMC6224597/ /pubmed/30410005 http://dx.doi.org/10.1038/s41467-018-07149-2 Text en © The Author(s) 2018 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
Priti, Agarwal
Ong, Hui Ting
Toyama, Yusuke
Padmanabhan, Anup
Dasgupta, Sabyasachi
Krajnc, Matej
Zaidel-Bar, Ronen
Syncytial germline architecture is actively maintained by contraction of an internal actomyosin corset
title Syncytial germline architecture is actively maintained by contraction of an internal actomyosin corset
title_full Syncytial germline architecture is actively maintained by contraction of an internal actomyosin corset
title_fullStr Syncytial germline architecture is actively maintained by contraction of an internal actomyosin corset
title_full_unstemmed Syncytial germline architecture is actively maintained by contraction of an internal actomyosin corset
title_short Syncytial germline architecture is actively maintained by contraction of an internal actomyosin corset
title_sort syncytial germline architecture is actively maintained by contraction of an internal actomyosin corset
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6224597/
https://www.ncbi.nlm.nih.gov/pubmed/30410005
http://dx.doi.org/10.1038/s41467-018-07149-2
work_keys_str_mv AT pritiagarwal syncytialgermlinearchitectureisactivelymaintainedbycontractionofaninternalactomyosincorset
AT onghuiting syncytialgermlinearchitectureisactivelymaintainedbycontractionofaninternalactomyosincorset
AT toyamayusuke syncytialgermlinearchitectureisactivelymaintainedbycontractionofaninternalactomyosincorset
AT padmanabhananup syncytialgermlinearchitectureisactivelymaintainedbycontractionofaninternalactomyosincorset
AT dasguptasabyasachi syncytialgermlinearchitectureisactivelymaintainedbycontractionofaninternalactomyosincorset
AT krajncmatej syncytialgermlinearchitectureisactivelymaintainedbycontractionofaninternalactomyosincorset
AT zaidelbarronen syncytialgermlinearchitectureisactivelymaintainedbycontractionofaninternalactomyosincorset