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Caenorhabditis elegans PIEZO Channel Coordinates Multiple Reproductive Tissues to Govern Ovulation

Bai, Xiaofei and Bouffard, Jeff and Lord, Avery and Brugman, Katherine and Sternberg, Paul W. and Cram, Erin J. and Golden, Andy (2020) Caenorhabditis elegans PIEZO Channel Coordinates Multiple Reproductive Tissues to Govern Ovulation. eLife, 9 . Art. No. e53603. ISSN 2050-084X. https://resolver.caltech.edu/CaltechAUTHORS:20191120-090302713

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Abstract

PIEZO1 and PIEZO2 are newly identified mechanosensitive ion channels that exhibit a preference for calcium in response to mechanical stimuli. In this study, we discovered the vital roles of pezo-1, the sole PIEZO ortholog in Caenorhabditiselegans, in regulating reproduction. A number of deletion alleles, as well as a putative gain-of-function mutant, of PEZO-1 caused a severe reduction in brood size. In vivo observations showed that oocytes undergo a variety of transit defects as they enter and exit the spermatheca during ovulation. Post-ovulation oocytes were frequently damaged during spermathecal contraction. However, the calcium signaling was not dramatically changed in the pezo-1 mutants during ovulation. Loss of PEZO-1 also led to an inability of self-sperm to navigate back to the spermatheca properly after being pushed out of the spermatheca during ovulation. These findings suggest that PEZO-1 acts in different reproductive tissues to promote proper ovulation and fertilization in C. elegans.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.7554/eLife.53603DOIArticle
https://doi.org/10.1101/847392DOIDiscussion Paper
ORCID:
AuthorORCID
Bai, Xiaofei0000-0001-8179-8162
Brugman, Katherine0000-0003-2625-2903
Sternberg, Paul W.0000-0002-7699-0173
Cram, Erin J.0000-0002-8129-1326
Golden, Andy0000-0002-8599-2031
Additional Information:© 2020 eLife Sciences Publications Ltd. This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Received: 14 November 2019; Accepted: 02 June 2020; Published: 03 June 2020. We thank the Caenorhabditis Genetics Center, which is funded by the National Institutes of Health Office of Research Infrastructure Programs (P40OD010440), for providing strains for this study. We thank Dr Orna Cohen-Fix for generously sharing the SP-12::GFP strain, and Dr Harold Smith for sharing the BA17 fem-1(hc17ts) strain. We also thank Dr David Greenstein for sharing fluorescein-tagged MSP and discussion about mating assays. We are grateful to the members of the Golden laboratory, Dr Peter Kropp, Dr Tao Cai, Rosie Bauer, Isabella Zafra, and Carina Graham for productive discussions and preparing reagents. We thank our summer intern Kyle Wilson for manuscript editing. We especially thank Dr Harold Smith, Dr Orna Cohen-Fix, Dr Kevin O’Connell, Dr Katherine McJunkin and Dan Konzman for critical inputs on the project and feedback on the manuscript. We thank all members of the Baltimore Worm Club for providing feedback and suggestions to our investigations. Funding: National Institute of General Medical Sciences (GM110268) - Erin J Cram; National Institute of Neurological Disorders and Stroke (R01 NS113119) - Paul W Sternberg; NIH Clinical Center (R24 0D023041) - Paul W Sternberg. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Author contributions: Xiaofei Bai, Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing - original draft; Jeff Bouffard, Data curation, Formal analysis, Investigation, Methodology; Avery Lord, Data curation, Investigation; Katherine Brugman, Formal analysis, Methodology; Paul W Sternberg, Conceptualization, Supervision, Funding acquisition; Erin J Cram, Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Methodology, Writing - review and editing; Andy Golden, Conceptualization, Supervision, Methodology, Writing - review and editing. Data availability: All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all Figures and figure supplements.
Funders:
Funding AgencyGrant Number
NIHGM110268
NIHR01 NS113119
NIHR24 0D023041
Record Number:CaltechAUTHORS:20191120-090302713
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20191120-090302713
Official Citation:Caenorhabditis elegans PIEZO channel coordinates multiple reproductive tissues to govern ovulation. Bai et al. eLife 2020;9:e53603. DOI: https://doi.org/10.7554/eLife.53603
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:99947
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:20 Nov 2019 18:57
Last Modified:08 Jul 2020 16:54

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