Caenorhabditis elegans PIEZO channel coordinates multiple reproductive tissues to govern ovulation

  1. Xiaofei Bai
  2. Jeff W Bouffard
  3. Avery Lord
  4. Katherine Brugman
  5. Paul W Sternberg
  6. Erin J Cram
  7. Andy Golden  Is a corresponding author
  1. National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, United States
  2. Northeastern University, United States
  3. California Institute of Technology, United States
  4. Howard Hughes Medical Institute, California Institute of Technology, United States

Abstract

PIEZO1 and PIEZO2 are newly identified mechano-sensitive 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 C. elegans, 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 revealed an inability of self-sperm to properly navigate back to the spermatheca 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.

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 Supplemental Figures

Article and author information

Author details

  1. Xiaofei Bai

    National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jeff W Bouffard

    Department of Bioengineering, Northeastern University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Avery Lord

    Department of Biology, Northeastern University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Katherine Brugman

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Paul W Sternberg

    Division of Biology & BIological Engineering, Howard Hughes Medical Institute, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7699-0173
  6. Erin J Cram

    Department of Biology, Northeastern University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Andy Golden

    National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, United States
    For correspondence
    andyg@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8599-2031

Funding

National Institute of General Medical Sciences (GM110268)

  • Erin J Cram

NIH Clinical Center (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.

Copyright

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.

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  1. Xiaofei Bai
  2. Jeff W Bouffard
  3. Avery Lord
  4. Katherine Brugman
  5. Paul W Sternberg
  6. Erin J Cram
  7. Andy Golden
(2020)
Caenorhabditis elegans PIEZO channel coordinates multiple reproductive tissues to govern ovulation
eLife 9:e53603.
https://doi.org/10.7554/eLife.53603

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https://doi.org/10.7554/eLife.53603

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