Epidermal PAR-6 and PKC-3 are essential for larval development of C. elegans and organize non-centrosomal microtubules

Abstract

The cortical polarity regulators PAR-6, PKC-3, and PAR-3 are essential for the polarization of a broad variety of cell types in multicellular animals. In C. elegans, the roles of the PAR proteins in embryonic development have been extensively studied, yet little is known about their functions during larval development. Using inducible protein degradation, we show that PAR-6 and PKC-3, but not PAR-3, are essential for postembryonic development. PAR-6 and PKC-3 are required in the epidermal epithelium for animal growth, molting, and the proper pattern of seam-cell divisions. Finally, we uncovered a novel role for PAR-6 in organizing non-centrosomal microtubule arrays in the epidermis. PAR-6 was required for the localization of the microtubule organizer NOCA-1/Ninein, and defects in a noca-1 mutant are highly similar to those caused by epidermal PAR-6 depletion. As NOCA-1 physically interacts with PAR-6, we propose that PAR-6 promotes non-centrosomal microtubule organization through localization of NOCA-1/Ninein.

Data availability

All quantative data generated during this study are included in the manuscript and supporting files. All microscopy images shown are supplied as source data files.

Article and author information

Author details

  1. Victoria G Castiglioni

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  2. Helena R Pires

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Rodrigo Rosas Bertolini

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Amalia Riga

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Jana Kerver

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Mike Boxem

    Department of Biology, Utrecht University, Utrecht, Netherlands
    For correspondence
    M.Boxem@uu.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3966-4173

Funding

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (824.14.021)

  • Mike Boxem

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (016.VICI.170.165)

  • Mike Boxem

H2020 Marie Skłodowska-Curie Actions (ITN 675407)

  • Mike Boxem

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States

Version history

  1. Received: August 12, 2020
  2. Accepted: December 9, 2020
  3. Accepted Manuscript published: December 10, 2020 (version 1)
  4. Version of Record published: December 22, 2020 (version 2)

Copyright

© 2020, Castiglioni et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Victoria G Castiglioni
  2. Helena R Pires
  3. Rodrigo Rosas Bertolini
  4. Amalia Riga
  5. Jana Kerver
  6. Mike Boxem
(2020)
Epidermal PAR-6 and PKC-3 are essential for larval development of C. elegans and organize non-centrosomal microtubules
eLife 9:e62067.
https://doi.org/10.7554/eLife.62067

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https://doi.org/10.7554/eLife.62067