Apical PAR complex proteins protect against programmed epithelial assaults to create a continuous and functional intestinal lumen

  1. Maria Danielle Sallee
  2. Melissa A Pickett
  3. Jessica L Feldman  Is a corresponding author
  1. Stanford University, United States

Abstract

Sustained polarity and adhesion of epithelial cells is essential for the protection of our organs and bodies, and this epithelial integrity emerges during organ development amidst numerous programmed morphogenetic assaults. Using the developing C. elegans intestine as an in vivo model, we investigated how epithelia maintain their integrity through cell division and elongation to build a functional tube. Live-imaging revealed that apical PAR complex proteins PAR-6/Par6 and PKC-3/aPkc remained apical during mitosis while apical microtubules and microtubule-organizing center (MTOC) proteins were transiently removed. Intestine-specific depletion of PAR-6, PKC-3, and the aPkc regulator CDC-42/Cdc42 caused persistent gaps in the apical MTOC as well as in other apical and junctional proteins after cell division and in non-dividing cells that elongated. Upon hatching, gaps coincided with luminal constrictions that blocked food, and larvae arrested and died. Thus, the apical PAR complex maintains apical and junctional continuity to construct a functional intestinal tube.

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 Figures 6 and 7.

Article and author information

Author details

  1. Maria Danielle Sallee

    Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Melissa A Pickett

    Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jessica L Feldman

    Biology, Stanford University, Stanford, United States
    For correspondence
    feldmanj@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5210-5045

Funding

National Institutes of Health (DP2 GM119136-01)

  • Jessica L Feldman

National Institutes of Health (R01 GM133950)

  • Jessica L Feldman

National Institutes of Health (F32 GM129900-01)

  • Melissa A Pickett

National Institutes of Health (K99 GM13548901)

  • Maria Danielle Sallee

National Institutes of Health (F32 GM120913-02)

  • Maria Danielle Sallee

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

Reviewing Editor

  1. Danelle Devenport, Princeton University, United States

Version history

  1. Received: October 28, 2020
  2. Accepted: June 16, 2021
  3. Accepted Manuscript published: June 17, 2021 (version 1)
  4. Version of Record published: June 30, 2021 (version 2)

Copyright

© 2021, Sallee 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. Maria Danielle Sallee
  2. Melissa A Pickett
  3. Jessica L Feldman
(2021)
Apical PAR complex proteins protect against programmed epithelial assaults to create a continuous and functional intestinal lumen
eLife 10:e64437.
https://doi.org/10.7554/eLife.64437

Share this article

https://doi.org/10.7554/eLife.64437

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