Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling

  1. Shelly TH McClatchey
  2. Zheng Wang
  3. Lara M Linden
  4. Eric L Hastie
  5. Lin Wang
  6. Wanqing Shen
  7. Alan Chen
  8. Qiuyi Chi
  9. David R Sherwood  Is a corresponding author
  1. Duke University, United States
  2. Huazhong University of Science and Technology, China

Abstract

Epithelial cells and their underlying basement membranes (BMs) slide along each other to renew epithelia, shape organs, and enlarge BM openings. How BM sliding is controlled, however, is poorly understood. Using genetic and live cell imaging approaches during uterine-vulval attachment in C. elegans, we have discovered that the invasive uterine anchor cell activates Notch signaling in neighboring uterine cells at the boundary of the BM gap through which it invades to promote BM sliding. Through an RNAi screen, we found that Notch activation upregulates expression of ctg-1, which encodes a Sec14-GOLD protein and member of the Sec14 phosphatidylinositol-transfer protein superfamily that is implicated in vesicle trafficking. Through photobleaching, targeted knockdown, and cell-specific rescue, our results suggest that CTG-1 restricts BM adhesion receptor DGN-1 (dystroglycan) trafficking to the cell-BM interface, which promotes BM sliding. Together, these studies reveal a new morphogenetic signaling pathway that controls BM sliding to remodel tissues.

Article and author information

Author details

  1. Shelly TH McClatchey

    Department of Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Zheng Wang

    Center for Tissue Engineering and Regenerative Medicine, Huazhong University of Science and Technology, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Lara M Linden

    Department of Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Eric L Hastie

    Department of Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Lin Wang

    Center for Tissue Engineering and Regenerative Medicine, Huazhong University of Science and Technology, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Wanqing Shen

    Center for Tissue Engineering and Regenerative Medicine, Huazhong University of Science and Technology, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Alan Chen

    Department of Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Qiuyi Chi

    Department of Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. David R Sherwood

    Department of Biology, Duke University, Durham, United States
    For correspondence
    david.sherwood@duke.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2245-2334

Funding

National Institute of General Medical Sciences (GM079320)

  • David R Sherwood

National Institute of General Medical Sciences (GM100083)

  • David R Sherwood

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

Reviewing Editor

  1. Janet Rossant, University of Toronto, Canada

Version history

  1. Received: April 25, 2016
  2. Accepted: September 22, 2016
  3. Accepted Manuscript published: September 23, 2016 (version 1)
  4. Version of Record published: October 12, 2016 (version 2)

Copyright

© 2016, McClatchey 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. Shelly TH McClatchey
  2. Zheng Wang
  3. Lara M Linden
  4. Eric L Hastie
  5. Lin Wang
  6. Wanqing Shen
  7. Alan Chen
  8. Qiuyi Chi
  9. David R Sherwood
(2016)
Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling
eLife 5:e17218.
https://doi.org/10.7554/eLife.17218

Share this article

https://doi.org/10.7554/eLife.17218

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