A multi-layered and dynamic apical extracellular matrix shapes the vulva lumen in Caenorhabditis elegans

  1. Jennifer D Cohen
  2. Alessandro P Sparacio
  3. Alexandra C Belfi
  4. Rachel Forman-Rubinsky
  5. David H Hall
  6. Hannah Maul-Newby
  7. Alison R Frand
  8. Meera V Sundaram  Is a corresponding author
  1. University of Pennsylvania Perelman School of Medicine, United States
  2. Albert Einstein College of Medicine, United States
  3. David Geffen School of Medicine, University of California, Los Angeles, United States
  4. University of Pennsylvania, United States

Abstract

Biological tubes must develop and maintain their proper diameter in order to transport materials efficiently. These tubes are molded and protected in part by apical extracellular matrices (aECMs) that line their lumens. Despite their importance, aECMs are difficult to image in vivo and therefore poorly understood. The C. elegans vulva has been a paradigm for understanding many aspects of organogenesis. Here we describe the vulva luminal matrix, which contains chondroitin proteoglycans, Zona Pellucida (ZP) domain proteins, and other glycoproteins and lipid transporters related to those in mammals. Confocal and transmission electron microscopy revealed, with unprecedented detail, a complex and dynamic aECM. Different matrix factors assemble on the apical surfaces of each vulva cell type, with clear distinctions seen between Ras-dependent (1˚) and Notch-dependent (2˚) cell types. Genetic perturbations suggest that chondroitin and other aECM factors together generate a structured scaffold that both expands and constricts lumen shape.

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 graphs in Figures 8, 8-1,10, 11.

Article and author information

Author details

  1. Jennifer D Cohen

    Genetics, University of Pennsylvania Perelman School of Medicine, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Alessandro P Sparacio

    Genetics, University of Pennsylvania Perelman School of Medicine, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Alexandra C Belfi

    Genetics, University of Pennsylvania Perelman School of Medicine, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Rachel Forman-Rubinsky

    Genetics, University of Pennsylvania Perelman School of Medicine, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. David H Hall

    Neuroscience, Albert Einstein College of Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8459-9820
  6. Hannah Maul-Newby

    Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles, Santa Cruz, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2187-7891
  7. Alison R Frand

    Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5972-989X
  8. Meera V Sundaram

    Genetics, University of Pennsylvania, Philadelphia, United States
    For correspondence
    sundaram@mail.med.upenn.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2940-8750

Funding

National Institute of General Medical Sciences (R01GM58540)

  • Meera V Sundaram

American Cancer Society (RSG-12-149-01-DDC)

  • Alison R Frand

National Institute of General Medical Sciences (R01GM125959)

  • Meera V Sundaram

National Institute of General Medical Sciences (T32 GM008216)

  • Jennifer D Cohen

National Institute of Arthritis and Musculoskeletal and Skin Diseases (T32 AR007465)

  • Jennifer D Cohen

Office of the Director (OD010943)

  • David H Hall

National Institute of General Medical Sciences (R35GM136315)

  • Meera V Sundaram

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

Copyright

© 2020, Cohen 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. Jennifer D Cohen
  2. Alessandro P Sparacio
  3. Alexandra C Belfi
  4. Rachel Forman-Rubinsky
  5. David H Hall
  6. Hannah Maul-Newby
  7. Alison R Frand
  8. Meera V Sundaram
(2020)
A multi-layered and dynamic apical extracellular matrix shapes the vulva lumen in Caenorhabditis elegans
eLife 9:e57874.
https://doi.org/10.7554/eLife.57874

Share this article

https://doi.org/10.7554/eLife.57874

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