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A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites

  1. Nan Jiang
  2. Jeffrey P Rasmussen
  3. Joshua A Clanton
  4. Marci F Rosenberg
  5. Kory P Luedke
  6. Mark R Cronan
  7. Edward D Parker
  8. Hyeon-Jin Kim
  9. Joshua C Vaughan
  10. Alvaro Sagasti
  11. Jay Z Parrish  Is a corresponding author
  1. University of Washington, United States
  2. University of California, Los Angeles, United States
  3. Duke University, United States
Research Article
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Cite this article as: eLife 2019;8:e42455 doi: 10.7554/eLife.42455

Abstract

Interactions between epithelial cells and neurons influence a range of sensory modalities including taste, touch, and smell. Vertebrate and invertebrate epidermal cells ensheath peripheral arbors of somatosensory neurons, including nociceptors, yet the developmental origins and functional roles of this ensheathment are largely unknown. Here, we describe an evolutionarily conserved morphogenetic mechanism for epidermal ensheathment of somatosensory neurites. We found that somatosensory neurons in Drosophila and zebrafish induce formation of epidermal sheaths, which wrap neurites of different types of neurons to different extents. Neurites induce formation of plasma membrane phosphatidylinositol 4,5-bisphosphate microdomains at nascent sheaths, followed by a filamentous actin network, and recruitment of junctional proteins that likely form autotypic junctions to seal sheaths. Finally, blocking epidermal sheath formation destabilized dendrite branches and reduced nociceptive sensitivity in Drosophila. Epidermal somatosensory neurite ensheathment is thus a deeply conserved cellular process that contributes to the morphogenesis and function of nociceptive sensory neurons.

Article and author information

Author details

  1. Nan Jiang

    Department of Biology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jeffrey P Rasmussen

    Department of Molecular, Cell, and Developmental Biology, 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:" 0000-0001-6997-3773
  3. Joshua A Clanton

    Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Marci F Rosenberg

    Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Kory P Luedke

    Department of Biology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Mark R Cronan

    Department of Molecular Genetics and Microbiology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Edward D Parker

    Department of Opthalmology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Hyeon-Jin Kim

    Department of Chemistry, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Joshua C Vaughan

    Department of Chemistry, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6550-8935
  10. Alvaro Sagasti

    Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Jay Z Parrish

    Department of Biology, University of Washington, Seattle, United States
    For correspondence
    jzp2@uw.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0656-9148

Funding

National Institute of Mental Health (NIMH R01 MH115767)

  • Joshua C Vaughan

National Institute of Neurological Disorders and Stroke (NINDS R01 NS076614)

  • Jay Z Parrish

National Institute of Arthritis and Musculoskeletal and Skin Diseases (NIAMS R01 AR064582)

  • Alvaro Sagasti

Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD K99 HD086271)

  • Jeffrey P Rasmussen

Jane Coffin Childs Memorial Fund for Medical Research

  • Jeffrey P Rasmussen

University of Washington (WRF-Hall fellowship)

  • Kory P Luedke

Japan Society for the Promotion of Science (Long term fellowship)

  • Jay Z Parrish

National Eye Institute (NEI P30EY001730)

  • Edward D Parker

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

Ethics

Animal experimentation: All zebrafish procedures were approved by the Chancellor's Animal Research Care Committee at UCLA (protocol #2005-117-41C)

Reviewing Editor

  1. Kang Shen, Howard Hughes Medical Institute, Stanford University, United States

Publication history

  1. Received: September 30, 2018
  2. Accepted: March 8, 2019
  3. Accepted Manuscript published: March 11, 2019 (version 1)

Copyright

© 2019, Jiang 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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