A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites
- University of Washington, United States
- University of California, Los Angeles, United States
- Duke University, United States
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.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files.
Article and author information
Author details
Jeffrey P Rasmussen
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
- Kang Shen, Howard Hughes Medical Institute, Stanford University, United States
Publication history
- Received: September 30, 2018
- Accepted: March 8, 2019
- Accepted Manuscript published: March 11, 2019 (version 1)
- Version of Record published: April 5, 2019 (version 2)
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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A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites
eLife 8:e42455.
https://doi.org/10.7554/eLife.42455
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