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A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites

Nan Jiang, Jeffrey P Rasmussen, Joshua A Clanton, Marci Rosenberg, Kory P Luedke, Mark R Cronan, Edward Parker, Hyeon-Jin Kim, Joshua C Vaughan, Alvaro Sagasti, Jay Parrish
doi: https://doi.org/10.1101/431197
Nan Jiang
Department of Biology, University of Washington, Seattle, WA 98195;
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Jeffrey P Rasmussen
Department of Molecular, Cell, and Developmental Biology, University of California Los Angeles;
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Joshua A Clanton
Department of Molecular, Cell, and Developmental Biology, University of California Los Angeles;
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Marci Rosenberg
Department of Molecular, Cell, and Developmental Biology, University of California Los Angeles;
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Kory P Luedke
Department of Biology, University of Washington, Seattle, WA 98195;
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Mark R Cronan
Department of Molecular Genetics and Microbiology, Duke University, Durham, NC 27710;
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Edward Parker
Department of Opthalmology, University of Washington, Seattle, WA 98195;
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Hyeon-Jin Kim
Dept of Chemistry and Dept of Department of Physiology and Biophysics, University of Washington;
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Joshua C Vaughan
Dept of Chemistry and Dept of Department of Physiology and Biophysics, University of Washington;
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Alvaro Sagasti
Department of Molecular, Cell, and Developmental Biology, University of California Los Angeles;
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Jay Parrish
University of Washington
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  • For correspondence: jzp2@uw.edu
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Abstract

Interactions between epithelial cells and neurons influence a range of sensory modalities including taste, touch, and smell. Vertebrate and invertebrate keratinocytes/keratinocyte-like 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.  

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted September 30, 2018.
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A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites
Nan Jiang, Jeffrey P Rasmussen, Joshua A Clanton, Marci Rosenberg, Kory P Luedke, Mark R Cronan, Edward Parker, Hyeon-Jin Kim, Joshua C Vaughan, Alvaro Sagasti, Jay Parrish
bioRxiv 431197; doi: https://doi.org/10.1101/431197
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A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites
Nan Jiang, Jeffrey P Rasmussen, Joshua A Clanton, Marci Rosenberg, Kory P Luedke, Mark R Cronan, Edward Parker, Hyeon-Jin Kim, Joshua C Vaughan, Alvaro Sagasti, Jay Parrish
bioRxiv 431197; doi: https://doi.org/10.1101/431197

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