A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites
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 t...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2019-03-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/42455 |
| _version_ | 1811180558900789248 |
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| author | Nan Jiang Jeffrey P Rasmussen Joshua A Clanton Marci F Rosenberg Kory P Luedke Mark R Cronan Edward D Parker Hyeon-Jin Kim Joshua C Vaughan Alvaro Sagasti Jay Z Parrish |
| author_facet | Nan Jiang Jeffrey P Rasmussen Joshua A Clanton Marci F Rosenberg Kory P Luedke Mark R Cronan Edward D Parker Hyeon-Jin Kim Joshua C Vaughan Alvaro Sagasti Jay Z Parrish |
| author_sort | Nan Jiang |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-11T09:05:21Z |
| format | Article |
| id | doaj.art-b7d9fc63257949cb847bf97bd78c6b4d |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:05:21Z |
| publishDate | 2019-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-b7d9fc63257949cb847bf97bd78c6b4d2022-12-22T04:32:40ZengeLife Sciences Publications LtdeLife2050-084X2019-03-01810.7554/eLife.42455A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neuritesNan Jiang0Jeffrey P Rasmussen1https://orcid.org/0000-0001-6997-3773Joshua A Clanton2Marci F Rosenberg3Kory P Luedke4Mark R Cronan5Edward D Parker6Hyeon-Jin Kim7Joshua C Vaughan8https://orcid.org/0000-0002-6550-8935Alvaro Sagasti9https://orcid.org/0000-0002-6823-0692Jay Z Parrish10https://orcid.org/0000-0002-0656-9148Department of Biology, University of Washington, Seattle, United StatesDepartment of Molecular Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Molecular Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Molecular Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Biology, University of Washington, Seattle, United StatesDepartment of Molecular Genetics and Microbiology, Duke University, Durham, United StatesDepartment of Opthalmology, University of Washington, Seattle, United StatesDepartment of Chemistry, University of Washington, Seattle, United States; Department of Physiology and Biophysics, University of Washington, Seattle, United StatesDepartment of Chemistry, University of Washington, Seattle, United States; Department of Physiology and Biophysics, University of Washington, Seattle, United StatesDepartment of Molecular Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Biology, University of Washington, Seattle, United StatesInteractions 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.https://elifesciences.org/articles/42455somatosensory neuronensheathmentepidermisDrosophilazebrafishnociception |
| spellingShingle | Nan Jiang Jeffrey P Rasmussen Joshua A Clanton Marci F Rosenberg Kory P Luedke Mark R Cronan Edward D Parker Hyeon-Jin Kim Joshua C Vaughan Alvaro Sagasti Jay Z Parrish A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites eLife somatosensory neuron ensheathment epidermis Drosophila zebrafish nociception |
| title | A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites |
| title_full | A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites |
| title_fullStr | A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites |
| title_full_unstemmed | A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites |
| title_short | A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites |
| title_sort | conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites |
| topic | somatosensory neuron ensheathment epidermis Drosophila zebrafish nociception |
| url | https://elifesciences.org/articles/42455 |
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