Drosophila epidermal cells are intrinsically mechanosensitive and modulate nociceptive behavioral outputs
Somatosensory neurons (SSNs) that detect and transduce mechanical, thermal, and chemical stimuli densely innervate an animal’s skin. However, although epidermal cells provide the first point of contact for sensory stimuli, our understanding of roles that epidermal cells play in SSN function, particu...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2025-05-01
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| Online Access: | https://elifesciences.org/articles/95379 |
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| author | Jiro Yoshino Sonali S Mali Claire R Williams Takeshi Morita Chloe E Emerson Christopher J Arp Sophie E Miller Chang Yin Lydia Thé Chikayo Hemmi Mana Motoyoshi Kenichi Ishii Kazuo Emoto Diana M Bautista Jay Z Parrish |
| author_facet | Jiro Yoshino Sonali S Mali Claire R Williams Takeshi Morita Chloe E Emerson Christopher J Arp Sophie E Miller Chang Yin Lydia Thé Chikayo Hemmi Mana Motoyoshi Kenichi Ishii Kazuo Emoto Diana M Bautista Jay Z Parrish |
| author_sort | Jiro Yoshino |
| collection | DOAJ |
| description | Somatosensory neurons (SSNs) that detect and transduce mechanical, thermal, and chemical stimuli densely innervate an animal’s skin. However, although epidermal cells provide the first point of contact for sensory stimuli, our understanding of roles that epidermal cells play in SSN function, particularly nociception, remains limited. Here, we show that stimulating Drosophila epidermal cells elicits activation of SSNs including nociceptors and triggers a variety of behavior outputs, including avoidance and escape. Further, we find that epidermal cells are intrinsically mechanosensitive and that epidermal mechanically evoked calcium responses require the store-operated calcium channel Orai. Epidermal cell stimulation augments larval responses to acute nociceptive stimuli and promotes prolonged hypersensitivity to subsequent mechanical stimuli. Hence, epidermal cells are key determinants of nociceptive sensitivity and sensitization, acting as primary sensors of noxious stimuli that tune nociceptor output and drive protective behaviors. |
| format | Article |
| id | doaj-art-bf4de3dad69f4623b257d2558675fa8e |
| institution | OA Journals |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-bf4de3dad69f4623b257d2558675fa8e2025-08-20T01:50:21ZengeLife Sciences Publications LtdeLife2050-084X2025-05-011310.7554/eLife.95379Drosophila epidermal cells are intrinsically mechanosensitive and modulate nociceptive behavioral outputsJiro Yoshino0https://orcid.org/0000-0001-9761-4882Sonali S Mali1https://orcid.org/0000-0003-0737-813XClaire R Williams2https://orcid.org/0000-0001-5467-149XTakeshi Morita3https://orcid.org/0000-0002-8570-6744Chloe E Emerson4https://orcid.org/0000-0003-1188-0501Christopher J Arp5https://orcid.org/0000-0002-5059-6178Sophie E Miller6https://orcid.org/0000-0001-6805-7036Chang Yin7Lydia Thé8https://orcid.org/0009-0008-0297-776XChikayo Hemmi9https://orcid.org/0009-0002-3815-8164Mana Motoyoshi10https://orcid.org/0009-0005-4759-0065Kenichi Ishii11https://orcid.org/0000-0002-8834-5729Kazuo Emoto12https://orcid.org/0000-0003-4194-801XDiana M Bautista13https://orcid.org/0000-0002-6809-8951Jay Z Parrish14https://orcid.org/0000-0002-0656-9148Department of Biology, University of Washington, Seattle, United States; Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, Japan; Division of Education, Marine Biological Laboratory, Woods Hole, United StatesDivision of Education, Marine Biological Laboratory, Woods Hole, United States; Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United StatesDepartment of Biology, University of Washington, Seattle, United States; Division of Education, Marine Biological Laboratory, Woods Hole, United StatesDivision of Education, Marine Biological Laboratory, Woods Hole, United States; Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, United StatesDivision of Education, Marine Biological Laboratory, Woods Hole, United StatesDivision of Education, Marine Biological Laboratory, Woods Hole, United StatesDivision of Education, Marine Biological Laboratory, Woods Hole, United StatesDepartment of Biology, University of Washington, Seattle, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, JapanDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, JapanDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, JapanDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, Japan; International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo, Tokyo, JapanDivision of Education, Marine Biological Laboratory, Woods Hole, United States; Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States; Howard Hughes Medical Institute, University of California at Berkeley, Berkeley, United StatesDepartment of Biology, University of Washington, Seattle, United States; Division of Education, Marine Biological Laboratory, Woods Hole, United StatesSomatosensory neurons (SSNs) that detect and transduce mechanical, thermal, and chemical stimuli densely innervate an animal’s skin. However, although epidermal cells provide the first point of contact for sensory stimuli, our understanding of roles that epidermal cells play in SSN function, particularly nociception, remains limited. Here, we show that stimulating Drosophila epidermal cells elicits activation of SSNs including nociceptors and triggers a variety of behavior outputs, including avoidance and escape. Further, we find that epidermal cells are intrinsically mechanosensitive and that epidermal mechanically evoked calcium responses require the store-operated calcium channel Orai. Epidermal cell stimulation augments larval responses to acute nociceptive stimuli and promotes prolonged hypersensitivity to subsequent mechanical stimuli. Hence, epidermal cells are key determinants of nociceptive sensitivity and sensitization, acting as primary sensors of noxious stimuli that tune nociceptor output and drive protective behaviors.https://elifesciences.org/articles/95379mechanosensationepidermisnociceptionsomatosensation |
| spellingShingle | Jiro Yoshino Sonali S Mali Claire R Williams Takeshi Morita Chloe E Emerson Christopher J Arp Sophie E Miller Chang Yin Lydia Thé Chikayo Hemmi Mana Motoyoshi Kenichi Ishii Kazuo Emoto Diana M Bautista Jay Z Parrish Drosophila epidermal cells are intrinsically mechanosensitive and modulate nociceptive behavioral outputs eLife mechanosensation epidermis nociception somatosensation |
| title | Drosophila epidermal cells are intrinsically mechanosensitive and modulate nociceptive behavioral outputs |
| title_full | Drosophila epidermal cells are intrinsically mechanosensitive and modulate nociceptive behavioral outputs |
| title_fullStr | Drosophila epidermal cells are intrinsically mechanosensitive and modulate nociceptive behavioral outputs |
| title_full_unstemmed | Drosophila epidermal cells are intrinsically mechanosensitive and modulate nociceptive behavioral outputs |
| title_short | Drosophila epidermal cells are intrinsically mechanosensitive and modulate nociceptive behavioral outputs |
| title_sort | drosophila epidermal cells are intrinsically mechanosensitive and modulate nociceptive behavioral outputs |
| topic | mechanosensation epidermis nociception somatosensation |
| url | https://elifesciences.org/articles/95379 |
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