Steroid hormone signaling activates thermal nociception during Drosophila peripheral nervous system development
Sensory neurons enable animals to detect environmental changes and avoid harm. An intriguing open question concerns how the various attributes of sensory neurons arise in development. Drosophila melanogaster larvae undergo a behavioral transition by robustly activating a thermal nociceptive escape b...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-03-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/76464 |
| _version_ | 1797991911171031040 |
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| author | Jacob S Jaszczak Laura DeVault Lily Yeh Jan Yuh Nung Jan |
| author_facet | Jacob S Jaszczak Laura DeVault Lily Yeh Jan Yuh Nung Jan |
| author_sort | Jacob S Jaszczak |
| collection | DOAJ |
| description | Sensory neurons enable animals to detect environmental changes and avoid harm. An intriguing open question concerns how the various attributes of sensory neurons arise in development. Drosophila melanogaster larvae undergo a behavioral transition by robustly activating a thermal nociceptive escape behavior during the second half of larval development (third instar). The Class IV dendritic arborization (C4da) neurons are multimodal sensors which tile the body wall of Drosophila larvae and detect nociceptive temperature, light, and mechanical force. In contrast to the increase in nociceptive behavior in the third instar, we find that ultraviolet light-induced Ca2+ activity in C4da neurons decreases during the same period of larval development. Loss of ecdysone receptor has previously been shown to reduce nociception in third instar larvae. We find that ligand-dependent activation of ecdysone signaling is sufficient to promote nociceptive responses in second instar larvae and suppress expression of subdued (encoding a TMEM16 channel). Reduction of subdued expression in second instar C4da neurons not only increases thermal nociception but also decreases the response to ultraviolet light. Thus, steroid hormone signaling suppresses subdued expression to facilitate the sensory switch of C4da neurons. This regulation of a developmental sensory switch through steroid hormone regulation of channel expression raises the possibility that ion channel homeostasis is a key target for tuning the development of sensory modalities. |
| first_indexed | 2024-04-11T08:59:48Z |
| format | Article |
| id | doaj.art-bb6fa6b9b23b49e18e9b5d2d3d5be7b6 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T08:59:48Z |
| publishDate | 2022-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-bb6fa6b9b23b49e18e9b5d2d3d5be7b62022-12-22T04:32:49ZengeLife Sciences Publications LtdeLife2050-084X2022-03-011110.7554/eLife.76464Steroid hormone signaling activates thermal nociception during Drosophila peripheral nervous system developmentJacob S Jaszczak0https://orcid.org/0000-0003-3752-1152Laura DeVault1https://orcid.org/0000-0001-6801-5098Lily Yeh Jan2https://orcid.org/0000-0003-3938-8498Yuh Nung Jan3https://orcid.org/0000-0003-1367-6299Department of Physiology, Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States; Howard Hughes Medical Institute, Chevy Chase, United StatesDepartment of Physiology, Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States; Department of Developmental Biology, Washington University Medical School, Saint Louis, United StatesDepartment of Physiology, Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States; Howard Hughes Medical Institute, Chevy Chase, United StatesDepartment of Physiology, Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States; Howard Hughes Medical Institute, Chevy Chase, United StatesSensory neurons enable animals to detect environmental changes and avoid harm. An intriguing open question concerns how the various attributes of sensory neurons arise in development. Drosophila melanogaster larvae undergo a behavioral transition by robustly activating a thermal nociceptive escape behavior during the second half of larval development (third instar). The Class IV dendritic arborization (C4da) neurons are multimodal sensors which tile the body wall of Drosophila larvae and detect nociceptive temperature, light, and mechanical force. In contrast to the increase in nociceptive behavior in the third instar, we find that ultraviolet light-induced Ca2+ activity in C4da neurons decreases during the same period of larval development. Loss of ecdysone receptor has previously been shown to reduce nociception in third instar larvae. We find that ligand-dependent activation of ecdysone signaling is sufficient to promote nociceptive responses in second instar larvae and suppress expression of subdued (encoding a TMEM16 channel). Reduction of subdued expression in second instar C4da neurons not only increases thermal nociception but also decreases the response to ultraviolet light. Thus, steroid hormone signaling suppresses subdued expression to facilitate the sensory switch of C4da neurons. This regulation of a developmental sensory switch through steroid hormone regulation of channel expression raises the possibility that ion channel homeostasis is a key target for tuning the development of sensory modalities.https://elifesciences.org/articles/76464nociceptionecdysoneTMEM16 channelda neuronmultimodal sensory processingbehavior |
| spellingShingle | Jacob S Jaszczak Laura DeVault Lily Yeh Jan Yuh Nung Jan Steroid hormone signaling activates thermal nociception during Drosophila peripheral nervous system development eLife nociception ecdysone TMEM16 channel da neuron multimodal sensory processing behavior |
| title | Steroid hormone signaling activates thermal nociception during Drosophila peripheral nervous system development |
| title_full | Steroid hormone signaling activates thermal nociception during Drosophila peripheral nervous system development |
| title_fullStr | Steroid hormone signaling activates thermal nociception during Drosophila peripheral nervous system development |
| title_full_unstemmed | Steroid hormone signaling activates thermal nociception during Drosophila peripheral nervous system development |
| title_short | Steroid hormone signaling activates thermal nociception during Drosophila peripheral nervous system development |
| title_sort | steroid hormone signaling activates thermal nociception during drosophila peripheral nervous system development |
| topic | nociception ecdysone TMEM16 channel da neuron multimodal sensory processing behavior |
| url | https://elifesciences.org/articles/76464 |
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