G protein-coupled receptor-based thermosensation determines temperature acclimatization of Caenorhabditis elegans
Abstract Animals must sense and acclimatize to environmental temperatures for survival, yet their thermosensing mechanisms other than transient receptor potential (TRP) channels remain poorly understood. We identify a trimeric G protein-coupled receptor (GPCR), SRH-40, which confers thermosensitivit...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-02-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-46042-z |
| _version_ | 1827327015546519552 |
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| author | Kohei Ohnishi Takaaki Sokabe Toru Miura Makoto Tominaga Akane Ohta Atsushi Kuhara |
| author_facet | Kohei Ohnishi Takaaki Sokabe Toru Miura Makoto Tominaga Akane Ohta Atsushi Kuhara |
| author_sort | Kohei Ohnishi |
| collection | DOAJ |
| description | Abstract Animals must sense and acclimatize to environmental temperatures for survival, yet their thermosensing mechanisms other than transient receptor potential (TRP) channels remain poorly understood. We identify a trimeric G protein-coupled receptor (GPCR), SRH-40, which confers thermosensitivity in sensory neurons regulating temperature acclimatization in Caenorhabditis elegans. Systematic knockdown of 1000 GPCRs by RNAi reveals GPCRs involved in temperature acclimatization, among which srh-40 is highly expressed in the ADL sensory neuron, a temperature-responsive chemosensory neuron, where TRP channels act as accessorial thermoreceptors. In vivo Ca2+ imaging demonstrates that an srh-40 mutation reduced the temperature sensitivity of ADL, resulting in supranormal temperature acclimatization. Ectopically expressing SRH-40 in a non-warmth-sensing gustatory neuron confers temperature responses. Moreover, temperature-dependent SRH-40 activation is reconstituted in Drosophila S2R+ cells. Overall, SRH-40 may be involved in thermosensory signaling underlying temperature acclimatization. We propose a dual thermosensing machinery through a GPCR and TRP channels in a single sensory neuron. |
| first_indexed | 2024-03-07T14:53:51Z |
| format | Article |
| id | doaj.art-bd908bf5ad7945a0bc9364b20fcf2161 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-07T14:53:51Z |
| publishDate | 2024-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-bd908bf5ad7945a0bc9364b20fcf21612024-03-05T19:33:18ZengNature PortfolioNature Communications2041-17232024-02-0115111310.1038/s41467-024-46042-zG protein-coupled receptor-based thermosensation determines temperature acclimatization of Caenorhabditis elegansKohei Ohnishi0Takaaki Sokabe1Toru Miura2Makoto Tominaga3Akane Ohta4Atsushi Kuhara5Graduate school of Natural Science, Konan UniversityDivision of Cell Signaling, National Institute for Physiological SciencesFaculty of Science and Engineering, Konan UniversityDivision of Cell Signaling, National Institute for Physiological SciencesGraduate school of Natural Science, Konan UniversityGraduate school of Natural Science, Konan UniversityAbstract Animals must sense and acclimatize to environmental temperatures for survival, yet their thermosensing mechanisms other than transient receptor potential (TRP) channels remain poorly understood. We identify a trimeric G protein-coupled receptor (GPCR), SRH-40, which confers thermosensitivity in sensory neurons regulating temperature acclimatization in Caenorhabditis elegans. Systematic knockdown of 1000 GPCRs by RNAi reveals GPCRs involved in temperature acclimatization, among which srh-40 is highly expressed in the ADL sensory neuron, a temperature-responsive chemosensory neuron, where TRP channels act as accessorial thermoreceptors. In vivo Ca2+ imaging demonstrates that an srh-40 mutation reduced the temperature sensitivity of ADL, resulting in supranormal temperature acclimatization. Ectopically expressing SRH-40 in a non-warmth-sensing gustatory neuron confers temperature responses. Moreover, temperature-dependent SRH-40 activation is reconstituted in Drosophila S2R+ cells. Overall, SRH-40 may be involved in thermosensory signaling underlying temperature acclimatization. We propose a dual thermosensing machinery through a GPCR and TRP channels in a single sensory neuron.https://doi.org/10.1038/s41467-024-46042-z |
| spellingShingle | Kohei Ohnishi Takaaki Sokabe Toru Miura Makoto Tominaga Akane Ohta Atsushi Kuhara G protein-coupled receptor-based thermosensation determines temperature acclimatization of Caenorhabditis elegans Nature Communications |
| title | G protein-coupled receptor-based thermosensation determines temperature acclimatization of Caenorhabditis elegans |
| title_full | G protein-coupled receptor-based thermosensation determines temperature acclimatization of Caenorhabditis elegans |
| title_fullStr | G protein-coupled receptor-based thermosensation determines temperature acclimatization of Caenorhabditis elegans |
| title_full_unstemmed | G protein-coupled receptor-based thermosensation determines temperature acclimatization of Caenorhabditis elegans |
| title_short | G protein-coupled receptor-based thermosensation determines temperature acclimatization of Caenorhabditis elegans |
| title_sort | g protein coupled receptor based thermosensation determines temperature acclimatization of caenorhabditis elegans |
| url | https://doi.org/10.1038/s41467-024-46042-z |
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