Sperm Affects Head Sensory Neuron in Temperature Tolerance of Caenorhabditis elegans
Tolerance to environmental temperature change is essential for the survival and proliferation of animals. The process is controlled by various body tissues, but the orchestration of activity within the tissue network has not been elucidated in detail. Here, we show that sperm affects the activity of...
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| Format: | Article |
| Language: | English |
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Elsevier
2016-06-01
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| Series: | Cell Reports |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S221112471630691X |
| _version_ | 1819088529571971072 |
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| author | Satoru Sonoda Akane Ohta Ayana Maruo Tomoyo Ujisawa Atsushi Kuhara |
| author_facet | Satoru Sonoda Akane Ohta Ayana Maruo Tomoyo Ujisawa Atsushi Kuhara |
| author_sort | Satoru Sonoda |
| collection | DOAJ |
| description | Tolerance to environmental temperature change is essential for the survival and proliferation of animals. The process is controlled by various body tissues, but the orchestration of activity within the tissue network has not been elucidated in detail. Here, we show that sperm affects the activity of temperature-sensing neurons (ASJ) that control cold tolerance in Caenorhabditis elegans. Genetic impairment of sperm caused abnormal cold tolerance, which was unexpectedly restored by impairment of temperature signaling in ASJ neurons. Calcium imaging revealed that ASJ neuronal activity in response to temperature was decreased in sperm mutant gsp-4 with impaired protein phosphatase 1 and rescued by expressing gsp-4 in sperm. Genetic analysis revealed a feedback network in which ASJ neuronal activity regulates the intestine through insulin and a steroid hormone, which then affects sperm and, in turn, controls ASJ neuronal activity. Thus, we propose that feedback between sperm and a sensory neuron mediating temperature tolerance. |
| first_indexed | 2024-12-21T21:53:29Z |
| format | Article |
| id | doaj.art-ae20a7de8d854421b7d670410ad39426 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-12-21T21:53:29Z |
| publishDate | 2016-06-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-ae20a7de8d854421b7d670410ad394262022-12-21T18:49:01ZengElsevierCell Reports2211-12472016-06-01161566510.1016/j.celrep.2016.05.078Sperm Affects Head Sensory Neuron in Temperature Tolerance of Caenorhabditis elegansSatoru Sonoda0Akane Ohta1Ayana Maruo2Tomoyo Ujisawa3Atsushi Kuhara4Laboratory of Molecular and Cellular Regulation, Faculty of Science and Engineering, and Institute for Integrative Neurobiology, Konan University, 8-9-1 Okamoto, Higashinada-ku, Kobe 658-8501, JapanLaboratory of Molecular and Cellular Regulation, Faculty of Science and Engineering, and Institute for Integrative Neurobiology, Konan University, 8-9-1 Okamoto, Higashinada-ku, Kobe 658-8501, JapanLaboratory of Molecular and Cellular Regulation, Faculty of Science and Engineering, and Institute for Integrative Neurobiology, Konan University, 8-9-1 Okamoto, Higashinada-ku, Kobe 658-8501, JapanLaboratory of Molecular and Cellular Regulation, Faculty of Science and Engineering, and Institute for Integrative Neurobiology, Konan University, 8-9-1 Okamoto, Higashinada-ku, Kobe 658-8501, JapanLaboratory of Molecular and Cellular Regulation, Faculty of Science and Engineering, and Institute for Integrative Neurobiology, Konan University, 8-9-1 Okamoto, Higashinada-ku, Kobe 658-8501, JapanTolerance to environmental temperature change is essential for the survival and proliferation of animals. The process is controlled by various body tissues, but the orchestration of activity within the tissue network has not been elucidated in detail. Here, we show that sperm affects the activity of temperature-sensing neurons (ASJ) that control cold tolerance in Caenorhabditis elegans. Genetic impairment of sperm caused abnormal cold tolerance, which was unexpectedly restored by impairment of temperature signaling in ASJ neurons. Calcium imaging revealed that ASJ neuronal activity in response to temperature was decreased in sperm mutant gsp-4 with impaired protein phosphatase 1 and rescued by expressing gsp-4 in sperm. Genetic analysis revealed a feedback network in which ASJ neuronal activity regulates the intestine through insulin and a steroid hormone, which then affects sperm and, in turn, controls ASJ neuronal activity. Thus, we propose that feedback between sperm and a sensory neuron mediating temperature tolerance.http://www.sciencedirect.com/science/article/pii/S221112471630691XCaenorhabditis eleganscold tolerancetemperature tolerancesperm |
| spellingShingle | Satoru Sonoda Akane Ohta Ayana Maruo Tomoyo Ujisawa Atsushi Kuhara Sperm Affects Head Sensory Neuron in Temperature Tolerance of Caenorhabditis elegans Cell Reports Caenorhabditis elegans cold tolerance temperature tolerance sperm |
| title | Sperm Affects Head Sensory Neuron in Temperature Tolerance of Caenorhabditis elegans |
| title_full | Sperm Affects Head Sensory Neuron in Temperature Tolerance of Caenorhabditis elegans |
| title_fullStr | Sperm Affects Head Sensory Neuron in Temperature Tolerance of Caenorhabditis elegans |
| title_full_unstemmed | Sperm Affects Head Sensory Neuron in Temperature Tolerance of Caenorhabditis elegans |
| title_short | Sperm Affects Head Sensory Neuron in Temperature Tolerance of Caenorhabditis elegans |
| title_sort | sperm affects head sensory neuron in temperature tolerance of caenorhabditis elegans |
| topic | Caenorhabditis elegans cold tolerance temperature tolerance sperm |
| url | http://www.sciencedirect.com/science/article/pii/S221112471630691X |
| work_keys_str_mv | AT satorusonoda spermaffectsheadsensoryneuronintemperaturetoleranceofcaenorhabditiselegans AT akaneohta spermaffectsheadsensoryneuronintemperaturetoleranceofcaenorhabditiselegans AT ayanamaruo spermaffectsheadsensoryneuronintemperaturetoleranceofcaenorhabditiselegans AT tomoyoujisawa spermaffectsheadsensoryneuronintemperaturetoleranceofcaenorhabditiselegans AT atsushikuhara spermaffectsheadsensoryneuronintemperaturetoleranceofcaenorhabditiselegans |