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 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.
Laboratory 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, Japan.
Satoru
S
Sonoda
Laboratory 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, Japan. Electronic address: aohta@center.konan-u.ac.jp.
Akane
A
Ohta
Laboratory 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, Japan.
Ayana
A
Maruo
Laboratory 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, Japan.
Tomoyo
T
Ujisawa
Laboratory 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, Japan. Electronic address: kuhara@center.konan-u.ac.jp.
Atsushi
A
Kuhara
D000222:Adaptation, Physiological; D000818:Animals; D017173:Caenorhabditis elegans / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism; D002118:Calcium / Q000378:metabolism; D003080:Cold Temperature; D006257:Head; D007422:Intestines / Q000502:physiology; D008297:Male; D008954:Models, Biological; D009928:Organ Specificity; D011956:Receptors, Cell Surface / Q000378:metabolism; D011984:Sensory Receptor Cells / Q000502:physiology*; D015398:Signal Transduction; D013094:Spermatozoa / Q000502:physiology*; D013256:Steroids / Q000378:metabolism
D029742:Caenorhabditis elegans Proteins; D011956:Receptors, Cell Surface; D013256:Steroids; D002118:Calcium
Caenorhabditis elegans; cold tolerance; sperm; temperature tolerance