Sperm Affects Head Sensory Neuron in Temperature Tolerance of Caenorhabditis elegans

• Published in: Cell reports (Cambridge) 2016-06, Vol.16 (1), p.56-65
• Main Authors: Sonoda, Satoru, Ohta, Akane, Maruo, Ayana, Ujisawa, Tomoyo, Kuhara, Atsushi
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological; Animals; Caenorhabditis elegans; Caenorhabditis elegans - physiology; Caenorhabditis elegans Proteins - metabolism; Calcium - metabolism; Cold Temperature; cold tolerance; Head; Intestines - physiology; Male; Models, Biological; Organ Specificity; Receptors, Cell Surface - metabolism; Sensory Receptor Cells - physiology; Signal Transduction; sperm; Spermatozoa - physiology; Steroids - metabolism; temperature tolerance
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2016.05.078

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. [Display omitted] •PP1 in sperm is required for cold tolerance•Sperm is downstream of intestinal insulin signaling in cold tolerance•Sperm affects the activity of ASJ temperature-sensing neurons•Steroid-hormone receptors are required for tissue network of cold tolerance Sonoda et al. find a feedback network between sperm and neurons in cold tolerance of Caenorhabditis elegans. ASJ temperature-sensing neurons regulate the intestine through insulin and steroid hormone, which then affects sperm, which, in turn, controls ASJ neuronal activity.