Low Temperature-Induced Circulating Triiodothyronine Accelerates Seasonal Testicular Regression

Abstract

In temperate zones, animals restrict breeding to specific seasons to maximize the survival of their offspring. Birds have evolved highly sophisticated mechanisms of seasonal regulation, and their testicular mass can change 100-fold within a few weeks. Recent studies on Japanese quail revealed that seasonal gonadal development is regulated by central thyroid hormone activation within the hypothalamus, depending on the photoperiodic changes. By contrast, the mechanisms underlying seasonal testicular regression remain unclear. Here we show the effects of short day and low temperature on testicular regression in quail. Low temperature stimulus accelerated short day-induced testicular regression by shutting down the hypothalamus-pituitary-gonadal axis and inducing meiotic arrest and germ cell apoptosis. Induction of T3 coincided with the climax of testicular regression. Temporal gene expression analysis over the course of apoptosis revealed the suppression of LH response genes and activation of T3 response genes involved in amphibian metamorphosis within the testis. Daily ip administration of T3 mimicked the effects of low temperature stimulus on germ cell apoptosis and testicular mass. Although type 2 deiodinase, a thyroid hormone-activating enzyme, in the brown adipose tissue generates circulating T3 under low-temperature conditions in mammals, there is no distinct brown adipose tissue in birds. In birds, type 2 deiodinase is induced by low temperature exclusively in the liver, which appears to be caused by increased food consumption. We conclude that birds use low temperature-induced circulating T3 not only for adaptive thermoregulation but also to trigger apoptosis to accelerate seasonal testicular regression.

Different Photoperiodic Responses in Four Lines of Japanese Quail

“…Once the quail had been transferred to LD conditions, testes developed into fully mature size within 4 weeks in all lines (Fig. 1A) (Follett and Maung, 1978;Ikegami et al, 2015). The speed of testicular development of NIES-Br was faster than that of the AMRP line (Fig.…”

“…Hence, birds are often used as experimental animals in the photoperiodism research. In previous studies, we have uncovered the signal transduction pathway regulating seasonal testicular development and regression from photoreceptor to neuroendocrine output (Yoshimura et al, 2003;Nakao et al, 2008;Nakane et al, 2010;2014;Ikegami et al, 2015).…”

“…Recently, we investigated the mechanism of seasonal testicular regression using commercial quail (Ikegami et al, 2015). We noticed that the response of quail to SD conditions varied among quail obtained from different commercial dealers.…”

Effects of Dietary and Lighting Conditions on Diurnal Locomotor Activity and Body Temperature in Microminipigs

“…Pigs were anesthetized using ketamine (5 mg/kg), medetomidine (0.04 mg/kg), and midazolam (0.2 mg/kg), and local anesthesia at the neck (lidocaine). Then the BT recording module (Thermochron Type-SL, KN Laboratories, Inc., Osaka, Japan) was implanted in the neck subcutaneously behind the ear (25). In all studies, BT was recorded once per hour throughout the experiment.…”

“…However, to exclude the influence of ambient temperature, a probe placed in the body was used here. BT depends on the placement of the probe (25). In the present study, a location subcutaneously on the neck behind the ear was used for BT measurement.…”