Abstract
The annual cycle of changing day length (photoperiod) is widely used by animals to synchronise their biology to environmental seasonality. In mammals, melatonin is the key hormonal relay for the photoperiodic message, governing thyroid-stimulating hormone (TSH) production in the pars tuberalis (PT) of the pituitary stalk. TSH acts on neighbouring hypothalamic cells known as tanycytes, which in turn control hypothalamic function through effects on thyroid hormone (TH) signalling, mediated by changes in expression of the type II and III deiodinases (Dio2 and Dio3, respectively). Among seasonally breeding rodents, voles of the genus Microtus are notable for a high degree of sensitivity to nutritional and social cues, which act in concert with photoperiod to control reproductive status. In the present study, we investigated whether the TSH/Dio2/Dio3 signalling pathway of female common voles (Microtus arvalis) shows a similar degree of photoperiodic sensitivity to that described in other seasonal mammal species. Additionally, we sought to determine whether the plant metabolite 6-methoxy-2-benzoxazolinone (6-MBOA), described previously as promoting reproductive activation in voles, had any influence on the TSH/Dio2/Dio3 system. Our data demonstrate a high degree of photoperiodic sensitivity in this species, with no observable effects of 6-MBOA on upstream pituitary/hypothalamic gene expression. Further studies are required to characterise how photoperiodic and nutritional signals interact to modulate hypothalamic TH signalling pathways in mammals.
Highlights
Timing of seasonal breeding in animals has important fitness consequences, because it affects both offspring survival and the chance of survival of parents to the breeding event
This region is noted for photoperiodic expression of the orphan melatonin-related receptor GPR50 [3], which has been linked to metabolic rate in mice [4,24]
The levels of TSHb and Dio2 expression were regulated by photoperiod, with high levels in voles exposed to summer photoperiod, and minimal or undetectable levels of expression under winter or spring photoperiods
Summary
Timing of seasonal breeding in animals has important fitness consequences, because it affects both offspring survival and the chance of survival of parents to the breeding event. The annual change in day length (photoperiod) provides animals with the most reliable information on the time of year and forthcoming season [18,23]. Recent work has demonstrated that melatonin acts through type 1 melatonin receptors (MT1) localised in the pars tuberalis (PT) of the anterior pituitary gland to control thyroid hormone action in the hypothalamus, leading to changes in seasonal. This involves the release of thyroid-stimulating hormone (TSH, a heterodimeric complex of a common glycoprotein hormone a-subunit and specific TSHb-subunit) from the PT, at levels that increase in long photoperiod and decrease in short photoperiod, mainly due to changes in TSHb gene expression [13]. The balance between Dio and Dio determines local concentrations of T3 in the mediobasal hypothalamus (MBH) and seasonal changes in the activity of the hypothalamo-pituitary–gonadal axis
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