Orchestration of gene expression across the seasons: Hypothalamic gene expression in natural photoperiod throughout the year in the Siberian hamster

Abstract

In nature Siberian hamsters utilize the decrement in day length following the summer solstice to implement physiological adaptations in anticipation of the forthcoming winter, but also exploit an intrinsic interval timer to initiate physiological recrudescence following the winter solstice. However, information is lacking on the temporal dynamics in natural photoperiod of photoperiodically regulated genes and their relationship to physiological adaptations. To address this, male Siberian hamsters born and maintained outdoors were sampled every month over the course of one year. As key elements of the response to photoperiod, thyroid hormone signalling components were assessed in the hypothalamus. From maximum around the summer solstice (late-June), Dio2 expression rapidly declined in advance of physiological adaptations. This was followed by a rapid increase in Mct8 expression (T3/T4 transport), peaking early-September before gradually declining to minimum expression by the following June. Dio3 showed a transient peak of expression beginning late-August. A recrudescence of testes and body mass occurred from mid-February, but Dio2 expression remained low until late-April of the following year, converging with the time of year when responsiveness to short-day length is re-established. Other photoperiodically regulated genes show temporal regulation, but of note is a transient peak in Gpr50 around late-July.

A unifying hypothesis for control of body weight and reproduction in seasonally breeding mammals

“…Dio2 and 3 are key enzymes that regulate thyroid hormone bioactivity. An overt increase in hypothalamic T3 levels in response to long day has been observed in the quail, 18 whereas, in F344 rats, changes in T3 in response to a long photoperiod are subtler, despite large changes in 22,40,48 and, in the F344 rats, Oatp1c1 is more highly expressed in long photoperiod. 36 Thus, the expression of Dio2 and Dio3 enzymes provide a key molecular step to regulate the local hypothalamic availability of T3.…”

“…48 Clearly, temporal organisation is a key element for the function of each gene, but it is also important to note that, in the Petri et al experiments, hamsters were housed outside in natural photoperiod and ambient temperatures.…”

“…96,98 These results suggest that the mode and time-course of the knockout is key to determining the phenotypic outcome. 48 We propose that a decrease in T3 as a result of a decline By regulating the balance between neurodegeneration and neurogenesis, it is proposed that the population of AgRP neurones is maintained at a steady level so that there are no overall changes to energy balance.…”

An integrative view of mammalian seasonal neuroendocrinology

“…TSH directly up‐regulates the expression of Dio2 and, although there is evidence for Dio3 down‐regulation as well, the underlying mechanism remains unknown . Strong evidence in sheep and hamsters shows that rapid activation/deactivation of this axis is sufficient to prime long‐term seasonal changes in physiology . However, the long‐term dynamics of these responses differ between species.…”

“…Clearly, more sophisticated experimental tools will be necessary to understand better the seasonal function of this peptidergic system. Another peptidergic system worthy of further study is somatostatin because hypothalamic expression of this gene decreases markedly in LP in Siberian hamsters, then increases in SP, and expression is down‐regulated by i.c.v. infusion of TSH in hamsters, suggesting again that it is a target of tanycyte‐produced TH .…”