Hypothalamic Ventricular Ependymal Thyroid Hormone Deiodinases Are an Important Element of Circannual Timing in the Siberian Hamster (Phodopus sungorus)

Annika Herwig,Matei Bolborea,Julian G. Mercer,Dana Wilson,Francis J. P. Ebling,Emmely M. de Vries,Perry Barrett,Peter J. Morgan,Eric M. Mintz

doi:10.1371/journal.pone.0062003

Annika Herwig, Matei Bolborea + Show 7 more

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https://doi.org/10.1371/journal.pone.0062003

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Abstract

Exposure to short days (SD) induces profound changes in the physiology and behaviour of Siberian hamsters, including gonadal regression and up to 30% loss in body weight. In a continuous SD environment after approximately 20 weeks, Siberian hamsters spontaneously revert to a long day (LD) phenotype, a phenomenon referred to as the photorefractory response. Previously we have identified a number of genes that are regulated by short photoperiod in the neuropil and ventricular ependymal (VE) cells of the hypothalamus, although their importance and contribution to photoperiod induced physiology is unclear. In this refractory model we hypothesised that the return to LD physiology involves reversal of SD expression levels of key hypothalamic genes to their LD values and thereby implicate genes required for LD physiology. Male Siberian hamsters were kept in either LD or SD for up to 39 weeks during which time SD hamster body weight decreased before increasing, after more than 20 weeks, back to LD values. Brain tissue was collected between 14 and 39 weeks for in situ hybridization to determine hypothalamic gene expression. In VE cells lining the third ventricle, expression of nestin, vimentin, Crbp1 and Gpr50 were down-regulated at 18 weeks in SD photoperiod, but expression was not restored to the LD level in photorefractory hamsters. Dio2, Mct8 and Tsh-r expression were altered by SD photoperiod and were fully restored, or even exceeded values found in LD hamsters in the refractory state. In hypothalamic nuclei, expression of Srif and Mc3r mRNAs was altered at 18 weeks in SD, but were similar to LD expression values in photorefractory hamsters. We conclude that in refractory hamsters not all VE cell functions are required to establish LD physiology. However, thyroid hormone signalling from ependymal cells and reversal of neuronal gene expression appear to be essential for the SD refractory response.

Highlights

The Siberian hamster’s natural habitat ranges from the Steppes of Kazakhstan to Mongolia and southern Siberia
Post-hoc test was carried out which showed within the long day (LD) group body weight remained unchanged, whereas a significant increase occurred within short days (SD) group between week 18 and week 37 (Tukey p = 0.011)
This cohort of hamsters constituted a group to analyse gene expression changes during the course of restoration to LD physiology

Summary

Introduction

The Siberian hamster’s natural habitat ranges from the Steppes of Kazakhstan to Mongolia and southern Siberia. Body weight and reproduction peak during the long days of late spring-early summer, whereas appetite and body weight are reduced and reproduction ceases during the shorter days of autumn and early winter [1,2] These adaptations are driven by the annual cycle in photoperiod and can be induced in the artificial environment of the laboratory by changing photoperiod from a long day length (LD) to a short day length (SD). Spontaneous reversal of physiology and behavior will occur if Siberian hamsters are held in SD for a period of more than 20 weeks [3,4,5,6,7,8] This phenomenon is referred to as the photorefractory response and maybe regarded as a manifestation of an innate long-term (circannual) timing mechanism. The mechanism underlying long term or circannual timing is not known

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