Photoperiod history-dependent responses to intermediate day lengths engage hypothalamic iodothyronine deiodinase type III mRNA expression

Abstract

Perihypothalamic thyroid hormone signaling features prominently in the seasonal control of reproductive physiology. Triiodothyronine (T(3)) signaling stimulates gonadal development, and decrements in T(3) signaling are associated with gonadal regression. Type 3 iodothyronine deiodinase (DIO3) converts the prohormone thyroxine (T(4)) into biologically inactive 3,3',5'-triiodothyronine, and in long-day breeding Siberian hamsters exposure to long (LD) and short (SD) photoperiods, respectively, inhibit and stimulate hypothalamic dio3 mRNA expression. Reproductive responses to intermediate-duration photoperiods (IntD) occur in a history-dependent manner; IntDs are interpreted as inhibitory only when preceded by longer photoperiods. Because dio3 expression has only been evaluated under LD or SD photoperiods, it is not known whether hypothalamic dio3 encodes absolute photoperiod duration or the reproductive interpretation of photoperiod. Male Siberian hamsters with and without a prior history of LD were exposed to IntD photoperiods, and hypothalamic dio3 mRNA expression was measured 6 wk later. Hamsters with a LD photoperiod history exhibited gonadal regression in IntD and a marked upregulation of hypothalamic dio3 expression, whereas in hamsters without prior exposure to LD, gonadal responses to IntD were absent, and dio3 expression remained low. Patterns of deiodinase expression in hamsters maintained in chronic IntD photoperiods did not appear to reflect feedback effects of gonadal status. Hypothalamic expression of dio3 does not exclusively reflect ambient photoperiod, but rather the context-dependent reproductive interpretation of photoperiod. Neuroendocrine mechanisms that compare current and prior photoperiods, which permit detection of directional changes in day length, occur either upstream, or at the level, of hypothalamic dio3 expression.

A domestication related mutation in the thyroid stimulating hormone receptor gene (TSHR) modulates photoperiodic response and reproduction in chickens

“…Hamsters transferred from LD (15/9 light/dark) to intermediate-duration (13.5/10.5 light/dark) photoperiods showed increased levels of DIO3 expression and exhibited gonadal regression, whereas those with no prior exposure to LD showed no increased DIO3 expression or gonadal regression in intermediate-duration photoperiods (Kampf-Lassin and Prendergast, 2013b). Hence, the length of the intermediate photoperiod for our TSHR birds at 12/12 light/dark was perhaps not sufficient to induce DIO3 expression and therefore comparable to the absent prior exposure as described for the hamsters (Kampf-Lassin and Prendergast, 2013b). If elevated expression of DIO3 is sufficient to terminate reproduction, as suggested from the NDL-RJF/WL data, the absent induction of DIO3 expression could explain why all birds were still in an active laying phase by the end of the study.…”

Maternal photoperiodic programming enlightens the internal regulation of thyroid‐hormone deiodinases in tanycytes

“…Adult Siberian hamsters transferred from LP or SP to IP show history‐dependent changes in hypothalamic dio3 gene expression, reflecting the subjective interpretation of the photoperiodic signal, rather than its actual duration. This was the first indication that hypothalamic TH signalling reflects photoperiodic history dependence …”

Acute downregulation of Type II and Type III iodothyronine deiodinases by photoperiod in peripubertal male and female Siberian hamsters

“…In the same report, no effect of photoperiod on hypothalamic dio2 expression was detected between PND 18–32; although mean levels of dio2 mRNA were quantitatively greater in both males and females housed in LD, these differences were not statistically different from those of SD hamsters (Prendergast et al, 2013). Several other reports have likewise failed to resolve effects of photoperiod on dio2 mRNA in the hamster hypothalamus (Barrett et al, 2007; Kampf-Lassin & Prendergast, 2013; Stevenson & Prendergast, in review; Watanabe et al, 2007). This is in marked contrast to the present study, in which dio2 mRNA was > 2-fold higher in LD relative to SD hamsters.…”

“…In Siberian hamsters, a canonical mammalian model for dissecting mechanisms of seasonal timekeeping, hypothalamic dio3 mRNA levels increase markedly following exposure to reproductively-inhibitory SD photoperiods (Barrett et al, 2007; Kampf-Lassin & Prendergast, 2013; Prendergast et al, 2013; Watanabe et al, 2007; Watanabe et al, 2004). In mammals, SD photoperiods are internalized by a lengthening of the duration of nocturnal pineal melatonin (MEL) secretion (Bartness & Goldman, 1988; Hoffman & Reiter, 1965; review, see Goldman, 2001).…”

“…Photoperiodically-induced changes in hypothalamic dio2 expression have been well-documented in Syrian hamsters ( Mesocricetus auratus ; Yasuo et al, 2009) and in Japanese quail (Watanabe et al, 2007), but dio2 responses to photoperiod appear to be of little reproductive consequence in European starlings (Bentley et al, 2013) and have yet to be consistently established in Siberian hamsters. Several studies using standard photoperiod treatments have failed to identify effects of photoperiod on dio2 expression (Barrett et al, 2007, Kampf-Lassin et al, 2013; Prendergast et al, 2013). Two earlier reports identified a robust increase in perihypothalamic dio2 expression after transfer from SD to LD for 2 weeks (Watanabe et al, 2007; Watanabe et al, 2004).…”