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.

Fig. 1.

Values are expressed as means ± SE. A: paired testis weights. B: paired seminal vesicle weights. C: duration of nocturnal locomotor activity. Hypothalamic (D) dio3 and (E) dio2 mRNA expression of adult male Siberian hamsters after 6 wk of exposure to long- (LD), intermediate- (IntD), or short-duration (SD) photoperiods is shown. Group abbreviations indicate photoperiod treatments prior to and following experimental week 0. LD-LD (n = 6) and LD-SD (n = 14) hamsters were reared in a LD photoperiod (15L:9D) and subsequently exposed to LD and SD (12L:12D) photoperiods, respectively. LD-IntD (n = 9) and IntD-IntD (n = 16) were reared in LD and IntD photoperiods, respectively, and on week 0 were transferred to an IntD (13.5L:10.5D) photoperiod. SD-NR designates hamsters (n = 7) that failed to exhibit gonadal regression in SD. *P < 0.05, **P < 0.01, ***P < 0.001 vs. LD-LD value. #P < 0.05, ##P < 0.01, ###P < 0.001 vs. IntD-IntD value. †P < 0.05, †††P < 0.001 vs. LD-SD value.

Fig. 2.

Values are expressed as means ± se. A: paired testis weights. B: paired seminal vesicle weights. Hypothalamic dio3 (C) and dio2 (D) mRNA expression of adult male Siberian hamsters gestated and reared in an intermediate-duration (IntD) photoperiod. Hamsters were classified as having undeveloped (n = 5), moderately developed (n = 19), or fully developed (n = 8) testes based on paired testis weights at autopsy (see results for criteria). C: horizontal lines indicate means ± se hypothalamic dio3 mRNA expression in LD-LD and LD-SD groups. ***P < 0.001 vs. all other groups.

Fig. 3.

Linear regression between paired testis weight (A and B) and paired seminal vesicle weight (C and D) and hypothalamic dio3 and dio2 mRNA expression in adult male Siberian hamsters (n = 32) gestated and reared in an intermediate-duration (IntD) photoperiod.