Exogenous T3 mimics long day lengths in Siberian hamsters

2007 ◽  
Vol 292 (6) ◽  
pp. R2368-R2372 ◽  
Author(s):  
David A. Freeman ◽  
Brett J. W. Teubner ◽  
Carlesia D. Smith ◽  
Brian J. Prendergast

Siberian hamsters ( Phodopus sungorus) exhibit seasonal cycles of reproduction driven by changes in day length. Day length is encoded endogenously by the duration of nocturnal melatonin (Mel) secretion from the pineal gland. Short-duration Mel signals stimulate reproduction and long-duration signals inhibit reproduction. The mechanism by which Mel signals are decoded at the level of neural target tissues remains uncharacterized. In Siberian hamsters, exposure to short day lengths or injections of Mel in long days results in a decrease in hypothalamic expression of type 2 iodothyronine deiodinase (Dio2) mRNA. Dio2 catalyzes the conversion of the thyroid hormone thyroxine to triiodothyronine (T3). Thus exposure to short and long day lengths should decrease and increase hypothalamic T3 concentrations, respectively. We tested the hypothesis that exogenous T3 administered to short-day hamsters would mimic exposure to long day lengths with respect to gonadal stimulation. Hamsters gestated and raised in short day lengths that exhibited photoinhibition of the testes were given daily subutaneous injections of T3 or saline vehicle for 4 wk beginning at week 12 of life. The results indicate that exogenous T3 induced gonadal growth in short-day hamsters and delayed spontaneous gonadal development by an interval equal to the number of weeks during which T3 was administered. T3 injections delayed gonadal regression if given coincident with the transfer of hamsters from long to short day lengths. These results suggest that T3 mimics long day exposure in Siberian hamsters and may serve as an intermediate step between the Mel rhythm and the reproductive response.

2013 ◽  
Vol 304 (8) ◽  
pp. R628-R635 ◽  
Author(s):  
August Kampf-Lassin ◽  
Brian J. Prendergast

Perihypothalamic thyroid hormone signaling features prominently in the seasonal control of reproductive physiology. Triiodothyronine (T3) signaling stimulates gonadal development, and decrements in T3 signaling are associated with gonadal regression. Type 3 iodothyronine deiodinase (DIO3) converts the prohormone thyroxine (T4) 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.


Endocrinology ◽  
2013 ◽  
Vol 154 (2) ◽  
pp. 831-841 ◽  
Author(s):  
Brian J. Prendergast ◽  
Leah M. Pyter ◽  
August Kampf-Lassin ◽  
Priyesh N. Patel ◽  
Tyler J. Stevenson

Production of T3 in the mediobasal hypothalamus is critical for regulation of seasonal reproductive physiology. Type 2 iodothyronine deiodinase (DIO2) and DIO3 enzymes catalyze the prohormone T4 into biologically-active T3 and biologically-inactive rT3, respectively. In several seasonally-breeding vertebrates, DIO2 and DIO3 expression is implicated in photoperiod signal transduction in adulthood. These experiments tested the hypothesis that juvenile Siberian hamsters, which are highly responsive to photoperiod at weaning (postnatal day [PND]18), exhibit rapid and sustained changes in hypothalamic dio3 mRNA expression during photoperiod-induced and photoperiod-inhibited puberty. Hypothalamic dio2 and dio3 expression was measured via quantitative PCR in hamsters born and reared in a long-day photoperiod (15L:9D) and weaned on PND18 into short-day photoperiods (9L:15D). In SD males, hypothalamic dio3 mRNA was elevated 2.5-fold within 3 days (PND21) and continued to increase (>20-fold) through PND32; changes in dio3 mRNA preceded inhibition of gonadotropin (FSH) secretion and gonadal regression in SD. Females exhibited comparable dio3 responses to SD. In LD males, dio3 remained low and invariant from PND18–PND32. In contrast, dio2 mRNA rose conspicuously on PND21, independent of photoperiod, returning to basal levels thereafter. In LD, a single afternoon melatonin (MEL) injection on PND18 or PND20 was sufficient to increase hypothalamic dio3 mRNA, and dio3 increased in proportion to the number of successive days of MEL treatment. SD photoperiods and MEL exert rapid, sustained, and additive effects on hypothalamic dio3 mRNA, which may play a central role in inhibiting maturation of the peripubertal hypothalamo-pituitary-gonadal axis.


Endocrinology ◽  
2006 ◽  
Vol 147 (10) ◽  
pp. 4680-4687 ◽  
Author(s):  
Florent G. Revel ◽  
Michel Saboureau ◽  
Paul Pévet ◽  
Jens D. Mikkelsen ◽  
Valérie Simonneaux

In seasonal species, photoperiod organizes various physiological processes, including reproduction. Recent data indicate that the expression of type 2 iodothyronine deiodinase (Dio2) is modulated by photoperiod in the mediobasal hypothalamus of some seasonal species. Dio2 is believed to control the local synthesis of bioactive T3 to regulate gonadal response. Here we used in situ hybridization to study Dio2 expression in the hypothalamus of a photoperiodic rodent, the Syrian hamster. Dio2 was highly expressed in reproductively active hamsters in long day, whereas it was dramatically reduced in sexually inhibited hamsters maintained in short day. This contrasted with the laboratory rat, a nonphotoperiodic species, in which no evidence for Dio2 photoperiodic modulation was seen. We also demonstrate that photoperiodic variations of Dio2 expression in hamsters are independent from secondary changes in gonadal steroids. Studies in pinealectomized hamsters showed that the photoperiodic variation of Dio2 expression is melatonin dependent, and injections of long day hamsters with melatonin for only 7 d were sufficient to inhibit Dio2 expression to that of short day levels. Finally, because in some seasonal species thyroid hormones are involved in photorefractoriness, we examined Dio2 expression in short day-refractory hamsters and found that Dio2 mRNA levels remained low despite full reproductive recrudescence. Altogether, these results demonstrate that in the Syrian hamster Dio2 is photoperiodically modulated via a melatonin-dependent process. Furthermore, refractoriness to photoperiod in hamsters appears to occur independently of Dio2. These results raise new perspectives for understanding how thyroid hormones are involved in the control of photoperiodic neuroendocrine processes.


Endocrinology ◽  
2013 ◽  
Vol 154 (5) ◽  
pp. 1813-1819 ◽  
Author(s):  
George E. Bentley ◽  
Shanna Tucker ◽  
Heather Chou ◽  
Michaela Hau ◽  
Nicole Perfito

Abstract Timing of seasonal breeding in birds and mammals is regulated by changing the day length and is dependent on the presence of thyroid hormones. A mechanism for thyroid-dependent control of seasonality has been proposed, in which exposure to long day lengths induces rapid local conversion of T4 to its bioactive form, T3, via the up-regulation of the enzyme type 2 iodothyronine deiodinase (Dio2) in the brain, and the down-regulation of Dio3 (which inactivates T3). Such changes were correlated with gonadotropin release and gonadal growth in quail. This mechanism was elucidated in a domesticated species (quail) exposed to unnatural acute changes in day length. Here we investigated the Dio2/Dio3 mechanism in a wild species, the European starling, under naturally changing day length. Although Dio2 expression varied seasonally, Dio3 did not. We found no correlation of Dio2 with photoperiod, seasonal regulation of GnRH, or testicular volume. The observed differences in data from starlings and quail could be a result of phylogeny, genetic drift from founder populations, or differences in reproductive seasonality in addition to or instead of arising from domestication or use of artificially changing photoperiods. Overall, the data indicate that in a wild species exposed to natural changes in day length, the current proposed mechanism for photoperiodic timing is less straightforward than is generally accepted and might not be as universally applicable as previously thought.


1989 ◽  
Vol 257 (1) ◽  
pp. R142-R149 ◽  
Author(s):  
T. J. Bartness ◽  
J. A. Elliott ◽  
B. D. Goldman

Two experiments were designed to assess whether the short-day-induced patterns of shallow daily torpor, body weight, and other seasonal responses (food intake and pelage pigmentation) exhibited by Siberian hamsters (Phodopus sungorus sungorus) are under the control of a "seasonal timekeeping mechanism" that is independent of reproductive status [testosterone, (T)]. We examined whether the patterning and expression of these seasonal responses were altered by decreases in serum T that accompany gonadal regression during the first 8 wk of short-day exposure (i.e., the "preparatory phase" of the torpor season) or by experimental increases in serum T after this phase. Short-day-housed, castrated hamsters bearing T implants had long-day levels of the hormone and did not exhibit torpor. Appropriate seasonal patterns and levels of torpor, body weight, pelage color stage, and food intake were exhibited after T implant removal although serum T was clamped to long-day levels during the preparatory phase. In animals that were gonad intact during the preparatory phase and were subsequently castrated and given T implants, torpor did not occur as long as the implants were in place. However, the patterns and levels of daily torpor, food intake, and body weight rapidly returned to appropriate seasonal values compared with the castrated, blank-implanted controls on T implant removal; these effects occurred whether the T implants were removed when torpor frequency was increasing, at its peak, or decreasing across the torpor season. T did not affect pelage color stage under any condition.(ABSTRACT TRUNCATED AT 250 WORDS)


2003 ◽  
Vol 285 (4) ◽  
pp. R873-R879 ◽  
Author(s):  
Gregory E. Demas ◽  
Timothy J. Bartness ◽  
Randy J. Nelson ◽  
Deborah L. Drazen

Siberian hamsters ( Phodopus sungorus) rely on photoperiod to coordinate seasonally appropriate changes in physiology, including immune function. Immunity is regulated, in part, by the sympathetic nervous system (SNS), although the precise role of the SNS in regulating photoperiodic changes in immunity remains unspecified. The goal of the present study was to examine the contributions of norepinephrine (NE), the predominant neurotransmitter of the SNS, to photoperiodic changes in lymphocyte proliferation. In experiment 1, animals were maintained in long [16:8-h light-dark cycle (16:8 LD)] or short days (8:16 LD) for 10 wk, and splenic NE content was determined. In experiment 2, in vitro splenocyte proliferation in response to mitogenic stimulation (concanavalin A) was assessed in spleen cell suspensions taken from long- or short-day hamsters in which varying concentrations of NE were added to the cultures. In experiment 3, splenocyte proliferation was examined in the presence of NE and selective α- and β-noradrenergic receptor antagonists (phenoxybenzamine and propranolol, respectively) in vitro. Short-day animals had increased splenic NE content compared with long-day animals. Long-day animals had higher proliferation compared with short-day animals independent of NE. NE (1 μM) further suppressed splenocyte proliferation in short but not long days. Last, NE-induced suppression of proliferation in short-day hamsters was blocked by propranolol but not phenoxybenzamine. The present results suggest that NE plays a role in photoperiodic changes in lymphocyte proliferation. Additionally, the data suggest that the effects of NE on proliferation are specific to activation of β-adrenergic receptors located on splenic tissue. Collectively, these results provide further support that photoperiodic changes in immunity are influenced by changes in SNS activity.


1989 ◽  
Vol 257 (6) ◽  
pp. R1533-R1540 ◽  
Author(s):  
T. J. Bartness ◽  
J. M. Hamilton ◽  
G. N. Wade ◽  
B. D. Goldman

Siberian hamsters exhibit decreased body weight and fat after initial exposure to short photoperiods and increased body weight and fat after extended short photoperiod exposure. The purpose of the present experiments was to determine if uniform changes in white adipose tissue (WAT) pad weights and lipid metabolism correspond to these short photoperiod-induced changes in body fat. Carcass lipid content and testes and fat pad weights [retroperitoneal WAT (RWAT), epididymal WAT (EWAT), and inguinal and dorsal subcutaneous WAT, respectively] were decreased in male hamsters relative to their long day counterparts after 6 and 12 wk of short-day exposure. Moreover, EWAT and RWAT weight, EWAT specific lipoprotein lipase activity, and specific and total lipogenesis were disproportionately decreased relative to the subcutaneous fat pads. The changes in fat pad weight and metabolism were generally reversed coincident with the return to a long-day-like reproductive status after prolonged short-day exposure (24 and 30 wk). In a less detailed experiment, female Siberian hamsters had decreased body, fat pad, and uterine weights after 6 wk of short-day exposure; however, no fat pad-specific changes in weight were observed. The results of these experiments demonstrate that short-day-exposed male Siberian hamsters may be a useful model for examining mechanisms underlying fat pad-specific responses. In addition, gender appears to influence the pattern of short-day-induced lipid depletion in this species.


1997 ◽  
Vol 272 (1) ◽  
pp. R68-R77 ◽  
Author(s):  
M. M. Mauer ◽  
T. J. Bartness

Long-day (LD)-housed Siberian hamsters show compensatory increases in white adipose tissue (WAT) weight after lipectomy, whereas hamsters exposed to short days (SDs) for a long duration (22 wk) do not. We tested whether SD-induced body weight changes prevent fat pad compensation after lipectomy. In experiment 1, hamsters with lesions of the paraventricular nucleus of the hypothalamus (PVNx) rapidly increased body weight similarly to 22-wk SD-exposed hamsters. In experiment 2, LD-housed hamsters were food restricted for 22 wk and then pair fed with SD-housed hamsters for 12 wk to produce body weight changes mimicking those of ad libitum-fed SD-exposed animals. Epididymal WAT (EWAT) lipectomy (EWATx) of PVNx or food-restricted hamsters elicited compensatory increases in retroperitoneal and inguinal WAT (RWAT and IWAT) weights. Unlike other fat pads, EWAT was less affected by food restriction or PVNx than by SD exposure. In general, food restriction decreased adipocyte number, whereas SD exposure decreased adipocyte size. PVNx increased RWAT adipocyte size and IWAT adipocyte number. These results suggest that the lack of body fat compensation by EWATx hamsters exposed to SDs for a long duration is due to SD-associated responses other than body weight changes per se.


1999 ◽  
Vol 276 (3) ◽  
pp. R776-R781 ◽  
Author(s):  
John Dark ◽  
Daniel A. Lewis ◽  
Irving Zucker

We tested whether reduced blood glucose concentrations are necessary and sufficient for initiation of torpor in Siberian hamsters. During spontaneous torpor bouts, body temperature (Tb) decreases from the euthermic value of 37 to <31°C. Among hamsters that displayed torpor during maintenance in a short-day length (10 h light/day) at an air temperature of 15°C, blood glucose concentrations decreased significantly by 28% as Tb fell from 37 to <31°C and increased during rewarming so that by the time Tb first was >36°C, glucose concentrations had returned to the value preceding torpor. Hamsters did not display torpor when maintained in a long-day length (16 h light/day) and injected with a range of insulin doses (1–50 U/kg body mass), some of which resulted in sustained, pronounced hypoglycemia. We conclude that changes in blood glucose concentrations may be a consequence rather than a cause of the torpid state and question whether induction of torpor by 2-deoxy-d-glucose is due to its general glucoprivic actions.


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