Seasonal mammals register photoperiodic changes through the photoneuroendocrine system enabling them to time seasonal changes in growth, metabolism, and reproduction. To a varying extent, proximate ...environmental factors like ambient temperature (Ta) modulate timing of seasonal changes in physiology, conferring adaptive flexibility. While the molecular photoneuroendocrine pathway governing the seasonal responses is well defined, the mechanistic integration of nonphotoperiodic modulatory cues is poorly understood. Here, we explored the interaction between Ta and photoperiod in tundra voles, Microtus oeconomus, a boreal species in which the main impact of photoperiod is on postnatal somatic growth. We demonstrate that postweaning growth potential depends on both gestational and postweaning patterns of photoperiodic exposure, with the highest growth potential seen in voles experiencing short (8 h) gestational and long (16 h) postweaning photoperiods—corresponding to a spring growth program. Modulation by Ta was asymmetric: low Ta (10 °C) enhanced the growth potential of voles gestated on short photoperiods independent of postweaning photoperiod exposure, whereas in voles gestated on long photoperiods, showing a lower autumn-programmed growth potential, the effect of Ta was highly dependent on postweaning photoperiod. Analysis of the primary molecular elements involved in the expression of a neuroendocrine response to photoperiod, thyrotropin beta subunit (tshβ) in the pars tuberalis, somatostatin (srif) in the arcuate nucleus, and type 2/3 deiodinase (dio2/dio3) in the mediobasal hypothalamus identified dio2 as the most Ta-sensitive gene across the study, showing increased expression at higher Ta, while higher Ta reduced somatostatin expression. Contrastingly dio3 and tshβ were largely insensitive to Ta. Overall, these observations reveal a complex interplay between Ta and photoperiodic control of postnatal growth in M. oeconomus, and suggest that integration of Ta into the control of growth occurs downstream of the primary photoperiodic response cascade revealing potential adaptivity of small herbivores facing rising temperatures at high latitudes.
The evidence that diel patterns of physiology and behaviour in mammals are governed by circadian 'clocks' is based almost entirely on studies of nocturnal rodents. The emergent circadian paradigm, ...however, neglects the roles of energy metabolism and alimentary function (feeding and digestion) as determinants of activity pattern. The temporal control of activity varies widely across taxa, and ungulates, microtine rodents, and insectivores provide examples in which circadian timekeeping is vestigial. The nocturnal rodent/human paradigm of circadian organisation is unhelpful when considering the broader manifestation of activity patterns in mammals.
Epidemiological and experimental evidence correlates adverse intrauterine conditions with the onset of disease later in life. For a fetus to achieve a successful transition to extrauterine life, a ...myriad of temporally integrated humoral/biophysical signals must be accurately provided by the mother. We and others have shown the existence of daily rhythms in the fetus, with peripheral clocks being entrained by maternal cues, such as transplacental melatonin signaling. Among developing tissues, the fetal hippocampus is a key structure for learning and memory processing that may be anticipated as a sensitive target of gestational chronodisruption. Here, we used pregnant rats exposed to constant light treated with or without melatonin as a model of gestational chronodisruption, to investigate effects on the putative fetal hippocampus clock, as well as on adult offspring's rhythms, endocrine and spatial memory outcomes. The hippocampus of fetuses gestated under light:dark photoperiod (12:12 LD) displayed daily oscillatory expression of the clock genes Bmal1 and Per2, clock-controlled genes Mtnr1b, Slc2a4, Nr3c1 and NMDA receptor subunits 1B-3A-3B. In contrast, in the hippocampus of fetuses gestated under constant light (LL), these oscillations were suppressed. In the adult LL offspring (reared in LD during postpartum), we observed complete lack of day/night differences in plasma melatonin and decreased day/night differences in plasma corticosterone. In the adult LL offspring, overall hippocampal day/night difference of gene expression was decreased, which was accompanied by a significant deficit of spatial memory. Notably, maternal melatonin replacement to dams subjected to gestational chronodisruption prevented the effects observed in both, LL fetuses and adult LL offspring. Collectively, the present data point to adverse effects of gestational chronodisruption on long-term cognitive function; raising challenging questions about the consequences of shift work during pregnancy. The present study also supports that developmental plasticity in response to photoperiodic cues may be modulated by maternal melatonin.
Thyroid hormone and seasonal rhythmicity Dardente, Hugues; Hazlerigg, David G; Ebling, Francis J P
Frontiers in endocrinology (Lausanne),
01/2014, Letnik:
5
Journal Article
Recenzirano
Odprti dostop
Living organisms show seasonality in a wide array of functions such as reproduction, fattening, hibernation, and migration. At temperate latitudes, changes in photoperiod maintain the alignment of ...annual rhythms with predictable changes in the environment. The appropriate physiological response to changing photoperiod in mammals requires retinal detection of light and pineal secretion of melatonin, but extraretinal detection of light occurs in birds. A common mechanism across all vertebrates is that these photoperiod-regulated systems alter hypothalamic thyroid hormone (TH) conversion. Here, we review the evidence that a circadian clock within the pars tuberalis of the adenohypophysis links photoperiod decoding to local changes of TH signaling within the medio-basal hypothalamus (MBH) through a conserved thyrotropin/deiodinase axis. We also focus on recent findings which indicate that, beyond the photoperiodic control of its conversion, TH might also be involved in longer-term timing processes of seasonal programs. Finally, we examine the potential implication of kisspeptin and RFRP3, two RF-amide peptides expressed within the MBH, in seasonal rhythmicity.
In mammals, day-length-sensitive (photoperiodic) seasonal breeding cycles depend on the pineal hormone melatonin, which modulates secretion of reproductive hormones by the anterior pituitary gland
1. ...It is thought that melatonin acts in the hypothalamus to control reproduction through the release of neurosecretory signals into the pituitary portal blood supply, where they act on pituitary endocrine cells
2. Contrastingly, we show here that during the reproductive response of Soay sheep exposed to summer day lengths, the reverse applies: Melatonin acts directly on anterior-pituitary cells, and these then relay the photoperiodic message back into the hypothalamus to control neuroendocrine output. The switch to long days causes melatonin-responsive cells in the pars tuberalis (PT) of the anterior pituitary to increase production of thyrotrophin (TSH). This acts locally on TSH-receptor-expressing cells in the adjacent mediobasal hypothalamus, leading to increased expression of type II thyroid hormone deiodinase (DIO2). DIO2 initiates the summer response by increasing hypothalamic tri-iodothyronine (T3) levels. These data and recent findings in quail
3 indicate that the TSH-expressing cells of the PT play an ancestral role in seasonal reproductive control in vertebrates. In mammals this provides the missing link between the pineal melatonin signal and thyroid-dependent seasonal biology.
The high Arctic archipelago of Svalbard (74°–81° north) experiences extended periods of uninterrupted daylight in summer and uninterrupted night in winter, apparently relaxing the major driver for ...the evolution of circadian rhythmicity. Svalbard ptarmigan (Lagopus muta hyperborea) is the only year-round resident terrestrial bird species endemic to the high Arctic and is remarkably adapted to the extreme annual variation in environmental conditions.1 Here, we demonstrate that, although circadian control of behavior disappears rapidly upon transfer to constant light conditions, consistent with the loss of daily activity patterns observed during the polar summer and polar night, Svalbard ptarmigans nonetheless employ a circadian-based mechanism for photoperiodic timekeeping. First, we show the persistence of rhythmic clock gene expression under constant light within the mediobasal hypothalamus and pars tuberalis, the key tissues in the seasonal neuroendocrine cascade. We then employ a “sliding skeleton photoperiod” protocol, revealing that the driving force behind seasonal biology of the Svalbard ptarmigan is rhythmic sensitivity to light, a feature that depends on a functioning circadian rhythm. Hence, the unusual selective pressures of life in the high Arctic have favored decoupling of the circadian clock from organization of daily activity patterns, while preserving its importance for seasonal synchronization.
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•Ptarmigan circadian activity patterns rapidly dampen under controlled constant light•Clock gene expression is rhythmic in the seasonal neuroendocrine cascade circuit•Skeleton photoperiods stimulate summer-associated phenotype and genetic markers•Svalbard ptarmigan likely time their seasonal biology using a circadian mechanism
During the Arctic summer, Svalbard ptarmigan have weak/absent circadian activity patterns. Appenroth et al. show that despite this unusual phenotype, the circadian clock persists in constant conditions and forms the basis for photoperiodic sensitivity. Their findings emphasize the importance of the circadian clock for seasonal timekeeping.
Animals living in temperate zones anticipate seasonal environmental changes to adapt their biological functions, especially reproduction and metabolism. Two main physiological mechanisms have evolved ...for this adaptation: intrinsic long-term timing mechanisms with an oscillating period of approximately 1 year, driven by a circannual clock 1, and synchronization of biological rhythms to the sidereal year using day length (photoperiod) 2. In mammals, the pineal hormone melatonin relays photoperiodic information to the hypothalamus to control seasonal physiology through well-defined mechanisms 3–6. In contrast, little is known about how the circannual clock drives endogenous changes in seasonal functions. The aim of this study was to determine whether genes involved in photoperiodic time measurement (TSHβ and Dio2) and central control of reproduction (Rfrp and Kiss1) display circannual rhythms in expression under constant conditions. Male European hamsters, deprived of seasonal time cues by pinealectomy and maintenance in constant photoperiod, were selected when expressing a subjective summer or subjective winter state in their circannual cycle of body weight, temperature, and testicular size. TSHβ expression in the pars tuberalis (PT) displayed a robust circannual variation with highest level in the subjective summer state, which was positively correlated with hypothalamic Dio2 and Rfrp expression. The negative sex steroid feedback was found to act specifically on arcuate Kiss1 expression. Our findings reveal TSH as a circannual output of the PT, which in turn regulates hypothalamic neurons controlling reproductive activity. Therefore, both the circannual and the melatonin signals converge on PT TSHβ expression to synchronize seasonal biological activity.
•TSHβ in the pars tuberalis displays circannual variation in the European hamster•Generation of circannual rhythms is independent of melatonin and sex steroids•The circannual clock and melatonin use the same neuroendocrine reproductive pathway•We propose that the circannual clock is located within the pars tuberalis
By studying pinealectomized European hamsters under constant conditions, Sáenz de Miera and Monecke et al. show that circannual variation in the production of thyroid-stimulating hormone by the pars tuberalis is an important element of an endogenous seasonal clock driving reproductive changes.
Across taxa, circadian control of physiology and behavior arises from cell-autonomous oscillations in gene expression, governed by a networks of so-called 'clock genes', collectively forming ...transcription-translation feedback loops. In modern vertebrates, these networks contain multiple copies of clock gene family members, which arose through whole genome duplication (WGD) events during evolutionary history. It remains unclear to what extent multiple copies of clock gene family members are functionally redundant or have allowed for functional diversification. We addressed this problem through an analysis of clock gene expression in the Atlantic salmon, a representative of the salmonids, a group which has undergone at least 4 rounds of WGD since the base of the vertebrate lineage, giving an unusually large complement of clock genes. By comparing expression patterns across multiple tissues, and during development, we present evidence for gene- and tissue-specific divergence in expression patterns, consistent with functional diversification of clock gene duplicates. In contrast to mammals, we found no evidence for coupling between cortisol and circadian gene expression, but cortisol mediated non-circadian regulated expression of a subset of clock genes in the salmon gill was evident. This regulation is linked to changes in gill function necessary for the transition from fresh- to sea-water in anadromous fish. Overall, this analysis emphasises the potential for a richly diversified clock gene network to serve a mixture of circadian and non-circadian functions in vertebrate groups with complex genomes.
Seasonal synchronization based on day length (photoperiod) allows organisms to anticipate environmental change. Photoperiodic decoding relies on circadian clocks, but the underlying molecular ...pathways have remained elusive 1. In mammals and birds, photoperiodic responses depend crucially on expression of thyrotrophin β subunit RNA (TSHβ) in the pars tuberalis (PT) of the pituitary gland 2–4. Now, using our well-characterized Soay sheep model 2, we describe a molecular switch governing TSHβ transcription through the circadian clock. Central to this is a conserved D element in the TSHβ promoter, controlled by the circadian transcription factor thyrotroph embryonic factor (Tef). In the PT, long-day exposure rapidly induces expression of the coactivator eyes absent 3 (Eya3), which synergizes with Tef to maximize TSHβ transcription. The pineal hormone melatonin, secreted nocturnally, sets the phase of rhythmic Eya3 expression in the PT to peak 12 hr after nightfall. Additionally, nocturnal melatonin levels directly suppress Eya3 expression. Together, these effects form a switch triggering a strong morning peak of Eya3 expression under long days. Species variability in the TSHβ D element influences sensitivity to TEF, reflecting species variability in photoperiodic responsiveness. Our findings define a molecular pathway linking the circadian clock to the evolution of seasonal timing in mammals.
► EYA3 and TEF synergistically transactivate TSHβ through a D element in its promoter ► Pars tuberalis Eya3 expression increases rapidly on exposure to long photoperiod ► A melatonin-based “coincidence timer” may account for photoperiodic Eya3 expression ► TSHβ D element species differences are linked to differing photoperiodic sensitivity
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