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Circadian clock genes and photoperiodism: Comprehensive analysis of clock gene expression in the mediobasal hypothalamus, the Suprachiasmatic nucleus, and the pineal gland of Japanese quail under various light schedules

Division of Biomodeling, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan.
Endocrinology (Impact Factor: 4.64). 10/2003; 144(9):3742-8. DOI: 10.1210/en.2003-0435
Source: PubMed

ABSTRACT In birds, the mediobasal hypothalamus (MBH) including the infundibular nucleus, inferior hypothalamic nucleus, and median eminence is considered to be an important center that controls the photoperiodic time measurement. Here we show expression patterns of circadian clock genes in the MBH, putative suprachiasmatic nucleus (SCN), and pineal gland, which constitute the circadian pacemaker under various light schedules. Although expression patterns of clock genes were different between long and short photoperiod in the SCN and pineal gland, the results were not consistent with those under night interruption schedule, which causes testicular growth. These results indicate that different expression patterns of the circadian clock genes in the SCN and pineal gland are not an absolute requirement for encoding and decoding of seasonal information. In contrast, expression patterns of clock genes in the MBH were stable under various light conditions, which enables animals to keep a steady-state photoinducible phase.

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    • "Changes in photoperiod have also been shown to alter the pattern of Fos expression within the MBH and ME, reinforcing roles for these regions in transducing photoperiod into an endocrine response (Meddle and Follett, 1997). The expression of multiple clock genes within both the MBH and the suprachiasmatic nuclei (SCN) has suggested a location within the hypothalamus for the photoperiodic clock (Yasuo et al., 2003). In parallel with these findings, It has been known for many years that thyroid hormones play a critically important role in regulating the avian photoperiodic response (Follett and Nicholls, 1985) but a series of recent studies by Yoshimura and colleagues have placed these observations into a physiological context suggesting that long daylengths regulate thyroid hormone metabolism within the MBH itself (Nakao et al., 2008; Yoshimura et al., 2003). "
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    ABSTRACT: Extraretinal photoreceptors located within the medio-basal hypothalamus regulate the photoperiodic control of seasonal reproduction in birds. An action spectrum for this response describes an opsin photopigment with a λmax of ∼492nm. Beyond this however, the specific identity of the photopigment remains unresolved. Several candidates have emerged including rod-opsin; melanopsin (OPN4); neuropsin (OPN5); and vertebrate ancient (VA) opsin. These contenders are evaluated against key criteria used routinely in photobiology to link orphan photopigments to specific biological responses. To date, only VA opsin can easily satisfy all criteria and we propose that this photopigment represents the prime candidate for encoding daylength and driving seasonal breeding in birds. We also show that VA opsin is co-expressed with both gonadotropin-releasing hormone (GnRH) and arginine-vasotocin (AVT) neurons. These new data suggest that GnRH and AVT neurosecretory pathways are endogenously photosensitive and that our current understanding of how these systems are regulated will require substantial revision. Copyright © 2014. Published by Elsevier Inc.
    Frontiers in Neuroendocrinology 11/2014; 37. DOI:10.1016/j.yfrne.2014.11.001 · 7.58 Impact Factor
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    • "Of note, daily variations in this gene have been highlighted in the SCN of a diurnal non-human primate, the capuchin monkey (Valenzuela et al., 2008). Furthermore, in other classes of vertebrates, Clock oscillations have also been found in diurnal birds such as the quail (Yasuo et al., 2003). Therefore, this comparative phylogenetic survey gives clues to our assertion. "
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    ABSTRACT: A major challenge in the field of circadian rhythms is to understand the neural mechanisms controlling the oppositely phased temporal organization of physiology and behaviour between night- and day-active animals. Most identified components of the master clock in the suprachiasmatic nuclei (SCN), called circadian genes, display similar oscillations according to the time of day, independent of the temporal niche. This has led to the predominant view that the switch between night- and day-active animals occurs downstream of the master clock, likely also involving differential feedback of behavioral cues onto the SCN. The Barbary striped grass mouse, Lemniscomys barbarus is known as a day-active Muridae. Here we show that this rodent, when housed in constant darkness, displays a temporal rhythmicity of metabolism matching its diurnal behaviour (i.e., high levels of plasma leptin and hepatic glycogen during subjective midday and dusk, respectively). Regarding clockwork in their SCN, these mice show peaks in the mRNA profiles of the circadian gene Period1 (Per1) and the clock-controlled gene Vasopressin (Avp), which occur during the middle and late subjective day, respectively, in accordance with many observations in both diurnal and nocturnal species. Strikingly, expression of the circadian gene Clock in the SCN of the Barbary striped grass mouse was not constitutive as in nocturnal rodents, but it was rhythmic. As this is also the case for the other diurnal species investigated in the literature (sheep, marmoset, and quail), a hypothesis is that the transcriptional control of Clock within the SCN participates in the mechanisms underlying diurnality and noctumality.
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    • "These genes encode positive proteins like CLOCK, MOP4 (NPAS2) and BMAL1-2, negative proteins CRY1-2 and PER2-3, and regulatory factors, e.g. E4BP4 (Bailey et al., 2003; Fukada & Okano, 2002; Yoshimura et al., 2000; Yasuo et al., 2003). The transcription of negative factors, together with clock-controlled genes, is switched on by the binding of positive factors BMAL1-2 and CLOCK to an E-box (CACGTG) cassette in the promoter regions of these genes (Okano et al., 2001). "
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    ABSTRACT: The avian pineal gland, apart from the hypothalamic master clock (suprachiasmatic nuclei, SCN) and retina, functions as an independent circadian oscillator, receiving external photic cues that it translates into the rhythmical synthesis of melatonin, a biochemical signal of darkness. Functional similarity to the mammalian SCN makes the avian pineal gland a convenient model for studies on biological clock mechanisms in general. Pineal melatonin is produced not only in a light-dependent manner but also remains under the control of the endogenous oscillator, while the possible involvement of melatonin in maintaining cyclic expression of the avian clock genes remains to be elucidated. The aim of the present study was to characterize the diurnal profiles of main clock genes transcription in the pineal glands of chickens exposed to continuous light (LL) and supplemented with exogenous melatonin. We hypothesized that rearing chickens from the day of hatch under LL conditions would evoke a functional pinealectomy, influencing, in turn, pineal clock function. To verify this hypothesis, we examined the diurnal transcriptional profiles of selected clock genes as well as the essential parameters of pineal gland function: transcription of the genes encoding arylalkylamine N-acetyltransferase (Aanat), a key enzyme in melatonin biosynthesis, and the melatonin receptor (Mel1c), along with the blood melatonin level. Chickens hatched in summer or winter were maintained under LD 16:8 and 8:16, corresponding to the respective photoperiods, as the seasonal control groups. Another set of chickens was kept in parallel under LL conditions and some were supplemented with melatonin to check the ability of exogenous hormone to antagonize the effects evoked by continuous light. Twelve-day-old chickens were sacrificed every 3 h over a 24-h period and the mRNAs of selected clock genes, Bmal1, Cry1, Per3, E4bp4, together with those of Aanat and Mel1c, were quantified in the isolated pineal glands. Our results indicate that the profiles of clock gene transcription are not dependent on the duration of the light phase, while LL conditions decrease the amplitude of diurnal changes, but do not abolish them entirely. Melatonin supplied in drinking water to the birds kept in LL seems to desynchronize transcription of the majority of clock genes in the summer, while in the winter, it restores the pattern, but not the diurnal rhythmicity. Rhythmic expression of Bmal1 appears to provide a direct link between the circadian clock and the melatonin output pathway, while the availability of cyclic melatonin is clearly involved in the canonical transcription pattern of Per3 in the chicken pineal gland. Regardless of the experimental conditions, a negative correlation was identified between the transcription of genes involved in melatonin biosynthesis (Aanat) and melatonin signal perception (Mel1c receptor).
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