Thyrotrophin in the pars tuberalis triggers photoperiodic response
TL;DR: Two waves of gene expression are identified in the quail MBH associated with the initiation of photoinduced secretion of luteinizing hormone and increased TSH in the pars tuberalis seems to trigger long-day photoinduced seasonal breeding.
Abstract: Molecular mechanisms regulating animal seasonal breeding in response to changing photoperiod are not well understood. Rapid induction of gene expression of thyroid-hormone-activating enzyme (type 2 deiodinase, DIO2) in the mediobasal hypothalamus (MBH) of the Japanese quail (Coturnix japonica) is the earliest event yet recorded in the photoperiodic signal transduction pathway. Here we show cascades of gene expression in the quail MBH associated with the initiation of photoinduced secretion of luteinizing hormone. We identified two waves of gene expression. The first was initiated about 14 h after dawn of the first long day and included increased thyrotrophin (TSH) beta-subunit expression in the pars tuberalis; the second occurred approximately 4 h later and included increased expression of DIO2. Intracerebroventricular (ICV) administration of TSH to short-day quail stimulated gonadal growth and expression of DIO2 which was shown to be mediated through a TSH receptor-cyclic AMP (cAMP) signalling pathway. Increased TSH in the pars tuberalis therefore seems to trigger long-day photoinduced seasonal breeding.
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TL;DR: The authors used massively parallel sequencing to identify selective sweeps of favorable alleles and candidate mutations that have had a prominent role in the domestication of domestic chickens and their subsequent specialization into broiler (meat-producing) and layer (egg-consuming) chickens.
Abstract: Domestic animals are excellent models for genetic studies of phenotypic evolution They have evolved genetic adaptations to a new environment, the farm, and have been subjected to strong human-driven selection leading to remarkable phenotypic changes in morphology, physiology and behaviour Identifying the genetic changes underlying these developments provides new insight into general mechanisms by which genetic variation shapes phenotypic diversity Here we describe the use of massively parallel sequencing to identify selective sweeps of favourable alleles and candidate mutations that have had a prominent role in the domestication of chickens (Gallus gallus domesticus) and their subsequent specialization into broiler (meat-producing) and layer (egg-producing) chickens We have generated 445-fold coverage of the chicken genome using pools of genomic DNA representing eight different populations of domestic chickens as well as red jungle fowl (Gallus gallus), the major wild ancestor We report more than 7,000,000 single nucleotide polymorphisms, almost 1,300 deletions and a number of putative selective sweeps One of the most striking selective sweeps found in all domestic chickens occurred at the locus for thyroid stimulating hormone receptor (TSHR), which has a pivotal role in metabolic regulation and photoperiod control of reproduction in vertebrates Several of the selective sweeps detected in broilers overlapped genes associated with growth, appetite and metabolic regulation We found little evidence that selection for loss-of-function mutations had a prominent role in chicken domestication, but we detected two deletions in coding sequences that we suggest are functionally important This study has direct application to animal breeding and enhances the importance of the domestic chicken as a model organism for biomedical research
943 citations
TL;DR: It seems clear that deiodinases play a much broader role than once thought, with great ramifications for the control of thyroid hormone signaling during vertebrate development and metamorphosis, as well as injury response, tissue repair, hypothalamic function, and energy homeostasis in adults.
Abstract: The iodothyronine deiodinases initiate or terminate thyroid hormone action and therefore are critical for the biological effects mediated by thyroid hormone. Over the years, research has focused on their role in preserving serum levels of the biologically active molecule T3 during iodine deficiency. More recently, a fascinating new role of these enzymes has been unveiled. The activating deiodinase (D2) and the inactivating deiodinase (D3) can locally increase or decrease thyroid hormone signaling in a tissue- and temporal-specific fashion, independent of changes in thyroid hormone serum concentrations. This mechanism is particularly relevant because deiodinase expression can be modulated by a wide variety of endogenous signaling molecules such as sonic hedgehog, nuclear factor-κB, growth factors, bile acids, hypoxia-inducible factor-1α, as well as a growing number of xenobiotic substances. In light of these findings, it seems clear that deiodinases play a much broader role than once thought, with great ramifications for the control of thyroid hormone signaling during vertebrate development and metamorphosis, as well as injury response, tissue repair, hypothalamic function, and energy homeostasis in adults.
715 citations
TL;DR: Melatonin acts directly on anterior-pituitary cells, and these then relay the photoperiodic message back into the hypothalamus to control neuroendocrine output, which provides the missing link between the pineal melatonin signal and thyroid-dependent seasonal biology.
350 citations
Cites result from "Thyrotrophin in the pars tuberalis ..."
...This pathway shows remarkable similarity to the pathway very recently described in the Japanese quail, the key difference being that in the quail, the photoperiodic reproductive response to LP exposure is more rapid and is believed to depend on an uncharacterized deep-brain photoreceptor [3] rather than melatonin....
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...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....
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TL;DR: The skeleton represents an ideal physiological system in which to characterize thyroid hormone transport, metabolism, and action during development and adulthood and in response to injury, and will provide new insights into cell-specific molecular mechanisms and may ultimately identify novel therapeutic targets for chronic degenerative diseases such as osteoporosis and osteoarthritis.
Abstract: The skeleton is an exquisitely sensitive and archetypal T3-target tissue that demonstrates the critical role for thyroid hormones during development, linear growth, and adult bone turnover and maintenance. Thyrotoxicosis is an established cause of secondary osteoporosis, and abnormal thyroid hormone signaling has recently been identified as a novel risk factor for osteoarthritis. Skeletal phenotypes in genetically modified mice have faithfully reproduced genetic disorders in humans, revealing the complex physiological relationship between centrally regulated thyroid status and the peripheral actions of thyroid hormones. Studies in mutant mice also established the paradigm that T3 exerts anabolic actions during growth and catabolic effects on adult bone. Thus, the skeleton represents an ideal physiological system in which to characterize thyroid hormone transport, metabolism, and action during development and adulthood and in response to injury. Future analysis of T3 action in individual skeletal cell lineages will provide new insights into cell-specific molecular mechanisms and may ultimately identify novel therapeutic targets for chronic degenerative diseases such as osteoporosis and osteoarthritis. This review provides a comprehensive analysis of the current state of the art.
299 citations
TL;DR: It is found that short-wavelength light, i.e., between UV-B and blue light, induced photoperiodic responses in eye-patched, pinealectomized quail, and Opsin 5 appears to be one of the deep brain photoreceptive molecules that regulates seasonal reproduction in birds.
Abstract: It has been known for many decades that nonmammalian vertebrates detect light by deep brain photoreceptors that lie outside the retina and pineal organ to regulate seasonal cycle of reproduction. However, the identity of these photoreceptors has so far remained unclear. Here we report that Opsin 5 is a deep brain photoreceptive molecule in the quail brain. Expression analysis of members of the opsin superfamily identified as Opsin 5 (OPN5; also known as Gpr136, Neuropsin, PGR12, and TMEM13) mRNA in the paraventricular organ (PVO), an area long believed to be capable of phototransduction. Immunohistochemistry identified Opsin 5 in neurons that contact the cerebrospinal fluid in the PVO, as well as fibers extending to the external zone of the median eminence adjacent to the pars tuberalis of the pituitary gland, which translates photoperiodic information into neuroendocrine responses. Heterologous expression of Opsin 5 in Xenopus oocytes resulted in light-dependent activation of membrane currents, the action spectrum of which showed peak sensitivity (λmax) at ∼420 nm. We also found that short-wavelength light, i.e., between UV-B and blue light, induced photoperiodic responses in eye-patched, pinealectomized quail. Thus, Opsin 5 appears to be one of the deep brain photoreceptive molecules that regulates seasonal reproduction in birds.
264 citations
Cites background from "Thyrotrophin in the pars tuberalis ..."
...PT TSH induces expression of type 2 deiodinase (DIO2) in tanycytes lining the ventrolateral walls of the third ventricle (3V) (17)....
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...Recently, long-day induction of TSH expression in the pars tuberalis was shown to trigger the photoperiodic response, and the pars tuberalis was reported to be the key organ that relays photoperiodic information to a neuroendocrine output (17, 20, 21)....
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...The recently available chicken genome sequence has facilitated comprehensive expression analyses in quail, because these species are both galliformes with high interspecies DNA sequence conservation (17)....
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References
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TL;DR: Genetic and genomic analysis suggests that a relatively small number of output genes are directly regulated by core oscillator components, and major processes regulated by the SCN and liver were found to be under circadian regulation.
2,227 citations
TL;DR: This review examines how birds use the annual cycle in photoperiod to ensure that seasonal events—breeding, molt, and song production—happen at the appropriate time of year.
Abstract: This review examines how birds use the annual cycle in photoperiod to ensure that seasonal events—breeding, molt, and song production—happen at the appropriate time of year. Differences in breeding strategies between birds and mammals reflect basic differences in biology. Avian breeding seasons tend to be of shorter duration and more asymmetric with respect to changes in photoperiod. Breeding seasons can occur at the same time each year (predictable) or at different times (opportunistic), depending on the food resource. In all cases, there is evidence for involvement of photoperiodic control, nonphotoperiodic control, and endogenous circannual rhythmicity. In predictable breeders (most nontropical species), photoperiod is the predominant proximate factor. Increasing photoperiods of spring stimulate secretion of gonadotropin-releasing hormone (GnRH) and consequent gonadal maturation. However, breeding ends before the return of short photoperiods. This is the consequence of a second effect of long photoperi...
901 citations
TL;DR: The role of the Rev-ErbA/ROR response element in gene expression during circadian night is demonstrated, which is in phase with Bmal1 and in antiphase to Per2 oscillations.
Abstract: evoked by square pulse stimuli (0.066 Hz, 5‐12 mA, 200 ms) delivered by means of bipolar tungsten electrodes positioned within the lateral amygdala close to the external capsule. Population spikes were recorded in the basolateral amygdala close to lateral amygdala using glass microelectrodes (2‐3 MQ) filled with artificial cerebrospinal fluid (ACSF) 29 . HFS (five trains at 100 Hz for 1 s, 10-s interstimulus interval) was applied to induce LTP, and LFS1 (900 pulses at 1 Hz) was applied to induce LTD. Whole-cell GABA-mediated currents were isolated by adding NBQX (0.005 mM) and D-(-)-2-amino-5phosphopentanoic acid (AP5; 0.05 mM) to ACSF (bubbled with 95% O2/5% CO2 ;p H 7.3), and were recorded from visually identified somata of principal neurons of the basolateral amygdala 30 by glass electrodes (4.5‐5 MQ) 16 containing (in mM): Mg-ATP 2, CsCH3SO3 100, CsCl 60, EGTA 0.2, HEPES 10, MgCl2 1, QX314 5 and Na3GTP 0.3 (pH 7.3). Patch clamp experiments were performed at 24 ^ 1 8C at a holding potential of 270 mV. LTDi was induced by 100 stimuli at 1 Hz (LFS 2). PPF was induced as described 30 . Data are expressed as means ^ s.e.m. We tested significance using the Student’s t-test.
857 citations
TL;DR: Unlike the conventional methods that label the 5' end of cDNAs, this method specifically labels the capped end of the mRNAs with a synthetic r-oligo prior to first-strand cDNA synthesis.
662 citations
TL;DR: The results reveal that signaling-dependent activation of mPer genes is distinct from the CLOCK/BMAL1-driven transcription required within the clock feedback loop, and constitute strong evidence that CREB acts as a pivotal endpoint of signaling pathways for the regulation of m per genes.
Abstract: Circadian rhythmicity in mammals is under the control of a molecular pacemaker constituted of clock gene products organized in transcriptional autoregulatory loops. Phase resetting of the clock in response to light involves dynamic changes in the expression of several clock genes. The molecular pathways used by light to influence pacemaker-driven oscillation of clock genes remain poorly understood. We explored the functional integration of both light- and clock-responsive transcriptional regulation at the promoter level of the Period (Per) genes. Three Per genes exist in the mouse. Whereas mPer1 and mPer2 are light-inducible in clock neurons of the hypothalamic suprachiasmatic nucleus, mPer3 is not. We have studied the promoter structure of the three mPer genes and compared their regulation. All three mPer promoters contain E-boxes and respond to the CLOCK/brain and muscle aryl hydrocarbon receptor nuclear translocator (ARNT)-like protein 1 (BMAL1) heterodimer. On the other hand, only mPer1 and mPer2 promoters contain bona fide cAMP-responsive elements (CREs) that bind CRE-binding protein (CREB) from suprachiasmatic nucleus protein extracts. The mPer1 promoter is responsive to synergistic activation of the cAMP and mitogen-activated protein kinase pathways, a physiological response that requires integrity of the CRE. In contrast, activation of mPer promoters by CLOCK/BMAL1 occurs regardless of an intact CRE. Altogether, these results constitute strong evidence that CREB acts as a pivotal endpoint of signaling pathways for the regulation of mPer genes. Our results reveal that signaling-dependent activation of mPer genes is distinct from the CLOCK/BMAL1-driven transcription required within the clock feedback loop.
540 citations