Seasonal breeding in mammals: From basic science to applications and back

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In mammals, melatonin is responsible for the synchronisation of seasonal cycles to the solar year. Melatonin is secreted by the pineal gland with a profile reflecting the duration of the night and acts via the pituitary pars tuberalis (PT), which in turn modulates hypothalamic thyroid hormone status via seasonal changes in the production of locally-acting thyrotrophin. Recently, we demonstrated that, in the Soay sheep, photoperiodic induction of Tshb expression and consequent downstream hypothalamic changes occur over a narrow range of photoperiods between 12 and 14 hours in duration. In the present study, we aimed to extend our molecular characterisation of this pathway, based on transcriptomic analysis of photoperiodic changes in the pituitary and hypothalamus of ovariectomised, oestradiol-implanted Ile-de-France ewes. We demonstrate that photoperiodic treatments applied before the winter solstice elicit two distinctive modes of accelerated reproductive switch off compared to ewes held on a simulated natural photoperiod, with shut-down occurring markedly faster on photoperiods of 13 hours or more than on photoperiods of 12 hours and less. This pattern of response was reflected in gene expression profiles of photoperiodically sensitive markers, both in the PT (Tshb, Fam150b, Vmo1, Ezh2 and Suv39H2) and in tanycytes (Tmem252 and Dct). Unexpectedly, the expression of Dio2 in tanycytes did not show any noticeable increase in expression with lengthening photoperiods. Finally, the expression of Kiss1, the key activator of gonadotrophin-releasing hormone release, was proportionately decreased by lengthening photoperiods, in a pattern that correlated strongly with gonadotrophin suppression. These data show that stepwise increases in photoperiod lead to graded molecular responses at the level of the PT, a progressive suppression of Kiss1 in the hypothalamic arcuate nucleus and luteinising hormone/ follicle-stimulating hormone release by the pituitary, despite apparently unchanged Dio2 expression in tanycytes. We hypothesise that this apparent discontinuity in the seasonal neuroendocrine response illustrates the transient nature of the thyroid hormone-mediated response to long days in the control of circannual timing.

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Discontinuity in the molecular neuroendocrine response to increasing daylengths in Ile‐de‐France ewes: Is transient Dio2 induction a key feature of circannual timing?

Dardente

Lomet

Chesneau

et al. 2019

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“…Thus, for sheep and deer, shortening photoperiod is associated with increased reproductive competence, which means that the "breeding season" is during the autumn, allowing offspring to be born 6 months later in the warming days of spring when food availability is optimal. 2,3 The shortening photoperiod is also associated with reduced food intake and decreased body weight (fatness). 4 By contrast, for Siberian (also known as Djungarian hamsters, Phodopus sungorus) and Syrian hamsters (Mesocricetus auratus), reproductive competence is associated with long photoperiod (the opposite to sheep), yet they exploit different strategies for energy balance.…”

Section: Introductionmentioning

confidence: 99%

A unifying hypothesis for control of body weight and reproduction in seasonally breeding mammals

Helfer

Barrett

Morgan

2019

Animals have evolved diverse seasonal variations in physiology and reproduction to accommodate yearly changes in environmental and climatic conditions. These changes in physiology are initiated by changes in photoperiod (daylength) and are mediated through melatonin, which relays photoperiodic information to the pars tuberalis of the pituitary gland. Melatonin drives thyroid‐stimulating hormone transcription and synthesis in the pars tuberalis, which, in turn, regulates thyroid hormone and retinoic acid synthesis in the tanycytes lining the third ventricle of the hypothalamus. Seasonal variation in central thyroid hormone signalling is conserved among photoperiodic animals. Despite this, different species adopt divergent phenotypes to cope with the same seasonal changes. A common response amongst different species is increased hypothalamic cell proliferation/neurogenesis in short photoperiod. That cell proliferation/neurogenesis may be important for seasonal timing is based on (i) the neurogenic potential of tanycytes; (ii) the fact that they are the locus of striking seasonal morphological changes; and (iii) the similarities to mechanisms involved in de novo neurogenesis of energy balance neurones. We propose that a decrease in hypothalamic thyroid hormone and retinoic acid signalling initiates localised neurodegeneration and apoptosis, which leads to a reduction in appetite and body weight. Neurodegeneration induces compensatory cell proliferation from the neurogenic niche in tanycytes and new cells are born under short photoperiod. Because these cells have the potential to differentiate into a number of different neuronal phenotypes, this could provide a mechanistic basis to explain the seasonal regulation of energy balance, as well as reproduction. This cycle can be achieved without changes in thyroid hormone/retinoic acid and explains recent data obtained from seasonal animals held in natural conditions. However, thyroid/retinoic acid signalling is required to synchronise the cycles of apoptosis, proliferation and differentiation. Thus, hypothalamic neurogenesis provides a framework to explain diverse photoperiodic responses.

“…This results in an opposite transcriptional control of two deiodinases Dio2 and Dio3 that dictate local levels of triiodothyronine (T3) and govern downstream seasonal physiology. How T3 impinges on seasonal breeding in mammals is unknown, although current data suggest a pivotal role for the RF‐amide peptides KISS‐1 and RFamide‐related peptide‐3 …”

Section: Introductionmentioning

confidence: 99%

Photoperiod and thyroid hormone regulate expression of l‐dopachrome tautomerase (Dct), a melanocyte stem‐cell marker, in tanycytes of the ovine hypothalamus

Dardente

Lomet

2018

Self Cite

The pars tuberalis (PT) of the pituitary is central to the control of seasonal breeding. In mammals, the PT translates the photoperiodic message carried by melatonin into an endocrine thyroid-stimulating hormone output, which controls local thyroid hormone (TH) signalling in tanycytes of the neighbouring hypothalamus. In the present study, we identify l-dopachrome tautomerase (Dct) as a novel marker of ovine tanycytes and show that Dct displays marked seasonal variations in expression, with higher levels during spring and summer. This seasonal profile is photoperiod-dependent because an acute exposure to long days induces Dct expression. In addition, we find that TH also modulates Dct expression. DCT functions as an enzyme in the melanin synthesis pathway within skin melanocytes, whereas expression in other tissues is comparatively low. We demonstrate that both Tyr and Tyrp1, which are enzymes that intervene upstream and downstream of Dct in the melanin synthesis pathway, respectively, are expressed at very low levels in the ovine hypothalamus. This suggests that Dct in tanycytes may not be involved in melanin synthesis. We speculate that DCT function is linked to its protective role towards oxidative stress and/or its function in the control of neural progenitor cell proliferation.