Reversible DNA methylation regulates seasonal photoperiodic time measurement

Stevenson, Tyler J.; Prendergast, Brian J.

doi:10.1073/pnas.1310643110

Cited by 163 publications

(166 citation statements)

References 48 publications

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“…During muscle cell differentiation, dio2 gene expression is up-regulated by histone demethylation and acetylation leading to myoblast differentiation (32), whereas dio3 sits in an imprinted locus, tightly regulated by epigenetic mechanisms essential for normal growth and viability (33). In addition, it has been reported that photoperiodic information regulates dio3 gene expression by acting upon promoter methylation in adult Siberian hamsters (34). In view of these results, we favor a hypothesis where TSHR-mediated changes in the epigenetic regulation of dio2 gene expression underlie the shift in TSH sensitivity caused by the MPP effect on fetal TSH signaling.…”

Section: Discussionmentioning

confidence: 99%

Maternal photoperiod programs hypothalamic thyroid status via the fetal pituitary gland

Miera

Bothorel

Jaeger

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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In wild mammals, offspring development must anticipate forthcoming metabolic demands and opportunities. Within species, different developmental strategies may be used, dependent on when in the year conception takes place. This phenotypic flexibility is initiated before birth and is linked to the pattern of day length (photoperiod) exposure experienced by the mother during pregnancy. This programming depends on transplacental communication via the pineal hormone melatonin. Here, we show that, in the Siberian hamster (Phodopus sungorus), the programming effect of melatonin is mediated by the pars tuberalis (PT) of the fetal pituitary gland, before the fetal circadian system and autonomous melatonin production is established. Maternal melatonin acts on the fetal PT to control expression of thyroid hormone deiodinases in ependymal cells (tanycytes) of the fetal hypothalamus, and hence neuroendocrine output. This mechanism sets the trajectory of reproductive and metabolic development in pups and has a persistent effect on their subsequent sensitivity to the photoperiod. This programming effect depends on tanycyte sensitivity to thyroid stimulating hormone (TSH), which is dramatically and persistently increased by short photoperiod exposure in utero. Our results define the role of the fetal PT in developmental programming of brain function by maternal melatonin and establish TSH signal transduction as a key substrate for the encoding of internal calendar time from birth to puberty.photoperiodism | developmental programming | hypothalamus | pars tuberalis | thyroid

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Section: Discussionmentioning

confidence: 99%

Maternal photoperiod programs hypothalamic thyroid status via the fetal pituitary gland

Miera

Bothorel

Jaeger

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…In diverse reproductive events, hormone-driven temporal changes of DNA methylation have been revealed. For example, to control seasonal reproductive neuroendocrine function in the hamster, thyroid hormone reversibly reduces promoter DNA methylation and upregulates expression of photoperiodic sensor gene dio3 (51). During transition from follicle to corpus luteum after ovulation, LH induced DNA methylation and histone modifications are associated with repression of the inhibin α expression in the ovary (52).…”

Section: Dna Methylation and Uterine Physiologymentioning

confidence: 99%

Epigenetic regulations through DNA methylation and hydroxymethylation: clues for early pregnancy in decidualization

Gao

Das

2014

Biomolecular Concepts

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DNA methylation at cytosines is an important epigenetic modification that participates in gene expression regulation without changing the original DNA sequence. With the rapid progress of high-throughput sequencing techniques, whole-genome distribution of methylated cytosines and their regulatory mechanism have been revealed gradually. This has allowed the uncovering of the critical roles played by DNA methylation in the maintenance of cell pluripotency, determination of cell fate during development, and in diverse diseases. Recently, rediscovery of 5-hydroxymethylcytosine, and other types of modification on DNA, have uncovered more dynamic aspects of cell methylome regulation. The interaction of DNA methylation and other epigenetic changes remodel the chromatin structure and determine the state of gene transcription, not only permanently, but also transiently under certain stimuli. The uterus is a reproductive organ that experiences dramatic hormone stimulated changes during the estrous cycle and pregnancy, and thus provides us with a unique model for studying the dynamic regulation of epigenetic modifications. In this article, we review the current findings on the roles of genomic DNA methylation and hydroxymethylation in the regulation of gene expression, and discuss the progress of studies for these epigenetic changes in the uterus during implantation and decidualization.

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“…For example, it has been shown that the timing of flowering in plants (induced by seasonal changes in day length) involves various epigenetic modifications, including DNA methylation (Yaish et al 2011). Moreover, in mammals, DNA methylation of the type III deiodinase (dio3) gene has recently been shown to be critical for measuring photoperiod (Stevenson and Prendergast 2013).…”

mentioning

confidence: 99%

DNA methylation changes induced by long and short photoperiods inNasonia

et al. 2015

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Many organisms monitor the annual change in day length and use this information for the timing of their seasonal response. However, the molecular mechanisms underlying photoperiodic timing are largely unknown. The wasp Nasonia vitripennis is an emerging model organism that exhibits a strong photoperiodic response: Short autumnal days experienced by females lead to the induction of developmental arrest (diapause) in their progeny, allowing winter survival of the larvae. How female Nasonia control the developmental trajectory of their offspring is unclear. Here, we took advantage of the recent discovery that DNA methylation is pervasive in Nasonia and tested its role in photoperiodism. We used reduced representation bisulfite sequencing (RRBS) to profile DNA methylation in adult female wasps subjected to different photoperiods and identified substantial differential methylation at the single base level. We also show that knocking down DNA methyltransferase 1a (Dnmt1a), Dnmt3, or blocking DNA methylation pharmacologically, largely disrupts the photoperiodic diapause response of the wasps. To our knowledge, this is the first example for a role of DNA methylation in insect photoperiodic timing.

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Reversible DNA methylation regulates seasonal photoperiodic time measurement

Cited by 163 publications

References 48 publications

Maternal photoperiod programs hypothalamic thyroid status via the fetal pituitary gland

Maternal photoperiod programs hypothalamic thyroid status via the fetal pituitary gland

Epigenetic regulations through DNA methylation and hydroxymethylation: clues for early pregnancy in decidualization

DNA methylation changes induced by long and short photoperiods inNasonia

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