Disrupting the circadian photo-period alters the release of follicle-stimulating hormone, luteinizing hormone, progesterone, and estradiol in maternal and fetal sheep

Abstract

Although a large number of studies show that photo-period disruption potentially affects hormone secretion in mammals, information about the effects of circadian photo-period disruption during pregnancy on fetal blood reproductive hormone levels is scarce. This study used ewes and their fetuses to determine the effects of circadian photo-period disruption (deprivation of darkness) on follicle-stimulating hormone, luteinizing hormone, estradiol, and progesterone in maternal and fetal circulation at late gestation. Pregnant ewes (gestational age: 135 ± 3 days) were randomly placed into control and dark deprivation groups. The control (N = 5) and dark deprivation (N = 5) groups were exposed to a fixed 12 h light/12 h dark cycle and a 24 h constant light cycle, respectively, for 2 days. Dark deprivation up-regulated follicle-stimulating hormone and estradiol levels and down-regulated progesterone levels in both maternal and fetal circulation, and up-regulated luteinizing hormone levels in fetal but not maternal circulation. These results provide new information about how circadian photo-period disruption during pregnancy could alter the release of certain reproductive hormones into fetal blood, which may influence the development of fetal organs in utero, as well as long-term health.

Effect of circadian system disruption on the concentration and daily oscillations of cortisol, progesterone, melatonin, serotonin, growth hormone, and core body temperature in periparturient dairy cattle

“…Exposure to constant light did not affect rhythms nor did timed administration of MEL, suggesting that P4 rhythms are generated by endogenous clocks during pregnancy (Matsumoto et al, 1991). The finding that circadian disruption by exposure to constant light caused a drop in circulating P4 in pregnant ewes and their fetuses (Gao et al, 2016) supports circadian clock regulation of daily P4 rhythms. Idealized models of mean levels across all CON cows at 23 d BEC support that P4 showed circadian rhythms of concentration.…”

Circadian clocks and their integration with metabolic and reproductive systems: our current understanding and its application to the management of dairy cows

“…The endocrine milieu of late pregnant ewes and their fetuses was significantly altered when transitioned to constant light for 48 h compared to control groups that remained on 12 h light-12 h dark cycles. The constant light increased levels of follicle-stimulating hormone and estradiol and decreased progesterone levels in both maternal and fetal circulation ( Gao et al, 2016 ). Low levels of melatonin are linked with adverse pregnancy outcomes, and supplementing pregnant ewes with melatonin was shown to increase arterial blood flow in the placenta ( Shukla et al, 2014 ).…”

Chronodisruption: effects on reproduction, transgenerational health of offspring and epigenome

“…These results will provide much needed information on the effects of the circadian rhythm during pregnancy and its consequences on the fetal and the first year of life of the infant's growth. In addition, several studies in chicken, rat or sheep embryos report that a functional molecular circadian clock is important for the developmental processes including tissue homeostasis, histogenesis during early chondrogenesis (Alagha et al 2020) and the release of reproductive hormones into the fetal bloodstream (Gao et al 2016). Disruptions of any or all of these processes could influence fetal organ development in utero, as well as long-term health.…”

“…Animal studies Varcoe et al (2011) Albino Wistar female rats; chronic phase shifts (CPS) in every 3-4 days Short-term and long-term gender and age dependent metabolic alterations and metabolic syndrome (e.g. increased adiposity, hyperleptinemia and alterations to glucose metabolism) Varcoe et al (2016) ClockΔ19+MEL mice No negative effects on pregnancy outcomes, growth or metabolic homeostasis in heterozygous offspring through to adulthood Gao et al (2016) Pregnant ewes; dark deprivation Effects on the release of reproductive hormones into the fetal bloodstream Salazar et al (2018) Sprague-Dawley rats; CPS in every 3-4 days Alterations on fetal adrenal function and transcriptome Chaves et al (2019) Mice; gestational jet lag protocol Pathological phenotype (e.g. altered heart structure and function, altered bone thickness and strength) and impairment in postnatal growth and effects on circadian behavior Voiculescu et al (2016) Wistar rats; prenatal continuous light exposure Short-term memory impairment in adult offspring with a relationship between serotonin-melatonin axis Motta-Teixeira et al…”