Abstract
Disrupting maternal circadian rhythms through exposure to chronic phase shifts of the photoperiod has lifelong consequences for the metabolic homeostasis of the fetus, such that offspring develop increased adiposity, hyperinsulinaemia and poor glucose and insulin tolerance. In an attempt to determine the mechanisms by which these poor metabolic outcomes arise, we investigated the impact of chronic phase shifts (CPS) on maternal and fetal hormonal, metabolic and circadian rhythms. We assessed weight gain and food consumption of dams exposed to either CPS or control lighting conditions throughout gestation. At day 20, dams were assessed for plasma hormone and metabolite concentrations and glucose and insulin tolerance. Additionally, the expression of a range of circadian and metabolic genes was assessed in maternal, placental and fetal tissue. Control and CPS dams consumed the same amount of food, yet CPS dams gained 70% less weight during the first week of gestation. At day 20, CPS dams had reduced retroperitoneal fat pad weight (−15%), and time-of-day dependent decreases in liver weight, whereas fetal and placental weight was not affected. Melatonin secretion was not altered, yet the timing of corticosterone, leptin, glucose, insulin, free fatty acids, triglycerides and cholesterol concentrations were profoundly disrupted. The expression of gluconeogenic and circadian clock genes in maternal and fetal liver became either arrhythmic or were in antiphase to the controls. These results demonstrate that disruptions of the photoperiod can severely disrupt normal circadian profiles of plasma hormones and metabolites, as well as gene expression in maternal and fetal tissues. Disruptions in the timing of food consumption and the downstream metabolic processes required to utilise that food, may lead to reduced efficiency of growth such that maternal weight gain is reduced during early embryonic development. It is these perturbations that may contribute to the programming of poor metabolic homeostasis in the offspring.
Highlights
It has become increasingly clear that early environmental influences can have long lasting impact on the normal development and physiology of the fetus
In this study we investigated the impact of chronic phase shifts on maternal and fetal hormonal, metabolic and circadian rhythms
Growth Trajectories and Food Consumption The weight gain of control and chronic phase shift (CPS) dams was fitted to the polynomial quadratic equation (r = 0.92 and 0.91 respectively), with comparisons between groups revealing significant differences in B1 (P,0.001) and B2 (P,0.01, Figure 1a), suggesting differences in weight gain over gestation
Summary
It has become increasingly clear that early environmental influences can have long lasting impact on the normal development and physiology of the fetus Factors such as poor maternal nutrition, prenatal stress and exposure to medicinal and social drugs can all have negative health consequences for the offspring that persist into adulthood [1,2,3]. Shift work is characterised by forced disruptions in the timing of activity, sleep and light exposure, leading to disordered endocrine, metabolic and behavioural rhythms While it is known from epidemiological and experimental studies that these changes can increase the risk to the individual of developing a myriad of chronic health disorders, it raises the important question of whether exposure to shift work during pregnancy can affect the developing fetus
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