Characterisation of the Maternal Response to Chronic Phase Shifts during Gestation in the Rat: Implications for Fetal Metabolic Programming
Open accessAbstract
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.
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Pregnant rats exposed to simulated shift-work showed substantially reduced weight gain during early pregnancy and reduced fat-pad and liver weights, and also exhibited lower-amplitude rhythms of corticosterone, glucose, insulin and leptin levels.
“Pregnant rats exposed to simulated shift-work (that is, complete reversal of the light–dark cycle every 3–4 days for several weeks) showed substantially reduced weight gain during early pregnancy and reduced fat-pad and liver weights, and also exhibited lower-amplitude rhythms of corticosterone, glucose, insulin and leptin levels41.”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [41]
The same simulated shift-work manipulation affected metabolic and circadian gene expression rhythms in the fetal liver, but did not affect placental or fetal growth.
“The same manipulation also affected metabolic and circadian gene expression rhythms in the fetal liver, but did not affect placental or fetal growth41.”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [41]
Maternal circadian disruption alters offspring metabolic functioning in adulthood, including regulation of glucocorticoids and insulin.
“Likewise, maternal circadian disruption alters offspring metabolic functioning in adulthood13, 17–19, including the regulation of glucocorticoids17 and insulin18.”
From Maternal and Early-Life Circadian Disruption Have Long-Lasting Negative Consequences on Offspring Development and Adult Behavior in Mice (2017) · cites this paper as [19]
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Developmental Circadian Disruption Alters Placental Signaling in MicePreprint
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- Authors
- Varcoe, T. J., Boden, M. J., Voultsios, A., Salkeld, M. D., Rattanatray, L., & Kennaway, D. J.
- Affiliations
- The University of Adelaide (AU)
- Corresponding author
- Varcoe, Tamara J.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-01-14
- Volume
- 8
- Issue
- 1
- Pages
- e53800
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3544759
- OpenAlex
- W2048914193
- Cited by
- 78
- References
- 38
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 2 · 2023: 6 · 2022: 2 · 2021: 11 · 2020: 6 · 2019: 6 · 2018: 12 · 2017: 6 · 2016: 6 · 2015: 6 · 2014: 3
- FWCI
- 2.67
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- Australian Government
- National Health and Medical Research Council (1009877)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Physiology › Dietary Effects on Health
- Keywords
- circadian rhythm disruption, photoperiod, gestational weight gain, corticosterone, leptin, insulin tolerance, glucose tolerance, retroperitoneal fat, hepatic gene expression, clock genes, gluconeogenesis, placenta, adiposity, hyperinsulinemia
- MeSH terms
- Animals, Circadian Rhythm, Eating, Female, Fetus, Glucose Tolerance Test, Hormones, Insulin, Liver, Male, Mothers, Placenta, Pregnancy, Rats, Wistar, Photoperiod, Gene Expression Regulation, Developmental, Rats, Circadian Clocks
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