Abstract
Surprisingly, in our modern 24/7 society, there is scant information on the impact of developmental chronodisruption like the one experienced by shift worker pregnant women on fetal and postnatal physiology. There are important differences between the maternal and fetal circadian systems; for instance, the suprachiasmatic nucleus is the master clock in the mother but not in the fetus. Despite this, several tissues/organs display circadian oscillations in the fetus. Our hypothesis is that the maternal plasma melatonin rhythm drives the fetal circadian system, which in turn relies this information to other fetal tissues through corticosterone rhythmic signaling. The present data show that suppression of the maternal plasma melatonin circadian rhythm, secondary to exposure of pregnant rats to constant light along the second half of gestation, had several effects on fetal development. First, it induced intrauterine growth retardation. Second, in the fetal adrenal in vivo it markedly affected the mRNA expression level of clock genes and clock-controlled genes as well as it lowered the content and precluded the rhythm of corticosterone. Third, an altered in vitro fetal adrenal response to ACTH of both, corticosterone production and relative expression of clock genes and steroidogenic genes was observed. All these changes were reversed when the mother received a daily dose of melatonin during the subjective night; supporting a role of melatonin on overall fetal development and pointing to it as a ‘time giver’ for the fetal adrenal gland. Thus, the present results collectively support that the maternal circadian rhythm of melatonin is a key signal for the generation and/or synchronization of the circadian rhythms in the fetal adrenal gland. In turn, low levels and lack of a circadian rhythm of fetal corticosterone may be responsible of fetal growth restriction; potentially inducing long term effects in the offspring, possibility that warrants further research.
Highlights
The environment of mother, baby and child is a key contributor to diseases and conditions that account for approximately one third of the global burden of disease in both developed and developing countries [1]
We demonstrated that the rat fetal adrenal gland is a strong peripheral circadian clock, at 18 days of gestation, in which corticosterone content follows a circadian rhythm as reported in adult individuals [13]
The present data show that exposure of pregnant rats to constant light along the second half of gestation effectively suppressed maternal plasma melatonin rhythm, whilst it shifted the phase of the rhythm but did not change the integrated levels of maternal circulating corticosterone
Summary
The environment of mother, baby and child is a key contributor to diseases and conditions that account for approximately one third of the global burden of disease in both developed and developing countries [1] In this context, chronodisruption (i.e., a significant disturbance of the temporal organization of endocrinology, physiology, metabolism and behavior) along pregnancy has been associated with an increased risk of miscarriage, and preterm delivery and low birth weight [2,3,4,5]; both strong predictors of chronic disease later in life [6,7]. It is presently unknown which maternal signal(s) may generate and/or maintain a fetal corticosterone circadian rhythm
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