Maternal Feeding Controls Fetal Biological Clock

Hidenobu Ohta,Tadashi Matsuda,Masayuki Iigo,Hajime Tei,Shigeru Tsuchiya,Toshihiro Ohura,Shanhai Xu,Nobuo Yaegashi,Hiroshi Chisaka,Tatsuya Watanabe,Takushi Hanita,Takahiro Moriya,Norimichi Nakahata,Yoshitaka Kimura,Kunihiro Okamura,Naomi Rogers

doi:10.1371/journal.pone.0002601

Hidenobu Ohta, Tadashi Matsuda + Show 14 more

Open Access

https://doi.org/10.1371/journal.pone.0002601

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Abstract

BackgroundIt is widely accepted that circadian physiological rhythms of the fetus are affected by oscillators in the maternal brain that are coupled to the environmental light-dark (LD) cycle.Methodology/Principal FindingsTo study the link between fetal and maternal biological clocks, we investigated the effects of cycles of maternal food availability on the rhythms of Per1 gene expression in the fetal suprachiasmatic nucleus (SCN) and liver using a transgenic rat model whose tissues express luciferase in vitro. Although the maternal SCN remained phase-locked to the LD cycle, maternal restricted feeding phase-advanced the fetal SCN and liver by 5 and 7 hours respectively within the 22-day pregnancy.Conclusions/SignificanceOur results demonstrate that maternal feeding entrains the fetal SCN and liver independently of both the maternal SCN and the LD cycle. This indicates that maternal-feeding signals can be more influential for the fetal SCN and particular organ oscillators than hormonal signals controlled by the maternal SCN, suggesting the importance of a regular maternal feeding schedule for appropriate fetal molecular clockwork during pregnancy.

Highlights

Most living organisms exhibit circadian rhythms, oscillations with a period of approximately 24 hours, in their behaviors and physiological functions, including activity, sleep, metabolism and body temperature
We focused on a maternal signal, which is not directly controlled by the maternal suprachiasmatic nuclei (SCN), by using a restricted feeding (RF) schedule to examine the possibility of feeding-related factors being a synchronizer for the fetal SCN
Despite the marked effects of this regimen on maternal locomotor behavior, the phase of the maternal SCN rhythm was unaffected (one-way ANOVA, p.0.05; the peak times for ad lib and restricted feeding were 43.961.4 h and 44.260.8 h respectively) and remained phase-locked to the light cycle, even after 21 days of RF (Fig. 4). This result is consistent with previous studies which report that RF does not entrain the adult SCN and supports the general notion that entrainment to cycles of food availability does not directly involve the maternal SCN [12,13,14]

Summary

Introduction

Most living organisms exhibit circadian rhythms, oscillations with a period of approximately 24 hours, in their behaviors and physiological functions, including activity, sleep, metabolism and body temperature. Despite the marked effects of this regimen on maternal locomotor behavior, the phase of the maternal SCN rhythm was unaffected (one-way ANOVA, p.0.05; the peak times for ad lib and restricted feeding were 43.961.4 h and 44.260.8 h (mean6s.d., throughout) respectively) and remained phase-locked to the light cycle, even after 21 days of RF (Fig. 4).

Results

Conclusion