Abstract
BackgroundBrown adipose tissue (BAT) is specialized to dissipate energy in the form of heat. BAT-mediated heat production in rodents and humans is critical for effective temperature adaptation of newborns to the extrauterine environment immediately after birth. However, very little is known about whether and how fetal BAT development is modulated in-utero in response to changes in maternal thermal environment during pregnancy. Using BL6 mice, we evaluated the impact of different maternal environmental temperatures (28 °C and 18 °C) on the transcriptome of the placenta and fetal BAT to test if maternal cold exposure influences fetal BAT development via placental remodeling.ResultsMaternal weight gain during pregnancy, the average number of fetuses per pregnancy, and placental weight did not differ between the groups at 28 °C and 18 °C. However, the average fetal weight at E18.5 was 6% lower in the 18 °C-group compared to the 28 °C-group. In fetal BATs, cold exposure during pregnancy induced increased expression of genes involved in de novo lipogenesis and lipid metabolism while decreasing the expression of genes associated with muscle cell differentiation, thus suggesting that maternal cold exposure may promote fetal brown adipogenesis by suppressing the myogenic lineage in bidirectional progenitors. In placental tissues, maternal cold exposure was associated with upregulation of genes involved in complement activation and downregulation of genes related to muscle contraction and actin-myosin filament sliding. These changes may coordinate placental adaptation to maternal cold exposure, potentially by protecting against cold stress-induced inflammatory damage and modulating the vascular and extravascular contractile system in the placenta.ConclusionsThese findings provide evidence that environmental cold temperature sensed by the mother can modulate the transcriptome of placental and fetal BAT tissues. The ramifications of the observed gene expression changes warrant future investigation.
Highlights
Brown adipose tissue (BAT) is specialized to dissipate energy in the form of heat
Effects of maternal cold exposure on placental and fetal weight In mice, the thermoneutral zone lies at approximately 30 °C at which BAT thermogenesis is lowest, whereas the mice housed at room temperature (22–23 °C) experience mild cold stress and must increase their metabolism and BAT thermogenesis to defend their body temperature [13, 14]
To evaluate the effects of maternal thermal environments on the placenta and fetal BAT development, female mice were acclimated for 1 week at near thermoneutrality (28 °C) or 18 °C prior to mating with male mice, and pregnant females were maintained at their respective temperature until embryonic day 18.5 (Fig. 1A)
Summary
Brown adipose tissue (BAT) is specialized to dissipate energy in the form of heat. BAT-mediated heat production in rodents and humans is critical for effective temperature adaptation of newborns to the extrauterine environment immediately after birth. In rodents and small mammals, including infant humans, BAT-mediated heat production enables newborns to adapt to the extrauterine environment after birth. BAT is first detectable at embryonic day 15.5 and increases in size until birth [5, 6]. During this stage of development, BAT is derived from rapidly proliferating progenitors that express myogenic markers such as Myf, MyoD, and Myogenin [7, 8]. Transcriptional factor PRDM16 is a key regulator that promotes the brown adipocyte lineage from a bidirectional progenitor [9,10,11]
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