Maternal cold exposure induces distinct transcriptome changes in the placenta and fetal brown adipose tissue in mice
Abstract Background 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. However, very little is know...
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doaj-856288f4ffc7472480217c7987fc85ba2021-07-04T11:33:38ZengBMCBMC Genomics1471-21642021-07-0122111210.1186/s12864-021-07825-6Maternal cold exposure induces distinct transcriptome changes in the placenta and fetal brown adipose tissue in miceSujoy Ghosh0Chul-Hong Park1Jisu Lee2Nathan Lee3Rui Zhang4Clara Huesing5Dorien Reijnders6Jennifer Sones7Heike Münzberg8Leanne Redman9Ji Suk Chang10Genomics and Bioinformatics Core, Pennington Biomedical Research CenterGene Regulation and Metabolism, Pennington Biomedical Research CenterGene Regulation and Metabolism, Pennington Biomedical Research CenterLeptin Signaling in The Brain, Pennington Biomedical Research CenterLeptin Signaling in The Brain, Pennington Biomedical Research CenterLeptin Signaling in The Brain, Pennington Biomedical Research CenterLouisiana State University School of Veterinary MedicineLouisiana State University School of Veterinary MedicineLeptin Signaling in The Brain, Pennington Biomedical Research CenterReproductive Endocrinology and Women’s Health, Pennington Biomedical Research CenterGene Regulation and Metabolism, Pennington Biomedical Research CenterAbstract Background 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. 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. Results Maternal 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. Conclusions These 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.https://doi.org/10.1186/s12864-021-07825-6Brown adipose tissue thermogenesisFetal brown adipogenesisPlacentaRNA-sequencingGene expressionMaternal-fetal crosstalk |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Sujoy Ghosh Chul-Hong Park Jisu Lee Nathan Lee Rui Zhang Clara Huesing Dorien Reijnders Jennifer Sones Heike Münzberg Leanne Redman Ji Suk Chang |
spellingShingle |
Sujoy Ghosh Chul-Hong Park Jisu Lee Nathan Lee Rui Zhang Clara Huesing Dorien Reijnders Jennifer Sones Heike Münzberg Leanne Redman Ji Suk Chang Maternal cold exposure induces distinct transcriptome changes in the placenta and fetal brown adipose tissue in mice BMC Genomics Brown adipose tissue thermogenesis Fetal brown adipogenesis Placenta RNA-sequencing Gene expression Maternal-fetal crosstalk |
author_facet |
Sujoy Ghosh Chul-Hong Park Jisu Lee Nathan Lee Rui Zhang Clara Huesing Dorien Reijnders Jennifer Sones Heike Münzberg Leanne Redman Ji Suk Chang |
author_sort |
Sujoy Ghosh |
title |
Maternal cold exposure induces distinct transcriptome changes in the placenta and fetal brown adipose tissue in mice |
title_short |
Maternal cold exposure induces distinct transcriptome changes in the placenta and fetal brown adipose tissue in mice |
title_full |
Maternal cold exposure induces distinct transcriptome changes in the placenta and fetal brown adipose tissue in mice |
title_fullStr |
Maternal cold exposure induces distinct transcriptome changes in the placenta and fetal brown adipose tissue in mice |
title_full_unstemmed |
Maternal cold exposure induces distinct transcriptome changes in the placenta and fetal brown adipose tissue in mice |
title_sort |
maternal cold exposure induces distinct transcriptome changes in the placenta and fetal brown adipose tissue in mice |
publisher |
BMC |
series |
BMC Genomics |
issn |
1471-2164 |
publishDate |
2021-07-01 |
description |
Abstract Background 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. 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. Results Maternal 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. Conclusions These 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. |
topic |
Brown adipose tissue thermogenesis Fetal brown adipogenesis Placenta RNA-sequencing Gene expression Maternal-fetal crosstalk |
url |
https://doi.org/10.1186/s12864-021-07825-6 |
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