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Maternal Experience Leads to Lasting Gene Expression Changes in Some Regions of the Mouse Brain.

ABSTRACT: Rodent maternal behaviors are due to the coordinated effects of fluctuating hormones, with their onset triggered by interactions with newborn pups. Previous studies have shown that many genes have changes in expression during peripartum stages. However, it is unclear if there are long-lasting changes in gene expression, well after the performance of maternal behaviors, that could influence physiology and behavior throughout the remaining lifespan. Here, gene expression differences were examined in mouse between age-matched virgin and primiparous females, at least 4 weeks after weaning. Of the five brain regions examined-hypothalamus, hippocampus, cortex, cerebellum, and the amygdala-only the hypothalamus had thousands of genes with significant expression differences. The cerebellum had 130 genes with expression differences, and the other brain regions had no significant changes detected. The expression changes in the hypothalamus include an enrichment of genes that could mediate long-lasting behavioral and physiological changes, given their known roles in parental behavior, including galanin and prolactin receptor.

SUBMITTER: Arbeitman MN

PROVIDER: S-EPMC6686928 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Maternal Experience Leads to Lasting Gene Expression Changes in Some Regions of the Mouse Brain.

Arbeitman Michelle N MN

G3 (Bethesda, Md.) 20190808 8

Rodent maternal behaviors are due to the coordinated effects of fluctuating hormones, with their onset triggered by interactions with newborn pups. Previous studies have shown that many genes have changes in expression during peripartum stages. However, it is unclear if there are long-lasting changes in gene expression, well after the performance of maternal behaviors, that could influence physiology and behavior throughout the remaining lifespan. Here, gene expression differences were examined ...[more]

PMID: 31164388

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Project description:Pregestational diabetes complicates one million pregnancies in the United States and is associated with placental dysfunction. Placental dysfunction can manifest as stillbirth, spontaneous abortions, fetal growth restriction, and preeclampsia in the mother. However, the underlying mechanisms of placental dysfunction are not well understood. We hypothesize that maternal hyperglycemia disrupts cellular processes important for normal vascular development and function. Hyperglycemia, defined as a non-fasting glucose concentration of >250 mg/dL was induced in eight-week-old female CD1 mice by injecting a one-time intraperitoneal dose of 150mg/kg streptozotocin. Control mice received an equal volume of normal saline. Hyperglycemic and control females were mated with CD-1 males. At Embryonic Day 17.5, the pregnant mice were euthanized. Sixty-eight placentas were harvested from the six euglycemic dams and twenty-six placentas were harvested from three hyperglycemic dams. RNA was extracted from homogenized placental tissue (N=12/group; 2-4 placentas per litter of each group). Total RNA was prepared and sequenced. Differentially expressed genes that were >2-fold change was considered significant. Placentas (9-20/group) were fixed in paraffin wax and sectioned at 6 μm. Cross-sectional areas of placental zones were evaluated using slides stained for hematoxylin and eosin, glycogen, collagen, proliferation and apoptosis. Quantification of staining intensity and percent positive nuclei was done using Leica Image Hub Data software. Data were compared between the control and experimental group using t-tests. Values of p < 0.05 were considered to be statistically significant. The average maternal blood glucose concentrations for control and diabetic dams were 112+/-24 and 473+/-47 respectively (p<0.0001). A higher rate of resorptions was noted in the hyperglycemia exposed placentas compared to euglycemic exposed placentas (24% vs 7%; p=0.04). A total of 24 RNA libraries (12/group) were prepared. Placentas from hyperglycemic pregnancies exhibited 1374 differentially expressed genes (DEGs). The 10 most significantly differentially expressed genes are Filip 1, Prom 2, Fam 78a, Pde4d, Pou3f1, Kcnk5, Dusp4, Cxcr4, Slc6a4 and D430019H16Rik. Their corresponding biologic functions are related to chemotaxis, ossification, cellular and vascular development. Histologically, we found that hyperglycemia exposed placentas demonstrated increased proliferation, apoptosis, and glycogen content and decreased collagen deposition. There was a higher rate of resorptions in the pregnancies of hyperglycemic dams. Pregestational diabetes resulted in significant changes in placental morphology, including increased glycogen content in the spongiotrophoblast, decreased collagen deposition, increased apoptosis and proliferation in the junction zone. Maternal diabetes causes widespread disruption in multiple cellular processes important for normal vascular development and sets the platform for placenta dysfunction.

Dataset Information

Maternal Experience Leads to Lasting Gene Expression Changes in Some Regions of the Mouse Brain.

Publications

Maternal Experience Leads to Lasting Gene Expression Changes in Some Regions of the Mouse Brain.

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