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Placental gene network modules are associated with maternal stress during pregnancy and infant temperament.

ABSTRACT: Maternal psychosocial stress during pregnancy (MPSP) is a known contributor to maladaptive neurobehavioral development of the offspring; however, the underlying molecular mechanisms linking MPSP with childhood outcome remain largely unknown. Transcriptome-wide gene expression data were generated using RNA-seq from placenta samples collected in a multi-ethnic urban birth cohort in New York City (n = 129). Weighted gene co-expression network analysis (WGCNA) was used to characterize placental co-expression modules, which were then evaluated for their associations with MPSP and infant temperament. WGCNA revealed 16 gene coexpression modules. One module, enriched for regulation of chromosome organization/gene expression, was positively associated with MPSP and negatively associated with Regulatory Capacity (REG), a component of infant temperament. Two other modules, enriched for cotranslational protein targeting and cell cycle regulation, respectively, displayed negative associations with MPSP and positive associations with REG. A module enriched with oxidative phosphorylation/mitochondrial translation was positively associated with REG. These findings support the notion that the placenta provides a functional in utero link between MPSP and infant temperament, possibly through transcriptional regulation of placental gene expression.

SUBMITTER: Aushev VN

PROVIDER: S-EPMC8577271 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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Placental gene network modules are associated with maternal stress during pregnancy and infant temperament.

Aushev Vasily N VN Li Qian Q Deyssenroth Maya M Zhang Wei W Finik Jackie J Hurd Yasmin L YL Nomura Yoko Y Chen Jia J

FASEB journal : official publication of the Federation of American Societies for Experimental Biology 20211001 10

Maternal psychosocial stress during pregnancy (MPSP) is a known contributor to maladaptive neurobehavioral development of the offspring; however, the underlying molecular mechanisms linking MPSP with childhood outcome remain largely unknown. Transcriptome-wide gene expression data were generated using RNA-seq from placenta samples collected in a multi-ethnic urban birth cohort in New York City (n = 129). Weighted gene co-expression network analysis (WGCNA) was used to characterize placental co-e ...[more]

PMID: 34533879

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Project description:BackgroundGene-environment interactions mediate through the placenta and shape the fetal brain development. Between the environmental determinants of the fetal brain, maternal psychosocial stress in pregnancy has been shown to negatively influence the infant temperament development. This in turn may have adverse consequences on the infant neurodevelopment extending throughout the entire life-span. However little is known about the underlying biological mechanisms of the effects of maternal psychosocial stress in pregnancy on infant temperament. Environmental stressors such as maternal psychosocial stress in pregnancy activate the stress response cascade that in turn drives the increase in the cellular energy demand of vital organs with high metabolic rates such as, in pregnancy, the placenta. Key players of the stress response cascade are the mitochondria.ResultsHere, we tested the expression of all 13 protein-coding genes encoded by the mitochondria in 108 placenta samples from the Stress in Pregnancy birth cohort, a study that aims at determining the influence of in utero exposure to maternal psychosocial stress in pregnancy on infant temperament. We showed that the expression of the protein-coding mitochondrial-encoded gene MT-ND2 was positively associated with indices of maternal psychosocial stress in pregnancy including Prenatal Perceived Stress (β = 0.259; p-regression = 0.004; r2-regression = 0.120), State Anxiety (β = 0.218; p-regression = 0.003; r2-regression = 0.153), Trait Anxiety (β = 0.262; p-regression = 0.003; r2-regression = 0.129) and Pregnancy Anxiety Total (β = 0.208; p-regression = 0.010; r2-regression = 0.103). In the meantime MT-ND2 was negatively associated with the infant temperament indices of Activity Level (β = -0.257; p-regression = 0.008; r2-regression = 0.165) and Smile and Laughter (β = -0.286; p-regression = 0.036; r2-regression = 0.082). Additionally, MT-ND6 was associated with the maternal psychosocial stress in pregnancy index of Prenatal Perceived Stress (β = -0.231; p-regression = 0.004; r2-regression = 0.120), while MT-CO2 was associated with the maternal psychosocial stress in pregnancy indices of State Anxiety (β = 0.206; p-regression = 0.003; r2-regression = 0.153) and Trait Anxiety (β = 0.205; p-regression = 0.003; r2-regression = 0.129).ConclusionsOur data support the role of mitochondria in responding to maternal psychosocial stress in pregnancy, as assessed in placenta, while also suggesting an important role for the mitochondria in the infant temperament development.

Project description:BackgroundMaternal psychological stress during pregnancy, including stress resulting from disasters and trauma, has been linked to temperamental difficulties in offspring. Although heightened cortisol concentrations are often hypothesized as an underlying mechanism, evidence supporting this mechanism is not consistent, potentially because of methodological issues and low stress in the population.AimTo address these issues, this preregistered study investigated the following associations between: 1) prenatal psychological stress and hair cortisol, as a biomarker for chronic stress, during the COVID-19 outbreak (i.e., as a major worldwide psychological stressor), and 2) maternal hair cortisol during the COVID-19 outbreak and later infant temperamental negative affectivity and orienting/regulation. Additionally, we explored whether associations were different for women with low versus high socioeconomic status (SES; maternal education and annual household income) and at different stages of pregnancy.MethodPregnant women (N = 100) filled out online questionnaires during the first COVID-19 lockdown. Six months later, when most mothers were still pregnant or had just given birth, maternal hair samples were collected during home visits. When infants were six months old, mothers reported on their infant's temperament.ResultsAlthough hierarchical regression analyses revealed no associations between prenatal COVID-19 psychological stress and hair cortisol during the COVID-19 outbreak, SES proved to be a moderator in this association. Only pregnant women with higher levels of SES, not lower levels, showed a positive association between work-related and social support-related COVID-19 worries and hair cortisol. Finally, prenatal hair cortisol was not associated with later infant temperamental negative affectivity and orienting/regulation.ConclusionAlthough the COVID-19 outbreak proved to be a major psychological stressor worldwide, the physiological impact of the crisis might be different for pregnant women with higher SES as compared to lower SES.

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Placental gene network modules are associated with maternal stress during pregnancy and infant temperament.

Publications

Placental gene network modules are associated with maternal stress during pregnancy and infant temperament.

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