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Mitochondrial Gene Expression Profiles Are Associated with Maternal Psychosocial Stress in Pregnancy and Infant Temperament.

Lambertini L, Chen J, Nomura Y - PLoS ONE (2015)

Bottom Line: However little is known about the underlying biological mechanisms of the effects of maternal psychosocial stress in pregnancy on infant temperament.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).Our 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America; Department of Obstetrics, Gynecology and Reproductive Science, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America.

ABSTRACT

Background: Gene-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.

Results: Here, 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).

Conclusions: Our 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.

No MeSH data available.


Related in: MedlinePlus

Mitochondrial Expression Clusters.The graph represents the five expression clusters identified for the expression of the 13 protein-coding mitochondrial-encoded genes. The expression clusters have been determined by Ward Linkage. The cutoff level used to generate the clusters in the clustering tree have been chosen accordingly to the multidimensional scaling analysis (see S1 Fig) that showed that the expression data can efficiently be fit into a 5-dimensional space without imposing an excessive degree of stress to the dataset.
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pone.0138929.g002: Mitochondrial Expression Clusters.The graph represents the five expression clusters identified for the expression of the 13 protein-coding mitochondrial-encoded genes. The expression clusters have been determined by Ward Linkage. The cutoff level used to generate the clusters in the clustering tree have been chosen accordingly to the multidimensional scaling analysis (see S1 Fig) that showed that the expression data can efficiently be fit into a 5-dimensional space without imposing an excessive degree of stress to the dataset.

Mentions: As suggested by the role that protein-coding mitochondrial-encoded genes play in the OXPHOS, the expression profiles of the mitochondrial-encoded genes tested showed, for several genes, a relevant degree of colinearity as determined by the high (rho > /0.4/) and significant (p < 0.01) bivariate correlation between samples (S2 Table). To address the effect of colinearity on the significance of our findings we first conducted a clustering analysis that revealed the existence of 5 expression clusters (Fig 2). The expression clusters were then validated by dimensional stress analysis conducted by using multidimensional scaling showing that the expression of the mitochondrial genes can efficiently be fit into a 5 dimension space (e.g. 5 clusters) without imposing an excessive degree of stress to the dataset (S1 Fig). Finally we calculated a summary score for each expression cluster by using principal component analysis (PCA). The efficacy of this approach was further supported by the low bivariate correlation found between the 5 summary scores (S3 Table). Similarly we calculated PCA summary scores for MPSP and infant temperament indices as well as maternal weight (including overweight and obesity) and infant birth measures (including birth weight, birth length and head circumference).


Mitochondrial Gene Expression Profiles Are Associated with Maternal Psychosocial Stress in Pregnancy and Infant Temperament.

Lambertini L, Chen J, Nomura Y - PLoS ONE (2015)

Mitochondrial Expression Clusters.The graph represents the five expression clusters identified for the expression of the 13 protein-coding mitochondrial-encoded genes. The expression clusters have been determined by Ward Linkage. The cutoff level used to generate the clusters in the clustering tree have been chosen accordingly to the multidimensional scaling analysis (see S1 Fig) that showed that the expression data can efficiently be fit into a 5-dimensional space without imposing an excessive degree of stress to the dataset.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4587925&req=5

pone.0138929.g002: Mitochondrial Expression Clusters.The graph represents the five expression clusters identified for the expression of the 13 protein-coding mitochondrial-encoded genes. The expression clusters have been determined by Ward Linkage. The cutoff level used to generate the clusters in the clustering tree have been chosen accordingly to the multidimensional scaling analysis (see S1 Fig) that showed that the expression data can efficiently be fit into a 5-dimensional space without imposing an excessive degree of stress to the dataset.
Mentions: As suggested by the role that protein-coding mitochondrial-encoded genes play in the OXPHOS, the expression profiles of the mitochondrial-encoded genes tested showed, for several genes, a relevant degree of colinearity as determined by the high (rho > /0.4/) and significant (p < 0.01) bivariate correlation between samples (S2 Table). To address the effect of colinearity on the significance of our findings we first conducted a clustering analysis that revealed the existence of 5 expression clusters (Fig 2). The expression clusters were then validated by dimensional stress analysis conducted by using multidimensional scaling showing that the expression of the mitochondrial genes can efficiently be fit into a 5 dimension space (e.g. 5 clusters) without imposing an excessive degree of stress to the dataset (S1 Fig). Finally we calculated a summary score for each expression cluster by using principal component analysis (PCA). The efficacy of this approach was further supported by the low bivariate correlation found between the 5 summary scores (S3 Table). Similarly we calculated PCA summary scores for MPSP and infant temperament indices as well as maternal weight (including overweight and obesity) and infant birth measures (including birth weight, birth length and head circumference).

Bottom Line: However little is known about the underlying biological mechanisms of the effects of maternal psychosocial stress in pregnancy on infant temperament.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).Our 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America; Department of Obstetrics, Gynecology and Reproductive Science, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America.

ABSTRACT

Background: Gene-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.

Results: Here, 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).

Conclusions: Our 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.

No MeSH data available.


Related in: MedlinePlus