The placental programming hypothesis: Placental endocrine insufficiency and the co-occurrence of low birth weight and maternal mood disorders

Creeth, Hugo; Roshan, John

doi:10.1016/j.placenta.2020.03.011

Cited by 16 publications

(14 citation statements)

References 115 publications

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“…However, we acknowledge that clinical and mechanistic research examining fetal sex-differential levels of these hormones and other biological effectors in relation to PPD remains limited. Other research has shown sex-differential expression of imprinted genes in the placenta that in turn have been linked to maternal mood disorders [62]. For example, PEG3 is an imprinted gene that plays important roles in controlling fetal growth and nurturing behaviors.…”

Section: Discussionmentioning

confidence: 99%

Fetal sex and maternal postpartum depressive symptoms: findings from two prospective pregnancy cohorts

et al. 2021

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Background Fetal sex is known to modify the course and complications of pregnancy, with recent evidence of sex-differential fetal influences on the maternal immune and endocrine systems. In turn, heightened inflammation and surges in reproductive hormone levels associated with pregnancy and parturition have been linked with the development of perinatal depression. Here, we examined whether there is an association between fetal sex and maternal depression assessed during the prenatal and postnatal periods. Methods The study included two multi-ethnic, prospective pregnancy cohorts that enrolled women from prenatal clinics in the Northeastern United States between 2001 and 2018. Maternal depressive symptoms were measured during the prenatal and postnatal periods using the Edinburgh Postpartum Depression Scale (EPDS), and newborn sex was reported by the mother following delivery. We used logistic regression to examine associations between fetal sex and maternal depressive symptoms (EPDS > 10) during the prenatal period only, postnatal period only, or both periods versus no depressive symptoms during either period. We considered both unadjusted models and models adjusted for a core set of sociodemographic and lifestyle variables. Results In adjusted models using PRISM data (N = 528), women pregnant with a male versus female fetus had significantly greater odds of depressive symptoms during the postnatal period compared to women without depressive symptoms during either period (odds ratio [OR] = 5.24, 95% confidence interval [CI] = 1.93, 14.21). The direction of results was consistent in the ACCESS cohort, although the findings did not reach statistical significance (OR = 2.05, 95% CI = 0.86, 4.93). Significant associations were not observed in either cohort among women with prenatal symptoms only or women with prenatal and postnatal symptoms. Conclusions Male fetal sex was associated with the onset of depressive symptoms during the postnatal period.

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Section: Discussionmentioning

confidence: 99%

Fetal sex and maternal postpartum depressive symptoms: findings from two prospective pregnancy cohorts

et al. 2021

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“…Decreased placental expression of PEG3 has also been linked to perinatal depression in mothers [ 91 ]. Although again this is tentative, correlative evidence for a role in humans, the link between imprinted genes, placental function and maternal mental health is an exciting area for future study [ 92 ].…”

Section: Indirect Action Of Imprinted Genes On Brain and Behaviourmentioning

confidence: 99%

The contribution of imprinted genes to neurodevelopmental and neuropsychiatric disorders

Isles

2022

Transl Psychiatry

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Imprinted genes are a subset of mammalian genes that are subject to germline parent-specific epigenetic modifications leading monoallelic expression. Imprinted gene expression is particularly prevalent in the brain and it is unsurprising that mutations affecting their expression can lead to neurodevelopmental and/or neuropsychiatric disorders in humans. Here I review the evidence for this, detailing key neurodevelopmental disorders linked to imprinted gene clusters on human chromosomes 15q11-q13 and 14q32, highlighting genes and possible regulatory links between these different syndromes. Similarly, rare copy number variant mutations at imprinted clusters also provide strong links between abnormal imprinted gene expression and the predisposition to severe psychiatric illness. In addition to direct links between brain-expressed imprinted genes and neurodevelopmental and/or neuropsychiatric disorders, I outline how imprinted genes that are expressed in another tissue hotspot, the placenta, contribute indirectly to abnormal brain and behaviour. Specifically, altered nutrient provisioning or endocrine signalling by the placenta caused by abnormal expression of imprinted genes may lead to increased prevalence of neurodevelopmental and/or neuropsychiatric problems in both the offspring and the mother.

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“…Normal growth and survival of the fetus depends on the adequate placentation. Besides providing sufficient amounts of nutrients and oxygen, the placenta establishes a privileged immune environment for fetal growth by orchestrating maternal adaptations to pregnancy and acting as a selective and protective barrier to prevent feto-maternal diseases (Creeth and John, 2020). Poor placentation and placental failure compromises fetal development leading to potential chronic diseases in adult (Sharma et al, 2016;Perez-Garcia et al, 2018;Woods et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Early Abnormal Placentation and Evidence of Vascular Endothelial Growth Factor System Dysregulation at the Feto-Maternal Interface After Periconceptional Alcohol Consumption

et al. 2022

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Adequate placentation, placental tissue remodeling and vascularization is essential for the success of gestation and optimal fetal growth. Recently, it was suggested that abnormal placenta induced by maternal alcohol consumption may participate in fetal growth restriction and relevant clinical manifestations of the Fetal Alcohol Spectrum Disorders (FASD). Particularly, periconceptional alcohol consumption up to early gestation can alter placentation and angiogenesis that persists in pregnancy beyond the exposure period. Experimental evidence suggests that abnormal placenta following maternal alcohol intake is associated with insufficient vascularization and defective trophoblast development, growth and function in early gestation. Accumulated data indicate that impaired vascular endothelial growth factor (VEGF) system, including their downstream effectors, the nitric oxide (NO) and metalloproteinases (MMPs), is a pivotal spatio-temporal altered mechanism underlying the early placental vascular alterations induced by maternal alcohol consumption. In this review we propose that the periconceptional alcohol intake up to early organogenesis (first trimester) alters the VEGF-NO-MMPs system in trophoblastic-decidual tissues, generating imbalances in the trophoblastic proliferation/apoptosis, insufficient trophoblastic development, differentiation and migration, deficient labyrinthine vascularization, and uncompleted remodelation and transformation of decidual spiral arterioles. Consequently, abnormal placenta with insufficiency blood perfusion, vasoconstriction and reduced labyrinthine blood exchange can be generated. Herein, we review emerging knowledge of abnormal placenta linked to pregnancy complications and FASD produced by gestational alcohol ingestion and provide evidence of the early abnormal placental angiogenesis-vascularization and growth associated to decidual-trophoblastic dysregulation of VEGF system after periconceptional alcohol consumption up to mid-gestation, in a mouse model.

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The placental programming hypothesis: Placental endocrine insufficiency and the co-occurrence of low birth weight and maternal mood disorders

Cited by 16 publications

References 115 publications

Fetal sex and maternal postpartum depressive symptoms: findings from two prospective pregnancy cohorts

Fetal sex and maternal postpartum depressive symptoms: findings from two prospective pregnancy cohorts

The contribution of imprinted genes to neurodevelopmental and neuropsychiatric disorders

Early Abnormal Placentation and Evidence of Vascular Endothelial Growth Factor System Dysregulation at the Feto-Maternal Interface After Periconceptional Alcohol Consumption

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