Maternal PUFAs, Placental Epigenetics, and Their Relevance to Fetal Growth and Brain Development

Basak, Sanjay; Duttaroy, Asim K.

doi:10.1007/s43032-022-00989-w

Cited by 21 publications

(21 citation statements)

References 189 publications

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“…We refer to [73 ▪▪ ,123] for recent overviews. We cite recent reviews addressing these complex, multifacted processes involving: mother-fetus-placenta unit [78]; HPA axis and cortisol [120,124 ▪ ,125]; autonomic nervous system [125]; iron deficiency [126]; maternal inflammation and offspring microglial activity [127]; mitochondria [128]; microbiome [10,129–131]; maternal metabolic risk factors including diabetes, obesity, undernutrition, specific macro- and micronutrient intake (e.g., long-chain polyunsaturated fatty acids (PUFAs) [132–135]; epigenetic changes, epigenome wide associations studies, relevant for e.g., the HPA axis or oxytocin system [136] including DNA methylation, histone modification, microRNA and other-non coding RNA [73 ▪▪ ,135,137–139] or multiomics data (transcriptomics, proteomics, metabolomics, and microbiomics [140]); telomere length [57]; paternal mediated effects [141,142]; oxidative stress [143], breast milk composition [78]; oxytocin system [73 ▪▪ ]; serotonin functions (e.g., SCL6A4) [73 ▪▪ ]; brain-derived neurotrophic factor (BDNF) [73 ▪▪ ]; structural and functional brain alterations beyond regions previously identified as relevant (i.e., prefrontal cortex, hippocampus, amygdala (limbic system)) additionally including basal ganglia, anterior cingulate cortex, thalamus, middle and superior frontal gyri, occipital gyrus and precentral gyrus [9,31,108].…”

Section: Perinatal Mental Health and Offspring Outcome: Results Mecha...mentioning

confidence: 99%

“…Progress in the field of perinatal mental health includes: contextualized measures of parental perinatal exposures including socioeconomic disadvantage measures, racial/ethnic discrimination and environmental factors in single cohort [109,151,152] and multicohort studies [8, 135,[153][154][155][156][157][158][159][160][161]162 && ]; improvement in measures of offspring neurobehavioral development, including neuropsychological and neuroimaging studies which take relevant and necessary confounders [163] into account [164][165][166][167] and scan the offspring at different ages [31,168 && , [169][170][171][172][173]; studies of the influence of genetic architecture as well environmental toxins and early-life adversity (including poverty) on neurobehavioral development [8, 109,135,158,159,[174][175][176].…”

Section: Progress and Challenges In Pre/perinatal Mental Health Researchmentioning

confidence: 99%

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Current perspectives on perinatal mental health and neurobehavioral development: focus on regulation, coregulation and self-regulation

Van den Bergh,

Antonelli,

Stein

2024

Current Opinion in Psychiatry

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Purpose of review Perinatal mental health research provides an important perspective on neurobehavioral development. Here, we aim to review the association of maternal perinatal health with offspring neurodevelopment, providing an update on (self-)regulation problems, hypothesized mechanistic pathways, progress and challenges, and implications for mental health. Recent findings (1) Meta-analyses confirm that maternal perinatal mental distress is associated with (self-)regulation problems which constitute cognitive, behavioral, and affective social-emotional problems, while exposure to positive parental mental health has a positive impact. However, effect sizes are small. (2) Hypothesized mechanistic pathways underlying this association are complex. Interactive and compensatory mechanisms across developmental time are neglected topics. (3) Progress has been made in multiexposure studies. However, challenges remain and these are shared by clinical, translational and public health sciences. (4) From a mental healthcare perspective, a multidisciplinary and system level approach employing developmentally-sensitive measures and timely treatment of (self-)regulation and coregulation problems in a dyadic caregiver-child and family level approach seems needed. The existing evidence-base is sparse. Summary During the perinatal period, addressing vulnerable contexts and building resilient systems may promote neurobehavioral development. A pluralistic approach to research, taking a multidisciplinary approach to theoretical models and empirical research needs to be fostered.

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Section: Perinatal Mental Health and Offspring Outcome: Results Mecha...mentioning

confidence: 99%

Section: Progress and Challenges In Pre/perinatal Mental Health Researchmentioning

confidence: 99%

Current perspectives on perinatal mental health and neurobehavioral development: focus on regulation, coregulation and self-regulation

Van den Bergh,

Antonelli,

Stein

2024

Current Opinion in Psychiatry

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“…It has been shown that LC n-3 PUFA given to dams or to mothers had epigenetic effects (86)(87)(88) . MicroRNA-143 (miR-143) seems to stimulate adipocytes' differentiation and is correlated with obese condition in mice fed with a HF diet.…”

Section: Discussionmentioning

confidence: 99%

Long-chainn-3 PUFA given before and throughout gestation and lactation in rats prevent high-fat diet-induced insulin resistance in male offspring in a tissue-specific manner

Guriec¹,

Foll

Delarue

2023

Br J Nutr

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This study investigated whether long chain n-3 polyunsaturated fatty acids (LC n-3 PUFAs) given to pregnant rats fed a high fat (HF) diet may prevent fetal programming in male offspring at adulthood. Six weeks before mating, and throughout gestation and lactation, female nulliparous Sprague-Dawley rats were given a chow (C) diet, HF (60.6% fat from corn, rapeseed oils and lard) or HF in which one third of fat was replaced by fish oil (HF n-3). At weaning, the 3 offspring groups were randomly separated in 2 groups fed C diet, or HF without LC n-3 PUFAs, for 7 weeks until adulthood. Glucose tolerance and insulin sensitivity were assessed by an oral glucose tolerance test both at weaning and at adulthood. Insulin signaling was determined in liver, muscle and adipose tissue by quantification of the phosphorylation of Akt on Ser 473 at adulthood. At weaning, as at adulthood, offspring from HF-fed dams were obese, and displayed glucose intolerance (GI) and insulin-resistance (IR), but not those from HFn-3 fed dams. Following the post-weaning C diet, phosphorylation of Akt was strongly reduced in all tissues of offspring from HF dams, but to a lesser extent in liver and muscle of offspring from HFn-3 dams. However, it was abolished in all tissues of all offspring groups fed the HF post-weaning diet. Thus, LC n-3 PUFAs introduced in a HF in dams, partially prevented the transmission of GI and IR in adult offspring even though they were fed without LC n-3 PUFAs from weaning.

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“…125 For ω-3 PUFAs, the activation of transcription factor cascades is likely 126,127 as a result of the modulatory action of epigenetic regulators, such as DNA (de-)methylation globally or through gene-specific promoter modifications. 128,129 As such, reduced DNA methyltransferase (DNMT) 3A and 3B activity was proposed as a potential molecular underpinning of variations in placental DNA methylation upon insufficient ω-3 PUFA availability. Particularly, ω-3 PUFAs could sustain or even increase Bdnf transcription (encoding brain-derived neurotrophic factor), a hypothesis derived from loss-of-function studies with ω-3 PUFA-deficient diets increasing the methylation of the Bdnf promoter.…”

Section: Epigenetic Mechanisms Underpin Pufa Actionmentioning

confidence: 99%

“…Indeed, the maternal diet can re‐model epigenetic patterns during prenatal development, with the incorporation of repressive marks being likely negative for long‐term outcomes in the offspring 125 . For ω‐3 PUFAs, the activation of transcription factor cascades is likely 126,127 as a result of the modulatory action of epigenetic regulators, such as DNA (de‐)methylation globally or through gene‐specific promoter modifications 128,129 . As such, reduced DNA methyltransferase (DNMT) 3A and 3B activity was proposed as a potential molecular underpinning of variations in placental DNA methylation upon insufficient ω‐3 PUFA availability.…”

Section: Maternal Diet As a Risk Factor For Mental Disorders In Their...mentioning

confidence: 99%

Adverse effects of gestational ω‐3 and ω‐6 polyunsaturated fatty acid imbalance on the programming of fetal brain development

Cinquina

Keimpema

Pollak

et al. 2023

J Neuroendocrinology

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Obesity is a key medical challenge of our time. The increasing number of children born to overweight or obese women is alarming. During pregnancy, the circulation of the mother and her fetus interact to maintain the uninterrupted availability of essential nutrients for fetal organ development. In doing so, the mother's dietary preference determines the amount and composition of nutrients reaching the fetus. In particular, the availability of polyunsaturated fatty acids (PUFAs), chiefly their ω‐3 and ω‐6 subclasses, can change when pregnant women choose a specific diet. Here, we provide a succinct overview of PUFA biochemistry, including exchange routes between ω‐3 and ω‐6 PUFAs, the phenotypes, and probable neurodevelopmental disease associations of offspring born to mothers consuming specific PUFAs, and their mechanistic study in experimental models to typify signaling pathways, transcriptional, and epigenetic mechanisms by which PUFAs can imprint long‐lasting modifications to brain structure and function. We emphasize that the ratio, rather than the amount of individual ω‐3 or ω‐6 PUFAs, might underpin physiologically correct cellular differentiation programs, be these for neurons or glia, during pregnancy. Thereupon, the PUFA‐driven programming of the brain is contextualized for childhood obesity, metabolic, and endocrine illnesses.

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Maternal PUFAs, Placental Epigenetics, and Their Relevance to Fetal Growth and Brain Development

Cited by 21 publications

References 189 publications

Current perspectives on perinatal mental health and neurobehavioral development: focus on regulation, coregulation and self-regulation

Current perspectives on perinatal mental health and neurobehavioral development: focus on regulation, coregulation and self-regulation

Long-chainn-3 PUFA given before and throughout gestation and lactation in rats prevent high-fat diet-induced insulin resistance in male offspring in a tissue-specific manner

Adverse effects of gestational ω‐3 and ω‐6 polyunsaturated fatty acid imbalance on the programming of fetal brain development

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