Omega-3 reverses the metabolic and epigenetically regulated placental phenotype acquired from preconceptional and peri-conceptional exposure to air pollutants

IF 4.8 2区 医学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY Journal of Nutritional Biochemistry Pub Date : 2024-08-07 DOI:10.1016/j.jnutbio.2024.109735
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Abstract

Air pollution is detrimental to pregnancy adversely affecting maternal and child health. Our objective was to unravel epigenetic mechanisms mediating the effect of preconception, periconception, and gestational exposure to inhaled air pollutants (AP) upon the maternal and placental-fetal phenotype and explore the benefit of an omega-3 rich dietary intervention. To this end, we investigated intranasal instilled AP during 8 weeks of preconception, periconception, and gestation (G; D0 to 18) upon GD16-19 maternal mouse metabolic status, placental nutrient transporters, placental-fetal size, and placental morphology. Prepregnant mice were glucose intolerant and insulin resistant, while pregnant mice were glucose intolerant but displayed no major placental macro-nutrient transporter changes, except for an increase in CD36. Placentas revealed inflammatory cellular infiltration with cellular edema, necrosis, hemorrhage, and an increase in fetal body weight. Upon examination of placental genome-wide epigenetic processes of DNA sequence specific 5′-hydroxymethylation (5′-hmC) and 5′-methylation (5′-mC) upon RNA sequenced gene expression profiles, revealed changes in key metabolic, inflammatory, transcriptional, and cellular processing genes and pathways. An omega-3 rich anti-inflammatory diet from preconception (8 weeks) through periconception and gestation (GD0-18), ameliorated all these maternal and placental-fetal adverse effects. We conclude that preconceptional, periconceptional and gestational exposures to AP incite a maternal inflammatory response resulting in features of pre-existing maternal diabetes mellitus with injury to the placental-fetal unit. DNA 5′-mC more than 5′-hmC mediated AP induced maternal inflammatory and metabolic dysregulation which together alter placental gene expression and phenotype. A dietary intervention partially reversing these adversities provides possibilities for a novel nutrigenomic therapeutic strategy.

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Omega-3能逆转孕前和孕周暴露于空气污染物所导致的代谢和表观遗传调节胎盘表型。
空气污染对妊娠有害,会对母婴健康产生不利影响。我们的目标是揭示介导孕前、围孕期和妊娠期吸入空气污染物(AP)对母体和胎盘-胎儿表型影响的表观遗传学机制,并探索富含欧米伽-3的饮食干预的益处。为此,我们研究了在孕前、围孕期和妊娠期(G;D0 至 18)的 8 周内鼻内灌注空气污染物对 GD16-19 母鼠代谢状态、胎盘营养转运体、胎盘-胎儿大小和胎盘形态的影响。孕前小鼠葡萄糖不耐受和胰岛素抵抗,而怀孕小鼠葡萄糖不耐受,但除了 CD36 增加外,胎盘大营养素转运体没有发生重大变化。胎盘显示炎性细胞浸润,伴有细胞水肿、坏死、出血和胎儿体重增加。在对胎盘全基因组的表观遗传过程进行 DNA 序列特异性 5'-hydroxymethylation (5'-hmC) 和 5'-methylation (5'-mC) RNA 序列基因表达谱检测后,发现关键的代谢、炎症、转录和细胞处理基因及通路发生了变化。从孕前(8 周)到围孕期和妊娠期(GD0-18),富含欧米伽-3 的抗炎饮食可改善所有这些母体和胎盘-胎儿不良影响。我们的结论是,孕前、围孕期和妊娠期暴露于 AP 会引发母体炎症反应,导致母体原有的糖尿病特征,并对胎盘-胎儿单元造成伤害。DNA 5'-mC比5'-hmC更能介导AP诱导的母体炎症和代谢失调,从而共同改变胎盘基因表达和表型。饮食干预可部分逆转这些不利因素,为新型营养基因组治疗策略提供了可能性。
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来源期刊
Journal of Nutritional Biochemistry
Journal of Nutritional Biochemistry 医学-生化与分子生物学
CiteScore
9.50
自引率
3.60%
发文量
237
审稿时长
68 days
期刊介绍: Devoted to advancements in nutritional sciences, The Journal of Nutritional Biochemistry presents experimental nutrition research as it relates to: biochemistry, molecular biology, toxicology, or physiology. Rigorous reviews by an international editorial board of distinguished scientists ensure publication of the most current and key research being conducted in nutrition at the cellular, animal and human level. In addition to its monthly features of critical reviews and research articles, The Journal of Nutritional Biochemistry also periodically publishes emerging issues, experimental methods, and other types of articles.
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