The Placenta Epigenome–Brain Axis: Placental Epigenomic and Transcriptomic Responses that Preprogram Cognitive Impairment

References

• Tomlinson MS , SantosHP , StewartJRet al. Neurocognitive and social-communicative function of children born very preterm at 10 years of age: associations with microorganisms recovered from the placenta parenchyma. J. Perinatol.40(2), 306–315 (2020).
   PubMed Web of Science ®Google Scholar
• Miguel PM , PereiraLO , SilveiraPP , MeaneyMJ. Early environmental influences on the development of children’s brain structure and function. Dev. Med. Child Neurol.61(10), 1127–1133 (2019).
   PubMed Web of Science ®Google Scholar
• O’Donnell KJ , MeaneyMJ. Fetal origins of mental health: the developmental origins of health and disease hypothesis. Am. J. Psychiatry174(4), 319–328 (2017).
   PubMed Web of Science ®Google Scholar
• Burton GJ , FowdenAL , ThornburgKL. Placental origins of chronic disease. Physiol. Rev.96(4), 1509–1565 (2016).
   PubMed Web of Science ®Google Scholar
• Lester BM , MarsitCJ. Epigenetic mechanisms in the placenta related to infant neurodevelopment. Epigenomics10(3), 321–333 (2018).
   PubMed Web of Science ®Google Scholar
• Rosenfeld CS . The placenta–brain-axis. J. Neurosci. Res. doi:10.1002/jnr.24603 (2020) (Epub ahead of print).
   PubMed Web of Science ®Google Scholar
• Gabory A , RoseboomTJ , MooreT , MooreLG , JunienC. Placental contribution to the origins of sexual dimorphism in health and diseases: sex chromosomes and epigenetics. Biol Sex Differ.4(1), 5 (2013).
   PubMedGoogle Scholar
• Barker DJ , BullAR , OsmondC , SimmondsSJ. Fetal and placental size and risk of hypertension in adult life. BMJ (Clinical Research Ed.)301(6746), 259–262 (1990).
   PubMed Web of Science ®Google Scholar
• Ilekis JV , TsilouE , FisherSet al. Placental origins of adverse pregnancy outcomes: potential molecular targets: an executive workshop summary of the Eunice Kennedy Shriver National Institute of Child Health and Human Development. Am. J. Obstet. Gynecol.215(Suppl. 1), S1–S46 (2016).
   PubMed Web of Science ®Google Scholar
• Redline RW , MinichN , TaylorHG , HackM. Placental lesions as predictors of cerebral palsy and abnormal neurocognitive function at school age in extremely low birth weight infants (<1 kg). Pediatr. Dev. Pathol.10(4), 282–292 (2007).
   PubMed Web of Science ®Google Scholar
• Nugent BM , BaleTL. The omniscient placenta: metabolic and epigenetic regulation of fetal programming. Front. Neuroendocrinol.39, 28–37 (2015).
   PubMed Web of Science ®Google Scholar
• Tilley SK , MartinEM , SmeesterLet al. Placental CpG methylation of infants born extremely preterm predicts cognitive impairment later in life. PlOS ONE13(3), e0193271 (2018).
   PubMed Web of Science ®Google Scholar
• Boekelheide K , BlumbergB , ChapinREet al. Predicting later-life outcomes of early-life exposures. Environ Health Perspect.120(10), 1353–1361 (2012).
   PubMed Web of Science ®Google Scholar
• Yan W , YueH , JiX , LiG , SangN. Prenatal NO2 exposure and neurodevelopmental disorders in offspring mice: transcriptomics reveals sex-dependent changes in cerebral gene expression. Environ. Int.138, 105659 (2020).
   PubMed Web of Science ®Google Scholar
• Bangma JT , HartwellH , SantosHPJr , O’SheaTM , FryRC. Placental programming, perinatal inflammation, and neurodevelopment impairment among those born extremely preterm. Pediatr. Res. doi:10.1038/s41390-020-01236-1 (2020) ( Epub ahead of print).
   PubMed Web of Science ®Google Scholar
• Martin EM , FryRC. Environmental influences on the epigenome: exposure-associated DNA methylation in human populations. Annu. Rev. Public Health39, 309–333 (2018).
   PubMed Web of Science ®Google Scholar
• Jang HS , ShinWJ , LeeJE , DoJT. CpG and non-CpG methylation in epigenetic gene regulation and brain function. Genes (Basel)8(6), 148 (2017).
   PubMed Web of Science ®Google Scholar
• Meakin CJ , MartinEM , SantosHPJret al. Placental CpG methylation of HPA-axis genes is associated with cognitive impairment at age 10 among children born extremely preterm. Hormones and behavior101, 29–35 (2018).
   PubMed Web of Science ®Google Scholar
• Van Dongen J , HagenbeekFA , SudermanMet al. DNA methylation signatures of aggression and closely related constructs: a meta-analysis of epigenome-wide studies across the lifespan. Mol. Psychiatry doi:10.1038/s41380-020-00987-x (2021) (Epub ahead of print).
   Web of Science ®Google Scholar
• Van Dongen J , NivardMG , BaselmansBMet al. Epigenome-wide association study of aggressive behavior. Twin Res. Hum. Genet.18(6), 686–698 (2015).
   PubMed Web of Science ®Google Scholar
• Cai M , KolluruGK , AhmedA. Small molecule, big prospects: microRNA in pregnancy and its complications. J. Pregnancy2017, 6972732 (2017).
   PubMed Web of Science ®Google Scholar
• Vaschetto LM . miRNA activation is an endogenous gene expression pathway. RNA Biol.15(6), 826–828 (2018).
   PubMed Web of Science ®Google Scholar
• Gu Y , SunJ , GroomeLJ , WangY. Differential miRNA expression profiles between the first and third trimester human placentas. Am. J. Physiol. Endocrinol. Metab.304(8), e836–e843 (2013).
   PubMed Web of Science ®Google Scholar
• Gheorghe CP , GoyalR , MittalA , LongoLD. Gene expression in the placenta: maternal stress and epigenetic responses. Int. J. Dev. Biol.54(2-3), 507–523 (2010).
   PubMed Web of Science ®Google Scholar
• Maccani MA , PadburyJF , LesterBM , KnopikVS , MarsitCJ. Placental miRNA expression profiles are associated with measures of infant neurobehavioral outcomes. Pediatr. Res.74(3), 272–278 (2013).
   PubMed Web of Science ®Google Scholar
• Eaves LA , PhookphanP , RagerJEet al. A role for microRNAs in the epigenetic control of sexually dimorphic gene expression in the human placenta. Epigenomics12(17), 1543–1558 (2020).
   PubMed Web of Science ®Google Scholar
• Martin E , SmeesterL , BommaritoPAet al. Sexual epigenetic dimorphism in the human placenta: implications for susceptibility during the prenatal period. Epigenomics9(3), 267–278 (2017).
   PubMed Web of Science ®Google Scholar
• Baron-Cohen S , LombardoMV , AuyeungB , AshwinE , ChakrabartiB , KnickmeyerR. Why are autism spectrum conditions more prevalent in males?PLOS Biol.9(6), e1001081 (2011).
   PubMed Web of Science ®Google Scholar
• Frondas-Chauty A , SimonL , BrangerBet al. Early growth and neurodevelopmental outcome in very preterm infants: impact of gender. Arch. Dis. Child. Fetal Neonatal Ed.99(5), F366–F372 (2014).
   PubMed Web of Science ®Google Scholar
• Johnston MV , HagbergH. Sex and the pathogenesis of cerebral palsy. Dev. Med. Child Neurol.49(1), 74–78 (2007).
   PubMed Web of Science ®Google Scholar
• Kuban KCK , HeerenT , O’SheaTMet al. Among children born extremely preterm a higher level of circulating neurotrophins is associated with lower risk of cognitive impairment at school age. J. Pediatr.201, 40–48e44 (2018).
   PubMed Web of Science ®Google Scholar
• O’Shea TM , AllredEN , DammannOet al. The ELGAN study of the brain and related disorders in extremely low gestational age newborns. Early Hum. Dev.85(11), 719–725 (2009).
   PubMed Web of Science ®Google Scholar
• 3′ mRNA-seq library prep ktt user guide (2020). www.lexogen.com/wp-content/uploads/2015/11/015UG009V0211_QuantSeq-Illumina.pdf
   Google Scholar
• Patro R , DuggalG , LoveMI , IrizarryRA , KingsfordC. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods14(4), 417–419 (2017).
   PubMed Web of Science ®Google Scholar
• Harrow J , FrankishA , GonzalezJMet al. GENCODE: the reference human genome annotation for the ENCODE Project. Genome Res.22(9), 1760–1774 (2012).
   PubMed Web of Science ®Google Scholar
• Clark J , AvulaV , RingCet al. Comparing the predictivity of human placental gene, microRNA, and CpG methylation signatures in relation to perinatal outcomes. Toxicol. Sci.183(2), 269–284 (2021).
   PubMed Web of Science ®Google Scholar
• Payton A , ClarkJ , EavesLet al. Placental genomic and epigenomic signatures associated with infant birth weight highlight mechanisms involved in collagen and growth factor signaling. Reprod. Toxicol.96, 221–230 (2020).
   PubMed Web of Science ®Google Scholar
• Kozomara A , Griffiths-JonesS. miRbase: integrating microRNA annotation and deep-sequencing data. NAR39, D152–D157 (2011).
   PubMed Web of Science ®Google Scholar
• NCBI . Gene expression omnibus. Placental Genomic and Epigenomic Signatures in Infants Born at Extremely Low Gestational Age.MD, USA (2020).
   Google Scholar
• Tilley SK , JosephRM , KubanKCK , DammannOU , O’SheaTM , FryRC. Genomic biomarkers of prenatal intrauterine inflammation in umbilical cord tissue predict later life neurological outcomes. PlOS ONE12(5), e0176953 (2017).
   PubMed Web of Science ®Google Scholar
• Heeren T , JosephRM , AllredEN , O’SheaTM , LevitonA , KubanKCK. Cognitive functioning at the age of 10 years among children born extremely preterm: a latent profile approach. Pediatr. Res.82(4), 614–619 (2017).
   PubMed Web of Science ®Google Scholar
• Rager JE , AuerbachSS , ChappellGA , MartinE , ThompsonCM , FryRC. Benchmark dose modeling estimates of the concentrations of inorganic arsenic that induce changes to the neonatal transcriptome, proteome, and epigenome in a pregnancy cohort. Chem. Res. Toxicol.30(10), 1911–1920 (2017).
   PubMed Web of Science ®Google Scholar
• Rager JE , BaileyKA , SmeesterLet al. Prenatal arsenic exposure and the epigenome: altered microRNAs associated with innate and adaptive immune signaling in newborn cord blood. Environ. Mol. Mutagen.55(3), 196–2008 (2014).
   PubMed Web of Science ®Google Scholar
• Rager JE , MoellerBC , MillerSKet al. Formaldehyde-associated changes in microRNAs: tissue and temporal specificity in the rat nose, white blood cells, and bone marrow. Toxicol. Sci.138(1), 36–46 (2014).
   PubMed Web of Science ®Google Scholar
• Klaren WD , RingC , HarrisMAet al. Identifying attributes that influence in vitro-to-in vivo concordance by comparing in vitro Tox21 bioactivity versus in vivo drug matrix transcriptomic responses across 130 chemicals. Toxicol. Sci.167(1), 157–171 (2019).
   PubMed Web of Science ®Google Scholar
• Rager JE , RingCL , FryRCet al. High-throughput screening data interpretation in the context of in vivo transcriptomic responses to oral Cr(VI) exposure. Toxicol. Sci.158(1), 199–212 (2017).
   PubMed Web of Science ®Google Scholar
• Textor J , VanDer Zander B , GilthorpeMS , LiśkiewiczM , EllisonGT. Robust causal inference using directed acyclic graphs: the R package ‘dagitty’. Int. J. Epidemiol.45(6), 1887–1894 (2016).
   PubMed Web of Science ®Google Scholar
• Juracek J , PilerP , JankuP , RadovaL , SlabyO. Identification of microRNA signatures in umbilical cord blood associated with maternal characteristics. PeerJ7, e6981 (2019).
   PubMed Web of Science ®Google Scholar
• Huan T , ChenG , LiuCet al. Age-associated microRNA expression in human peripheral blood is associated with all-cause mortality and age-related traits. Aging Cell17(1), e12687 (2018).
   PubMed Web of Science ®Google Scholar
• Noren Hooten N , FitzpatrickM , WoodWH3rdet al. Age-related changes in microRNA levels in serum. Aging (Albany NY)5(10), 725–740 (2013).
   PubMedGoogle Scholar
• Cui C , YangW , ShiJet al. Identification and analysis of human sex-biased microRNAs. Genomics Proteomics Bioinformatics16(3), 200–211 (2018).
   PubMed Web of Science ®Google Scholar
• Loher P , LondinER , RigoutsosI. IsomiR expression profiles in human lymphoblastoid cell lines exhibit population and gender dependencies. Oncotarget5(18), 8790–8802 (2014).
   PubMed Web of Science ®Google Scholar
• Telonis AG , RigoutsosI. Race disparities in the contribution of miRNA Isoforms and tRNA-derived fragments to triple-negative breast cancer. Cancer Res.78(5), 1140–1154 (2018).
   PubMed Web of Science ®Google Scholar
• Telonis AG , LoherP , JingY , LondinE , RigoutsosI. Beyond the one-locus-one-miRNA paradigm: microRNA isoforms enable deeper insights into breast cancer heterogeneity. Nucleic Acids Res.43(19), 9158–9175 (2015).
   PubMed Web of Science ®Google Scholar
• Ostling H , KruseR , HeleniusG , LodefalkM. Placental expression of microRNAs in infants born small for gestational age. Placenta81, 46–53 (2019).
   PubMed Web of Science ®Google Scholar
• Rodosthenous RS , BurrisHH , SandersAPet al. Second trimester extracellular microRNAs in maternal blood and fetal growth: an exploratory study. Epigenetics12(9), 804–810 (2017).
   PubMed Web of Science ®Google Scholar
• Higashijima A , MiuraK , MishimaHet al. Characterization of placenta-specific microRNAs in fetal growth restriction pregnancy. Prenat. Diagn.33(3), 214–222 (2013).
   PubMed Web of Science ®Google Scholar
• Conradt E , LesterBM , AppletonAA , ArmstrongDA , MarsitCJ. The roles of DNA methylation of NR3C1 and 11beta-HSD2 and exposure to maternal mood disorder in utero on newborn neurobehavior. Epigenetics8(12), 1321–1329 (2013).
   PubMed Web of Science ®Google Scholar
• Bromer C , MarsitCJ , ArmstrongDA , PadburyJF , LesterB. Genetic and epigenetic variation of the glucocorticoid receptor (NR3C1) in placenta and infant neurobehavior. Dev. Psychobiol.55(7), 673–683 (2013).
   PubMed Web of Science ®Google Scholar
• Ren X , KuanPF. Negative binomial additive model for RNA-seq data analysis. BMC Bioinformatics21(1), 171 (2020).
   PubMed Web of Science ®Google Scholar
• Love MI , HuberW , AndersS. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol.15(12), 550 (2014).
   PubMed Web of Science ®Google Scholar
• Benjamini Y , HochbergY. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc.: series B (Methodological)57(1), 289–300 (1995).
   Web of Science ®Google Scholar
• Lu TP , LeeCY , TsaiMHet al. miRSystem: an integrated system for characterizing enriched functions and pathways of microRNA targets. PLOS ONE7(8), e42390 (2012).
   PubMed Web of Science ®Google Scholar
• miRSystem (2016). http://mirsystem.cgm.ntu.edu.tw/
   Google Scholar
• Hess JL , RadonjicNV , PatakJ , GlattSJ , FaraoneSV. Autophagy, apoptosis, and neurodevelopmental genes might underlie selective brain region vulnerability in attention-deficit/hyperactivity disorder. Mol. Psychiatry doi:10.1038/s41380-020-00974-2 (2020) (Epub ahead of print).
   Web of Science ®Google Scholar
• Wang C , ChenQ , HamajimaYet al. Id2 regulates the proliferation of squamous cell carcinoma in vitro via the NF-kappaB/cyclin D1 pathway. Chin. J. Cancer31(9), 430–439 (2012).
   PubMedGoogle Scholar
• Jiang C , ZhuY , ZhouZet al. TMEM43/LUMA is a key signaling component mediating EGFR-induced NF-kappaB activation and tumor progression. Oncogene36(20), 2813–2823 (2017).
   PubMed Web of Science ®Google Scholar
• Zhang R , LiL , ChenLet al. MAP7 interacts with RC3H1 and cooperatively regulate cell-cycle progression of cervical cancer cells via activating the NF-kappaB signaling. Biochem. Biophys. Res. Commun.527(1), 56–63 (2020).
   PubMed Web of Science ®Google Scholar
• Murakawa Y , HinzM , MothesJet al. RC3H1 post-transcriptionally regulates A20 mRNA and modulates the activity of the IKK/NF-kappaB pathway. Nat. Commun.6, 7367 (2015).
   PubMed Web of Science ®Google Scholar
• Leviton A , GressensP , WolkenhauerO , DammannO. Systems approach to the study of brain damage in the very preterm newborn. Front. Syst. Neurosci.9, 58 (2015).
   PubMedGoogle Scholar
• Jiang NM , CowanM , MoonahSN , PetriWAJr. The impact of systemic inflammation on neurodevelopment. Trends Mol. Med.24(9), 794–804 (2018).
   PubMed Web of Science ®Google Scholar
• Oldenburg KS , O’SheaTM , FryRC. Genetic and epigenetic factors and early life inflammation as predictors of neurodevelopmental outcomes. Semin. Fetal Neonatal Med.25(3), 101115 (2020).
   PubMed Web of Science ®Google Scholar
• Tomlinson MS , BommaritoPA , MartinEMet al. Microorganisms in the human placenta are associated with altered CpG methylation of immune and inflammation-related genes. PLOS ONE12(12), e0188664 (2017).
   PubMed Web of Science ®Google Scholar
• Lesseur C , PaquetteAG , MarsitCJ. Epigenetic regulation of infant neurobehavioral outcomes. Med. Epigenet.2(2), 71–79 (2014).
   PubMedGoogle Scholar
• Lin J , ZhangD , FanYet al. Regulation of cancer stem cell self-renewal by HOXB9 antagonizes endoplasmic reticulum stress-induced melanoma cell apoptosis via the miR-765-FOXA2 axis. J. Invest. Dermatol.138(7), 1609–1619 (2018).
   PubMed Web of Science ®Google Scholar
• Liu S , GongY , XuXDet al. microRNA-936/ERBB4/AKT axis exhibits anticancer properties of gastric cancer through inhibition of cell proliferation, migration, and invasion. Kaohsiung J. Med. Sci.37(2), 111–120 (2021).
   PubMed Web of Science ®Google Scholar
• Fayyad-Kazan H , Fayyad-KazanM , MerimiMet al. The micronome of mesenchymal stromal cells is partially responsive to inflammation. Cell Biol. Int.42(2), 254–260 (2018).
   PubMed Web of Science ®Google Scholar
• Zhang X , GuH , WangL , HuangF , CaiJ. miR-885-3p is down-regulated in peripheral blood mononuclear cells from T1D patients and regulates the inflammatory response via targeting TLR4/NF-kappaB signaling. J. Gene Med.22(1), e3145 (2020).
   PubMed Web of Science ®Google Scholar
• Guo J , ZhaoX , LiuZet al. Transmissible gastroenteritis virus ORF3b up-regulates miR-885-3p to counteract TNF-alpha production via inhibiting NF-kappaB pathway. Vet. Microbiol.261, 109189 (2021).
   PubMed Web of Science ®Google Scholar
• Zhou W , WangY , WuR , HeY , SuQ , ShiG. microRNA-488 and -920 regulate the production of proinflammatory cytokines in acute gouty arthritis. Arthritis Res. Ther.19(1), 203 (2017).
   PubMedGoogle Scholar
• Santos HP Jr , BhattacharyaA , JosephRMet al. Evidence for the placenta–brain axis: multi-omic kernel aggregation predicts intellectual and social impairment in children born extremely preterm. Mol. Autism11(1), 97 (2020).
   PubMed Web of Science ®Google Scholar
• Strauss JF 3rd , RomeroR , Gomez-LopezNet al. Spontaneous preterm birth: advances toward the discovery of genetic predisposition. Am. J. Obstet. Gynecol.218(3), 294–314e292 (2018).
   PubMed Web of Science ®Google Scholar
• Bukowski R , SadovskyY , GoodarziHet al. Onset of human preterm and term birth is related to unique inflammatory transcriptome profiles at the maternal fetal interface. PeerJ5, e3685 (2017).
   PubMed Web of Science ®Google Scholar
• Rangaraju S , DammerEB , RazaSAet al. Identification and therapeutic modulation of a pro-inflammatory subset of disease-associated-microglia in Alzheimer’s disease. Mol. Neurodegener.13(1), 24 (2018).
   PubMedGoogle Scholar