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Research Article

Prenatal Neun+ Neurons of Down Syndrome Display Aberrant Integrative DNA Methylation and Gene Expression Profiles

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Pages 375-390 | Received 20 Dec 2021, Accepted 15 Feb 2022, Published online: 02 Mar 2022

References

  • Pierce MJ , LafranchiSH , PinterJD. Characterization of thyroid abnormalities in a large cohort of children with Down syndrome. Horm. Res. Paediatr.87(3), 170–178 (2017).
  • Aversa T , CoricaD , ZirilliGet al. Phenotypic expression of autoimmunity in children with autoimmune thyroid disorders. Front. Endocrinol. (Lausanne)10, 476 (2019).
  • Wiseman FK , Al-JanabiT , HardyJet al. A genetic cause of Alzheimer disease: mechanistic insights from Down syndrome. Nat. Rev. Neurosci.16(9), 564–574 (2015).
  • Asai M , KawakuboT , MoriR , IwataN. Elucidating pathogenic mechanisms of early-onset Alzheimer’s disease in Down syndrome patients. Yakugaku Zasshi137(7), 801–805 (2017).
  • Antonarakis SE , LyleR , DermitzakisET , ReymondA , DeutschS. Chromosome 21 and Down syndrome: from genomics to pathophysiology. Nat. Rev. Genet.5(10), 725–738 (2004).
  • Newton R . Quality of life in Down syndrome: a matter of perspective. Dev. Med. Child Neurol.60(4), 337–338 (2018).
  • Baburamani AA , PatkeePA , ArichiT , RutherfordMA. New approaches to studying early brain development in Down syndrome. Dev. Med. Child Neurol.61(8), 867–879 (2019).
  • Lyle R , BenaF , GagosSet al. Genotype-phenotype correlations in Down syndrome identified by array CGH in 30 cases of partial trisomy and partial monosomy chromosome 21. Eur. J. Hum. Genet.17(4), 454–466 (2009).
  • Schouten JP , McelgunnCJ , WaaijerR , ZwijnenburgD , DiepvensF , PalsG. Relative quantification of 40 nucleic acid sequences by multiplex ligation-dependent probe amplification. Nucleic Acids Res.30(12), e57 (2002).
  • Aref-Eshghi E , BendEG , ColaiacovoSet al. Diagnostic utility of genome-wide DNA methylation testing in genetically unsolved individuals with suspected hereditary conditions. Am. J. Hum. Genet.104(4), 685–700 (2019).
  • Henneman P , BoumanA , MulAet al. Widespread domain-like perturbations of DNA methylation in whole blood of Down syndrome neonates. PLoS One13(3), e0194938 (2018).
  • Oepkes D , Page-ChristiaensGC , BaxCJet al. Trial by Dutch laboratories for evaluation of non-invasive prenatal testing. Part I – clinical impact. Prenat. Diagn.36(12), 1083–1090 (2016).
  • Van Der Meij KRM , SistermansEA , MacvilleMVEet al. TRIDENT-2: national implementation of genome-wide non-invasive prenatal testing as a first-tier screening test in the Netherlands. Am. J. Hum. Genet. doi:10.1016/j.ajhg.2019.10.005 (2019).
  • Bakkeren IM , Kater-KuipersA , BunnikEMet al. Implementing non-invasive prenatal testing (NIPT) in the Netherlands: an interview study exploring opinions about and experiences with societal pressure, reimbursement, and an expanding scope. J. Genet. Couns. doi:10.1002/jgc4.1188 (2019).
  • Hill M , BarrettA , ChoolaniM , LewisC , FisherJ , ChittyLS. Has noninvasive prenatal testing impacted termination of pregnancy and live birth rates of infants with Down syndrome?Prenat. Diagn.37(13), 1281–1290 (2017).
  • Antonarakis SE . Down syndrome and the complexity of genome dosage imbalance. Nat. Rev. Genet.18(3), 147–163 (2017).
  • Lejeune J , GautierM , TurpinR. [Study of somatic chromosomes from 9 mongoloid children]. C. R. Hebd. Seances Acad. Sci.248(11), 1721–1722 (1959).
  • Korenberg JR , KawashimaH , PulstSMet al. Molecular definition of a region of chromosome 21 that causes features of the Down syndrome phenotype. Am. J. Hum. Genet.47(2), 236–246 (1990).
  • Patterson D . Genetic mechanisms involved in the phenotype of Down syndrome. Ment. Retard. Dev. Disabil. Res. Rev.13(3), 199–206 (2007).
  • Kurabayashi N , SanadaK. Molecular mechanism underlying abnormal differentiation of neural progenitor cells in the developing Down syndrome brain. Yakugaku Zasshi137(7), 795–800 (2017).
  • Koch A , DeMeyer T , JeschkeJ , Van CriekingeW. MEXPRESS: visualizing expression, DNA methylation and clinical TCGA data. BMC Genomics16, 636 (2015).
  • Kribelbauer JF , LuXJ , RohsR , MannRS , BussemakerHJ. Toward a mechanistic understanding of DNA methylation readout by transcription factors. J. Mol. Biol. doi:10.1016/j.jmb.2019.10.021 (2019).
  • Sarnat HB , NochlinD , BornDE. Neuronal nuclear antigen (NeuN): a marker of neuronal maturation in early human fetal nervous system. Brain Dev.20(2), 88–94 (1998).
  • Rizzardi LF , HickeyPF , RodriguezDiblasi Vet al. Neuronal brain-region-specific DNA methylation and chromatin accessibility are associated with neuropsychiatric trait heritability. Nat. Neurosci.22(2), 307–316 (2019).
  • Price AJ , Collado-TorresL , IvanovNAet al. Divergent neuronal DNA methylation patterns across human cortical development reveal critical periods and a unique role of CpH methylation. Genome Biol.20(1), 196 (2019).
  • Lu J , MccarterM , LianGet al. Global hypermethylation in fetal cortex of Down syndrome due to DNMT3L overexpression. Hum. Mol. Genet.25(9), 1714–1727 (2016).
  • Montano CM , IrizarryRA , KaufmannWEet al. Measuring cell-type specific differential methylation in human brain tissue. Genome Biol.14(8), R94 (2013).
  • Krishnaswami SR , GrindbergRV , NovotnyMet al. Using single nuclei for RNA-seq to capture the transcriptome of postmortem neurons. Nat. Protoc.11(3), 499–524 (2016).
  • Van Iterson M , TobiEW , SliekerRCet al. MethylAid: visual and interactive quality control of large Illumina 450k datasets. Bioinformatics30(23), 3435–3437 (2014).
  • Pidsley R , ZotenkoE , PetersTJet al. Critical evaluation of the Illumina MethylationEPIC BeadChip microarray for whole-genome DNA methylation profiling. Genome Biol.17(1), 208 (2016).
  • Tsai PC , BellJT. Power and sample size estimation for epigenome-wide association scans to detect differential DNA methylation. Int. J. Epidemiol.44(4), 1429–1441 (2015).
  • Peters TJ , BuckleyMJ , StathamALet al. De novo identification of differentially methylated regions in the human genome. Epigenetics Chromatin8, 6 (2015).
  • A quality control tool for high throughput sequence data. www.bioinformatics.babraham.ac.uk/projects/fastqc/
  • Chen Y , LunAT , SmythGK. From reads to genes to pathways: differential expression analysis of RNA-seq experiments using Rsubread and the edgeR quasi-likelihood pipeline. F1000Res5, 1438 (2016).
  • Dobin A , DavisCA , SchlesingerFet al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics29(1), 15–21 (2013).
  • Dobin A , GingerasTR. Optimizing RNA-seq mapping with STAR. Methods Mol. Biol.1415, 245–262 (2016).
  • Li H , HandsakerB , WysokerAet al. The Sequence Alignment/Map format and SAMtools. Bioinformatics25(16), 2078–2079 (2009).
  • Ewels P , MagnussonM , LundinS , KallerM. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics32(19), 3047–3048 (2016).
  • Anders S , HuberW. Differential expression analysis for sequence count data. Genome Biol.11(10), R106 (2010).
  • Li Yim AYF , DeBruyn JR , DuijvisNWet al. A distinct epigenetic profile distinguishes stenotic from non-inflamed fibroblasts in the ileal mucosa of Crohn’s disease patients. PLoS One13(12), e0209656 (2018).
  • Korotkevich G , SukhovV , BudinN , ShpakB , ArtyomovMN , SergushichevA. Fast gene set enrichment analysis. BioRxiv doi:10.1101/060012 (2021).
  • Mendioroz M , DoC , JiangXet al. Trans effects of chromosome aneuploidies on DNA methylation patterns in human Down syndrome and mouse models. Genome Biol.16, 263 (2015).
  • Kerkel K , SchupfN , HattaKet al. Altered DNA methylation in leukocytes with trisomy 21. PLoS Genet.6(11), e1001212 (2010).
  • Laufer BI , HwangH , Vogel CierniaA , MordauntCE , LasalleJM. Whole genome bisulfite sequencing of Down syndrome brain reveals regional DNA hypermethylation and novel disorder insights. Epigenetics14(7), 672–684 (2019).
  • Shi WL , LiuZZ , WangHDet al. Integrated miRNA and mRNA expression profiling in fetal hippocampus with Down syndrome. J. Biomed. Sci.23(1), 48 (2016).
  • Vetrini F , MckeeS , RosenfeldJAet al. De novo and inherited TCF20 pathogenic variants are associated with intellectual disability, dysmorphic features, hypotonia, and neurological impairments with similarities to Smith–Magenis syndrome. Genome Med.11(1), 12 (2019).
  • Barbosa RTA , DeOliveira ASB , DeLima Antao JYFet al. Augmentative and alternative communication in children with Down’s syndrome: a systematic review. BMC Pediatr.18(1), 160 (2018).
  • Jiang S , ZhouD , WangYYet al. Identification of de novo mutations in prenatal neurodevelopment-associated genes in schizophrenia in two Han Chinese patient-sibling family-based cohorts. Transl. Psychiatry10(1), 307 (2020).
  • Yang R , XuC , BiererLMet al. Longitudinal genome-wide methylation study of PTSD treatment using prolonged exposure and hydrocortisone. Transl. Psychiatry11(1), 398 (2021).
  • Startin CM , D’souzaH , BallGet al. Health comorbidities and cognitive abilities across the lifespan in Down syndrome. J. Neurodev. Disord.12(1), 4 (2020).
  • Malaga S , PardoR , MalagaI , OrejasG , Fernandez-ToralJ. Renal involvement in Down syndrome. Pediatr. Nephrol.20(5), 614–617 (2005).
  • Baumer N , BaumerS , BerkenfeldFet al. Maintenance of leukemia-initiating cells is regulated by the CDK inhibitor Inca1. PLoS One9(12), e115578 (2014).
  • Fang X , PoulsenR , ZhaoL , WangJ , RivkeesSA , WendlerCC. Knockdown of DNA methyltransferase 1 reduces DNA methylation and alters expression patterns of cardiac genes in embryonic cardiomyocytes. FEBS Open Bio. doi:10.1002/2211-5463.13252 (2021).
  • Monies D , AbouAl-Shaar H , GoljanEAet al. Identification of a novel genetic locus underlying tremor and dystonia. Hum. Genomics11(1), 25 (2017).
  • Marchionni E , MeneretA , KerenBet al. KIF1C variants are associated with hypomyelination, ataxia, tremor, and dystonia in fraternal twins. Tremor Other Hyperkinet Mov (NY)9, (2019).
  • Pinto B , MorelliG , RastogiMet al. Rescuing over-activated microglia restores cognitive performance in juvenile animals of the Dp(16) mouse model of Down syndrome. Neuron108(5), 887–904.e812 (2020).
  • Lewcock JW , SchlepckowK , DiPaolo G , TahirovicS , MonroeKM , HaassC. Emerging microglia biology defines novel therapeutic approaches for Alzheimer’s disease. Neuron108(5), 801–821 (2020).
  • Zhou W , TricheTJJr , LairdPW , ShenH. SeSAMe: reducing artifactual detection of DNA methylation by Infinium BeadChips in genomic deletions. Nucleic Acids Res.46(20), e123 (2018).