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Research Article

Allele-specific Methylation of Imprinted Genes in Fetal Cord Blood is Influenced By Cis-Acting Genetic Variants and Parental Factors

, , , , , , , & show all
Pages 1315-1326 | Received 18 Apr 2018, Accepted 12 Jul 2018, Published online: 21 Sep 2018

References

  • Nelson SM , TelferEE , AndersonRA . The aging ovary and uterus: new biological insights . Hum. Reprod. Update19 ( 1 ), 67 – 83 ( 2013 ).
  • Fragouli E , WellsD , DelhantyJD . Chromosome abnormalities in the human oocyte . Cytogenet. Genome Res.133 ( 2-4 ), 107 – 118 ( 2011 ).
  • Eichenlaub-Ritter U . Oocyte aging and its cellular basis . Int. J. Dev. Biol.56 ( 10-12 ), 841 – 852 ( 2012 ).
  • Maclennan M , CrichtonJH , PlayfootCJ , AdamsIR . Oocyte development, meiosis and aneuploidy . Semin. Cell Dev. Biol.45 , 68 – 76 ( 2015 ).
  • Jessberger R . Age-related aneuploidy through cohesion exhaustion . EMBO Rep.13 ( 6 ), 539 – 546 ( 2012 ).
  • Titus S , LiF , StobezkiRet al. Impairment of BRCA1-related DNA double-strand break repair leads to ovarian aging in mice and humans . Sci. Transl. Med.5 ( 172 ), 172ra121 ( 2013 ).
  • De La Rochebrochard E , ThonneauP . Paternal age and maternal age are risk factors for miscarriage; results of a multicentre European study . Hum. Reprod.17 ( 6 ), 1649 – 1656 ( 2002 ).
  • Luna M , FinklerE , BarrittJet al. Paternal age and assisted reproductive technology outcome in ovum recipients . Fertil. Steril.92 ( 5 ), 1772 – 1775 ( 2009 ).
  • Liu K , CaseA ; Reproductive Endocrinology and Infertility Committee . Advanced reproductive age and fertility . J. Obstet. Gynaecol. Can.33 ( 11 ), 1165 – 1175 ( 2011 ).
  • Kong A , FriggeML , MassonGet al. Rate of de novo mutations and the importance of father’s age to disease risk . Nature488 ( 7412 ), 471 – 475 ( 2012 ).
  • Crow JF . The origins, patterns and implications of human spontaneous mutation . Nat. Rev. Genet.1 ( 1 ), 40 – 47 ( 2000 ).
  • Bennett-Baker PE , WilkowskiJ , BurkeDT . Age-associated activation of epigenetically repressed genes in the mouse . Genetics165 ( 4 ), 2055 – 2062 ( 2003 ).
  • Milekic MH , XinY , O’DonnellAet al. Age-related sperm DNA methylation changes are transmitted to offspring and associated with abnormal behavior and dysregulated gene expression . Mol. Psychiatry20 ( 8 ), 995 – 1001 ( 2015 ).
  • Smith RG , ReichenbergA , KemberRLet al. Advanced paternal age is associated with altered DNA methylation at brain-expressed imprinted loci in inbred mice: implications for neuropsychiatric disease . Mol. Psychiatry18 ( 6 ), 635 – 636 ( 2013 ).
  • Jenkins TG , AstonKI , PfluegerC , CairnsBR , CarrellDT . Age-associated sperm DNA methylation alterations: possible implications in offspring disease susceptibility . PLoS Genet.10 ( 7 ), e1004458 ( 2014 ).
  • Atsem S , ReichenbachJ , PotabattulaRet al. Paternal age effects on sperm FOXK1 and KCNA7 methylation and transmission into the next generation . Hum. Mol. Genet.25 ( 22 ), 4996 – 5005 ( 2016 ).
  • Donkin I , VersteyheS , IngerslevLRet al. Obesity and bariatric surgery drive epigenetic variation of spermatozoa in humans . Cell Metab.23 ( 2 ), 369 – 378 ( 2016 ).
  • Soubry A , GuoL , HuangZet al. Obesity-related DNA methylation at imprinted genes in human sperm: results from the TIEGER study . Clin. Epigenetics8 , 51 ( 2016 ).
  • Chen YP , XiaoXM , LiJ , ReichetzederC , WangZN , HocherB . Paternal body mass index (BMI) is associated with offspring intrauterine growth in a gender dependent manner . PLoS ONE7 ( 5 ), e36329 ( 2012 ).
  • Freeman E , FletcherR , CollinsCE , MorganPJ , BurrowsT , CallisterR . Preventing and treating childhood obesity: time to target fathers . Int. J. Obes.36 ( 1 ), 12 – 15 ( 2012 ).
  • Yue MX , FuXW , ZhouGBet al. Abnormal DNA methylation in oocytes could be associated with a decrease in reproductive potential in old mice . J. Assist. Reprod. Genet.29 ( 7 ), 643 – 650 ( 2012 ).
  • Reik W , DeanW , WalterJ . Epigenetic reprogramming in mammalian development . Science293 ( 5532 ), 1089 – 1093 ( 2001 ).
  • Denomme MM , MannMR . Genomic imprints as a model for the analysis of epigenetic stability during assisted reproductive technologies . Reproduction144 ( 4 ), 393 – 409 ( 2012 ).
  • Leitão E , BeygoJ , ZeschnigkM , Klein-HitpassL , BargullM , RahmannS , HorsthemkeB . Locus-Specific DNA methylation analysis by targeted deep bisulfite sequencing . Methods Mol. Biol.1767 , 351 – 366 ( 2017 ).
  • Haertle L , MaierhoferA , BöckJet al. Hypermethylation of the non-imprinted maternal MEG3 and paternal MEST alleles is highly variable among normal individuals . PLoS ONE12 ( 8 ), e0184030 ( 2017 ).
  • Gillman MW . Developmental origins of health and disease . N. Engl. J. Med.353 ( 17 ), 1848 – 1850 ( 2005 ).
  • Barker DJ . The origins of the developmental origins theory . J. Intern. Med.261 ( 5 ), 412 – 417 ( 2007 ).
  • Wei Y , SchattenH , SunQY . Environmental epigenetic inheritance through gametes and implications for human reproduction . Hum. Reprod. Update21 ( 2 ), 194 – 208 ( 2015 ).
  • Blake GE , WatsonED . Unravelling the complex mechanisms of transgenerational epigenetic inheritance . Curr. Opin. Chem. Biol.33 , 101 – 107 ( 2016 ).
  • Weber M , HellmannI , StadlerMBet al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome . Nat. Genet.39 ( 4 ), 457 – 466 ( 2007 ).
  • Sontag LB , LorinczMC , Georg LuebeckE . Dynamics, stability and inheritance of somatic DNA methylation imprints . J. Theor. Biol.242 ( 4 ), 890 – 899 ( 2006 ).
  • Murphy SK , WylieAA , CovelerKJet al. Epigenetic detection of human chromosome 14 uniparental disomy . Hum. Mutat.22 ( 1 ), 92 – 97 ( 2003 ).
  • Laborda J . The role of the epidermal growth factor-like protein dlk in cell differentiation . Histol. Histopathol.15 ( 1 ), 119 – 129 ( 2000 ).
  • Zhou Y , ZhongY , WangYet al. Activation of p53 by MEG3 non-coding RNA . J. Biol. Chem.282 ( 34 ), 24731 – 24742 ( 2007 ).
  • Kameswaran V , BramswigNC , MckennaLBet al. Epigenetic regulation of the DLK1-MEG3 microRNA cluster in human type 2 diabetic islets . Cell Metab.19 ( 1 ), 135 – 145 ( 2014 ).
  • Li L , KeverneEB , AparicioSA , IshinoF , BartonSC , SuraniMA . Regulation of maternal behavior and offspring growth by paternally expressed Peg3 . Science284 ( 5412 ), 330 – 333 ( 1999 ).
  • Perera BP , KimJ . Sex and tissue specificity of Peg3 promoters . PLoS ONE11 ( 10 ), e0164158 ( 2016 ).
  • Riesewijk AM , HuL , SchulzUet al. Monoallelic expression of human PEG1/MEST is paralleled by parent-specific methylation in fetuses . Genomics42 ( 2 ), 236 – 244 ( 1997 ).
  • Kozak LP , NewmanS , ChaoPM , MendozaT , KozaRA . The early nutritional environment of mice determines the capacity for adipose tissue expansion by modulating genes of caveolae structure . PLoS ONE5 ( 6 ), e11015 ( 2010 ).
  • El Hajj N , PliushchG , SchneiderEet al. Metabolic programming of MEST DNA methylation by intrauterine exposure to gestational diabetes mellitus . Diabetes62 ( 4 ), 1320 – 1328 ( 2013 ).
  • Kamei Y , SuganamiT , KohdaTet al. Peg1/Mest in obese adipose tissue is expressed from the paternal allele in an isoform-specific manner . FEBS Lett.581 ( 1 ), 91 – 96 ( 2007 ).
  • Kosaki K , KosakiR , CraigenWJ , MatsuoN . Isoform-specific imprinting of the human PEG1/MEST gene . Am. J. Hum. Genet.66 ( 1 ), 309 – 312 ( 2000 ).
  • Uyar A , SeliE . The impact of assisted reproductive technologies on genomic imprinting and imprinting disorders . Curr. Opin. Obstet. Gynecol.26 ( 3 ), 210 – 221 ( 2014 ).
  • Zechner U , PliushchG , SchneiderEet al. Quantitative methylation analysis of developmentally important genes in human pregnancy losses after ART and spontaneous conception . Mol. Hum. Reprod.16 ( 9 ), 704 – 713 ( 2010 ).
  • Vincent RN , GoodingLD , LouieK , Chan WongE , MaS . Altered DNA methylation and expression of PLAGL1 in cord blood from assisted reproductive technology pregnancies compared with natural conceptions . Fertil. Steril.106 ( 3 ), 739.e3 – 748.e3 ( 2016 ).
  • Whitelaw N , BhattacharyaS , HoadG , HorganGW , HamiltonM , HaggartyP . Epigenetic status in the offspring of spontaneous and assisted conception . Hum. Reprod.29 ( 7 ), 1452 – 1458 ( 2014 ).
  • Tierling S , SourenNY , GriesJet al. Assisted reproductive technologies do not enhance the variability of DNA methylation imprints in human . J. Med. Genet.47 ( 6 ), 371 – 376 ( 2010 ).
  • Oliver VF , MilesHL , CutfieldWS , HofmanPL , LudgateJL , MorisonIM . Defects in imprinting and genome-wide DNA methylation are not common in the in vitro fertilization population . Fertil. Steril.97 ( 1 ), 147.e7 – 153.e7 ( 2012 ).
  • El Hajj N , HaertleL , DittrichMet al. DNA methylation signatures in cord blood of ICSI children . Hum. Reprod.32 ( 8 ), 1761 – 1769 ( 2017 ).
  • Schilling E , El ChartouniC , RehliM . Allele-specific DNA methylation in mouse strains is mainly determined by cis-acting sequences . Genome Res19 ( 11 ), 2028 – 2035 ( 2009 ).
  • Kerkel K , SpadolaA , YuanEet al. Genomic surveys by methylation-sensitive SNP analysis identify sequence-dependent allele-specific DNA methylation . Nat. Genet.40 ( 7 ), 904 – 908 ( 2008 ).
  • Schalkwyk LC , MeaburnEL , SmithRet al. Allelic skewing of DNA methylation is widespread across the genome . Am. J. Hum. Genet.86 ( 2 ), 196 – 212 ( 2010 ).
  • Meaburn EL , SchalkwykLC , MillJ . Allele-specific methylation in the human genome: implications for genetic studies of complex disease . Epigenetics5 ( 7 ), 578 – 582 ( 2010 ).
  • Cheung WA , ShaoX , MorinAet al. Functional variation in allelic methylomes underscores a strong genetic contribution and reveals novel epigenetic alterations in the human epigenome . Genome Biol.18 ( 1 ), 50 ( 2017 ).
  • Murrell A , ItoY , VerdeGet al. Distinct methylation changes at the IGF2-H19 locus in congenital growth disorders and cancer . PLoS ONE3 ( 3 ), e1849 ( 2008 ).
  • Sullivan MJ , TaniguchiT , JheeA , KerrN , ReeveAE . Relaxation of IGF2 imprinting in Wilms tumours associated with specific changes in IGF2 methylation . Oncogene18 ( 52 ), 7527 – 7534 ( 1999 ).
  • Cui H , OnyangoP , BrandenburgS , WuY , HsiehCL , FeinbergAP . Loss of imprinting in colorectal cancer linked to hypomethylation of H19 and IGF2 . Cancer Res.62 ( 22 ), 6442 – 6446 ( 2002 ).
  • Cui H , Cruz-CorreaM , GiardielloFMet al. Loss of IGF2 imprinting: a potential marker of colorectal cancer risk . Science299 ( 5613 ), 1753 – 1755 ( 2003 ).
  • Sakatani T , WeiM , KatohMet al. Epigenetic heterogeneity at imprinted loci in normal populations . Biochem. Biophys. Res. Commun.283 ( 5 ), 1124 – 1130 ( 2001 ).
  • Rancourt RC , HarrisHR , BaraultL , MichelsKB . The prevalence of loss of imprinting of H19 and IGF2 at birth . FASEB J.27 ( 8 ), 3335 – 3343 ( 2013 ).