Association of Grandmaternal Smoking During Pregnancy with DNA Methylation of Grandchildren: the Isle of Wight Study

Reference

• Gaysina D , FergussonDM , LeveLDet al. Maternal smoking during pregnancy and offspring conduct problems: evidence from 3 independent genetically sensitive research designs. JAMA Psychiatry70(9), 956–963 (2013).
   PubMed Web of Science ®Google Scholar
• Wang X , ZuckermanB , PearsonCet al. Maternal cigarette smoking, metabolic gene polymorphism, and infant birth weight. JAMA287(2), 195–202 (2002).
   PubMed Web of Science ®Google Scholar
• Stick SM , BurtonPR , GurrinL , SlyPD , LesouefPN. Effects of maternal smoking during pregnancy and a family history of asthma on respiratory function in newborn infants. Lancet348(9034), 1060–1064 (1996).
   PubMed Web of Science ®Google Scholar
• Cnattingius S . The epidemiology of smoking during pregnancy: smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine Tob. Res.6(Suppl. 2), S125–S140 (2004).
   PubMed Web of Science ®Google Scholar
• Hanrahan JP , TagerIB , SegalMRet al. The effect of maternal smoking during pregnancy on early infant lung function. Am. Rev. Respir. Dis.145(5), 1129–1135 (1992).
   PubMed Web of Science ®Google Scholar
• Horta BL , VictoraCG , MenezesAM , HalpernR , BarrosFC. Low birthweight, preterm births and intrauterine growth retardation in relation to maternal smoking. Paediatr. Perinat. Epidemiol.11(2), 140–151 (1997).
   PubMed Web of Science ®Google Scholar
• Chiolero A , BovetP , PaccaudF. Association between maternal smoking and low birth weight in Switzerland: the EDEN study. Swiss Med. Wkly135(35-36), 525–530 (2005).
   PubMed Web of Science ®Google Scholar
• Pereira PP , DaMata FA , FigueiredoAC , DeAndrade KR , PereiraMG. Maternal active smoking during pregnancy and low birth weight in the Americas: a systematic review and meta-analysis. Nicotine Tob. Res.19(5), 497–505 (2017).
   PubMed Web of Science ®Google Scholar
• Kyrklund-Blomberg NB , CnattingiusS. Preterm birth and maternal smoking: risks related to gestational age and onset of delivery. Am. J. Obstet. Gynecol.179(4), 1051–1055 (1998).
   PubMed Web of Science ®Google Scholar
• Kyrklund-Blomberg NB , GranathF , CnattingiusS. Maternal smoking and causes of very preterm birth. Acta Obstet. Gynecol. Scand.84(6), 572–577 (2005).
   PubMed Web of Science ®Google Scholar
• Jaakkola JJ , GisslerM. Maternal smoking in pregnancy, fetal development, and childhood asthma. Am. J. Public Health94(1), 136–140 (2004).
   PubMed Web of Science ®Google Scholar
• Burke H , Leonardi-BeeJ , HashimAet al. Prenatal and passive smoke exposure and incidence of asthma and wheeze: systematic review and meta-analysis. Pediatrics129(4), 735–744 (2012).
   PubMed Web of Science ®Google Scholar
• Power C , JefferisBJ. Fetal environment and subsequent obesity: a study of maternal smoking. Int. J. Epidemiol.31(2), 413–419 (2002).
   PubMed Web of Science ®Google Scholar
• Ino T . Maternal smoking during pregnancy and offspring obesity: meta-analysis. Pediatr. Int.52(1), 94–99 (2010).
   PubMed Web of Science ®Google Scholar
• Maritz GS , MutemwaM. The effect of grand maternal nicotine exposure during gestation and lactation on lung integrity of the F2 generation. Pediatr. Pulmonol.49(1), 67–75 (2014).
   PubMed Web of Science ®Google Scholar
• Magnus MC , HabergSE , KarlstadO , NafstadP , LondonSJ , NystadW. Grandmother’s smoking when pregnant with the mother and asthma in the grandchild: the Norwegian Mother and Child Cohort Study. Thorax70(3), 237–243 (2015).
   PubMed Web of Science ®Google Scholar
• Lodge CJ , BrabackL , LoweAJ , DharmageSC , OlssonD , ForsbergB. Grandmaternal smoking increases asthma risk in grandchildren: a nationwide Swedish cohort. Clin. Exp. Allergy48(2), 167–174 (2018).
   PubMed Web of Science ®Google Scholar
• Li YF , LangholzB , SalamMT , GillilandFD. Maternal and grandmaternal smoking patterns are associated with early childhood asthma. Chest127(4), 1232–1241 (2005).
   PubMed Web of Science ®Google Scholar
• Miller LL , HendersonJ , NorthstoneK , PembreyM , GoldingJ. Do grandmaternal smoking patterns influence the etiology of childhood asthma?Chest145(6), 1213–1218 (2014).
   PubMed Web of Science ®Google Scholar
• Breton CV , ByunHM , WentenM , PanF , YangA , GillilandFD. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am. J. Respir. Crit. Care Med.180(5), 462–467 (2009).
   PubMed Web of Science ®Google Scholar
• Maccani JZJ , KoestlerDC , HousemanEA , MarsitCJ , KelseyKT. Placental DNA methylation alterations associated with maternal tobacco smoking at the RUNX3 gene are also associated with gestational age. Epigenomics5(6), 619–630 (2013).
   PubMed Web of Science ®Google Scholar
• Richmond RC , SimpkinAJ , WoodwardGet al. Prenatal exposure to maternal smoking and offspring DNA methylation across the lifecourse: findings from the Avon Longitudinal Study of Parents and Children (ALSPAC). Hum. Mol. Genet.24(8), 2201–2217 (2015).
   PubMed Web of Science ®Google Scholar
• Arshad SH , HideDW. Effect of environmental factors on the development of allergic disorders in infancy. J. Allergy Clin. Immunol.90(2), 235–241 (1992).
   PubMed Web of Science ®Google Scholar
• Soto-Ramirez N , ZiyabAH , KarmausWet al. Epidemiologic methods of assessing asthma and wheezing episodes in longitudinal studies: measures of change and stability. J. Epidemiol.23(6), 399–410 (2013).
   PubMed Web of Science ®Google Scholar
• Arshad SH , HollowayJW , KarmausWet al. Cohort profile: the Isle Of Wight whole population birth cohort (IOWBC). Int. J. Epidemiol.47(4), 1043–1044i (2018).
   PubMed Web of Science ®Google Scholar
• Verification SSOB . Biochemical verification of tobacco use and cessation. Nicotine Tob. Res.4(2), 149–159 (2002).
   PubMedGoogle Scholar
• Balhara YPS , JainR. A receiver operated curve-based evaluation of change in sensitivity and specificity of cotinine urinalysis for detecting active tobacco use. J. Cancer Res. Ther9(1), 84–89 (2013).
   PubMed Web of Science ®Google Scholar
• Jiang Y , WeiJF , ZhangHMet al. Epigenome wide comparison of DNA methylation profile between paired umbilical cord blood and neonatal blood on Guthrie cards. Epigenetics15(5), 454–461 (2020).
   PubMed Web of Science ®Google Scholar
• Miller SA , DykesDD , PoleskyHF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res.16(3), 1215 (1988).
   PubMed Web of Science ®Google Scholar
• Beyan H , DownTA , RamagopalanSVet al. Guthrie card methylomics identifies temporally stable epialleles that are present at birth in humans. Genome Res.22(11), 2138–2145 (2012).
   PubMed Web of Science ®Google Scholar
• Bibikova M , FanJ-B. GoldenGate assay for DNA methylation profiling. Methods Mol. Biol.507, 149–163 (2009).
   PubMedGoogle Scholar
• Du P , ZhangX , HuangC-Cet al. Comparison of beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics11, 587 (2010).
   PubMed Web of Science ®Google Scholar
• Bakulski KM , FeinbergJI , AndrewsSVet al. DNA methylation of cord blood cell types: applications for mixed cell birth studies. Epigenetics11(5), 354–362 (2016).
   PubMed Web of Science ®Google Scholar
• Houseman EA , AccomandoWP , KoestlerDCet al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics13, 86 (2012).
   PubMed Web of Science ®Google Scholar
• Reinius LE , AcevedoN , JoerinkMet al. Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. PLoS ONE7(7), e41361 (2012).
   PubMed Web of Science ®Google Scholar
• Wang D , YanL , HuQet al. IMA: an R package for high-throughput analysis of Illumina’s 450K Infinium methylation data. Bioinformatics28(5), 729–730 (2012).
   PubMed Web of Science ®Google Scholar
• Johnson WE , LiC , RabinovicA. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics8(1), 118–127 (2007).
   PubMed Web of Science ®Google Scholar
• Lehne B , DrongAW , LohMet al. A coherent approach for analysis of the Illumina HumanMethylation450 BeadChip improves data quality and performance in epigenome-wide association studies. Genome Biol.16, 37 (2015).
   PubMed Web of Science ®Google Scholar
• Ogbuanu IU , KarmausW , ArshadSH , KurukulaaratchyRJ , EwartS. Effect of breastfeeding duration on lung function at age 10 years: a prospective birth cohort study. Thorax64(1), 62–66 (2009).
   PubMed Web of Science ®Google Scholar
• Ray MA , TongX , LockettGA , ZhangH , KarmausWJ. An efficient approach to screening epigenome-wide data. Biomed. Res. Int.2016, 2615348 (2016).
   PubMed Web of Science ®Google Scholar
• Zhang H , WangF , KranzlerHRet al. Identification of methylation quantitative trait loci (mQTLs) influencing promoter DNA methylation of alcohol dependence risk genes. Hum. Genet.133(9), 1093–1104 (2014).
   PubMed Web of Science ®Google Scholar
• Welch RP , WillerCJ , J.SL , BoehnkeM. Snipper: a research tool for extracting and searching biological annotations on genes near SNPs (2013). https://csg.sph.umich.edu/boehnke/snipper/
   Google Scholar
• Karolchik D , BaertschR , DiekhansMet al. The UCSC Genome Browser database. Nucleic Acids Res.31(1), 51–54 (2003).
   PubMed Web of Science ®Google Scholar
• Joubert BR , FelixJF , YousefiPet al. DNA methylation in newborns and maternal smoking in pregnancy: genome-wide consortium meta-analysis. Am. J. Hum. Genet.98(4), 680–696 (2016).
   PubMed Web of Science ®Google Scholar
• Joubert BR , HabergSE , NilsenRMet al. 450K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environ. Health Persp.120(10), 1425–1431 (2012).
   PubMed Web of Science ®Google Scholar
• Byrnes JJ , BabbJA , ScanlanVF , ByrnesEM. Adolescent opioid exposure in female rats: transgenerational effects on morphine analgesia and anxiety-like behavior in adult offspring. Behav. Brain Res.218(1), 200–205 (2011).
   PubMed Web of Science ®Google Scholar
• Barouki R , MelenE , HercegZet al. Epigenetics as a mechanism linking developmental exposures to long-term toxicity. Environ. Int.114, 77–86 (2018).
   PubMed Web of Science ®Google Scholar
• Van Otterdijk SD , MichelsKB. Transgenerational epigenetic inheritance in mammals: how good is the evidence?FASEB J.30(7), 2457–2465 (2016).
   PubMed Web of Science ®Google Scholar
• Ziller MJ , GuHC , MullerFet al. Charting a dynamic DNA methylation landscape of the human genome. Nature500(7463), 477–481 (2013).
   PubMed Web of Science ®Google Scholar
• Schoenauer R , LangeS , HirschyA , EhlerE , PerriardJC , AgarkovaI. Myomesin 3, a novel structural component of the M-band in striated muscle. J. Mol. Biol.376(2), 338–351 (2008).
   PubMed Web of Science ®Google Scholar
• Guler HP , ZapfJ , SchmidC , FroeschER. Insulin-like growth factors I and II in healthy man. Estimations of half-lives and production rates. Acta Endocrinol. (Copenh.)121(6), 753–758 (1989).
   PubMedGoogle Scholar
• Iniguez G , ArgandonaF , MedinaPet al. Acid-labile subunit (ALS) gene expression and protein content in human placentas: differences according to birth weight. J. Clin. Endocrinol. Metab.96(1), 187–191 (2011).
   PubMed Web of Science ®Google Scholar
• Ester WA , Hokken-KoelegaAC. Polymorphisms in the IGF1 and IGF1R genes and children born small for gestational age: results of large population studies. Best Pract. Res. Clin. Endocrinol. Metab.22(3), 415–431 (2008).
   PubMed Web of Science ®Google Scholar
• Beck KD , Powell-BraxtonL , WidmerHR , ValverdeJ , HeftiF. Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron14(4), 717–730 (1995).
   PubMed Web of Science ®Google Scholar
• D’Ercole AJ , YeP , O’KuskyJR. Mutant mouse models of insulin-like growth factor actions in the central nervous system. Neuropeptides36(2–3), 209–220 (2002).
   PubMed Web of Science ®Google Scholar
• Hess O , KhayatM , HwaVet al. A novel mutation in IGFALS, c.380T > C (p.L127P), associated with short stature, delayed puberty, osteopenia and hyperinsulinaemia in two siblings: insights into the roles of insulin growth factor-1 (IGF1). Clin. Endocrinol.79(6), 838–844 (2013).
   PubMed Web of Science ®Google Scholar
• Choi J-H , KangM , KimG-Het al. Clinical and functional characteristics of a novel heterozygous mutation of the IGF1R gene and IGF1R haploinsufficiency due to terminal 15q26.2->qter deletion in patients with intrauterine growth retardation and postnatal catch-up growth failure. J. Clin. Endocrinol. Metab.96(1), e130–e134 (2011).
   PubMed Web of Science ®Google Scholar
• Lock K , ZhangJ , LuJ , LeeSH , CrockerPR. Expression of CD33-related siglecs on human mononuclear phagocytes, monocyte-derived dendritic cells and plasmacytoid dendritic cells. Immunobiology209(1–2), 199–207 (2004).
   PubMed Web of Science ®Google Scholar
• Griciuc A , Serrano-PozoA , ParradoARet al. Alzheimer’s disease risk gene CD33 inhibits microglial uptake of amyloid beta. Neuron78(4), 631–643 (2013).
   PubMed Web of Science ®Google Scholar
• Dou D , ZhaoH , LiZet al. CHD1L promotes neuronal differentiation in human embryonic stem cells by upregulating PAX6. Stem Cells Dev.26(22), 1626–1636 (2017).
   PubMed Web of Science ®Google Scholar
• Brockschmidt A , ChungB , WeberSet al. CHD1L: a new candidate gene for congenital anomalies of the kidneys and urinary tract (CAKUT). Nephrol. Dial. Transplant.27(6), 2355–2364 (2012).
   PubMed Web of Science ®Google Scholar
• Li W , FengY , ChenAet al. Elmod3 knockout leads to progressive hearing loss and abnormalities in cochlear hair cell stereocilia. Hum. Mol. Genet.28(24), 4103–4112 (2019).
   PubMed Web of Science ®Google Scholar
• Loi E , MoiL , BloisSet al. ELMOD3-SH2D6 gene fusion as a possible co-star actor in autism spectrum disorder scenario. J. Cell. Mol. Med.24(2), 2064–2069 (2020).
   PubMed Web of Science ®Google Scholar
• Malagon SGG , MelidoniAN , HernandezDet al. The phenotype of a knockout mouse identifies flavin-containing monooxygenase 5 (FMO5) as a regulator of metabolic ageing. Biochem. Pharmacol.96(3), 267–277 (2015).
   PubMed Web of Science ®Google Scholar
• Scott F , MalagonSGG , O’BrienBAet al. Identification of flavin-containing monooxygenase 5 (FMO5) as a regulator of glucose homeostasis and a potential sensor of gut bacteria. Drug Metab. Dispos.45(9), 982–989 (2017).
   PubMed Web of Science ®Google Scholar
• Joubert BR , HabergSE , BellDAet al. Maternal smoking and DNA methylation in newborns: in utero effect or epigenetic inheritance? Cancer Epidemiol. Biomarkers Prev. 23(6), 1007–1017 (2014).
   PubMed Web of Science ®Google Scholar