Copper associates with differential methylation in placentae from two US birth cohorts

References

• Collins JF, Klevay LM. Copper. Adv Nutr. 2011;2:520–522.
   PubMed Web of Science ®Google Scholar
• Crisponi G, Nurchi VM, Fanni D, et al. Copper-related diseases: from chemistry to molecular pathology. Coord Chem Rev. 2010;254:876–889.
   Web of Science ®Google Scholar
• Zadrożna M, Gawlik M, Nowak B, et al. Antioxidants activities and concentration of selenium, zinc and copper in preterm and IUGR human placentas. J Trace Elem Med Biol. 2009;23:144–148.
   PubMed Web of Science ®Google Scholar
• Mbofung CMF, Subbarau VV. Trace element (Zinc, copper, iron and magnesium) concentrations in human placenta and their relationship to birth weight of babies. Nutr Res. 1990;10:359–366.
   Web of Science ®Google Scholar
• Kantola M, Purkunen R, Kröger P, et al. Accumulation of Cadmium, Zinc, and Copper in maternal blood and developmental placental tissue: differences between Finland, Estonia, and St. Petersburg. Environ Res. 2000;83:54–66.
   PubMed Web of Science ®Google Scholar
• Ergaz Z, Guillemin C, Neeman-azulay M, et al. Placental oxidative stress and decreased global DNA methylation are corrected by copper in the Cohen diabetic rat. Toxicol Appl Pharmacol. 2014;276:220–230.
   PubMed Web of Science ®Google Scholar
• Bermúdez L, García-Vicent C, López J, et al. Assessment of ten trace elements in umbilical cord blood and maternal blood: association with birth weight. J Transl Med. 2015;13:291.
   PubMed Web of Science ®Google Scholar
• Alebic-Juretic A, Frkovic A. Plasma copper concentrations in pathological pregnancies. J Trace Elem Med Biol. 2005;19:191–194.
   PubMed Web of Science ®Google Scholar
• Osada H, Watanabe Y, Nishimura Y, et al. Profile of trace element concentrations in the feto-placental unit in relation to fetal growth. Acta Obstet Gynecol Scand. 2002;81:931–937.
   PubMed Web of Science ®Google Scholar
• Bellos I, Papantoniou N, Pergialiotis V. Serum ceruloplasmin levels in preeclampsia: a meta-analysis. J Matern Fetal Neonatal Med. 2018;31:2342–2348.
   PubMed Web of Science ®Google Scholar
• Sak S, Barut M, Çelik H, et al. Copper and ceruloplasmin levels are closely related to the severity of preeclampsia. J Matern Fetal Neonatal Med. 2018;1–7.
   PubMed Web of Science ®Google Scholar
• Hardman B, Michalczyk A, Greenough M, et al. Distinct functional roles for the Menkes and Wilson copper translocating P-type ATPases in human placental cells. Cell Physiol Biochem Int J Exp Cell Physiol Biochem Pharmacol. 2007;20:1073–1084.
   PubMedGoogle Scholar
• Irwinda R, Wibowo N, Putri AS. The Concentration of micronutrients and heavy metals in maternal Serum, Placenta, and Cord Blood: a cross-sectional study in preterm birth [Internet]. J Pregnancy. 2019;2019:1–7. [cited 2019 Apr 17]. Available from: https://www.hindawi.com/journals/jp/2019/5062365/
   PubMedGoogle Scholar
• McArdle HJ, Andersen HS, Jones H, et al. Copper and Iron Transport Across the Placenta: regulation and Interactions. J Neuroendocrinol. 2008;20:427–431.
   PubMed Web of Science ®Google Scholar
• Sawicka-Kapusta K, Bydlon G, Zakrzewska M, et al. Heavy metal concentration in human Placenta from Southern Poland. [ cited 2019 Apr 24]. Available from: http://inis.iaea.org/Search/search.aspx?orig_q=RN:41131312
   Google Scholar
• Mukhacheva SV, Bezel’ VS. Heavy metals in the mother–placenta–fetus system in bank voles under conditions of environmental pollution from copper plant emissions. Russ J Ecol. 2015;46:564–572.
   Web of Science ®Google Scholar
• Malik A, Khawaja A, Sheikh L. Wilson’s disease in pregnancy: case series and review of literature. BMC Res Notes. 2013;6:421.
   PubMedGoogle Scholar
• Walker LR, Rattigan M, Canterino J. A case of isolated elevated copper levels during pregnancy. J Pregnancy. 2011;2011:385767.
   PubMedGoogle Scholar
• Medici V, Shibata NM, Kharbanda KK, et al. Wilson disease: changes in methionine metabolism and inflammation affect global DNA methylation in early liver disease. Hepatol Baltim Md. 2013;57:555–565.
   PubMed Web of Science ®Google Scholar
• Le A, Shibata NM, French SW, et al. Characterization of Timed changes in Hepatic copper concentrations, Methionine Metabolism, Gene Expression, and Global DNA Methylation in the Jackson Toxic milk mouse model of Wilson Disease. Int J Mol Sci. 2014;15:8004–8023.
   PubMed Web of Science ®Google Scholar
• Mordaunt CE, Shibata NM, Kieffer DA, et al. Epigenetic changes of the thioredoxin system in the tx-j mouse model and in patients with Wilson disease. Hum Mol Genet. 2018;27:3854–3869.
   PubMed Web of Science ®Google Scholar
• Delgado M, Pérez-Miguelsanz J, Garrido F, et al. Early effects of copper accumulation on methionine metabolism. Cell Mol Life Sci CMLS. 2008;65:2080–2090.
   PubMed Web of Science ®Google Scholar
• Hardman B, Michalczyk A, Greenough M, et al. Hormonal regulation of the Menkes and Wilson copper-transporting ATPases in human placental Jeg-3 cells. Biochem J. 2007;402:241–250.
   PubMed Web of Science ®Google Scholar
• Beshgetoor D, Hambidge M. Clinical conditions altering copper metabolism in humans. Am J Clin Nutr. 1998;67:1017S–1021S.
   PubMed Web of Science ®Google Scholar
• Ernst J, Kellis M. Chromatin-state discovery and genome annotation with ChromHMM. Nat Protoc. 2017;12:2478–2492.
   PubMed Web of Science ®Google Scholar
• Roadmap Epigenomics Consortium, Kundaje A, Meuleman W, et al. Integrative analysis of 111 reference human epigenomes. Nature. 2015;518:317–330.
   PubMed Web of Science ®Google Scholar
• Karolchik D, Hinrichs AS, Furey TS, et al. The UCSC Table Browser data retrieval tool. Nucleic Acids Res. 2004;32:D493–496.
   PubMed Web of Science ®Google Scholar
• Li Z, Wang D, Na X, et al. The VHL protein recruits a novel KRAB-A domain protein to repress HIF-1α transcriptional activity. Embo J. 2003;22:1857–1867.
   PubMed Web of Science ®Google Scholar
• Lambert SA, Jolma A, Campitelli LF, et al. The Human Transcription Factors. Cell. 2018;172:650–665.
   PubMed Web of Science ®Google Scholar
• Yates A, Akanni W, Amode MR, et al. Ensembl 2016. Nucleic Acids Res. 2016;44:D710–D716.
   PubMed Web of Science ®Google Scholar
• Pihur V, Datta S, Datta S. RankAggreg, an R package for weighted rank aggregation. BMC Bioinformatics. 2009;10:62.
   PubMed Web of Science ®Google Scholar
• Iyengar GV, Rapp A. Human placenta as a ‘dual’ biomarker for monitoring fetal and maternal environment with special reference to potentially toxic trace elements: part 2: essential minor, trace and other (non-essential) elements in human placenta. Sci Total Environ. 2001;280:207–219.
   PubMed Web of Science ®Google Scholar
• Kennedy EM, Goehring GN, Nichols MH, et al. An integrated -omics analysis of the epigenetic landscape of gene expression in human blood cells. BMC Genomics. 2018;19:476.
   PubMed Web of Science ®Google Scholar
• Zusterzeel PLM, Peters WHM, De Bruyn MAH, et al. Glutathione S-transferase isoenzymes in decidua and placenta of preeclamptic pregnancies. Obstet Gynecol. 1999;94:1033–1038.
   PubMed Web of Science ®Google Scholar
• Simpson DM, Beynon RJ, Robertson DHL, et al. Copper-associated liver disease: a proteomics study of copper challenge in a sheep model. PROTEOMICS. 2004;4:524–536.
   PubMed Web of Science ®Google Scholar
• Kaneko-Ishino T, Ishino F. The role of genes domesticated from LTR retrotransposons and retroviruses in mammals. Front Microbiol. 2012;3:262.
   PubMed Web of Science ®Google Scholar
• Edelstein LC, Collins T. The SCAN domain family of zinc finger transcription factors. Gene. 2005;359:1–17.
   PubMed Web of Science ®Google Scholar
• Crosley EJ, Elliot MG, Christians JK, et al. Placental invasion, preeclampsia risk and adaptive molecular evolution at the origin of the great apes: evidence from genome-wide analyses. Placenta. 2013;34:127–132.
   PubMed Web of Science ®Google Scholar
• Muller P, van Bakel H, van de Sluis B, et al. Gene expression profiling of liver cells after copper overload in vivo and in vitro reveals new copper-regulated genes. JBIC J Biol Inorg Chem. 2007;12:495–507.
   PubMed Web of Science ®Google Scholar
• Ugwuja EI, Akubugwo EI, Ibiam U, et al. lasma Copper and Zinc among Pregnant women in Abakaliki, Southeastern Nigeria. Internet J Nutr Wellness. 2010;10:unpaginated ref.41.
   Google Scholar
• Winiarska-Mieczan A. Cadmium, Lead, Copper and Zinc in breast milk in Poland. Biol Trace Elem Res. 2014;157:36–44.
   PubMed Web of Science ®Google Scholar
• Phillips-Krawczak CA, Singla A, Starokadomskyy P, et al. COMMD1 is linked to the WASH complex and regulates endosomal trafficking of the copper transporter ATP7A. Mol Biol Cell. 2015;26:91–103.
   PubMed Web of Science ®Google Scholar
• Tang C, Mei L, Pan L, et al. Hedgehog signaling through GLI1 and GLI2 is required for epithelial-mesenchymal transition in human trophoblasts. Biochim Biophys Acta. 2015;1850:1438–1448.
   PubMed Web of Science ®Google Scholar
• Yuen RK, Peñaherrera MS, von Dadelszen P, et al. DNA methylation profiling of human placentas reveals promoter hypomethylation of multiple genes in early-onset preeclampsia. Eur J Hum Genet. 2010;18:1006–1012.
   PubMed Web of Science ®Google Scholar
• Igakura T, Kadomatsu K, Kaname T, et al. A null mutation in Basigin, an Immunoglobulin superfamily member, indicates its important roles in Peri-implantation Development and Spermatogenesis. Dev Biol. 1998;194:152–165.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhou J, Xu Y-J, et al. Long non-coding RNA LINC00968 acts as oncogene in NSCLC by activating the Wnt signaling pathway. J Cell Physiol. 2018;233:3397–3406.
   PubMed Web of Science ®Google Scholar
• Wong NC, Novakovic B, Weinrich B, et al. Methylation of the adenomatous polyposis coli (APC) gene in human placenta and hypermethylation in choriocarcinoma cells. Cancer Lett. 2008;268:56–62.
   PubMed Web of Science ®Google Scholar
• Novakovic B, Rakyan V, Ng HK, et al. Specific tumour-associated methylation in normal human term placenta and first-trimester cytotrophoblasts. Mol Hum Reprod. 2008;14:547–554.
   PubMed Web of Science ®Google Scholar
• Li P, Yin J, Zhu Y, et al. Association between plasma concentration of copper and gestational diabetes mellitus. Clin Nutr Edinb Scotl. 2019.
   Google Scholar
• Atari-Hajipirloo S, Valizadeh N, Khadem-Ansari M-H, et al. Altered Concentrations of Copper, Zinc, and Iron are associated with increased levels of Glycated Hemoglobin in patients with type 2 diabetes mellitus and their first-degree relatives. Int J Endocrinol Metab. 2016;14:e33273.
   PubMed Web of Science ®Google Scholar
• Mishu FA, Muttalib MA, Sultana B. Serum zinc and copper levels in gestational diabetes mellitus in a tertiary care hospital of Bangladesh. BIRDEM Med J. 2018;8:52–55.
   Google Scholar
• Guller S, Buhimschi CS, Ma YY, et al. Placental expression of ceruloplasmin in pregnancies complicated by severe preeclampsia. Lab Investig J Tech Methods Pathol. 2008;88:1057–1067.
   PubMed Web of Science ®Google Scholar
• Mistry HD, Kurlak LO, Williams PJ, et al. Differential expression and distribution of placental glutathione peroxidases 1, 3 and 4 in normal and preeclamptic pregnancy. Placenta. 2010;31:401–408.
   PubMed Web of Science ®Google Scholar
• Collins JF, Prohaska JR, Knutson MD. Metabolic crossroads of iron and copper. Nutr Rev. 2010;68:133–147.
   PubMed Web of Science ®Google Scholar
• Thompson LP, Al-Hasan Y. Impact of oxidative stress in fetal programming. J Pregnancy. 2012;2012:582748.
   PubMedGoogle Scholar
• Lindsay RP, Tsoh JY, Sung H-Y, et al. Secondhand smoke exposure and serum cotinine levels among current smokers in the USA. Tob Control. 2016;25:224–231.
   PubMed Web of Science ®Google Scholar
• Houseman EA, Kile ML, Christiani DC, et al. Reference-free deconvolution of DNA methylation data and mediation by cell composition effects. BMC Bioinformatics. 2016;17:259.
   PubMed Web of Science ®Google Scholar
• Bakulski KM, Fallin MD. Epigenetic epidemiology: promises for public health research. Environ Mol Mutagen. 2014;55:171–183.
   PubMed Web of Science ®Google Scholar
• Fenton TR, Kim JH. A systematic review and meta-analysis to revise the Fenton growth chart for preterm infants. BMC Pediatr. 2013;13:59.
   PubMed Web of Science ®Google Scholar
• Fortin J-P, Triche TJ, Hansen KD. Preprocessing, normalization and integration of the Illumina HumanMethylationEPIC array with minfi. Bioinforma Oxf Engl. 2017;33:558–560.
   PubMed Web of Science ®Google Scholar
• Aryee MJ, Jaffe AE, Corrada-Bravo H, et al. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinforma Oxf Engl. 2014;30:1363–1369.
   PubMed Web of Science ®Google Scholar
• Triche TJ, Weisenberger DJ, Van Den Berg D, et al. Low-level processing of Illumina Infinium DNA Methylation BeadArrays. Nucleic Acids Res. 2013;41:e90.
   PubMed Web of Science ®Google Scholar
• Teschendorff AE, Marabita F, Lechner M, et al. A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinforma Oxf Engl. 2013;29:189–196.
   PubMed Web of Science ®Google Scholar
• Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostat Oxf Engl. 2007;8:118–127.
   PubMed Web of Science ®Google Scholar
• Leek JT, Johnson WE, Parker HS, et al. The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinforma Oxf Engl. 2012;28:882–883.
   PubMed Web of Science ®Google Scholar
• Du P, Zhang X, Huang -C-C, et al. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics. 2010;11:587.
   PubMed Web of Science ®Google Scholar
• Barfield RT, Almli LM, Kilaru V, et al. Accounting for population stratification in DNA methylation studies. Genet Epidemiol. 2014;38:231–241.
   PubMed Web of Science ®Google Scholar
• Chen Y, Lemire M, Choufani S, et al. Discovery of cross-reactive probes and polymorphic CpGs in the Illumina Infinium HumanMethylation450 microarray. Epigenetics. 2013;8:203–209.
   PubMed Web of Science ®Google Scholar
• Huang R, Jaritz M, Guenzl P, et al. An RNA-Seq strategy to detect the complete coding and non-coding transcriptome including full-length imprinted macro ncRNAs. PloS One. 2011;6:e27288.
   PubMed Web of Science ®Google Scholar
• Bentley DR, Balasubramanian S, Swerdlow HP, et al. Accurate whole human genome sequencing using reversible terminator chemistry. Nature. 2008;456:53–59.
   PubMed Web of Science ®Google Scholar
• Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinforma Oxf Engl. 2010;26:139–140.
   PubMed Web of Science ®Google Scholar
• Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010;11:R25.
   PubMed Web of Science ®Google Scholar
• Chen Y, Lun ATL, Smyth GK. From reads to genes to pathways: differential expression analysis of RNA-Seq experiments using Rsubread and the edgeR quasi-likelihood pipeline. F1000Res. 2016;5:1438.
   PubMedGoogle Scholar
• Durinck S, Spellman PT, Birney E, et al. Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt. Nat Protoc. 2009;4:1184–1191.
   PubMed Web of Science ®Google Scholar
• Leek JT. svaseq: removing batch effects and other unwanted noise from sequencing data. Nucleic Acids Res. 2014;42:e161–e161.
   Web of Science ®Google Scholar
• Punshon T, Li Z, Marsit CJ, et al. Placental Metal Concentrations in Relation to Maternal and Infant Toenails in a U.S. Cohort. Environ Sci Technol. 2016;50:1587–1594.
   PubMed Web of Science ®Google Scholar
• Venables WN, Ripley BD. Modern Applied Statistics with S [Internet]. 4th ed. New York (NY): Springer; 2002 [cited 2018 Nov 28]. Available from: www.springer.com/us/book/9780387954578
   Google Scholar
• Zeileis A, Hothorn T. Diagnostic checking in regression relationships. R News. 2002 Dec;2:7–10.
   Google Scholar
• Zeileis A. Object-oriented Computation of Sandwich Estimators. J Stat Softw. 2006;16:1–16.
   Web of Science ®Google Scholar
• Zeileis A. Econometric Computing with HC and HAC Covariance Matrix Estimators. J Stat Softw. 2004;11:1–17.
   Google Scholar
• Willer CJ, Li Y, Abecasis GR. METAL: fast and efficient meta-analysis of genomewide association scans. Bioinforma Oxf Engl. 2010;26:2190–2191.
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995;57:289–300.
   Web of Science ®Google Scholar
• Pedersen BS, Schwartz DA, Yang IV, et al. Comb-p: software for combining, analyzing, grouping and correcting spatially correlated P-values. Bioinformatics. 2012;28:2986–2988.
   PubMed Web of Science ®Google Scholar
• Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics. 2011;27:1017–1018.
   PubMed Web of Science ®Google Scholar
• Ritchie ME, Phipson B, Wu D, et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43:e47.
   PubMed Web of Science ®Google Scholar