Cumulative lifetime maternal stress and epigenome-wide placental DNA methylation in the PRISM cohort

References

• Su Q, Zhang H, Zhang Y, et al. Maternal stress in gestation: birth outcomes and stress-related hormone response of the neonates. Pediatr Neonatol. 2015;56:376–381.
   PubMed Web of Science ®Google Scholar
• Lee A, Mathilda Chiu YH, Rosa MJ, et al. Prenatal and postnatal stress and asthma in children: temporal- and sex-specific associations. J Allergy Clin Immunol. 2016;138(3):740–747 e743. PMC5011027.
   PubMed Web of Science ®Google Scholar
• Christopher M. A broader view of trauma: A biopsychosocial-evolutionary view of the role of the traumatic stress response in the emergence of pathology and/or growth. Clin Psychol Rev. 2004;4(1):75–98.
   Google Scholar
• Tiedje LB. Psychosocial pathways to prematurity: changing our thinking toward a lifecourse and community approach. J Obstet Gynecol Neonatal Nurs. 2003;32(5):650–658.
   PubMed Web of Science ®Google Scholar
• O’Donnell K, O’Connor TG, Glover V. Prenatal stress and neurodevelopment of the child: focus on the hpa axis and role of the placenta. Dev Neurosci. 2009;31(4):285–292.
   PubMed Web of Science ®Google Scholar
• Henrichs J, Schenk JJ, Roza SJ, et al. Maternal psychological distress and fetal growth trajectories: the generation r study. Psychological medicine. 2010;40(4):633–643.
   PubMed Web of Science ®Google Scholar
• Lane RH. Fetal programming, epigenetics, and adult onset disease. Clinics in perinatology. 2014;41(4):815–831.
   PubMed Web of Science ®Google Scholar
• Hatch SL, Dohrenwend BP. Distribution of traumatic and other stressful life events by race/ethnicity, gender, ses and age: A review of the research. Am J Community Psychol. 2007;40(3–4):313–332.
   PubMed Web of Science ®Google Scholar
• Santos F, Dean W. Epigenetic reprogramming during early development in mammals. Reproduction. 2004;127:643–651.
   PubMed Web of Science ®Google Scholar
• Wadhwa PD, Buss C, Entringer S, et al. Developmental origins of health and disease: brief history of the approach and current focus on epigentic mechanisms. Semin Reprod Med. 2009;27:358–368.
   PubMed Web of Science ®Google Scholar
• Dolinoy DC, Weidman JR, Waterland RA, et al. Maternal geinstein alters coat color and protects avy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect. 2006;114:567–572.PMC1440782.
   PubMed Web of Science ®Google Scholar
• Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci. 2001;24:1161–1192.
   PubMed Web of Science ®Google Scholar
• Oberlander TF, Weinberg J, Papsdorf M, et al. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (nr3c1) and infant cortisol stress responses. Epigenetics. 2008;3:97–106.
   PubMed Web of Science ®Google Scholar
• Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Porceedings Natl Acad Sci. 2008;105:17046–17049.
   PubMed Web of Science ®Google Scholar
• Appleton AA, Armstrong DA, Lesseaur C, et al. Patterning in placental 11-b hydroxysteroid dehydrogenase methylation according to prenatal socioeconomic adversity. PLoS One. 2013;8:e74691.
   PubMed Web of Science ®Google Scholar
• Vangeel EB, Izzi B, Hompes T, et al. DNA methylation in imprinted genes igf2 and gnasxl is associated with prenatal maternal stress. Psychoneuroendocrinology. 2015;61:16.
   Web of Science ®Google Scholar
• Braithwaite EC, Kundakovic M, Ramchandani PG, et al. Maternal prenatal depressive symptoms predict infant nr3c1 1f and bdnf iv DNA methylation. Epigenetics. 2015;10(5):408–417.
   PubMed Web of Science ®Google Scholar
• Palma-Gudiel H, Cordova-Palomera A, Eixarch E, et al. Maternal psychosocial stress during pregnancy alters the epigenetic signature of the glucocorticoid receptor gene promoter in their offspring: A meta-analysis. Epigenetics. 2015;10(10):893–902.
   PubMed Web of Science ®Google Scholar
• Kertes DA, Bhatt SS, Kamin HS, et al. Bndf methylation in mothers and newborns is associated with maternal exposure to war trauma. Clin Epigenetics. 2017;9(68):PMC5493129.
   Google Scholar
• Mulligan CJ, D’Errico NC, Stees J, et al. Methylation changes at nr3c1 in newborns associate with maternal prenatal stress exposure and newborn birth weight. Epigenetics. 2012;7(8):853–857. PMC3427280.
   PubMed Web of Science ®Google Scholar
• Nugent BM, Bale TL. The omniscient placenta: metabolic and epigenetic regulation of fetal programming. Front Neuroendocrinol. 2015;39:28–37. PMC4681645.
   PubMed Web of Science ®Google Scholar
• Burton GJ, Fowden AL, Thornburg KL. Placental origins of chronic disease. Physiol Rev. 2016;96(4):1509–1565.
   PubMed Web of Science ®Google Scholar
• Myllynen P, Pasanen M, Pelkonen O. Human placenta: A human organ for developmental toxicology research and biomonitoring. Placenta. 2005;26(5):361–371.
   PubMed Web of Science ®Google Scholar
• Janssen BG, Godderis L, Pieters N, et al. Placental DNA hypomethylation in association with particulate air pollution in early life. Part Fibre Toxicol. 2013;10(22):PMC3686623.
   Google Scholar
• Suter M, Ma J, Harris A, et al. Maternal tobacco use modestly alters correlated epigenome-wide placental DNA methylation and gene expression. Epigenetics. 2011;6(11):1284–1294. PMC3242811.
   PubMed Web of Science ®Google Scholar
• Gallou-Kabani C, Gabory A, Tost J, et al. Sex- and diet-specific changes of imprinted gene expression and DNA methylation in mouse placenta under a high-fat diet. PLoS One. 2010;5(12):e14398. PMC3006175.
   PubMed Web of Science ®Google Scholar
• Hogg K, Price EM, Hanna CW, et al. Prenatal and perinatal environmental influences on the human fetal and placental epigenome. Clin Pharmacol Ther. 2012;92(6):716–726.
   PubMed Web of Science ®Google Scholar
• Jensen Pena C, Monk C, Champagne FA. Epigenetic effects of prenatal stress on 11beta-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLoS One. 2012;7(6):e39791. PMC3383683.
   PubMed Web of Science ®Google Scholar
• Monk C, Feng T, Lee S, et al. Distress during pregnancy: epigenetic regulation of placenta glucocorticoid-related genes and fetal neurobehavior. Am J Psychiatry. 2016;173(7):705–713. PMC5026410.
   PubMed Web of Science ®Google Scholar
• Kertes DA, Kamin HS, Hughes DA, et al. Prenatal maternal stress predicts methylation of genes regulating the hypothalamic-pituitary-adrenocortical system in mothers and newborns in the democratic republic of congo. Child Dev. 2016;87(1):61–72. PMC4733886.
   PubMed Web of Science ®Google Scholar
• Rahmani E, Shenhav L, Schweiger R, et al. Genome-wide methylation data mirror ancestry information. Epigenetics Chromatin. 2017;10(1). PMC5267476. DOI:10.1186/s13072-016-0108-y
   PubMedGoogle Scholar
• Rahmani E, Zaitlen N, Baran Y, et al. Sparse pca corrects for cell type heterogeneity in epigenome-wide association studies. Nat Methods. 2016;13(5):443–445. PMC5548182.
   PubMed Web of Science ®Google Scholar
• Tibshirani R, Walther G, Hastie T. Estimating the number of clusters in a data set via the gap statistic. J Royal Stat Soc. 2001;63:411–423.
   Google Scholar
• Blair JD, Yuen RK, Lim BK, et al. Widespread DNA hypomethylation at gene enhancer regions in placentas associated with early-onset pre-eclampsia. Mol Hum Reprod. 2013;19(10):697–708. PMC3779005.
   PubMed Web of Science ®Google Scholar
• Hon GC, Rajagopal N, Shen Y, et al. Epigenetic memory at embryonic enhancers identified in DNA methylation maps from adult mouse tissues. Nat Genet. 2013;45(10):1198–1206. PMC4095776.
   PubMed Web of Science ®Google Scholar
• Hansen KD, Timp W, Bravo HC, et al. Increased methylation variation in epigenetic domains across cancer types. Nat Genet. 2011;43(8):768–775. PMC3145050.
   PubMed Web of Science ®Google Scholar
• Blattler A, Yao L, Witt H, et al. Global loss of DNA methylation uncovers intronic enhancers in genes showing expression changes. Genome Biol. 2014;15(9):469. PMC4203885.
   PubMed Web of Science ®Google Scholar
• Tutar Y. Pseudogenes. Comp Funct Genomics. 2012;2012:424526. PMC3352212.
   PubMedGoogle Scholar
• Soldati D, Schumperli D. Structures of four human pseudogenes for u7 small nuclear rna. Gene. 1990;95(2):305–306.
   PubMed Web of Science ®Google Scholar
• Paik MJ, Lee HJ, Kim KR. Simultaneous retention index analysis of urinary amino acids and carboxylic acids for graphic recognition of abnormal state. J Chromatogr B Analyt Technol Biomed Life Sci. 2005;821(1):94–104.
   PubMed Web of Science ®Google Scholar
• Kanehisa M, Sato Y, Kawashima M, et al. Kegg as a reference resource for gene and protein annotation. Nucleic acids research. 2016;44(D1):D457-462;4702792.
   PubMed Web of Science ®Google Scholar
• Jansson T, Scholtbach V, Powell TL. Placental transport of leucine and lysine is reduced in intrauterine growth restriction. Pediatric research. 1998;44(4):532–537.
   PubMed Web of Science ®Google Scholar
• Gabbe SG. Obstetrics: normal and problem pregnancies. 6th ed. Philadelphia: Elsevier/Saunders; 2012.
   Google Scholar
• Trump S, Bieg M, Gu Z, et al. Prenatal maternal stress and wheeze in children: novel insights into epigenetic regulation. Scientific reports. 2016;6:28616; 4923849.
   PubMed Web of Science ®Google Scholar
• Sumiyoshi M, Masuda N, Tanuma N, et al. Mice doubly-deficient in the arf gaps smap1 and smap2 exhibit embryonic lethality. FEBS Lett. 2015;589(19Pt B):2754–2762.
   PubMedGoogle Scholar
• Martinez-Pacheco M, Hidalgo-Miranda A, Romero-Cordoba S, et al. Mrna and mirna expression patterns associated to pathways linked to metal mixture health effects. Gene. 2014;533(2):508–514.
   PubMed Web of Science ®Google Scholar
• Ligthart S, Steenaard RV, Peters MJ, et al. Tobacco smoking is associated with DNA methylation of diabetes susceptibility genes. Diabetologia. 2016;59(5):998–1006. PMC4826423.
   PubMed Web of Science ®Google Scholar
• Filis P, Nagrath N, Fraser M, et al. Maternal smoking dysregulates protein expression in second trimester human fetal livers in a sex-specific manner. J Clin Endocrinol Metab. 2015;100(6):E861–870. PMC4533306.
   PubMed Web of Science ®Google Scholar
• Colaianna M, Schiavone S, Zotti M, et al. Neuroendocrine profile in a rat model of psychosocial stress: relation to oxidative stress. Antioxidants & redox signaling. 2013;18(12):1385–1399;3603501.
   PubMed Web of Science ®Google Scholar
• Jorgensen A. Oxidatively generated DNA/rna damage in psychological stress states. Danish medical journal. 2013;60(7):B4685.
   PubMed Web of Science ®Google Scholar
• Aschbacher K, O’Donovan A, Wolkowitz OM, et al. Good stress, bad stress and oxidative stress: insights from anticipatory cortisol reactivity. Psychoneuroendocrinology. 2013;38(9):1698–1708.
   PubMed Web of Science ®Google Scholar
• Gidron Y, Russ K, Tissarchondou H, et al. The relation between psychological factors and DNA-damage: A critical review. Biological psychology. 2006;72(3):291–304.
   PubMed Web of Science ®Google Scholar
• Noakes PS, Thomas R, Lane C, et al. Association of maternal smoking with increased infant oxidative stress at 3 months of age. Thorax. 2007;62(8):714–717. PMC2117280.
   PubMed Web of Science ®Google Scholar
• Chauhan S, Pandey R, Way JF, et al. Androgen regulation of the human ferm domain encoding gene ehm2 in a cell model of steroid-induced differentiation. Biochem Biophys Res Commun. 2003;310(2):421–432. PMC2740477.
   PubMed Web of Science ®Google Scholar
• Eckert JJ, Fleming TP. Tight junction biogenesis during early development. Biochim Biophys Acta. 2008;1778(3):717–728.
   PubMed Web of Science ®Google Scholar
• Wang JC, Derynck MK, Nonaka DF, et al. Chromatin immunoprecipitation (chip) scanning identifies primary glucocorticoid receptor target genes. Proc Natl Acad Sci U S A. 2004;101(44):15603–15608. PMC524211.
   PubMed Web of Science ®Google Scholar
• Constantinof A, Moisiadis VG, Matthews SG. Programming of stress pathways: A transgenerational perspective. J Steroid Biochem Mol Biol. 2016;160:175–180.
   PubMed Web of Science ®Google Scholar
• Murphy VE, Smith R, Giles WB, et al. Endocrine regulation of human fetal growth: the role of the mother, placenta, and fetus. Endocr Rev. 2006;27(2):141–169.
   PubMed Web of Science ®Google Scholar
• Tam WY, Jiang L, Kwan KM. Transmembrane 6 superfamily 1 (tm6sf1) is a novel lysosomal transmembrane protein. Protoplasma. 2015;252(4):977–983.
   PubMed Web of Science ®Google Scholar
• Remis NN, Wiwatpanit T, Castiglioni AJ, et al. Mucolipin co-deficiency causes accelerated endolysosomal vacuolation of enterocytes and failure-to-thrive from birth to weaning. PLoS Genet. 2014;10(12):e1004833. PMC4270466.
   PubMed Web of Science ®Google Scholar
• Rosenberg MJ, Wolff CR, El-Emawy A, et al. Effects of moderate drinking during pregnancy on placental gene expression. Alcohol. 2010;44(7–8):673–690. PMC3654802.
   PubMed Web of Science ®Google Scholar
• Shang Y, Das S, Rabold R, et al. Epigenetic alterations by DNA methylation in house dust mite-induced airway hyperresponsiveness. Am J Respir Cell Mol Biol. 2013;49(2):279–287. PMC3824034.
   PubMed Web of Science ®Google Scholar
• Schnatwinkel C, Christoforidis S, Lindsay MR, et al. The rab5 effector rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLoS Biol. 2004;2(9):E261. PMC514490.
   PubMed Web of Science ®Google Scholar
• Recouvreux MV, Commisso C. Macropinocytosis: A metabolic adaptation to nutrient stress in cancer. Frontiers in Endocrinology. 2017;8(261). DOI:10.3389/fendo.2017.00261
   PubMedGoogle Scholar
• Ogden LE. Nanoparticles in the environment: tiny size, large consequences? BioScience. 2013;63(3):236.
   Google Scholar
• Wick P, Malek A, Manser P, et al. Barrier capacity of human placenta for nanosized materials. Environ Health Perspect. 2010;118(3):432–436. PMC2854775.
   PubMed Web of Science ®Google Scholar
• Yamashita K, Yoshioka Y, Higashisaka K, et al. Silica and titanium dioxide nanoparticles cause pregnancy complications in mice. Nat Nanotechnol. 2011;6(5):321–328.
   PubMed Web of Science ®Google Scholar
• Riebeling C, Luch A, Gotz ME. Comparative modeling of exposure to airborne nanoparticles released by consumer spray products. Nanotoxicology. 2016;10(3):343–351.
   PubMed Web of Science ®Google Scholar
• Bowman DM, van Calster G, Friedrichs S. Nanomaterials and regulation of cosmetics. Nat Nanotechnol. 2010;5(2):92.
   PubMed Web of Science ®Google Scholar
• Rodney NC, Mulligan CJ. A biocultural study of the effects of maternal stress on mother and newborn health in the democratic republic of congo. Am J Phys Anthropol. 2014;155(2):200–209.
   PubMed Web of Science ®Google Scholar
• De Carli MM, Baccarelli AA, Trevisi L, et al. Epigenome-wide cross-tissue predictive modeling and comparison of cord blood and placental methylation in a birth cohort. Epigenomics. 2017;9(3):231–240. PMC5331917.
   PubMed Web of Science ®Google Scholar
• Zheng SC, Beck S, Jaffe AE, et al. Correcting for cell-type heterogeneity in epigenome-wide association studies: revisiting previous analyses. Nat Methods. 2017;14(3):216–217.
   PubMed Web of Science ®Google Scholar
• Wolfe J, Kimerling R. Gender issues in assessment of posttraumatic stress disorder. New York: Guilford; 1997.
   Google Scholar
• McHugo GJ, Caspi Y, Kammerer N, et al. The assessment of trauma history in women with co-occurring substance abuse and mental disorders and a history of interpersonal violence. J Behav Health Serv Res. 2005;32(2):113–127.
   PubMed Web of Science ®Google Scholar
• Janssen BG, Byun HM, Gyselaers W, et al. Placental mitochondrial methylation and exposure to airborne particulate matter in the early life environment: an environage birth cohort study. Epigenetics. 2015;10(6):536–544. PMC4623402.
   PubMed Web of Science ®Google Scholar
• Triche TJ Jr., Weisenberger DJ, Van Den Berg D, et al. Low-level processing of illumina infinium DNA methylation beadarrays. Nucleic acids research. 2013;41(7):e90; 3627582.
   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. Bioinformatics. 2013;29(2):189–196;3546795.
   PubMed Web of Science ®Google Scholar
• Pidsley R, Cc Yw V, Lunnon M, et al. LC. A data-driven approach to preprocessing illumina 450k methylation array data. BMC Genomics. 2013;14:293. PMC3769145.
   PubMed Web of Science ®Google Scholar
• Kumsta R, Marzi SJ, Viana J, et al. Severe psychosocial deprivation in early childhood is associated with increased DNA methylation across a region spanning the transcription start site of cyp2e1. Transl Psychiatry. 2016;6(6):e830. PMC4931613.
   PubMedGoogle Scholar
• Romens SE, McDonald J, Svaren J, et al. Associations between early life stress and gene methylation in children. Child Dev. 2015;86(1):303–309. PMC4305348.
   PubMed Web of Science ®Google Scholar
• Meinshausen N, Buhlmann P. Stability selection. J Royal Stat Soc. 2010;72:417–473.
   Google Scholar
• Phipson B, Maksimovic J, Oshlack A. Missmethyl: an r package for analyzing data from illumina’s humanmethylation450 platform. Bioinformatics. 2016;32(2):286–288.
   PubMed Web of Science ®Google Scholar
• Rivals I, Personnaz L, Taing L, et al. Enrichment or depletion of a go category within a class of genes: which test? Bioinformatics. 2007;23(4):401–407.
   PubMed Web of Science ®Google Scholar