Perinatal exposure to environmental tobacco smoke is associated with changes in DNA methylation that precede the adult onset of lung disease in a mouse model

References

• Barker DJ. (2004). Developmental origins of adult health and disease. J Epidemiol Community Health 58:114–15.
   PubMed Web of Science ®Google Scholar
• Basta PV, Basham KB, Ross WP, et al. (2000). Gestational nicotine exposure alone or in combination with ethanol down-modulates offspring immune function. Int J Immunopharmacol 22:159–69.
   PubMed Web of Science ®Google Scholar
• Beamer CA, Migliaccio CT, Jessop F, et al. (2010). Innate immune processes are sufficient for driving silicosis in mice. J Leukoc Biol 88:547–57.
   PubMed Web of Science ®Google Scholar
• Borthwick LA, Wynn TA, Fisher AJ. (2013). Cytokine mediated tissue fibrosis. Biochim Biophys Acta 1832:1049–60.
   PubMed Web of Science ®Google Scholar
• Breton CV, Byun HM, Wenten M, et al. (2009). Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am J Respir Crit Care Med 180:462–7.
   PubMed Web of Science ®Google Scholar
• Brown TA, Holian A, Pinkerton KE, et al. (2016). Early life exposure to environmental tobacco smoke alters immune response to asbestos via a shift in inflammatory phenotype resulting in increased disease development. Inhal Toxicol 28:349–56.
   PubMed Web of Science ®Google Scholar
• Brown TA, Lee JW, Holian A, et al. (2015). Alterations in DNA methylation corresponding with lung inflammation and as a biomarker for disease development after MWCNT exposure. Nanotoxicology 10:453–61.
   PubMed Web of Science ®Google Scholar
• de Araujo-Souza PS, Hanschke SC, Viola JP. (2015). Epigenetic control of interferon-gamma expression in CD8 T cells. J Immunol Res 2015:849573.
   PubMedGoogle Scholar
• Dietert RR, Zelikoff JT. (2008). Early-life environment, developmental immunotoxicology, and the risk of pediatric allergic disease including asthma. Birth Defects Res B Dev Reprod Toxicol 83:547–60.
   PubMed Web of Science ®Google Scholar
• DiFranza JR, Aligne CA, Weitzman M. (2004). Prenatal and postnatal environmental tobacco smoke exposure and children's health. Pediatrics 113:1007–15.
   PubMed Web of Science ®Google Scholar
• Feil R, Fraga MF. (2011). Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 13:97–109.
   Web of Science ®Google Scholar
• Fernandez-Plata R, Rojas-Martinez R, Martinez-Briseno D, et al. (2016). Effect of passive smoking on the growth of pulmonary function and respiratory symptoms in schoolchildren. Rev Invest Clin 68:119–27.
   PubMedGoogle Scholar
• Gibbs K, Collaco JM, McGrath-Morrow SA. (2016). Impact of tobacco smoke and nicotine exposure on lung development. Chest 149:552–61.
   PubMed Web of Science ®Google Scholar
• Gilliland FD, Berhane K, McConnell R, et al. (2000). Maternal smoking during pregnancy, environmental tobacco smoke exposure and childhood lung function. Thorax 55:271–6.
   PubMed Web of Science ®Google Scholar
• Guerrero-Preston R, Goldman LR, Brebi-Mieville P, et al. (2010). Global DNA hypomethylation is associated with in utero exposure to cotinine and perfluorinated alkyl compounds. Epigenetics 5:539–46.
   PubMed Web of Science ®Google Scholar
• Hagood JS, Prabhakaran P, Kumbla P, et al. (2005). Loss of fibroblast Thy-1 expression correlates with lung fibrogenesis. Am J Pathol 167:365–79.
   PubMed Web of Science ®Google Scholar
• Hamilton RF, Jr., Buford M, Xiang C, et al. (2012). NLRP3 inflammasome activation in murine alveolar macrophages and related lung pathology is associated with MWCNT nickel contamination. Inhal Toxicol 24:995–1008.
   PubMed Web of Science ®Google Scholar
• Ho SM. (2010). Environmental epigenetics of asthma: an update. J Allergy Clin Immunol 126:453–65.
   PubMed Web of Science ®Google Scholar
• Janson C. (2004). The effect of passive smoking on respiratory health in children and adults. Int J Tuberc Lung Dis 8:510–16.
   PubMed Web of Science ®Google Scholar
• Jinot J, Bayard SP. (1992). United States Environmental Protection Agency. Office of Health and Environmental Assessment., United States. Environmental Protection Agency. Indoor Air Division. Respiratory health effects of passive smoking: lung cancer and other disorders. Washington, DC: Office of Health and Environmental Assessment, Office of Research and Development, U.S. Environmental Protection Agency.
   Google Scholar
• Joad JP, Kott KS, Bric JM, et al. (2009). Effect of perinatal secondhand tobacco smoke exposure on in vivo and intrinsic airway structure/function in non-human primates. Toxicol Appl Pharmacol 234:339–44.
   PubMed Web of Science ®Google Scholar
• Karimi M, Johansson S, Ekstrom TJ. (2006a). Using LUMA: a Luminometric-based assay for global DNA-methylation. Epigenetics 1:45–8.
   PubMed Web of Science ®Google Scholar
• Karimi M, Johansson S, Stach D, et al. (2006b). LUMA (LUminometric Methylation Assay) - a high throughput method to the analysis of genomic DNA methylation. Exp Cell Res 312:1989–95.
   PubMed Web of Science ®Google Scholar
• Larsson ML, Frisk M, Hallstrom J, et al. (2001). Environmental tobacco smoke exposure during childhood is associated with increased prevalence of asthma in adults. Chest 120:711–7.
   PubMed Web of Science ®Google Scholar
• Lee DJ, Gaynor JJ, Trapido E. (2003). Secondhand smoke and earaches in adolescents: the Florida Youth Cohort Study. Nicotine Tob Res 5:943–6.
   PubMed Web of Science ®Google Scholar
• Lee DU, Agarwal S, Rao A. (2002). Th2 lineage commitment and efficient IL-4 production involves extended demethylation of the IL-4 gene. Immunity 16:649–60.
   PubMed Web of Science ®Google Scholar
• Lee HS, Barraza-Villarreal A, Hernandez-Vargas H, et al. (2013). Modulation of DNA methylation states and infant immune system by dietary supplementation with omega-3 PUFA during pregnancy in an intervention study. Am J Clin Nutr 98:480–7.
   PubMed Web of Science ®Google Scholar
• Lee JW, Jaffar Z, Pinkerton KE, et al. (2015). Alterations in DNA methylation and airway hyperreactivity in response to in utero exposure to environmental tobacco smoke. Inhal Toxicol 27:724–30.
   PubMed Web of Science ®Google Scholar
• Leenen FA, Muller CP, Turner JD. (2016). DNA methylation: conducting the orchestra from exposure to phenotype? Clin Epigenetics 8:92.
   PubMed Web of Science ®Google Scholar
• Li YF, Gilliland FD, Berhane K, et al. (2000). Effects of in utero and environmental tobacco smoke exposure on lung function in boys and girls with and without asthma. Am J Respir Crit Care Med 162:2097–104.
   PubMed Web of Science ®Google Scholar
• Liu F, Killian JK, Yang M, et al. (2010). Epigenomic alterations and gene expression profiles in respiratory epithelia exposed to cigarette smoke condensate. Oncogene 29:3650–64.
   PubMed Web of Science ®Google Scholar
• Lovasi GS, Diez Roux AV, Hoffman EA, et al. (2010). Association of environmental tobacco smoke exposure in childhood with early emphysema in adulthood among nonsmokers: the MESA-lung study. Am J Epidemiol 171:54–62.
   PubMed Web of Science ®Google Scholar
• Maritz GS, Harding R. (2011). Life-long programming implications of exposure to tobacco smoking and nicotine before and soon after birth: evidence for altered lung development. Int J Environ Res Public Health 8:875–98.
   PubMed Web of Science ®Google Scholar
• Meyer KF, Krauss-Etschmann S, Kooistra W, et al. (2017). Prenatal exposure to tobacco smoke sex dependently influences methylation and mRNA levels of the Igf axis in lungs of mouse offspring. Am J Physiol Lung Cell Mol Physiol 312:L542–55.
   PubMed Web of Science ®Google Scholar
• Miller RL, Ho SM. (2008). Environmental epigenetics and asthma: current concepts and call for studies. Am J Respir Crit Care Med 177:567–73.
   PubMed Web of Science ®Google Scholar
• Ouyang Y, Virasch N, Hao P, et al. (2000). Suppression of human IL-1beta, IL-2, IFN-gamma, and TNF-alpha production by cigarette smoke extracts. J Allergy Clin Immunol 106:280–7.
   PubMed Web of Science ®Google Scholar
• Penn AL, Rouse RL, Horohov DW, et al. (2007). In utero exposure to environmental tobacco smoke potentiates adult responses to allergen in BALB/c mice. Environ Health Perspect 115:548–55.
   PubMed Web of Science ®Google Scholar
• Pinkerton KE, Joad JP. (2006). Influence of air pollution on respiratory health during perinatal development. Clin Exp Pharmacol Physiol 33:269–72.
   PubMed Web of Science ®Google Scholar
• Prescott SL, Macaubas C, Holt BJ, et al. (1998). Transplacental priming of the human immune system to environmental allergens: universal skewing of initial T cell responses toward the Th2 cytokine profile. J Immunol 160:4730–7.
   PubMed Web of Science ®Google Scholar
• Pugmire J, Vasquez MM, Zhou M, et al. (2014). Exposure to parental smoking in childhood is associated with persistence of respiratory symptoms into young adult life. J Allergy Clin Immunol 134:962–5.e964.
   PubMed Web of Science ®Google Scholar
• Qiu W, Baccarelli A, Carey VJ, et al. (2012). Variable DNA methylation is associated with chronic obstructive pulmonary disease and lung function. Am J Respir Crit Care Med 185:373–81.
   PubMed Web of Science ®Google Scholar
• Rajini P, Last JA, Pinkerton KE, et al. (1994). Decreased fetal weights in rats exposed to sidestream cigarette smoke. Fundam Appl Toxicol 22:400–4.
   PubMedGoogle Scholar
• Renz H, Brandtzaeg P, Hornef M. (2011). The impact of perinatal immune development on mucosal homeostasis and chronic inflammation. Nat Rev Immunol 12:9–23.
   PubMed Web of Science ®Google Scholar
• Sanders YY, Ambalavanan N, Halloran B, et al. (2012). Altered DNA methylation profile in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 186:525–35.
   PubMed Web of Science ®Google Scholar
• Sanders YY, Pardo A, Selman M, et al. (2008). Thy-1 promoter hypermethylation: a novel epigenetic pathogenic mechanism in pulmonary fibrosis. Am J Respir Cell Mol Biol 39:610–8.
   PubMed Web of Science ®Google Scholar
• Seymour BW, Friebertshauser KE, Peake JL, et al. (2002). Gender differences in the allergic response of mice neonatally exposed to environmental tobacco smoke. Dev Immunol 9:47–54.
   PubMedGoogle Scholar
• Siegle JS, Hansbro N, Dong C, et al. (2011). Blocking induction of T helper type 2 responses prevents development of disease in a model of childhood asthma. Clin Exp Immunol 165:19–28.
   PubMed Web of Science ®Google Scholar
• Singh SP, Gundavarapu S, Pena-Philippides JC, et al. (2011). Prenatal secondhand cigarette smoke promotes Th2 polarization and impairs goblet cell differentiation and airway mucus formation. J Immunol 187:4542–52.
   PubMed Web of Science ®Google Scholar
• Slotkin TA, Pinkerton KE, Seidler FJ. (2006). Perinatal environmental tobacco smoke exposure in rhesus monkeys: critical periods and regional selectivity for effects on brain cell development and lipid peroxidation. Environ Health Perspect 114:34–9.
   PubMed Web of Science ®Google Scholar
• Smith ZD, Meissner A. (2013). DNA methylation: roles in mammalian development. Nat Rev Genet 14:204–20.
   PubMed Web of Science ®Google Scholar
• Stampfli MR, Anderson GP. (2009). How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat Rev Immunol 9:377–84.
   PubMed Web of Science ®Google Scholar
• Swanson JM, Entringer S, Buss C, Wadhwa PD. (2009). Developmental origins of health and disease: environmental exposures. Semin Reprod Med 27:391–402.
   PubMed Web of Science ®Google Scholar
• Tebow G, Sherrill DL, Lohman IC, et al. (2008). Effects of parental smoking on interferon gamma production in children. Pediatrics 121:e1563–9.
   PubMed Web of Science ®Google Scholar
• Thacher JD, Gruzieva O, Pershagen G, et al. (2014). Pre- and postnatal exposure to parental smoking and allergic disease through adolescence. Pediatrics 134:428–34.
   PubMed Web of Science ®Google Scholar
• van der Velden VH, Laan MP, Baert MR, et al. (2001). Selective development of a strong Th2 cytokine profile in high-risk children who develop atopy: risk factors and regulatory role of IFN-gamma, IL-4 and IL-10. Clin Exp Allergy 31:997–1006.
   PubMed Web of Science ®Google Scholar
• Vardavas CI, Hohmann C, Patelarou E, et al. (2016). The independent role of prenatal and postnatal exposure to active and passive smoking on the development of early wheeze in children. Eur Respir J 48:115–24.
   PubMed Web of Science ®Google Scholar
• Wang L, Joad JP, Abel K, et al. (2007). Effects of environmental tobacco smoke on the developing immune system of infant monkeys. J Allergy Clin Immunol 120:445–51.
   PubMed Web of Science ®Google Scholar
• Wang L, Pinkerton KE. (2008). Detrimental effects of tobacco smoke exposure during development on postnatal lung function and asthma. Birth Defects Res C Embryo Today 84:54–60.
   PubMedGoogle Scholar
• Wilhelm-Benartzi CS, Houseman EA, Maccani MA, et al. (2012). In utero exposures, infant growth, and DNA methylation of repetitive elements and developmentally related genes in human placenta. Environ Health Perspect 120:296–302.
   PubMed Web of Science ®Google Scholar
• Wynn TA. (2004). Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat Rev Immunol 4:583–94.
   PubMed Web of Science ®Google Scholar
• Xiao R, Perveen Z, Paulsen D, et al. (2012). In utero exposure to second-hand smoke aggravates adult responses to irritants: adult second-hand smoke. Am J Respir Cell Mol Biol 47:843–51.
   PubMed Web of Science ®Google Scholar
• Yano S, Ghosh P, Kusaba H, et al. (2003). Effect of promoter methylation on the regulation of IFN-gamma gene during in vitro differentiation of human peripheral blood T cells into a Th2 population. J Immunol 171:2510–6.
   PubMed Web of Science ®Google Scholar