Prenatal smoke exposure induces persistent Cyp2a5 methylation and increases nicotine metabolism in the liver of neonatal and adult male offspring

References

• Messina ES, Tyndale RF, Sellers EM. A major role for CYP2A6 in nicotine C-oxidation by human. J Pharmacol Exp Ther [Internet]. 1997;282(3):1608–1614. Available from: http://jpet.aspetjournals.org/content/282/3/1608.long#page
   PubMed Web of Science ®Google Scholar
• Raunio H, Pokela N, Puhakainen K, et al. Nicotine metabolism and urinary elimination in mouse: in vitro and in vivo. Xenobiotica. 2008;38(1):34–47.
   PubMed Web of Science ®Google Scholar
• Siu ECK, Tyndale RF, Metabolism D, et al. Characterization and comparison of nicotine and cotinine metabolism in vitro and in vivo in DBA/2 and C57BL/6 mice. Nicotine Tob Res [Internet]. 2009;71(3):826–834. Available from: http://molpharm.aspetjournals.org/cgi/doi/10.1124/mol.106.032086
   Google Scholar
• Cho MH, Castaldi PJ, Wan ES, et al. A genome-wide association study of COPD identifies a susceptibility locus on chromosome 19q13. Hum Mol Genet. 2012;21(4):947–957.
   PubMed Web of Science ®Google Scholar
• Furberg H, Kim Y, Dackor J, et al. Genome-wide meta-analyses identify multiple loci associated with smoking behavior. Nat Genet. 2010;42(5):441–447.
   PubMed Web of Science ®Google Scholar
• Thorgeirsson TE, Gudbjartsson DF, Surakka I, et al. Sequence variants at CHRNB3-CHRNA6 and CYP2A6 affect smoking behavior. Nat Genet. 2010;42(5):448–453.
   PubMed Web of Science ®Google Scholar
• Kubota T, Nakajima-Taniguchi C, Fukuda T, et al. CYP2A6 polymorphisms are associated with nicotine dependence and influence withdrawal symptoms in smoking cessation. Pharmacogenomics J. 2006;6(2):115–119.
   PubMed Web of Science ®Google Scholar
• Lee NP, Fry SJ. Systematic review of the evidence relating FEV1 decline to giving up smoking. BMC Med [Internet]. 2010;8:84.
   PubMed Web of Science ®Google Scholar
• Amos CI, Spitz MR, Cinciripini P. Chipping away at the genetics of smoking behavior. Nat Genet [Internet]. 2010;42(5):366–368.
   PubMed Web of Science ®Google Scholar
• Dempsey D, Tutka P, Jacob P, et al. Nicotine metabolite ratio as an index of cytochrome P450 2A6 metabolic activity. Clin Pharmacol Ther. 2004;76(1):64–72.
   PubMed Web of Science ®Google Scholar
• Nakajima M, Yoshihiko T, Noriaki K, et al. ROLE OF HUMAN CYTOCHROME P450A6 IN C-OXIDATION OF NICOTINE. Drug Metab Dispos. 1996;24(11):1212–1217.
   PubMed Web of Science ®Google Scholar
• Siu ECK, Tyndale RF. Characterization and comparison of nicotine and cotinine metabolism in vitro and in vivo in DBA/2 and C57BL/6 mice. Mol Pharmacol [Internet]. 2006;71(3):826–834. Available from: http://molpharm.aspetjournals.org/cgi/doi/10.1124/mol.106.032086
   PubMed Web of Science ®Google Scholar
• Zhou X, Zhuo X, Xie F, et al. Role of CYP2A5 in the clearance of nicotine and cotinine: insights from studies on a Cyp2a5-null mouse model. J Pharmacol Exp Ther. 2010;3332:578–587.
   Google Scholar
• Murphy SE, Raulinaitis V, Brown KM. Nicotine 5′-oxidation and methyl oxidation by P450 2A enzymes. Drug Metab Dispos. 2005;33(8):1166–1173.
   PubMed Web of Science ®Google Scholar
• Blacquie`re MJ, Timens W, Berg AVD, et al. Maternal smoking during pregnancy decreases Wnt signalling in neonatal mice. Thorax. 2010;65(6):553.
   Web of Science ®Google Scholar
• Stevens DR, Malek AM, Laggis C, et al. In utero exposure to tobacco smoke, subsequent cardiometabolic risks, and metabolic syndrome among U.S. adolescents. Ann Epidemiol. 2018;28(9):619–624.e1.
   PubMed Web of Science ®Google Scholar
• Wiklund P, Karhunen V, Richmond RC, et al. DNA methylation links prenatal smoking exposure to later life health outcomes in offspring. Clin Epigenetics. 2019;11(1):1–16.
   PubMedGoogle Scholar
• Kandel DB, Udry JR. Prenatal effects of maternal smoking on daughters’ smoking: nicotine or testosterone exposure? Am J Public Health. 1999;89(9):1377–1383.
   PubMed Web of Science ®Google Scholar
• Kandel DB, Wu P, Davies M. Maternal smoking during pregnancy and smoking by adolescent daughters. Am J Public Health. 1994;84(9):1407–1413.
   PubMed Web of Science ®Google Scholar
• Savran O, Ulrik CS. Early life insults as determinants of chronic obstructive pulmonary disease in adult life. Int J COPD. 2018;13:683–693.
   Google Scholar
• Blacquière MJ, Timens W, Melgert BN, et al. Maternal smoking during pregnancy induces airway remodelling in mice offspring. Eur Respir J. 2009;33:1133–1140.
   PubMed Web of Science ®Google Scholar
• Krauss-Etschmann S, Meyer KF, Dehmel S, et al. Inter-and transgenerational epigenetic inheritance: evidence in asthma and COPD? Clin Epigenetics [Internet]. 2015;7(1):1–13.
   PubMedGoogle Scholar
• Ferrini M, Carvalho S, Cho YH, et al. Prenatal tobacco smoke exposure predisposes offspring mice to exacerbated allergic airway inflammation associated with altered innate effector function. Part Fibre Toxicol. 2017;14(1):1–14.
   PubMedGoogle Scholar
• Dehmel S, Nathan P, Bartel S, et al. Intrauterine smoke exposure deregulates lung function, pulmonary transcriptomes, and in particular insulin-like growth factor (IGF)-1 in a sex-specific manner/631/136/3194/631/443/1784/692/699/1785/31/38/61/38/90/38/39/59/64/64/60 article. Sci Rep. 2018;8(1):1–12.
   PubMedGoogle Scholar
• Klein LC, Stine MM, Pfaff DW, et al. Maternal nicotine exposure increases nicotine preference in periadolescent male but not female C57B1/6J mice. Nicotine Tob Res. 2003;5(1):117–124.
   PubMed Web of Science ®Google Scholar
• Richmond RC, Simpkin AJ, Woodward G, et 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. 2015;24(8):2201–2217.
   PubMed Web of Science ®Google Scholar
• Maccani JZJ, Koestler DC, Houseman EA, et al. Placental DNA methylation alterations associated with maternal tobacco smoking at the RUNX3 gene are also associated with gestational age. Epigenomics. 2013;5(6):619–630.
   PubMed Web of Science ®Google Scholar
• Breton CV, Siegmund KD, Joubert BR, et al. Prenatal tobacco smoke exposure is associated with childhood DNA CpG methylation. PLoS One. 2014;9(6):e99716.
   Web of Science ®Google Scholar
• Meyer KF, Krauss-Etschmann S, Kooistra W, et al. 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 [Internet]. 2017;312(4):L542–55. Available from: http://ajplung.physiology.org/lookup/doi/10.1152/ajplung.00271.2016
   PubMed Web of Science ®Google Scholar
• Meyer KF, Verkaik-Schakel RN, Timens W, et al. The fetal programming effect of prenatal smoking on Igf1r and Igf1 methylation is organ- and sex-specific. Epigenetics [Internet]. 2017;12(12):1076–1091.
   PubMed Web of Science ®Google Scholar
• Eyring KR, Pedersen BS, Yang IV, et al. In utero cigarette smoke affects allergic airway disease but does not alter the lung methylome. PLoS One. 2015;10(12):1–10.
   Web of Science ®Google Scholar
• Benowitz NL. Nicotine Addiction. N Engl J Med. 2010;362(24):2295–2303.
   PubMed Web of Science ®Google Scholar
• Ho MK, Mwenifumbo JC, Al Koudsi N, et al. Association of nicotine metabolite ratio and CYP2A6 genotype with smoking cessation treatment in African-American light smokers. Clin Pharmacol Ther. 2009;85(6):635–643.
   PubMed Web of Science ®Google Scholar
• Tizabi Y, Popke EJ, Rahman MA, et al. Hyperactivity induced by prenatal nicotine exposure is associated with an increase in cortical nicotinic receptors. Pharmacol Biochem Behav. 1997;58(1):141–146.
   PubMed Web of Science ®Google Scholar
• van Otterdijk SD, Binder AM, Michels KB. Locus-specific DNA methylation in the placenta is associated with levels of pro-inflammatory proteins in cord blood and they are both independently affected by maternal smoking during pregnancy. Epigenetics [Internet]. 2017;12(10):875–885.
   PubMed Web of Science ®Google Scholar
• Lee KWK, Richmond R, Hu P, et al. Prenatal exposure to maternal cigarette smoking and DNA methylation: epigenome-wide association in a discovery sample of adolescents and replication in an independent cohort at birth through 17 years of age. Environ Health Perspect. 2015;123(2):193–199.
   PubMed Web of Science ®Google Scholar
• Yokomori N, Moore R, Negishi M. Sexually dimorphic DNA demethylation in the promoter of the Slp (sex-limited protein) gene in mouse liver. Proc Natl Acad Sci U S A [Internet]. 1995;92(5):1302–1306.
   PubMed Web of Science ®Google Scholar
• Yokomori N, Kobayashi R, Moore R, et al. A DNA methylation site in the male-specific P450 (Cyp 2d-9) promoter and binding of the heteromeric transcription factor GABP. Mol Cell Biol [Internet]. 1995;15(10):5355–5362.
   PubMed Web of Science ®Google Scholar
• Takasugi M, Hayakawa K, Arai D, et al. Age- and sex-dependent DNA hypomethylation controlled by growth hormone in mouse liver. Mech Ageing Dev [Internet]. 2013;134(7–8):331–337.
   PubMed Web of Science ®Google Scholar
• Nugent BM, Schwarz JM, Mccarthy MM. Hormonally mediated epigenetic changes to steroid receptors in the developing brain: implications for sexual differentiation. Horm Behav [Internet]. 2011;59(3):338–344.
   PubMed Web of Science ®Google Scholar
• Al Koudsi N, Hoffmann EB, Assadzadeh A, et al. Hepatic CYP2A6 levels and nicotine metabolism: impact of genetic, physiological, environmental, and epigenetic factors. Eur J Clin Pharmacol. 2010;66(3):239–251.
   PubMed Web of Science ®Google Scholar
• The ROF, Cytochrome H. Transcriptional regulation of the hepatic cytochrome P450 2a5 gene [Internet]. 2007. 1–130 p. Available from: http://herkules.oulu.fi/isbn9789514285653/isbn9789514285653.pdf%5Cnpapers3://publication/uuid/04328BDE-78AD-421C-BB7F-E84F9DAEA6E7
   Google Scholar
• Liu F, Killian JK, Yang M, et al. Epigenomic alterations and gene expression profiles in respiratory epithelia exposed to cigarette smoke condensate. Oncogene. 2010;29(25):3650–3664.
   PubMed Web of Science ®Google Scholar
• Sundar IK, Rahman I. Gene expression profiling of epigenetic chromatin modification enzymes and histone marks by cigarette smoke: implications for COPD and lung cancer. Am J Physiol Lung Cell Mol Physiol. 2016;311(6):L1245–58.
   PubMed Web of Science ®Google Scholar
• Dempsey D, Jacob P, Benowitz NL. Nicotine metabolism and elimination kinetics in newborns. Clin Pharmacol Ther. 2000;67(5):458–465.
   PubMed Web of Science ®Google Scholar
• Gow PJ, Ghabrial H, Smallwood RA, et al. Neonatal hepatic drug elimination. Toxicol Pharmacol. 2001;88(1):3–15.
   PubMedGoogle Scholar
• Dempsey D, Jacob P, Benowitz N. Accelerated metabolism of nicotine and cotinine in pregnant smokers. J Pharmacol Exp Ther [Internet]. 2002;301(2):594–598.
   PubMed Web of Science ®Google Scholar
• Novakovic B, Ryan J, Pereira N, et al. Postnatal stability and tissue- and time-specific effects of AHRR methylation change in response to maternal smoking in pregnancy. Epigenetics. 2013;9:3.
   Web of Science ®Google Scholar
• Massart R, Nemoda Z, Suderman MJ, et al. Early life adversity alters normal sex-dependent developmental dynamics of DNA methylation. Dev Psychopathol. 2016;28(4):1259–1272.
   PubMed Web of Science ®Google Scholar
• Chhabra D, Sharma S, Kho AT, et al. Fetal lung and placental methylation is associated with in utero nicotine exposure. Epigenetics. 2014;9(11):1473–1484.
   PubMed Web of Science ®Google Scholar
• Gao X, Jia M, Zhang Y, et al. DNA methylation changes of whole blood cells in response to active smoking exposure in adults: a systematic review of DNA methylation studies. Clin Epigenetics [Internet]. 2015;7(1). DOI:10.1186/s13148-015-0148-3
   Google Scholar
• Benowitz NL, Lessov-Schlaggar CN, Swan GE, et al. Female sex and oral contraceptive use accelerate nicotine metabolism. Clin Pharmacol Ther. 2006;79(5):480–488.
   PubMed Web of Science ®Google Scholar
• Berlin I, Gasior MJ, Moolchan ET. Sex-based and hormonal contraception effects on the metabolism of nicotine among adolescent tobacco-dependent smokers. Nicotine Tob Res. 2007;9(4):493–498.
   PubMed Web of Science ®Google Scholar
• Liu Z, Li L, Wu H, et al. Characterization of CYP2B6 in a CYP2B6-humanized mouse model: inducibility in the liver by phenobarbital and dexamethasone and role in nicotine metabolism in vivos. Drug Metab Dispos. 2015;43(2):208–216.
   PubMed Web of Science ®Google Scholar
• Lamba V, Lamba J, Yasuda K, et al. Hepatic CYP2B6 expression: gender and ethnic differences and relationship to CYP2B6 genotype and CAR (Constitutive Androstane Receptor) expression. J Pharmacol Exp Ther. 2003;307(3):906–922.
   PubMed Web of Science ®Google Scholar
• Dickmann LJ, Isoherranen N. Quantitative prediction of CYP2B6 induction by estradiol during pregnancy: potential explanation for increased methadone clearance during pregnancy. Drug Metab Dispos. 2013;41(2):270–274.
   PubMed Web of Science ®Google Scholar
• Pogun S, Yararbas G, Nesil T, et al. Sex differences in nicotine preference. J Neurosci Res. 2017;95(1–2):148–162.
   PubMed Web of Science ®Google Scholar
• Shiffman S, Paton S. Individual differences in smoking: gender and nicotine addiction. Nicotine Tob Res. 1999;1(1):153–157.
   PubMedGoogle Scholar
• Hamdani N, Ades J, Gorwood P. [Heritability and candidate genes in tobacco use]. Encephale. 2006;32:966–975.
   PubMed Web of Science ®Google Scholar
• Arger CA, Taghavi T, Heil SH, et al. Pregnancy-Induced increases in the nicotine metabolite ratio: examining changes during antepartum and postpartum. Nicotine Tob Res. 2018;12(12)1–5.
   Web of Science ®Google Scholar
• Higashi E, Fukami T, Itoh M, et al. Human CYP2A6 is induced by estrogen via estrogen receptor. Drug Metab Dispos. 2007;35(10):1935–1941.
   PubMed Web of Science ®Google Scholar
• Torres OV, Natividad LA, Tejeda HA, et al. Female rats display dose-dependent differences to the rewarding and aversive effects of nicotine in an age-, hormone-, and sex-dependent manner. Psychopharmacology (Berl). 2009;206(2):303–312.
   PubMed Web of Science ®Google Scholar
• Harrod SB, Booze RM, Mactutus CF. Sex differences in nicotine levels following repeated intravenous injection in rats are attenuated by gonadectomy. Pharmacol Biochem Behav. 2007;86(1):32–36.
   PubMed Web of Science ®Google Scholar
• Weinberg CR, Wilcox AJ, Baird DD. Reduced fecundability in women with prenatal exposure to cigarette smoking. Am J Epidemiol. 1989;129(5):1072–1078.
   PubMed Web of Science ®Google Scholar
• Jensen TK, Henriksen TB, Hjollund NHI, et al. Adult and prenatal exposures to tobacco smoke as risk indicators of fertility among 430 Danish couples. Am J Epidemiol. 1998;148(10):992–997.
   PubMed Web of Science ®Google Scholar
• Holloway AC, Kellenberger LD, Petrik JJ. Fetal and neonatal exposure to nicotine disrupts ovarian function and fertility in adult female rats. Endocrine. 2006;30(2):213–216.
   PubMed Web of Science ®Google Scholar
• Lambert JF, Benoit BO, Colvin GA, et al. Quick sex determination of mouse fetuses. J Neurosci Methods. 2000;95(2):127–132.
   PubMed Web of Science ®Google Scholar
• EME VS, Bloks VW, Huijkman NCA, et al. The liver X-receptor gene promoter is hypermethylated in a mouse model of prenatal protein restriction. Am J Epidemiol. 2010;298(2):275–282.
   Google Scholar
• Siu ECK, Wildenauer DB, Tyndale RF. Nicotine self-administration in mice is associated with rates of nicotine inactivation by CYP2A5. Psychopharmacology (Berl). 2006;184(3–4):401–408.
   PubMed Web of Science ®Google Scholar
• Massadeh AM, Gharaibeh AA, Omari KW. A single-step extraction method for the determination of nicotine and cotinine in Jordanian smokers ’ blood and urine samples by RP-HPLC and GC – MS. J Chromatogr Sci. 2009;47(February):170–7.
   PubMedGoogle Scholar