In utero exposure to maternal smoking is associated with DNA methylation alterations and reduced neuronal content in the developing fetal brain

Epigenetics and Chromatin

Volumn 10, Issue 1, 2017, Pages

  Chatterton, Zac ^a,d   Hartley, Brigham J ^a   Seok, Man Ho ^a   Mendelev, Natalia ^a,d   Chen, Sean ^a,d   Milekic, Maria ^b   Rosoklija, Gorazd ^b,e,f   Stankov, Aleksandar ^f   Trencevsja Ivanovska, Iskra ^g   Brennand, Kristen ^a   Ge, Yongchao ^a   Dwork, Andrew J ^b,c,e   Haghighi, Fatemeh ^a,d  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c Department of Medicine   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e MACEDONIAN ACADEMY OF SCIENCES AND ARTS   (Macedonia)

^f School of Medicine   (United States)

^g Psychiatric Hospital Skopje   (Macedonia)

Author keywords

Brain; DNA methylation; Epigenetics; Fetal; Neurodevelopment; Neuron; Nicotine; Prenatal; Smoking; Tobacco

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; BRAIN DERIVED NEUROTROPHIC FACTOR; CATECHOL METHYLTRANSFERASE; CELL PROTEIN; CHROMOSOME 21 OPEN READING FRAME 56; G PROTEIN SUBUNIT ALPHA 15; GUANINE NUCLEOTIDE BINDING PROTEIN; MESSENGER RNA; NEURON SPECIFIC NUCLEAR PROTEIN; NICOTINE; NICOTINIC RECEPTOR; SPERM ASSOCIATED ANTIGEN 1; SYNAPTONEMAL COMPLEX CENTRAL ELEMENT PROTEIN 3; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; G PROTEIN ALPHA 16; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; SDHB PROTEIN, HUMAN; SUCCINATE DEHYDROGENASE; TUBB3 PROTEIN, HUMAN; TUBULIN;

ARTICLE; BRAIN DEVELOPMENT; BRAIN WEIGHT; C21 GENE; CELL DEATH; CELL DIFFERENTIATION; CELL SIZE; CONTROLLED STUDY; CPG ISLAND; DECISION MAKING; DNA DAMAGE; DNA METHYLATION; DORSOLATERAL PREFRONTAL CORTEX; EPIGENETICS; EXECUTIVE FUNCTION; FETUS; GENE; GENE EXPRESSION; GESTATIONAL AGE; GNA15 GENE; HUMAN; IMMUNOFLUORESCENCE; LSS GENE; MATERNAL SMOKING; MENTAL DISEASE; MICROARRAY ANALYSIS; MULTIPOTENT STEM CELL; NERVE CELL DIFFERENTIATION; NEURITE OUTGROWTH; OPEN READING FRAME; PHENOTYPE; POLDIP3 GENE; PRE T LYMPHOCYTE; PRENATAL EXPOSURE; PROMOTER REGION; RNU12 GENE; SDHAP3 GENE; SECOND TRIMESTER PREGNANCY; SMOKING; SPAG1 GENE; SYCE3 GENE; UNTRANSLATED REGION; UPREGULATION; WORKING MEMORY; BRAIN; CYTOLOGY; FEMALE; FETUS DEVELOPMENT; GENETICS; IMMUNOHISTOCHEMISTRY; INDUCED PLURIPOTENT STEM CELL; MALE; MATERNAL EXPOSURE; METABOLISM; NERVE CELL; NEURAL STEM CELL; PATHOLOGY; PREGNANCY;

BRAIN; DNA METHYLATION; FEMALE; FETAL DEVELOPMENT; FETUS; GESTATIONAL AGE; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HUMANS; IMMUNOHISTOCHEMISTRY; INDUCED PLURIPOTENT STEM CELLS; MALE; MATERNAL EXPOSURE; NEURAL STEM CELLS; NEURONS; PREGNANCY; PREGNANCY TRIMESTER, SECOND; PROMOTER REGIONS, GENETIC; SMOKING; SUCCINATE DEHYDROGENASE; TUBULIN;

EID: 85010773969     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/s13072-017-0111-y     Document Type: Article

References (78)

1. Cornelius MD, et al. Effects of prenatal cigarette smoke exposure on neurobehavioral outcomes in 10-year-old children of adolescent mothers. Neurotoxicol Teratol. 2011;33(1):137-44.
2. Huijbregts SC, et al. Hot and cool forms of inhibitory control and externalizing behavior in children of mothers who smoked during pregnancy: an exploratory study. J Abnorm Child Psychol. 2008;36(3):323-33.
3. Robinson M, et al. Smoking cessation in pregnancy and the risk of child behavioural problems: a longitudinal prospective cohort study. J Epidemiol Community Health. 2010;64(7):622-9.
4. Roza SJ, et al. Effects of maternal smoking in pregnancy on prenatal brain development. The Generation R Study. Eur J Neurosci. 2007;25(3):611-7.
5. El Marroun H, et al. Prenatal tobacco exposure and brain morphology: a prospective study in young children. Neuropsychopharmacology. 2014;39(4):792-800.
6. Eskenazi B, Bergmann JJ. Passive and active maternal smoking during pregnancy, as measured by serum cotinine, and postnatal smoke exposure. I. Effects on physical growth at age 5 years. Am J Epidemiol. 1995;142(9 Suppl):S10-8.
7. Wakschlag LS, et al. Maternal smoking during pregnancy and severe antisocial behavior in offspring: a review. Am J Public Health. 2002;92(6):966-74.
8. Talhout R, et al. Hazardous compounds in tobacco smoke. Int J Environ Res Public Health. 2011;8(2):613-28.
9. Li Y, et al. Perinatal nicotine exposure increases vulnerability of hypoxic-ischemic brain injury in neonatal rats: role of angiotensin II receptors. Stroke J Cereb Circ. 2012;43(9):2483-90.
10. Mychasiuk R, et al. Long-term alterations to dendritic morphology and spine density associated with prenatal exposure to nicotine. Brain Res. 2013;1499:53-60.
11. Slotkin TA, et al. Effects of prenatal nicotine exposure on primate brain development and attempted amelioration with supplemental choline or vitamin C: neurotransmitter receptors, cell signaling and cell development biomarkers in fetal brain regions of rhesus monkeys. Neuropsychopharmacology. 2005;30(1):129-44.
12. Bruin JE, Gerstein HC, Holloway AC. Long-term consequences of fetal and neonatal nicotine exposure: a critical review. Toxicol Sci Off J Soc Toxicol. 2010;116(2):364-74.
13. Dwyer JB, McQuown SC, Leslie FM. The dynamic effects of nicotine on the developing brain. Pharmacol Ther. 2009;122(2):125-39.
14. Button TM, Maughan B, McGuffin P. The relationship of maternal smoking to psychological problems in the offspring. Early Human Dev. 2007;83(11):727-32.
15. Lim R, Sobey CG. Maternal nicotine exposure and fetal programming of vascular oxidative stress in adult offspring. Br J Pharmacol. 2011;164(5):1397-9.
16. Mahar I, et al. Developmental hippocampal neuroplasticity in a model of nicotine replacement therapy during pregnancy and breastfeeding. PLoS ONE. 2012;7(5):e37219.
17. Pauly JR, Slotkin TA. Maternal tobacco smoking, nicotine replacement and neurobehavioural development. Acta Paediatr. 2008;97(10):1331-7.
18. Jones KL, Smith DW. Recognition of the fetal alcohol syndrome in early infancy. Lancet. 1973;302(7836):999-1001.
19. Grandjean P, Landrigan PJ. Developmental neurotoxicity of industrial chemicals. Lancet. 2006;368(9553):2167-78.
20. Julvez J, Grandjean P. Neurodevelopmental toxicity risks due to occupational exposure to industrial chemicals during pregnancy. Ind Health. 2009;47(5):459-68.
21. Gidekel S, Bergman Y. A unique developmental pattern of Oct-3/4 DNA methylation is controlled by a cis-demodification element. J Biol Chem. 2002;277(37):34521-30.
22. Adcock IM, et al. Epigenetic regulation of airway inflammation. Curr Opin Immunol. 2007;19(6):694-700.
23. Furniss CS, et al. Line region hypomethylation is associated with lifestyle and differs by human papillomavirus status in head and neck squamous cell carcinomas. Cancer Epidemiol Biomarkers Prev. 2008;17(4):966-71.
24. Kanai Y. Alterations of DNA methylation and clinicopathological diversity of human cancers. Pathol Int. 2008;58(9):544-58.
25. Lawrence J, et al. Foetal nicotine exposure causes PKCepsilon gene repression by promoter methylation in rat hearts. Cardiovasc Res. 2011;89(1):89-97.
26. Prescott SL, Clifton V. Asthma and pregnancy: emerging evidence of epigenetic interactions in utero. Curr Opin Allergy Clin Immunol. 2009;9(5):417-26.
27. Satta R, et al. Nicotine decreases DNA methyltransferase 1 expression and glutamic acid decarboxylase 67 promoter methylation in GABAergic interneurons. Proc Natl Acad Sci USA. 2008;105(42):16356-61.
28. Zochbauer-Muller S, et al. Aberrant methylation of multiple genes in the upper aerodigestive tract epithelium of heavy smokers. Int J Cancer. 2003;107(4):612-6.
29. Joubert BR, et al. DNA methylation in newborns and maternal smoking in pregnancy: genome-wide consortium meta-analysis. Am J Hum Genet. 2016;98(4):680-96.
30. Ladd-Acosta C, et al. Presence of an epigenetic signature of prenatal cigarette smoke exposure in childhood. Environ Res. 2016;144(Pt A):139-48.
31. Philibert RA, et al. MAOA methylation is associated with nicotine and alcohol dependence in women. Am J Med Genet B Neuropsychiatr Genet. 2008;147B(5):565-70.
32. Xu Q, et al. Determination of methylated CpG sites in the promoter region of catechol-O-methyltransferase (COMT) and their involvement in the etiology of tobacco smoking. Front Psychiatry. 2010;1:16.
33. Toledo-Rodriguez M, et al. Maternal smoking during pregnancy is associated with epigenetic modifications of the Brain-derived neurotrophic factor-6 exon in adolescent offspring. Am J Med Genet B Neuropsychiatr Genet. 2010;153B(7):1350-4.
34. Roebuck TM, Mattson SN, Riley EP. A review of the neuroanatomical findings in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res. 1998;22(2):339-44.
35. Sarnat HB, Nochlin D, Born DE. Neuronal nuclear antigen (NeuN): a marker of neuronal maturation in early human fetal nervous system. Brain Dev. 1998;20(2):88-94.
36. Kostovic I, et al. Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex. 2002;12(5):536-44.
37. Rados M, Judas M, Kostovic I. In vitro MRI of brain development. Eur J Radiol. 2006;57(2):187-98.
38. Shepard TH, et al. Organ weight standards for human fetuses. Pediatr Pathol. 1988;8(5):513-24.
39. Lee IS, et al. Characterization of molecular and cellular phenotypes associated with a heterozygous CNTNAP2 deletion using patient-derived hiPSC neural cells. Npj Schizophr. 2015;1:15019.
40. Topol A, et al. Dysregulation of miRNA-9 in a subset of schizophrenia patient-derived neural progenitor cells. Cell Rep. 2016;15(5):1024-36.
41. R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing. 2014; http://www.R-project.org/.
42. Bibikova M, et al. High-throughput DNA methylation profiling using universal bead arrays. Genome Res. 2006;16(3):383-93.
43. Gentleman RC, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5(10):R80.
44. Aryee MJ, et al. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics. 2014;30(10):1363-9.
45. Maksimovic J, Gordon L, Oshlack A. SWAN: subset-quantile within array normalization for illumina infinium HumanMethylation450 BeadChips. Genome Biol. 2012;13(6):R44.
46. Naeem H, et al. Reducing the risk of false discovery enabling identification of biologically significant genome-wide methylation status using the HumanMethylation450 array. BMC Genom. 2014;15:51.
47. Bibikova M, et al. High density DNA methylation array with single CpG site resolution. Genomics. 2011;98(4):288-95.
48. Jaffe AE, et al. Bump hunting to identify differentially methylated regions in epigenetic epidemiology studies. Int J Epidemiol. 2012;41(1):200-9.
49. Jaffe AE, et al. Developmental regulation of human cortex transcription and its clinical relevance at single base resolution. Nat Neurosci. 2015;18(1):154-61.
50. Kim M, et al. Dynamic changes in DNA methylation and hydroxymethylation when hES cells undergo differentiation toward a neuronal lineage. Hum Mol Genet. 2014;23(3):657-67.
51. Guintivano J, Aryee MJ, Kaminsky ZA. A cell epigenotype specific model for the correction of brain cellular heterogeneity bias and its application to age, brain region and major depression. Epigenetics. 2013;8(3):290-302.
52. Houseman EA, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinform. 2012;13:86.
53. BrainSpan: Atlas of the developing human brain [Internet]. Funded by ARRA Awards 1RC2MH089921-01, R.M.-., and 1RC2MH089929-01. © 2011. http://developinghumanbrain.org.
54. Penna I, et al. Selection of candidate housekeeping genes for normalization in human postmortem brain samples. Int J Mol Sci. 2011;12(9):5461-70.
55. Velculescu VE, et al. Analysis of human transcriptomes. Nat Genet. 1999;23(4):387-8.
56. Haghighi F, et al. Neuronal DNA methylation profiling of blast-related traumatic brain injury. J Neurotrauma. 2015;32(16):1200-9.
57. Sasaki T, et al. Type of feeding during infancy and later development of schizophrenia. Schizophr Res. 2000;42:79-82.
58. Mohn F, et al. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell. 2008;30(6):755-66.
59. Nguyen T, Di Giovanni S. NFAT signaling in neural development and axon growth. Int J Dev Neurosci. 2008;26(2):141-5.
60. Montano CM, et al. Measuring cell-type specific differential methylation in human brain tissue. Genome Biol. 2013;14(8):R94.
61. Rahmani E, et al. Sparse PCA corrects for cell type heterogeneity in epigenome-wide association studies. Nat Methods. 2016;13(5):443-5.
62. Jiang Y, et al. Isolation of neuronal chromatin from brain tissue. BMC Neurosci. 2008;9:42.
63. Lister R, et al. Global epigenomic reconfiguration during mammalian brain development. Science. 2013;341(6146):1237905.
64. Numata S, et al. DNA methylation signatures in development and aging of the human prefrontal cortex. Am J Hum Genet. 2012;90(2):260-72.
65. Schramm S, et al. A novel mouse synaptonemal complex protein is essential for loading of central element proteins, recombination, and fertility. PLoS Genet. 2011;7(5):e1002088.
66. Yankovskaya V, et al. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science. 2003;299(5607):700-4.
67. 2.-, oxidative stress, and genomic instability. Cancer Res. 2006;66(15):7615-20.
68. Ladd-Acosta C, et al. Common DNA methylation alterations in multiple brain regions in autism. Mol Psychiatry. 2014;19(8):862-71.
69. Wockner LF, et al. Brain-specific epigenetic markers of schizophrenia. Transl Psychiatry. 2015;5:e680.
70. Nardone S, et al. DNA methylation analysis of the autistic brain reveals multiple dysregulated biological pathways. Transl Psychiatry. 2014;4:e433.
71. Christensen J, et al. Prenatal valproate exposure and risk of autism spectrum disorders and childhood autism. JAMA. 2013;309(16):1696-703.
72. Pidsley R, et al. Methylomic profiling of human brain tissue supports a neurodevelopmental origin for schizophrenia. Genome Biol. 2014;15(10):483.
73. Jaffe AE, et al. Mapping DNA methylation across development, genotype and schizophrenia in the human frontal cortex. Nat Neurosci. 2016;19(1):40-7.
74. Wang J, et al. Genome-wide expression analysis reveals diverse effects of acute nicotine exposure on neuronal function-related genes and pathways. Front Psychiatry. 2011;2:5.
75. Census U.D.o.C.B. Current population survey, January 2007: Tobacco use supplement file: Tech. Doc. CPS-07. Washington, DC: US Department of Commerce; 2007.
76. Bhagwat SV, et al. Preferential effects of nicotine and 4-(N-methyl-N-nitrosamine)-1-(3-pyridyl)-1-butanone on mitochondrial glutathione S-transferase A4-4 induction and increased oxidative stress in the rat brain. Biochem Pharmacol. 1998;56(7):831-9.
77. Helen A, et al. Antioxidant effect of onion oil (Allium cepa. Linn) on the damages induced by nicotine in rats as compared to alpha-tocopherol. Toxicol Lett. 2000;116(1-2):61-8.
78. Guan ZZ, Yu WF, Nordberg A. Dual effects of nicotine on oxidative stress and neuroprotection in PC12 cells. Neurochem Int. 2003;43(3):243-9.