Frontal cortex transcriptome analysis of mice exposed to electronic cigarettes during early life stages

International Journal of Environmental Research and Public Health

Volumn 13, Issue 4, 2016, Pages

  Lauterstein, Dana E ^a   Tijerina, Pamella B ^a   Corbett, Kevin ^a   Oksuz, Betul Akgol ^a   Shen, Steven S ^a   Gordon, Terry ^a   Klein, Catherine B ^a   Zelikoff, Judith T ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Central nervous system; Development; E cigarettes; Frontal cortex; Nicotine; Pathway analysis; RNA Sequencing; Transcriptome

Indexed keywords

NICOTINE; TRANSCRIPTOME; GLYCEROL; PROPYLENE GLYCOL;

GENE EXPRESSION; HYPOTHESIS TESTING; NERVOUS SYSTEM; PREGNANCY; PUBLIC HEALTH; RNA; SMOKE;

AEROSOL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BREEDING; CONTROLLED STUDY; DAM (ANIMAL); ELECTRONIC CIGARETTE; FEMALE; FRONTAL CORTEX; GENE EXPRESSION; MALE; MOUSE; NEUROPATHOLOGY; NEWBORN; NONHUMAN; PERINATAL PERIOD; PROGENY; PUP (RODENT); RNA SEQUENCE; TRANSCRIPTOMICS; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; DRUG EFFECTS; FRONTAL LOBE; GENE EXPRESSION PROFILING; INHALATIONAL DRUG ADMINISTRATION; PATHOPHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE;

MUS;

ADMINISTRATION, INHALATION; ANIMALS; ELECTRONIC CIGARETTES; FEMALE; FRONTAL LOBE; GENE EXPRESSION PROFILING; GLYCEROL; MALE; MICE; MICE, INBRED C57BL; NICOTINE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROPYLENE GLYCOL; TRANSCRIPTOME;

EID: 84963565248     PISSN: 16617827     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph13040417     Document Type: Article

References (44)

1. Arrazola, R.A.; Singh, T.; Corey, C.G.; Husten, C.G.; Neff, L.J.; Apelberg, B.J.; Bunnell, R.E.; Choiniere, C.J.; King, B.A.; Cox, S.; et al. Tobacco use among middle and high school students-United States, 2011-2014. MMWR Morb. Mortal Wkly. Rep. 2015, 14, 381-385.
2. England, L.J.; Bunnell, R.E.; Pechacek, T.F.; Tong, V.T.; McAfee, T.A. Nicotine and the Developing Human: A Neglected Element in the Electronic Cigarette Debate. Am. J. Prev. Med. 2015, 2, 286-293.
3. Agaku, I.T.; King, B.A.; Husten, C.G.; Bunnell, R.; Ambrose, B.K.; Hu, S.S.; Holder-Hayes, E.; Day, H.R. Tobacco Product Use Among Adults-United States 2012-2013. MMWR Morb. Mortal Wkly. Rep. 2014, 25, 542-547.
4. Farquhar, B.; Mark, K.; Terplan, M.; Chisolm, M.S. Demystifying electronic cigarette use in pregnancy. J. Addict. Med. 2015, 2, 157-158.
5. Tong, V.T.; Dietz, P.M.; Farr, S.L.; D’Angelo, D.V.; England, L.J. Estimates of smoking before and during pregnancy: Comparing two population-based data sources. Public Health Rep. 2013, 3, 179-188.
6. Walton, K.M.; Abrams, D.B.; Bailey, W.C.; Clark, D.; Connolly, G.N.; Djordjevic, M.V.; Eissenberg, T.E.; Fiore, M.C.; Goniewicz, M.L.; Haverkos, L.; et al. NIH electronic cigarette workshop: developing a research agenda. Nicotine Tob. Res. 2015, 2, 259-269.
7. National Center for Chronic Disease Prevention and Health Promotion (US) Office on Smoking and Health. The Health Consequences of Smoking-50 Years of Progress: A Report of the Surgeon General. Available online: http://www.ncbi.nlm.nih.gov/books/NBK179276/ (accessed on 1 November 2015).
8. Hellström-Lindahl, E.; Gorbounova, O.; Seiger, A.; Mousavi, M.; Nord-berg, A. Regional distribution of nicotinic receptors during prenatal development of human brain and spinal cord. Brain Res. Dev. Brain Res. 1998, 108, 147-160.
9. Dwyer, J.B.; McQuown, S.C.; Leslie, F.M. The dynamic effects of nicotine on the developing brain. Pharmacol. Ther. 2009, 2, 125-139.
10. Jaspers, M.; de Winter, A.F.; Huisman, M.; Verhulst, F.C.; Ormel, J.; Stewart, R.E.; Reijneveld, S.A. Trajectories of psychosocial problems in adolescents predicted by findings from early well-child assessments. J. Adolesc. Health 2012, 5, 475-483.
11. Heijmans, B.T.; Tobi, E.W.; Lumey, L.H.; Slagboom, P.E. The epigenome: Archive of the prenatal environment. Epigenetics. 2009, 8, 526-531.
12. Goodwin, R.D.; Perkonigg, A.; Höfler, M.; Wittchen, H.U. Mental disorders and smoking trajectories: A 10-year prospective study among adolescents and young adults in the community. Drug Alcohol Depend. 2013, 130, 201-207.
13. Dome, P.; Lazary, J.; Kalapos, M.P.; Rihmer, Z. Smoking, nicotine and neuropsychiatric disorders. Neurosci. Biobehav. Rev. 2010, 3, 295-342.
14. Ikegame, T.; Bundo, M.; Murata, Y.; Kasai, K.; Kato, T.; Iwamoto, K. DNA methylation of the BDNF gene and its relevance to psychiatric disorders. J. Hum. Genet. 2013, 7, 434-438.
15. Fuchikami, M.; Morinobu, S.; Segawa, M.; Okamoto, Y.; Yamawaki, S.; Ozaki, N.; Inoue, T.; Kusumi, I.; Koyama, T.; Tsuchiyama, K.; et al. DNA methylation profiles of the brain-derived neurotrophic factor (BDNF) gene as a potent diagnostic biomarker in major depression. PLoS ONE 2011, 8.
16. Miller, M.; Borges, G.; Orozco, R.; Mukamal, K.; Rimm, E.B.; Benjet, C.; Medina-Mora, M.E. Exposure to alcohol, drugs and tobacco and the risk of subsequent suicidality: Findings from the Mexican Adolescent Mental Health Survey. Drug Alcohol Depend. 2011, 113, 110-117.
17. Yauk, C.L.; Williams, A.; Buick, J.K.; Chen, G.; Maertens, R.M.; Halappanavar, S.; White, P.A. Genetic toxicology and toxicogenomic analysis of three cigarette smoke condensates in vitro reveals few differences among full-flavor, blonde, and light products. Environ. Mol. Mutagen. 2012, 4, 281-296.
18. Krämer, A.; Green, J.; Pollard, J., Jr.; Tugendreich, S. Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics 2014, 4, 523-530.
19. Oliveros, J.C. (2007-2015) Venny. An Interactive Tool for Comparing Lists with Venn’s Diagrams. Available online: http:// bioinfogp.cnb.csic.es/tools/venny/index.html (accessed on 2 September 2015).
20. Jacobsen, L.K.; Slotkin, T.A.; Mencl, W.E.; Frost, S.J.; Pugh, K.R. Gender-specific effects of prenatal and adolescent exposure to tobacco smoke on auditory and visual attention. Neuropsychopharmacology 2007, 12, 2453-2464.
21. Blood-Siegfried, J.; Rende, E.K. The long-term effects of prenatal nicotine exposure on neurologic development. J. Midwifery Womens Health 2010, 2, 143-152.
22. Dwyer, J.B.; Broide, R.S.; Leslie, F.M. Nicotine and brain development. Birth Defects Res. C Embryo Today 2008, 1, 30-44.
23. Slotkin, T.A. Cholinergic systems in brain development and disruption by neurotoxicants: Nicotine, environmental tobacco smoke, organophosphates. Toxicol. Appl. Pharmacol. 2004, 2, 132-151.
24. Slotkin, T.A.; MacKillop, E.A.; Rudder, C.L.; Ryde, I.T.; Tate, C.A.; Seidler, F.J. Permanent, sex-selective effects of prenatal or adolescent nicotine exposure, separately or sequentially, in rat brain regions: Indices of cholinergic and serotonergic synaptic function, cell signaling, and neural cell number and size at 6 months of age. Neuropsychopharmacology 2007, 5, 1082-1097.
25. Smith, D.; Aherrera, A.; Lopez, A.; Neptune, E.; Winickoff, J.P.; Klein, J.D.; Chen, G.; Lazarus, P.; Collaco, J.M.; McGrath-Morrow, S.A. Adult Behavior in Male Mice Exposed to E-Cigarette Nicotine Vapors during Late Prenatal and Early Postnatal Life. PLoS ONE 2015, 9, e0137953.
26. Biegon, A.; Alia-Klein, N.; Fowler, J.S. Potential contribution of aromatase inhibition to the effects of nicotine and related compounds on the brain. Front. Pharmacol. 2012, 3, 185.
27. Bakker, J.; Honda, S.; Harada, N.; Balthazart, J. Restoration of male sexual behavior by adult exogenous estrogens in male aromatase knockout mice. Horm. Behav. 2004, 1, 1-10.
28. Meinhardt, U.; Mullis, P.E. The essential role of the aromatase/p450arom. Semin. Reprod. Med. 2002, 3, 277-284.
29. Cao, J.; Wang, J.; Dwyer, J.B.; Gautier, N.M.; Wang, S.; Leslie, F.M.; Li, M.D. Gestational nicotine exposure modifies myelin gene expression in the brains of adolescent rats with sex differences. Transl. Psychiatry. 2013, 3, e247.
30. Dalla, C.; Antoniou, K.; Papadopoulou-Daifoti, Z.; Balthazart, J.; Bakker, J. Oestrogen-deficient female aromatase knockout (ArKO) mice exhibit depressive-like symptomatology. Eur. J. Neurosci. 2004, 1, 217-228.
31. Dalla, C.; Antoniou, K.; Papadopoulou-Daifoti, Z.; Balthazart, J.; Bakker, J. Male aromatase-knockout mice exhibit normal levels of activity, anxiety and “depressive-like” symptomatology. Behav. Brain Res. 2005, 2, 186-193.
32. Romero, R.D.; Chen, W.J. Gender-related response in open-field activity following developmental nicotine exposure in rats. Pharmacol. Biochem. Behav. 2004, 4, 675-681.
33. Harrod, S.B.; Mactutus, C.F.; Bennett, K.; Hasselrot, U.; Wu, G.; Welch, M.; Booze, R.M. Sex differences and repeated intravenous nicotine: Behavioral sensitization and dopamine receptors. Pharmacol. Biochem. Behav. 2004, 3, 581-592.
34. Vaglenova, J.; Birru, S.; Pandiella, N.M.; Breese, C.R. An assessment of the long-term developmental and behavioral teratogenicity of prenatal nicotine exposure. Behav. Brain Res. 2004, 150, 159-170.
35. Farsalinos, K.E.; Romagna, G.; Tsiapras, D.; Kyrzopoulos, S.; Voudris, V. Characteristics, perceived side effects and benefits of electronic cigarette use: A worldwide survey of more than 19,000 consumers. Int. J. Environ. Res. Public Health 2014, 4, 4356-4373.
36. Farsalinos, K.E.; Kistler, K.A.; Gillman, G.; Voudris, V. Evaluation of electronic cigarette liquids and aerosol for the presence of selected inhalation toxins. Nicotine Tob. Res. 2015, 2, 168-174.
37. Tayyarah, R.; Long, G.A. Comparison of select analytes in aerosol from e-cigarettes with smoke from conventional cigarettes and with ambient air. Regul. Toxicol. Pharmacol. 2014, 3, 704-710.
38. Flavors and Extracts Manufacturers’ Association (FEMA). Safety Assessment and Regulatory Authority to Use Flavors: Focus on E-Cigarettes. Available online: https://www.femaflavor.org/safety-assessment-andregulatory-authority-use-flavors-focus-e-cigarettes (accessed on 3 March 2015).
39. Grana, R.; Benowitz, N.; Glantz, S.A. E-cigarettes: A scientific review. Circulation 2014, 19, 1972-1986.
40. Allen, J.G.; Flanigan, S.S.; LeBlanc, M.; Vallarino, J.; MacNaughton, P.; Stewart, J.H.; Christiani, D.C. Flavoring Chemicals in E-Cigarettes: Diacetyl, 2,3-Pentanedione, and Acetoin in a Sample of 51 Products, Including Fruit-, Candy-, and Cocktail-Flavored E-Cigarettes. Available online: http://ehp.niehs.nih.gov/wp-content/uploads/advpub/2015/12/ehp.1510185.acco.pdf (accessed on 8 December 2015).
41. Kanwal, R.; Kullman, G.; Piacitelli, C.; Boylstein, R.; Sahakian, N.; Martin, S.; Fedan, K.; Kreiss, K. Evaluation of flavorings-related lung disease risk at six microwave popcorn plants. J. Occup. Environ. Med. 2006, 2, 149-157.
42. Kreiss, K.; Gomaa, A.; Kullman, G.; Fedan, K.; Simoes, E.J.; Enright, P.L. Clinical bronchiolitis obliterans in workers at a microwave-popcorn plant. N. Engl. J. Med. 2002, 5, 330-338.
43. Saffari, A.; Daher, N.; Ruprecht, A.; De Marco, C.; Pozzi, P.; Boffi, R.; Hamad, S.H.; Shafer, M.M.; Schauer, J.J.; Westerdahl, D.; et al. Particulate metals and organic compounds from electronic and tobacco-containing cigarettes: Comparison of emission rates and secondhand exposure. Environ. Sci. Process Impacts 2014, 10, 2259-2267.
44. Farsalinos, K.E.; Le Houezec, J. Regulation in the face of uncertainty: The evidence on electronic nicotine delivery systems (e-cigarettes). Risk Manag. Healthc. Policy 2015, 8, 157-167.