Prenatal Exposure to Environmental Tobacco Smoke Alters Gene Expression in the Developing Murine Hippocampus

Overview

Journal Reprod Toxicol

Specialties Reproductive Medicine
Toxicology

Date 2009 Dec 9

PMID 19969065

Citations 19

Authors

Partha Mukhopadhyay

Kristin H Horn

Robert M Greene

M Michele Pisano

Affiliations

Soon will be listed here.

Abstract

Background: Little is known about the effects of passive smoke exposures on the developing brain.

Objective: The purpose of the current study was to identify changes in gene expression in the murine hippocampus as a consequence of in utero exposure to sidestream cigarette smoke (an experimental equivalent of environmental tobacco smoke (ETS)) at exposure levels that do not result in fetal growth inhibition.

Methods: A whole body smoke inhalation exposure system was utilized to deliver ETS to pregnant C57BL/6J mice for 6 h/day from gestational days 6-17 (gd 6-17) [for microarray] or gd 6-18.5 [for fetal phenotyping].

Results: There were no significant effects of ETS exposure on fetal phenotype. However, 61 "expressed" genes in the gd 18.5 fetal hippocampus were differentially regulated (up- or down-regulated by 1.5-fold or greater) by maternal exposure to ETS. Of these 61 genes, 25 genes were upregulated while 36 genes were down-regulated. A systems biology approach, including computational methodologies, identified cellular response pathways, and biological themes, underlying altered fetal programming of the embryonic hippocampus by in utero cigarette smoke exposure.

Conclusions: Results from the present study suggest that even in the absence of effects on fetal growth, prenatal smoke exposure can alter gene expression during the "early" period of hippocampal growth and may result in abnormal hippocampal morphology, connectivity, and function.

Citing Articles

miR-153-3p via PIK3R1 Is Involved in Cigarette Smoke-Induced Neurotoxicity in the Brain.

Sun Q, Wang H, Yang M, Xia H, Wu Y, Liu Q Toxics. 2023; 11(12).

PMID: 38133370 PMC: 10747656. DOI: 10.3390/toxics11120969.

Apolipoprotein D as a Potential Biomarker in Neuropsychiatric Disorders.

Del Valle E, Rubio-Sardon N, Menendez-Perez C, Martinez-Pinilla E, Navarro A Int J Mol Sci. 2023; 24(21).

PMID: 37958618 PMC: 10650001. DOI: 10.3390/ijms242115631.

Multidimensional Intersection of Nicotine, Gene Expression, and Behavior.

Sherafat Y, Bautista M, Fowler C Front Behav Neurosci. 2021; 15:649129.

PMID: 33828466 PMC: 8019722. DOI: 10.3389/fnbeh.2021.649129.

Impact of prenatal arsenate exposure on gene expression in a pure population of migratory cranial neural crest cells.

Mukhopadhyay P, Seelan R, Greene R, Pisano M Reprod Toxicol. 2019; 86:76-85.

PMID: 30953684 PMC: 6545154. DOI: 10.1016/j.reprotox.2019.04.001.

Influence of exposure to nicotine during pregnancy on the learning and memory for adult offspring.

Ma X, Li B, Han Y, Tian Y, Wu L, Wang H Exp Ther Med. 2018; 15(3):2404-2410.

PMID: 29456645 PMC: 5795752. DOI: 10.3892/etm.2018.5687.

References

Lazic S, Grote H, Armstrong R, Blakemore C, Hannan A, Dellen A . Decreased hippocampal cell proliferation in R6/1 Huntington's mice. Neuroreport. 2004; 15(5):811-3. DOI: 10.1097/00001756-200404090-00014. View

Zhang Q, Skepper J, Yang F, Davies J, Hegyi L, Roberts R . Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J Cell Sci. 2002; 114(Pt 24):4485-98. DOI: 10.1242/jcs.114.24.4485. View

Gros-Louis F, Dupre N, Dion P, Fox M, Laurent S, Verreault S . Mutations in SYNE1 lead to a newly discovered form of autosomal recessive cerebellar ataxia. Nat Genet. 2006; 39(1):80-5. DOI: 10.1038/ng1927. View

Amisten S, Braun O, Bengtsson A, Erlinge D . Gene expression profiling for the identification of G-protein coupled receptors in human platelets. Thromb Res. 2007; 122(1):47-57. DOI: 10.1016/j.thromres.2007.08.014. View

Windham G, Eaton A, Hopkins B . Evidence for an association between environmental tobacco smoke exposure and birthweight: a meta-analysis and new data. Paediatr Perinat Epidemiol. 1999; 13(1):35-57. DOI: 10.1046/j.1365-3016.1999.00150.x. View

Windham G, Von Behren J, Waller K, Fenster L . Exposure to environmental and mainstream tobacco smoke and risk of spontaneous abortion. Am J Epidemiol. 1999; 149(3):243-7. DOI: 10.1093/oxfordjournals.aje.a009798. View

Angevine Jr J . Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp Neurol Suppl. 1965; :Suppl 2:1-70. View

Pirkle J, Bernert J, Caudill S, Sosnoff C, Pechacek T . Trends in the exposure of nonsmokers in the U.S. population to secondhand smoke: 1988-2002. Environ Health Perspect. 2006; 114(6):853-8. PMC: 1480505. DOI: 10.1289/ehp.8850. View

Meyer M, Comstock G . Maternal cigarette smoking and perinatal mortality. Am J Epidemiol. 1972; 96(1):1-10. DOI: 10.1093/oxfordjournals.aje.a121427. View

10.

Goel P, Radotra A, Singh I, Aggarwal A, Dua D . Effects of passive smoking on outcome in pregnancy. J Postgrad Med. 2004; 50(1):12-6. View

11.

Stabbert R, Voncken P, Rustemeier K, Haussmann H, Roemer E, Schaffernicht H . Toxicological evaluation of an electrically heated cigarette. Part 2: Chemical composition of mainstream smoke. J Appl Toxicol. 2003; 23(5):329-39. DOI: 10.1002/jat.924. View

12.

Good P, Alapat D, Hsu A, Chu C, Perl D, Wen X . A role for semaphorin 3A signaling in the degeneration of hippocampal neurons during Alzheimer's disease. J Neurochem. 2004; 91(3):716-36. DOI: 10.1111/j.1471-4159.2004.02766.x. View

13.

Flatscher-Bader T, Wilce P . Chronic smoking and alcoholism change expression of selective genes in the human prefrontal cortex. Alcohol Clin Exp Res. 2006; 30(5):908-15. DOI: 10.1111/j.1530-0277.2006.00106.x. View

14.

Sgubin D, Aztiria E, Perin A, Longatti P, Leanza G . Activation of endogenous neural stem cells in the adult human brain following subarachnoid hemorrhage. J Neurosci Res. 2007; 85(8):1647-55. DOI: 10.1002/jnr.21303. View

15.

Hammond S, Sorensen G, Youngstrom R, Ockene J . Occupational exposure to environmental tobacco smoke. JAMA. 1995; 274(12):956-60. View

16.

Ward C, Lewis S, Coleman T . Prevalence of maternal smoking and environmental tobacco smoke exposure during pregnancy and impact on birth weight: retrospective study using Millennium Cohort. BMC Public Health. 2007; 7:81. PMC: 1884144. DOI: 10.1186/1471-2458-7-81. View

17.

Gospe Jr S, Zhou S, Pinkerton K . Effects of environmental tobacco smoke exposure in utero and/or postnatally on brain development. Pediatr Res. 1996; 39(3):494-8. DOI: 10.1203/00006450-199603000-00018. View

18.

Persico A, Baldi A, DellAcqua M, Moessner R, Murphy D, Lesch K . Reduced programmed cell death in brains of serotonin transporter knockout mice. Neuroreport. 2003; 14(3):341-4. DOI: 10.1097/00001756-200303030-00009. View

19.

Jordan T, Price J, Dake J, Shah S . Adolescent exposure to and perceptions of environmental tobacco smoke. J Sch Health. 2005; 75(5):178-86. View

20.

Wada A, Yokoo H, Yanagita T, Kobayashi H . New twist on neuronal insulin receptor signaling in health, disease, and therapeutics. J Pharmacol Sci. 2005; 99(2):128-43. DOI: 10.1254/jphs.crj05006x. View