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Exposure of rats to environmental tobacco smoke during cerebellar development alters behavior and perturbs mitochondrial energetics.

ABSTRACT: BACKGROUND:Environmental tobacco smoke (ETS) exposure is linked to developmental deficits and disorders with known cerebellar involvement. However, direct biological effects and underlying neurochemical mechanisms remain unclear. OBJECTIVES:We sought to identify and evaluate underlying neurochemical change in the rat cerebellum with ETS exposure during critical period development. METHODS:We exposed rats to daily ETS (300, 100, and 0 µg/m3 total suspended particulate) from postnatal day 8 (PD8) to PD23 and then assayed the response at the behavioral, neuroproteomic, and cellular levels. RESULTS:Postnatal ETS exposure induced heightened locomotor response in a novel environment on par initially with amphetamine stimulation. The cerebellar mitochondrial subproteome was significantly perturbed in the ETS-exposed rats. Findings revealed a dose-dependent up-regulation of aerobic processes through the modification and increased translocation of Hk1 to the mitochondrion with corresponding heightened ATP synthase expression. ETS exposure also induced a dose-dependent increase in total Dnm1l mitochondrial fission factor; although more active membrane-bound Dnm1l was found at the lower dose. Dnm1l activation was associated with greater mitochondrial staining, particularly in the molecular layer, which was independent of stress-induced Bcl-2 family dynamics. Further, electron microscopy associated Dnm1l-mediated mitochondrial fission with increased biogenesis, rather than fragmentation. CONCLUSIONS:The critical postnatal period of cerebellar development is vulnerable to the effects of ETS exposure, resulting in altered behavior. The biological effect of ETS is underlain in part by a Dnm1l-mediated mitochondrial energetic response at a time of normally tight control. These findings represent a novel mechanism by which environmental exposure can impact neurodevelopment and function.

SUBMITTER: Fuller BF

PROVIDER: S-EPMC3548280 | biostudies-literature | 2012 Dec

REPOSITORIES: biostudies-literature

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Exposure of rats to environmental tobacco smoke during cerebellar development alters behavior and perturbs mitochondrial energetics.

Fuller Brian F BF Cortes Diego F DF Landis Miranda K MK Yohannes Hiyab H Griffin Hailey E HE Stafflinger Jillian E JE Bowers M Scott MS Lewis Mark H MH Fox Michael A MA Ottens Andrew K AK

Environmental health perspectives 20120926 12

<h4>Background</h4>Environmental tobacco smoke (ETS) exposure is linked to developmental deficits and disorders with known cerebellar involvement. However, direct biological effects and underlying neurochemical mechanisms remain unclear.<h4>Objectives</h4>We sought to identify and evaluate underlying neurochemical change in the rat cerebellum with ETS exposure during critical period development.<h4>Methods</h4>We exposed rats to daily ETS (300, 100, and 0 µg/m3 total suspended particulate) from ...[more]

PMID: 23014793

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Project description:The developing fetus is especially vulnerable to environmental toxicants, including tobacco constituents. The aim of this study was to assess the impact of environmental tobacco smoke (ETS) exposure during pregnancy on child neurodevelopment within the first two years of life. The study population consisted of 461 non-smoking pregnant women (saliva cotinine level <10 ng/mL). Maternal passive smoking was assessed based on the cotinine level in saliva analyzed by the use of high-performance liquid chromatography coupled with tandem mass spectrometry (HPLC-ESI + MS/MS) and by questionnaire data. The cotinine cut-off value for passive smoking was established at 1.5 ng/mL (sensitivity 63%, specificity 71%). Psychomotor development was assessed in children at the age of one- and two-years using the Bayley Scales of Infant and Toddler Development. Approximately 30% of the women were exposed to ETS during pregnancy. The multivariate linear regression model indicated that ETS exposure in the 1st and the 2nd trimesters of pregnancy were associated with decreasing child language functions at the age of one (? = -3.0, p = 0.03, and ? = -4.1, p = 0.008, respectively), and two years (? = -3.8, p = 0.05, and ? = -6.3, p = 0.005, respectively). A negative association was found for cotinine level ?1.5 ng/mL in the 2nd trimester of pregnancy and child cognition at the age of 2 (? = -4.6, p = 0.05), as well as cotinine levels ?1.5 ng/mL in all trimesters of pregnancy and child motor abilities at two years of age (? = -3.9, p = 0.06, ? = -5.3, p = 0.02, and ? = -4.2, p = 0.05, for the 1st, the 2nd, and the 3rd trimester of pregnancy, respectively; for the 1st trimester the effect was of borderline statistical significance). This study confirmed that ETS exposure during pregnancy can have a negative impact on child psychomotor development within the first two years of life and underscore the importance of public health interventions aiming at reducing this exposure.

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Exposure of rats to environmental tobacco smoke during cerebellar development alters behavior and perturbs mitochondrial energetics.

Publications

Exposure of rats to environmental tobacco smoke during cerebellar development alters behavior and perturbs mitochondrial energetics.

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