Environmental Tobacco Smoke During the Early Postnatal Period of Mice Interferes With Brain 18 F-FDG Uptake From Infancy to Early Adulthood – A Longitudinal Study

Torres, Larissa Helena; Real, Caroline Cristiano; Turato, Walter Miguel; Spelta, Lídia Wiazowski; Durão, Ana Carolina Cardoso dos Santos; Andrioli, Tatiana Costa; Pozzo, Lorena; Squair, Peterson Lima; Pistis, Marco; Faria, Daniele de Paula; Marcourakis, Tânia

doi:10.3389/fnins.2020.00005

Cited by 8 publications

(7 citation statements)

References 49 publications

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“…The exposure biomarkers found in this study are consistent with those reported in previous studies of our research group ( Lobo Torres et al, 2012 ; Torres et al, 2015a , 2015b ; Torres et al, 2019a ; Torres et al, 2019b ; Torres et al, 2020 ), as well as with those of other studies ( Mello et al, 2001 ). Due to the rapid metabolization of nicotine, cotinine and 3-hydroxycotinine were used as biological biomarkers of ETS exposure ( Man et al, 2006 ).…”

Section: Discussionsupporting

confidence: 93%

“…Moreover, early postnatal exposure to ETS impairs myelination, learning, and memory, besides decreasing brain-derived neurotrophic factor (BDNF) and synaptic proteins levels ( Toledo-Rodriguez et al, 2010 ; Torres et al, 2015a , b ). In a study conducted by Torres et al (2020) , the authors found that ETS exposure during the early postnatal period decreased 18 fluorine-fluorodeoxyglucose ( 18 F-FDG) uptake, a marker of brain metabolic activity, in several brain areas of males and females from late infancy to early adulthood.…”

Section: Discussionmentioning

confidence: 99%

“…Exposure was performed in a chamber measuring 564 mm width × 385 mm depth × 371 mm height, in which carbon monoxide (CO) level was measured every 10 min using a gas detector (ToxiPro, Biosystems, United States). Fourteen control pregnant mice were placed in a similar chamber and exposed to compressed air at 2 ml/min (pressure: 4 bar) ( Lobo-Torres et al, 2012 ; Torres et al, 2019a ; Torres et al, 2020 ). A different group of females ( n = 6) was also exposed to compressed air and ETS, having blood samples collected from their inferior vena cava immediately after the last exposure to quantify biological exposure markers.…”

Section: Methodsmentioning

confidence: 99%

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In Utero Exposure to Environmental Tobacco Smoke Increases Neuroinflammation in Offspring

et al. 2022

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The embryonic stage is the most vulnerable period for congenital abnormalities. Due to its prolonged developmental course, the central nervous system (CNS) is susceptible to numerous genetic, epigenetic, and environmental influences. During embryo implantation, the CNS is more vulnerable to external influences such as environmental tobacco smoke (ETS), increasing the risk for delayed fetal growth, sudden infant death syndrome, and immune system abnormalities. This study aimed to evaluate the effects of in utero exposure to ETS on neuroinflammation in the offspring of pregnant mice challenged or not with lipopolysaccharide (LPS). After the confirmation of mating by the presence of the vaginal plug until offspring birth, pregnant C57BL/6 mice were exposed to either 3R4F cigarettes smoke (Kentucky University) or compressed air, twice a day (1h each), for 21 days. Enhanced glial cell and mixed cell cultures were prepared from 3-day-old mouse pups. After cell maturation, both cells were stimulated with LPS or saline. To inhibit microglia activation, minocycline was added to the mixed cell culture media 24 h before LPS challenge. To verify the influence of in utero exposure to ETS on the development of neuroinflammatory events in adulthood, a different set of 8-week-old animals was submitted to the Autoimmune Experimental Encephalomyelitis (EAE) model. The results indicate that cells from LPS-challenged pups exposed to ETS in utero presented high levels of proinflammatory cytokines such as interleukin 6 (IL-6) and tumor necrosis factor-alpha (TNFα) and decreased cell viability. Such a proinflammatory environment could modulate fetal programming by an increase in microglia and astrocytes miRNA155. This scenario may lead to the more severe EAE observed in pups exposed to ETS in utero.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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In Utero Exposure to Environmental Tobacco Smoke Increases Neuroinflammation in Offspring

et al. 2022

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“…Nevertheless, one caveat of these studies is that a causal relationship can’t be drawn solely based on human population studies since the risk factors of developing MS later in life is multifaceted and may not be simply due to early-life ETS exposure. New findings in animal studies are emerging strengthening the idea that exposure to tobacco smoke in a critical period interferes with brain development of mice from late infancy to early adulthood (Wu et al, 2009, 2012; Torres et al, 2019, 2020).…”

Section: Introductionmentioning

confidence: 97%

Early Postnatal Tobacco Smoke Exposure Aggravates Experimental Autoimmune Encephalomyelitis in Adult Rats

Wang

Zhong

et al. 2020

Preprint

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Although substantial evidence supports smoking as a risk factor for the development of multiple sclerosis (MS) in adulthood, it remains controversial as to whether early-life exposure to environmental tobacco smoke (ETS) increases the risk of MS later in life. Here, using experimental autoimmune encephalomyelitis (EAE) as an animal model for MS, we show that exposing neonatal rats during the 1st week (ETS1-EAE), but not the 2nd week (ETS2-EAE) and the 3rd week (ETS3-EAE) after birth, increased the severity of EAE in adulthood in comparison to pups exposed to filtered compressed air (AIR-EAE). The EST1-EAE rats showed a worse neurological deficit score and a significant increase in CD4+ cell infiltration, demyelination, and axonal injury in the spinal cord compared to AIR-EAE, ETS2-EAE, and ETS3-EAE groups. Flow cytometry analysis showed that the ETS1 group had decreased numbers of regulatory T (Treg) cells and increased effector T (Teff) cells in the brain and spinal cord. The expressions of Treg upstream regulator Foxp3 and downstream cytokines such as IL-10 were also altered accordingly. Together, these findings demonstrate that neonatal ETS exposure suppresses Treg functions and aggravates the severity of EAE, confirming early-life exposure to EST as a potential risk factor for multiple sclerosis in adulthood.

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“…Exposure to tobacco smoke is also associated with irritability (Froggatt et al, 2020), attention deficit hyperactivity disorder (Kovess et al, 2015), and sudden infant death syndrome (Alm et al, 2006). In rodents, exposure to tobacco smoke during the early postnatal period induces learning and memory impairment (Torres, Annoni, et al, 2015) and inhibits the expression of genes required for myelin formation and maintenance, thus contributing to white matter degeneration (Yu et al, 2016); decreases brain 2‐deoxy‐2‐[ 18 F]‐fluoro‐ d ‐glucose ( 18 F‐FDG) metabolism in hippocampus (Torres et al, 2020); increases the preference of adult mice for the drug in two‐bottle‐choice test (Romoli et al, 2019); and affects lung maturation (Blaskovic et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Nicotine exposure through breastfeeding affects brain‐derived neurotrophic factor and synaptic proteins levels in the brain of stressed adult female mice

Pereira-Júnior

Amorim

Garcia

et al. 2022

Intl J of Devlp Neuroscience

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Nicotine has been used during pregnancy and lactation as a tobacco harm reduction strategy. However, it is unclear whether nicotine exposure during a critical development period negatively impacts stress responses in adulthood. This study investigated how nicotine, administered via breastfeeding, affects the brain‐derived neurotrophic factor (BDNF), synaptic proteins levels, and anxiety‐like behavior in adult female mice subjected to stress. Female Swiss mice were exposed to saline or nicotine (8 mg/kg/day) through breastfeeding between their fourth and 17th postnatal days (P) via implanted osmotic mini pumps. The unpredictable chronic mild stress (UCMS) protocol was performed during their adulthood (P65) for 10 consecutive days, followed by the elevated plus maze (EPM) test 1 day after the protocol. Animals were euthanized and their blood, collected for plasma corticosterone measurements and their brain structures, dissected for BDNF and synaptic proteins analyses. We found no significant differences in corticosterone levels between groups (Saline/Non‐stress, Nicotine/Non‐stress, Saline/Stress, and Nicotine/Stress). The UCMS protocol hindered weight gain. Mice exposed to nicotine through breastfeeding with or without the UCMS protocol in adulthood showed higher grooming and head dipping frequency; decreased BDNF levels in cerebellum and striatum; increased postsynaptic density protein 95 (PSD‐95), synapsin I, and synaptophysin levels in cerebellum; and decreased PSD‐95 and synapsin I levels in brainstem. Our results indicate that nicotine exposure through breastfeeding leads to long‐lasting behavioral effects and synaptic protein changes, most of which were independent of the UCMS protocol, even after a long nicotine‐free period, highlighting the importance of further studies on nicotine exposure during development.

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Environmental Tobacco Smoke During the Early Postnatal Period of Mice Interferes With Brain 18 F-FDG Uptake From Infancy to Early Adulthood – A Longitudinal Study

Cited by 8 publications

References 49 publications

In Utero Exposure to Environmental Tobacco Smoke Increases Neuroinflammation in Offspring

In Utero Exposure to Environmental Tobacco Smoke Increases Neuroinflammation in Offspring

Early Postnatal Tobacco Smoke Exposure Aggravates Experimental Autoimmune Encephalomyelitis in Adult Rats

Nicotine exposure through breastfeeding affects brain‐derived neurotrophic factor and synaptic proteins levels in the brain of stressed adult female mice

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