Extended secondhand tobacco smoke exposure induces plasticity in nucleus tractus solitarius second‐order lung afferent neurons in young guinea pigs

Sekizawa, Shin‐ichi; Chen, Chao-Yin; Bechtold, Andrea G.; Tabor, Jocelyn; Bric, John M.; Pinkerton, Kent E.; Joad, Jesse P.; Bonham, Ann C.

doi:10.1111/j.1460-9568.2008.06378.x

Cited by 39 publications

(30 citation statements)

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“…Another possible contributing factor to the differences we report may be due to species variations that are independent of the ability to hibernate. However, the following two facts support the view that the major contributor to the differences we saw in this study arose because the hamster is a hibernator and the rat is not: (1) the amplitudes of TS-evoked evoked EPSCs in the NTS at 33°C are similar between rats, guinea pigs, and rhesus monkeys (all non-hibernators) while evoked EPSCs in the hamsters were significantly larger (Sekizawa et al 2008; Sekizawa et al 2010b); and (2) neurons in the medial septum-diagonal band complex of the Yakutian ground squirrel ( Cittelus undulatus ), a hibernating species, have firing rates approximately twice that of corresponding neurons in the guinea pig, and these ground squirrel neurons have been postulated to actively participate in terminating a hibernation bout to ensure full arousal (Belousov et al 1990). Our study plus that of Belousov, et al (1990) indicate that electrical excitability is enhanced in at least two subcortical neural populations in hibernating species.…”

Section: Discussionsupporting

confidence: 76%

Realignment of signal processing within a sensory brainstem nucleus as brain temperature declines in the Syrian hamster, a hibernating species

et al. 2012

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Crucial for survival, the central nervous system must reliably process sensory information over all stages of a hibernation bout to ensure homeostatic regulation is maintained and well-matched to dramatically altered behavioral states. Comparing neural responses in the nucleus tractus solitarius of rats and euthermic Syrian hamsters, we tested the hypothesis that hamster nucleus tractus solitarius neurons have adaptations sustaining signal processing while conserving energy. Using patch-clamp techniques, we classified second-order nucleus tractus solitarius neurons as rapid-onset or delayed-onset spiking phenotypes based on their spiking-onset to a depolarizing pulse (following a −80 mV prepulse). As temperature decreased from 33°C to 15°C, the excitability of all neurons decreased. However, hamster rapid-onset neurons had the highest spiking response and shortest action potential width at every temperature, while hamster delayed-onset neurons had the most negative resting membrane potential. Spontaneous excitatory post-synaptic current frequency in both phenotypes decreased as temperature decreased, yet tractus solitarius stimulation-evoked excitatory post-synaptic current amplitudes were greater in hamsters than in rats regardless of phenotype and temperature. Changes were significant (P<0.05), supporting our hypothesis by showing that, as temperature falls, rapid-onset neurons contribute more to signal processing but less to energy conservation than do delayed-onset neurons.

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Section: Discussionsupporting

confidence: 76%

Realignment of signal processing within a sensory brainstem nucleus as brain temperature declines in the Syrian hamster, a hibernating species

et al. 2012

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“…As a nicotinic acetylcholine receptor agonist, nicotine preempts normal cholinergic signals that are critical to the control of neuronal cell replication and differentiation, to the formation of axons and synapses, and to the development of neural circuits. A comparison of nicotine alone vs. tobacco smoke exposure in a variety of models shows similar effects on neurogenesis (Bruijnzeel et al, 2011; Gospe et al, 1996; Slotkin, 2004), oxidative stress (Lobo Torres et al, 2012; Qiao et al, 2005), neural plasticity (Heath and Picciotto, 2009; Sekizawa et al, 2008; Shingo and Kito, 2005), and on indices of cholinergic function, synaptic signaling, and neural cell differentiation into specific neurotransmitter phenotypes (Slotkin, 2004; Slotkin et al, 2000, 2001, 2002, 2006a, b). …”

Section: Introductionmentioning

confidence: 99%

Effects of tobacco smoke on PC12 cell neurodifferentiation are distinct from those of nicotine or benzo[a]pyrene

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et al. 2014

Neurotoxicology and Teratology

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Although nicotine accounts for a great deal of the neurodevelopmental damage associated with maternal smoking or second-hand exposure, tobacco smoke contains thousands of potentially neurotoxic compounds. We used PC12 cells, a standard in vitro model of neurodifferentiation, to compare tobacco smoke extract (TSE) to nicotine, matching TSE exposure (with its inherent nicotine content) to parallel concentrations of nicotine, or to benzo[a]pyrene, a tobacco combustion product. TSE promoted the transition from cell replication to differentiation, resulting in fewer, but larger cells with greater neurite extension. TSE also biased differentiation into the dopaminergic versus the cholinergic phenotype, evidenced by an increase in tyrosine hydroxylase activity but not choline acetyltransferase. Nicotine likewise promoted differentiation at the expense of cell numbers, but its effect on growth and neurite extension was smaller than that of TSE; furthermore, nicotine did not promote the dopaminergic phenotype. Benzo[a]pyrene had effects opposite to those of TSE, retarding neurodifferentiation, which resulted in higher cell numbers, smaller cells, reduced neurite information, and impaired emergence of both dopaminergic and cholinergic phenotypes. Our studies show that the complex mixture of compounds in tobacco smoke exerts direct effects on neural cell replication and differentiation that resemble those of nicotine in some ways but not others, and most importantly, that are greater in magnitude than can be accounted for from just the nicotine content of TSE. Thus, fetal tobacco smoke exposure, including lower levels associated with second-hand smoke, could be more injurious than would be anticipated from measured levels of nicotine or its metabolites.

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“…However, given the advent of nicotine replacement products for smoking cessation, as well as alternative nicotine delivery devices, it becomes important to distinguish whether the thousands of other components of tobacco smoke also play a role in adverse neurodevelopmental outcomes. A number of animal studies have identified effects of cigarette smoke that, in general, resemble those of nicotine at the biochemical, structural and functional levels (Bruijnzeel et al 2011; Fuller et al 2012; Golub et al 2007; Gospe et al 2009; Lobo Torres et al 2012; Sekizawa et al 2008; Slotkin et al 2006a, b). Nevertheless, these exposure models simply reinforce the resemblance between smoke exposure and the effects of nicotine, rather than distinguishing between them.…”

Section: Introductionmentioning

confidence: 99%

Amelioration strategies fail to prevent tobacco smoke effects on neurodifferentiation: Nicotinic receptor blockade, antioxidants, methyl donors

et al. 2015

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Tobacco smoke exposure is associated with neurodevelopmental disorders. We used neuronotypic PC12 cells to evaluate the mechanisms by which tobacco smoke extract (TSE) affects neurodifferentiation. In undifferentiated cells, TSE impaired DNA synthesis and cell numbers to a much greater extent than nicotine alone; TSE also impaired cell viability to a small extent. In differentiating cells, TSE enhanced cell growth at the expense of cell numbers and promoted emergence of the dopaminergic phenotype. Nicotinic receptor blockade with mecamylamine was ineffective in preventing the adverse effects of TSE and actually enhanced the effect of TSE on the dopamine phenotype. A mixture of antioxidants (Vitamin C, Vitamin E, N-acetyl-L-cysteine) provided partial protection against cell loss but also promoted loss of the cholinergic phenotype in response to TSE. Notably, the antioxidants themselves altered neurodifferentiation, reducing cell numbers and promoting the cholinergic phenotype at the expense of the dopaminergic phenotype, an effect that was most prominent for N-acetyl-L-cysteine. Treatment with methyl donors (Vitamin B12, folic acid, choline) had no protectant effect and actually enhanced the cell loss evoked by TSE; they did have a minor, synergistic interaction with antioxidants protecting against TSE effects on growth. Thus, components of tobacco smoke perturb neurodifferentiation through mechanisms that cannot be attributed to the individual effects of nicotine, oxidative stress or interference with one-carbon metabolism. Consequently, attempted amelioration strategies may be partially effective at best, or, as seen here, can actually aggravate injury interfering with normal developmental signals and/or by sensitizing cells to TSE effects on neurodifferentiation.

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Extended secondhand tobacco smoke exposure induces plasticity in nucleus tractus solitarius second‐order lung afferent neurons in young guinea pigs

Cited by 39 publications

References 53 publications

Realignment of signal processing within a sensory brainstem nucleus as brain temperature declines in the Syrian hamster, a hibernating species

Realignment of signal processing within a sensory brainstem nucleus as brain temperature declines in the Syrian hamster, a hibernating species

Effects of tobacco smoke on PC12 cell neurodifferentiation are distinct from those of nicotine or benzo[a]pyrene

Amelioration strategies fail to prevent tobacco smoke effects on neurodifferentiation: Nicotinic receptor blockade, antioxidants, methyl donors

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