Maternal nicotine exposure during lactation alters food preference, anxiety-like behavior and the brain dopaminergic reward system in the adult rat offspring

Pinheiro, C. R.; Moura, Egberto Gaspar de; Manhães, Alex C.; Fraga, Mabel Carneiro; Claudio-Neto, S.; Younes‐Rapozo, V.; Santos-Silva, Ana Paula; Lotufo, B.M.; Oliveira, Elaine de; Lisboa, Patrícia Cristina

doi:10.1016/j.physbeh.2015.05.040

Cited by 25 publications

(11 citation statements)

References 113 publications

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“…Decades of research on conventional cigarette smoke have reported the toxicological effects of smoking and nicotine on brain development. For example, studies utilizing various exposure paradigms to assess the developmental effects of prenatal and/or postnatal nicotine exposure in rodents reported increased hyperactivity (Lacy et al 2016;Newman et al 1999), impaired cognitive ability in terms of memory and attention, altered pre-pulse inhibition (Alkam et al 2013;Zhang et al 2018), and increased prevalence of anxiety-or depressive-like behaviors in adulthood (Lee et al 2016;Pinheiro et al 2015;Zhang et al 2019). Importantly, some of these behavioral alterations (e.g., increased activity) were reported in offspring of pregnant mice exposed to 2.4% nicotine through e-cigarette aerosol exposure (Smith et al 2015).…”

Section: Introductionmentioning

confidence: 99%

Neuroinflammatory and Behavioral Outcomes Measured in Adult Offspring of Mice Exposed Prenatally to E-Cigarette Aerosols

Church

Chace-Donahue

Blum

et al. 2020

Environ Health Perspect

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BACKGROUND: In an effort to decrease the rates of smoking conventional tobacco cigarettes, electronic cigarettes (e-cigarettes) have been proposed as an effective smoking cessation tool. However, little is known about their toxicological impacts. This is concerning given that e-cigarette use is perceived as less harmful than conventional tobacco cigarettes during pregnancy for both the mother and fetus. OBJECTIVE: The goal of this study was to test the neurodevelopmental consequences of maternal e-cigarette use on adult offspring behavior and neuroimmune outcomes. METHODS: Pregnant female CD-1 mice were randomly assigned to one of three treatment groups (n = 8-10 per group) and exposed daily to either filtered air, propylene glycol and vegetable glycerol (50:50 PG/VG vehicle), or to PG/VG with 16 mg=mL nicotine (+Nic). Whole-body exposures were carried out for 3 h/d, 7 d/week, from gestational day (GD)0.5 until GD17.5. Adult male and female offspring (8 weeks old) were assessed across a battery of behavioral assessments followed by region-specific quantification of brain cytokines using multiplex immunoassays. RESULTS: Adult offspring of both sexes exposed to +Nic exhibited elevated locomotor activity in the elevated plus maze and altered stress-coping strategies in the forced swim task. Moreover, male and female offspring exposed to PG/VG with and without nicotine had a 5.2% lower object discrimination score in the novel object recognition task. In addition to differences in offspring behavior, maternal e-cigarette exposure with nicotine led to a reduction in interleukin (IL)-4 and interferon-gamma (IFNc) in the diencephalon, as well as lower levels of hippocampal IFNc (females only). Ecigarette exposure without nicotine resulted in a 2-fold increase of IL-6 in the cerebellum. DISCUSSION: These findings support previous adverse findings of e-cigarette exposure on neurodevelopment in a mouse model and provide substantial evidence of persistent adverse behavioral and neuroimmunological consequences to adult offspring following maternal e-cigarette exposure during pregnancy.

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Section: Introductionmentioning

confidence: 99%

Neuroinflammatory and Behavioral Outcomes Measured in Adult Offspring of Mice Exposed Prenatally to E-Cigarette Aerosols

Church

Chace-Donahue

Blum

et al. 2020

Environ Health Perspect

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“…84 Also, these males show a higher preference for a high-sugar content diet than controls. 85 Concerning females, we have recently shown that these animals, despite having normal body mass, show reduced nAChRs as well as leptin resistance in the hypothalamus, suggesting a central inflammatory process, as observed in nicotineexposed males. 86 A limitation of the current study is that we have not assessed α7nAchR in the hypothalamus and adipose tissue.…”

Section: Discussionmentioning

confidence: 93%

Neonatal nicotine exposure changes insulin status in fat depots: sex-related differences

Rodrigues

Miranda

Soares

et al. 2021

J Dev Orig Health Dis

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Nicotine is the main psychoactive substance present in cigarette smoke that is transferred to the baby by breast milk. In rats, maternal nicotine exposure during breastfeeding induces obesogenesis and hormone dysfunctions in adult male offspring. As glucocorticoid (GC), insulin, and vitamin D change both adipogenesis and lipogenesis processes, we assessed parameters related to metabolism and action of these hormones in visceral and subcutaneous adipose tissues (VAT and SAT) of adult male and female rats in a model of neonatal nicotine exposure. At postnatal (PN) day 2, dams were kept with six pups (three per sex) and divided into nicotine and control groups for implantation of osmotic minipumps that released 6 mg/kg nicotine or saline, respectively. At PN180, fat mass, hormone levels, and protein contents of biomarkers of the GC activation and receptor (11beta-hydroxysteroid dehydrogenase type 1 and glucocorticoid receptor alpha), insulin signaling pathway [insulin receptor beta (IRβ), phosphorylated insulin receptor substrate 1, insulin receptor substrate 1 (IRS1), phosphorylated serine/threonine kinase (pAKT), serine/threonine kinase, glucose transporter type 4 (GLUT4)], and vitamin D activation and receptor (1α-hydroxylase and vitamin D receptor) were evaluated. While nicotine-exposed males showed increased fat mass, hypercorticosteronemia, hyperinsulinemia, and higher 25-hydroxyvitamin D, these alterations were not observed in nicotine-exposed females. Nicotine-exposed males only showed lower IRS1 in VAT, while the females had hyperglycemia, higher pAKT in VAT, while lower IRβ, IRS1, and GLUT4 in SAT. Parameters related to metabolism and action of GC and vitamin D were unaltered in both sexes. We evidence that exposure exclusively to nicotine during breastfeeding affects the hormone status and fat depots of the adult progeny in a sex-dependent manner.

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“…In agreement with results obtained in previous studies that used the same experimental model (Lima et al, 2010;Marcelino et al, 2004;Montanha-Rojas et al, 2005;Rocha et al, 2014), a significant loss in body mass was observed at P10 in the lactating dams that were subjected to the protein-free diet. Because Wistar rats have previously been shown to readily accept fat-and carbohydrate-rich chows and that chow consumption corrected for body mass is not significantly affected in our model (Pinheiro, Moura, Manhães, Fraga, Claudio-Neto, Abreu-Villaça, et al, 2015;Pinheiro, Moura, Manhães, Fraga, Claudio-Neto, Younes-Rapozo, et al, 2015), a likely explanation for this finding is the recourse, by the PFD dams, to endogenous reserves of amino acids (Woodside, Budin, Wellman, & Abizaid, 2012) in a physiological response to attempt to properly sustain the offspring. This possibility notwithstanding, the protein-free diet resulted in a significant reduction in the protein content of the milk produced by the undernourished dams, in line with previous reports that used a less severe protein restriction (Fukuda, Françolin-Silva, Hernandes, Valadares, & Almeida, 2007;Grigor et al, 1987;Pine, Jessop, & .0 (.0) .0 (.0) 1.5 (3.0)…”

Section: Body Mass Milk Content Maternal Behavior and Corticosterone ...mentioning

confidence: 85%

Maternal protein-free diet during lactation programs male Wistar rat offspring for increased novelty-seeking, locomotor activity, and visuospatial performance.

Lotufo

Tenório

Barradas

et al. 2018

Behavioral Neuroscience

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It is well established that chronic undernutrition has detrimental impacts on brain development and maturation. However, protein malnutrition during the period specifically encompassing the brain growth spurt has not been widely studied, particularly regarding its effects on adolescent and adult offspring behavior. Here, we assessed the effects of a protein-free diet during the 1st 10 postnatal days on the macronutrient content of the milk produced by lactating Wistar rats, on their maternal behavior, and on the offspring's behavior. Lactating dams were fed either a protein-free or a normoprotein diet from litter parturition to Postnatal Day 10 (P10). All dams received the normoprotein diet after P10. Offspring were tested in the elevated plus-maze (anxiety-like behavior), hole board arena (novelty-seeking and locomotor activity), and radial arm water maze (memory-learning) at either P40 (adolescents) or P90 (adults). The protein-free diet reduced milk protein content at P10 but not at P20. Carbohydrate and lipid contents were unaffected. Serum corticosterone levels in the offspring (at P10, P40, or P90) and dams (at P21) were not affected by the protein-free diet. Maternal behavior was also unchanged. In the offspring, no differences were observed between groups regarding anxiety-like behaviors at both ages. The protein-free diet increased adolescent locomotor activity as well as adult novelty-seeking behavior and memory performance. Our results indicate that the brain growth spurt period is particularly sensitive to protein malnutrition, showing that even a brief nutritional insult during this period can cause specific age-dependent behavioral effects on the offspring. (PsycINFO Database Record

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Maternal nicotine exposure during lactation alters food preference, anxiety-like behavior and the brain dopaminergic reward system in the adult rat offspring

Cited by 25 publications

References 113 publications

Neuroinflammatory and Behavioral Outcomes Measured in Adult Offspring of Mice Exposed Prenatally to E-Cigarette Aerosols

Neuroinflammatory and Behavioral Outcomes Measured in Adult Offspring of Mice Exposed Prenatally to E-Cigarette Aerosols

Neonatal nicotine exposure changes insulin status in fat depots: sex-related differences

Maternal protein-free diet during lactation programs male Wistar rat offspring for increased novelty-seeking, locomotor activity, and visuospatial performance.

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