Maternal nicotine intoxication before pregnancy induces depressive‐ and anxiety‐like behaviors as well as cognitive deficits in male offspring and correlates with neurobiological changes

Abstract Introduction Maternal nicotine use has been suggested to affect the behavior of children and is linked to changes in neurological systems; however, the specific mechanism is yet to be understood. Methods Mice were used to establish a maternal nicotine intoxication model. At postnatal day 60...

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Main Authors: Linglong Deng, Qing Wang, Ying Lou
Format: Article
Language:English
Published: Wiley 2023-07-01
Series:Brain and Behavior
Subjects:
Online Access:https://doi.org/10.1002/brb3.3052
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author Linglong Deng
Qing Wang
Ying Lou
author_facet Linglong Deng
Qing Wang
Ying Lou
author_sort Linglong Deng
collection DOAJ
description Abstract Introduction Maternal nicotine use has been suggested to affect the behavior of children and is linked to changes in neurological systems; however, the specific mechanism is yet to be understood. Methods Mice were used to establish a maternal nicotine intoxication model. At postnatal day 60 (adolescent stage), male offspring were tested for behavioral tasks including sucrose preference, open field, elevated plus maze, light/dark box, object recognition, Morris water maze (MWM), and forced swimming. Enzyme‐linked immunoassays were used to measure plasma concentrations of neurotransmitters including norepinephrine, dopamine, serotonin, and corticosterone. Serotonin transporter (Sert), brain‐derived neurotrophic factor (Bdnf), cAMP response element binding protein (Creb), and phosphorylated (p)Creb mRNA levels were measured using quantitative real‐time polymerase chain reaction. Results Male offspring of nicotine‐intoxicated dams had significantly reduced sucrose preference, mobility time in the forced swimming test, and locomotor and exploratory activities. Offspring in the maternal nicotine intoxication group showed increased signs of depressive‐ and anxiety‐like behavior. Recognition memory in the MWM was compromised in these animals. The hippocampal and prefrontal cortical regions showed significant changes in Bdnf, pCreb, and Sert gene expression, whereas CREB mRNA levels were unaffected. Moreover, compared to the controls, neurogenesis and neuronal viability were also reduced in these animals. Conclusion Prenatal nicotine exposure might affect the hypothalamic–pituitary–adrenal axis and reduce neurogenesis, potentially leading to depressive‐like behaviors and cognitive deficiencies in male offspring.
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spelling doaj.art-f099df113d9148c39939ec7c78a276cf2023-07-13T04:43:15ZengWileyBrain and Behavior2162-32792023-07-01137n/an/a10.1002/brb3.3052Maternal nicotine intoxication before pregnancy induces depressive‐ and anxiety‐like behaviors as well as cognitive deficits in male offspring and correlates with neurobiological changesLinglong Deng0Qing Wang1Ying Lou2Department of Nursing, Nanjing Vocational Health College Nanjing ChinaDepartment of Pharmacy, Nanjing Mochou Vocational School Nanjing ChinaDepartment of Nursing, Nanjing Vocational Health College Nanjing ChinaAbstract Introduction Maternal nicotine use has been suggested to affect the behavior of children and is linked to changes in neurological systems; however, the specific mechanism is yet to be understood. Methods Mice were used to establish a maternal nicotine intoxication model. At postnatal day 60 (adolescent stage), male offspring were tested for behavioral tasks including sucrose preference, open field, elevated plus maze, light/dark box, object recognition, Morris water maze (MWM), and forced swimming. Enzyme‐linked immunoassays were used to measure plasma concentrations of neurotransmitters including norepinephrine, dopamine, serotonin, and corticosterone. Serotonin transporter (Sert), brain‐derived neurotrophic factor (Bdnf), cAMP response element binding protein (Creb), and phosphorylated (p)Creb mRNA levels were measured using quantitative real‐time polymerase chain reaction. Results Male offspring of nicotine‐intoxicated dams had significantly reduced sucrose preference, mobility time in the forced swimming test, and locomotor and exploratory activities. Offspring in the maternal nicotine intoxication group showed increased signs of depressive‐ and anxiety‐like behavior. Recognition memory in the MWM was compromised in these animals. The hippocampal and prefrontal cortical regions showed significant changes in Bdnf, pCreb, and Sert gene expression, whereas CREB mRNA levels were unaffected. Moreover, compared to the controls, neurogenesis and neuronal viability were also reduced in these animals. Conclusion Prenatal nicotine exposure might affect the hypothalamic–pituitary–adrenal axis and reduce neurogenesis, potentially leading to depressive‐like behaviors and cognitive deficiencies in male offspring.https://doi.org/10.1002/brb3.3052anxietydepressionnicotineoffspring
spellingShingle Linglong Deng
Qing Wang
Ying Lou
Maternal nicotine intoxication before pregnancy induces depressive‐ and anxiety‐like behaviors as well as cognitive deficits in male offspring and correlates with neurobiological changes
Brain and Behavior
anxiety
depression
nicotine
offspring
title Maternal nicotine intoxication before pregnancy induces depressive‐ and anxiety‐like behaviors as well as cognitive deficits in male offspring and correlates with neurobiological changes
title_full Maternal nicotine intoxication before pregnancy induces depressive‐ and anxiety‐like behaviors as well as cognitive deficits in male offspring and correlates with neurobiological changes
title_fullStr Maternal nicotine intoxication before pregnancy induces depressive‐ and anxiety‐like behaviors as well as cognitive deficits in male offspring and correlates with neurobiological changes
title_full_unstemmed Maternal nicotine intoxication before pregnancy induces depressive‐ and anxiety‐like behaviors as well as cognitive deficits in male offspring and correlates with neurobiological changes
title_short Maternal nicotine intoxication before pregnancy induces depressive‐ and anxiety‐like behaviors as well as cognitive deficits in male offspring and correlates with neurobiological changes
title_sort maternal nicotine intoxication before pregnancy induces depressive and anxiety like behaviors as well as cognitive deficits in male offspring and correlates with neurobiological changes
topic anxiety
depression
nicotine
offspring
url https://doi.org/10.1002/brb3.3052
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AT qingwang maternalnicotineintoxicationbeforepregnancyinducesdepressiveandanxietylikebehaviorsaswellascognitivedeficitsinmaleoffspringandcorrelateswithneurobiologicalchanges
AT yinglou maternalnicotineintoxicationbeforepregnancyinducesdepressiveandanxietylikebehaviorsaswellascognitivedeficitsinmaleoffspringandcorrelateswithneurobiologicalchanges