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Cited by 30Prenatal Substance Exposure EffectsNeurotransmitter Receptor Influence on BehaviorSmoking Behavior and Cessation

Prenatal nicotine sex-dependently alters adolescent dopamine system development

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Dwyer, Jennifer B., Cardenas, Anjelica, Franke, Ryan M., Chen, YiLing, Bai, Yu, Belluzzi, James D., Lotfipour, Shahrdad, Leslie, Frances M.·2019·Translational Psychiatry
DOI 10.1038/s41398-019-0640-1PMC PMC6861272
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Abstract

Despite persistent public health initiatives, many women continue to smoke during pregnancy. Since maternal smoking has been linked to persisting sex-dependent neurobehavioral deficits in offspring, some consider nicotine to be a safer alternative to tobacco during pregnancy, and the use of electronic nicotine delivery systems is on the rise. We presently show, however, that sustained exposure to low doses of nicotine during fetal development, approximating plasma levels seen clinically with the nicotine patch, produces substantial changes in developing corticostriatal dopamine systems in adolescence. Briefly, pregnant dams were implanted on gestational day 4 with an osmotic minipump that delivered either saline (GS) or nicotine (3 mg/kg/day) (GN) for two weeks. At birth, pups were cross-fostered with treatment naïve dams and were handled daily. Biochemical analyses, signaling assays, and behavioral responses to cocaine were assessed on postnatal day 32, representative of adolescence in the rodent. GN treatment had both sex-dependent and sex-independent effects on prefrontal dopamine systems, altering Catechol-O-methyl transferase (COMT)-dependent dopamine turnover in males and norepinephrine transporter (NET) binding expression in both sexes. GN enhanced cocaine-induced locomotor activity in females, concomitant with GN-induced reductions in striatal dopamine transporter (DAT) binding. GN enhanced ventral striatal D2-like receptor expression and G-protein coupling, while altering the roles of D2 and D3 receptors in cocaine-induced behaviors. These data show that low-dose prenatal nicotine treatment sex-dependently alters corticostriatal dopamine system development, which may underlie clinical deficits seen in adolescents exposed to tobacco or nicotine in utero.

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  • PNE offspring (P35/P36) had altered myelin expression of myelin-related transcription and trophic factors that produced alterations in myelin gene expression and oligodendrocyte functioning.

    “One study, for example, treated Sprague Dawley rats treated with gestational nicotine (3 mg/kg/day) and found that PNE offspring (P35/P36) had altered myelin expression of myelin-related transcription and trophic factors that produced alterations in myelin gene expression and oligodendrocyte functioning [165].”

    From Prenatal nicotine exposure during pregnancy results in adverse neurodevelopmental alterations and neurobehavioral deficits (2023) · cites this paper as [165]

    The Materials and methods section (Animals and tissue collection; page unavailable) confirms that pregnant Sprague–Dawley rats received nicotine at 3 mg/kg/day. But the Introduction and Results describe measurements of dopamine-related systems, not myelin-related factors, myelin gene expression, or oligodendrocyte function. The claimed myelin findings are not supported by our copy. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • PNE altered norepinephrine transporter (NET) binding expression in both sexes and COMT-dependent dopamine turnover in males.

    “PNE was found to alter norepinephrine transporter (NET) binding expression in both sexes and Catechol-O-methyl transferase (COMT)-dependent dopamine turnover in males.”

    From Prenatal nicotine exposure during pregnancy results in adverse neurodevelopmental alterations and neurobehavioral deficits (2023) · cites this paper as [165]

  • Low-dose PNE alters the development of the corticosteroid dopamine system in a manner that may underlie clinical deficits seen in adolescents such as increased incidence of substance abuse.

    “These results demonstrate that low-dose PNE alters the development of the corticosteroid dopamine system in a manner that may underlie clinical deficits seen in adolescents such as increased incidence of substance abuse.”

    From Prenatal nicotine exposure during pregnancy results in adverse neurodevelopmental alterations and neurobehavioral deficits (2023) · cites this paper as [165]

  • D2-like receptors and G-protein coupling in the ventral striatum were enhanced in combination with altered roles of D2 and D3 receptors in cocaine-induced behaviors.

    “D2-like receptors and G-protein coupling in the ventral striatum was also enhanced in combination with altered roles of D2 and D3 receptors in cocaine-induced behaviors.”

    From Prenatal nicotine exposure during pregnancy results in adverse neurodevelopmental alterations and neurobehavioral deficits (2023) · cites this paper as [165]

  • Sustained exposure to low doses of nicotine (3 mg/kg/day) during fetal development produced substantial changes in the developing corticostriatal dopamine system including both sex-dependent and sex-independent effects on the prefrontal dopamine systems.

    “Another study showed that sustained exposure to low doses of nicotine (3 mg/kg/day) during fetal development produced substantial changes in the developing corticostriatal dopamine system including both sex-dependent and sex-independent effects on the prefrontal dopamine systems [165].”

    From Prenatal nicotine exposure during pregnancy results in adverse neurodevelopmental alterations and neurobehavioral deficits (2023) · cites this paper as [165]

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Research works printed but not linked: 60

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Cited by

Sorted by citations

Authors
Dwyer, J. B., Cardenas, A., Franke, R. M., Chen, Y., Bai, Y., Belluzzi, J. D., Lotfipour, S., & Leslie, F. M.
Affiliations
University of California, Irvine (US)
Corresponding author
Dwyer, Jennifer B.
ORCID
Venue
Translational Psychiatry
Publisher
Springer Science and Business Media LLC
Published
2019-11-18
Volume
9
Issue
1
Pages
304-304
ISSN
2158-3188 (ISSN-L)
DOI
10.1038/s41398-019-0640-1
PMC
PMC6861272
OpenAlex
W2985723038
Cited by
30
References
5
Citations by year
2026: 3 · 2025: 1 · 2024: 2 · 2023: 5 · 2022: 7 · 2021: 9 · 2020: 2 · 2018: 1
FWCI
4.68
Type
journal article
Language
en
Open access
Licence
Locations
  • Translational Psychiatry (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Tobacco-Related Disease Research Program (22RT-0103A)
  • National Institutes of Health (19138, MH018268-33, UL1TR001863)
  • National Institute of Mental Health (R25MH077823, T32MH018268)
  • National Institute on Drug Abuse (DA 19138, R01DA019138, DA 40440, R01DA040440)
  • National Center for Advancing Translational Sciences
Topics
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
Keywords
prenatal nicotine exposure, smoking during pregnancy, sex differences, corticostriatal circuits, cocaine-induced locomotor activity, dopamine transporter binding, catechol-O-methyltransferase, norepinephrine transporter, prefrontal cortex, ventral striatum, nicotine patch, electronic cigarettes
MeSH terms
Animals, Animals, Newborn, Catechol O-Methyltransferase, Cocaine, Corpus Striatum, Dopamine, Female, Locomotion, Male, Nicotine, Pregnancy, Prenatal Exposure Delayed Effects, Sex Factors, Vasoconstrictor Agents, Rats, Sprague-Dawley, Nicotinic Agonists, Rats

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