Effects of prenatal nicotine exposure on primate brain development and attempted amelioration with supplemental choline or vitamin c: neurotransmitter receptors, cell signaling and cell development biomarkers in fetal brain regions of rhesus monkeys
Abstract
Studies in developing rodents indicate that nicotine is a neuroteratogen that disrupts brain development by stimulating nicotinic acetylcholine receptors (nAChRs) that control neural cell replication and differentiation. We administered nicotine to pregnant Rhesus monkeys from gestational day 30 through 160 by continuous infusion, achieving maternal plasma levels comparable to those in smokers (30 ng/ml). Fetal brain regions and peripheral tissues were examined for nAChR subtypes, other neurotransmitter receptors, and indices of cell signaling and cell damage. Nicotine evoked nAChR upregulation, but with distinct regional disparities indicative of selective stimulatory responses. Similarly, indices of cell loss (reduced DNA), cell size and neuritic outgrowth (protein/DNA and membrane/total protein ratios) were distinct for each region and did not necessarily follow the rank order of nAChR upregulation, suggesting the involvement of additional mechanisms such as oxidative stress. We then attempted to offset the adverse effects of nicotine with standard dietary supplements known to interact with nicotine. By itself, choline elicited nicotine-like actions commensurate with its promotion of cholinergic neurotransmission. When given in combination with nicotine, choline protected some regions from damage but worsened nicotine's effects in other regions. Similarly, Vitamin C supplementation had mixed effects, increasing nAChR responses while providing protection from cell damage in the caudate, the brain region most susceptible to oxidative stress. Our results indicate that nicotine elicits neurodevelopmental damage that is highly selective for different brain regions, and that dietary supplements ordinarily thought to be neuroprotectant may actually worsen some of the adverse effects of nicotine on the fetal brain.
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Nicotine is a key cause of the neurodevelopmental harm from tobacco smoke exposure.
“and these studies show that nicotine itself is a critical contributor to the harmful neurodevelopmental effects of tobacco smoke exposure.(307-310)”
From Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products (2017) · cites this paper as [310]
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- Authors
- Slotkin, T. A., Seidler, F. J., Qiao, D., Aldridge, J. E., Tate, C. A., Cousins, M. M., Proskocil, B. J., Sekhon, H. S., Clark, J. A., Lupo, S. L., & Spindel, E. R.
- Affiliations
- Duke Medical Center (US)
- Oregon National Primate Research Center (US)
- Corresponding author
- Slotkin, Theodore A
- Venue
- Neuropsychopharmacology
- Published
- 2004-08-18
- Volume
- 30
- Issue
- 1
- Pages
- 129-144
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- OpenAlex
- W2023016145
- Cited by
- 101
- References
- 104
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 1 · 2023: 2 · 2022: 4 · 2021: 1 · 2020: 5 · 2019: 5 · 2018: 5 · 2017: 4 · 2016: 2 · 2015: 9 · 2014: 6 · 2013: 3 · 2012: 4
- FWCI
- 7.06
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (RR 00163)
- Oregon National Primate Research Center (RR00163)
- National Institute of Environmental Health Sciences (ES 07031, T32ES007031)
- National Center for Research Resources (RR-00163.)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD/HL-37131)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Keywords
- prenatal nicotine exposure, fetal brain development, nicotinic acetylcholine receptors, rhesus monkeys, choline supplementation, vitamin C supplementation, neuroprotection, oxidative stress, signal transduction, cell damage, caudate nucleus, neurotransmitter receptors
- MeSH terms
- Adenylyl Cyclases, Animals, Antioxidants, Ascorbic Acid, Brain, Choline, DNA, Female, Heart, Macaca mulatta, Nicotine, Pregnancy, Prenatal Exposure Delayed Effects, Signal Transduction, Biomarkers, Thiobarbituric Acid Reactive Substances, Receptors, Neurotransmitter, Oxidative Stress, Nootropic Agents, Nicotinic Agonists
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