Nicotine exposure during pregnancy is a factor which influences serotonin transporter density in the rat brain
Abstract
We examined the effects of nicotine exposure during pregnancy on serotonin transporter (SERT) expression in the brain. Nicotine (6 mg/kg/day) was administered to pregnant rats via subcutaneous injections or infusion pumps. Irrespective of the route of administration, nicotine increased SERT density in the forebrain on postnatal day 22, but not in the other brain regions. Our results suggest that nicotine use by pregnant women might be an environmental factor influencing SERT expression in their children.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Smoking exposes a developing fetus to many risks including thousands of potentially harmful chemicals and oxygen deprivation, causing changes in neurotransmitter activity in the developing brain.
“Smoking exposes a developing fetus to many risks including thousands of potentially harmful chemicals and oxygen deprivation, collectively causing changes in neurotransmitter activity within the developing brain [138, 139].”
From The contribution of environmental exposure to the etiology of autism spectrum disorder (2019) · cites this paper as [139]
Cites
PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT
Lowry, O. H., Rosebrough, N., Farr, A. L., & Randall, R. (1951) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52451-6 · Cited by 315,771 · see citing works
THE ATTRACTIONS OF PROTEINS FOR SMALL MOLECULES AND IONS
Scatchard, G. (1949) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1949.tb27297.x · Cited by 19,724 · see citing works
Arango, V., Underwood, M. D., Gubbi, A., & Mann, J. J. (1995) · Brain Research · doi:10.1016/0006-8993(95)00523-s · Cited by 458 · see citing works
Reduced Central Serotonin Transporters in Alcoholism
Heinz, A., Ragan, P. W., Jones, D. W., Hommer, D. W., Williams, W. A., Knable, M. B., Gorey, J. G., Doty, L., Geyer, C., Lee, K. S., et al. (1998) · American Journal of Psychiatry · doi:10.1176/ajp.155.11.1544 · Cited by 308 · see citing works
Crow, T. J. (1984) · Neuropharmacology · doi:10.1016/0028-3908(84)90100-x · Cited by 308 · see citing works
Decreased Imipramine Binding in the Brains of Patients with Depressive Illness
Perry, E. K., Marshall, E. F., Blessed, G., Tomlinson, B. E., & Perry, R. H. (1983) · The British Journal of Psychiatry · doi:10.1192/bjp.142.2.188 · Cited by 261 · see citing works
Prenatal stress: Effects on brain biogenic amine and plasma corticosterone levels
Peters, D. A. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90353-7 · Cited by 239 · see citing works
Selective Abnormalities of Prefrontal Serotonergic Receptors in Schizophrenia
Laruelle, M. A. (1993) · Archives of General Psychiatry · doi:10.1001/archpsyc.1993.01820220066007 · Cited by 235 · see citing works
Maternal Substance Abuse and the Developing Nervous System
(1992) · Elsevier eBooks · doi:10.1016/c2009-0-03214-0 · Cited by 177 · see citing works
Chronic cocaine enhances serotonin autoregulation and serotonin uptake binding
Cunningham, K. A., Paris, J. M., & Goeders, N. E. (1992) · Synapse · doi:10.1002/syn.890110204 · Cited by 150 · see citing works
Muneoka, K. T., Mikuni, M., Ogawa, T., Kitera, K., Kamei, K., Takigawa, M., & Takahashi, K. (1997) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1997.273.5.r1669 · Cited by 141 · see citing works
Self-citationMuneoka, K., Ogawa, T., Kamei, K., Muraoka, S., Tomiyoshi, R., Mimura, Y., Kato, H., Suzuki, M. R., & Takigawa, M. (1997) · Brain research. Developmental brain research · doi:10.1016/s0165-3806(97)00092-8 · Cited by 133 · see citing works
Self-citationWhitaker‐Azmitia, P. M., Zhang, X., & Clarke, C. (1994) · Neuropsychopharmacology · doi:10.1038/npp.1994.42 · Cited by 109 · see citing works
Prenatal Exposure to Nicotine: What Can We Learn from Animal Models?
Slotkin, T. A. (1992) · Elsevier eBooks · doi:10.1016/b978-0-08-092667-4.50010-6 · Cited by 91 · see citing works
Programming of brainstem serotonin transporter development by prenatal glucocorticoids
Slotkin, T. A., Barnes, G. A., McCook, E. C., & Seidler, F. J. (1996) · Developmental Brain Research · doi:10.1016/0165-3806(96)00027-2 · Cited by 84 · see citing works
Grecksch, G., Zhou, D., Franke, C., Schröder, U., Sabel, B. A., Becker, A., & Huether, G. (1997) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0701530 · Cited by 72 · see citing works
Ferris, C. F. (2000) · Experimental Physiology · doi:10.1111/j.1469-445x.2000.tb00011.x · Cited by 65 · see citing works
Prenatal Administration of Nicotine Results in Dopaminergic Alterations in the Neocortex
Muneoka, K. T., Nakatsu, T., Fuji, J., Ogawa, T., & Takigawa, M. (1999) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(99)00028-8 · Cited by 53 · see citing works
Self-citationZhou, D., Huether, G., Wiltfang, J., Hajak, G., & Rüther, E. (1996) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1996.67020656.x · Cited by 30 · see citing works
Dewar, K. M., Grondin, L., Nénonéné, E. K., Ohayon, M. M., & Reader, T. A. (1993) · European Journal of Pharmacology · doi:10.1016/0014-2999(93)90833-4 · Cited by 30 · see citing works
Whitaker‐Azmitia, P. M., Quartermain, D., & Shemer, A. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90044-y · Cited by 20 · see citing works
McReynolds, A. M., & Meyer, J. S. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09768.x · Cited by 14 · see citing works
Yeghiayan, S. K., Andersen, S. L., & Baldessarini, R. J. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00777-5 · Cited by 14 · see citing works
Dean, B., Pereira, A. M., Pavey, G., & SINGH, B. S. (1997) · Psychiatry Research · doi:10.1016/s0165-1781(97)00125-x · Cited by 10 · see citing works
Flagged first, then by citations
3 of the 27 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
The contribution of environmental exposure to the etiology of autism spectrum disorder
Bölte, S., Girdler, S., & Marschik, P. B. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2988-4 · Cited by 509 · see citing works
Maternal lifestyle and environmental risk factors for autism spectrum disorders
Lyall, K., Schmidt, R. J., & Hertz-Picciotto, I. (2014) · International Journal of Epidemiology · doi:10.1093/ije/dyt282 · Cited by 427 · see citing works
Prenatal tobacco smoke and postnatal secondhand smoke exposure and child neurodevelopment
Herrmann, M. S., King, K., & Weitzman, M. (2008) · Current opinion in pediatrics · doi:10.1097/mop.0b013e3282f56165 · Cited by 254 · see citing works
Cigarette smoking during pregnancy
Shea, A. K., & Steiner, M. S. (2008) · Nicotine & Tobacco Research · doi:10.1080/14622200701825908 · Cited by 203 · see citing works
Fetal and adolescent nicotine administration: effects on CNS serotonergic systems
Xu, Z., Seidler, F. J., Ali, S. F., Slikker, W., & Slotkin, T. A. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02797-4 · Cited by 186 · see citing works
Vaglenova, J., Birru, S., Pandiella, N. M., & Breese, C. R. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.07.005 · Cited by 180 · see citing works
Slotkin, T. A., MacKillop, E. A., Rudder, C. L., Ryde, I. T., Tate, C. A., & Seidler, F. J. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301231 · Cited by 149 · see citing works
Nicotinic–serotonergic interactions in brain and behaviour
Seth, P., Cheeta, S., Tucci, S., & File, S. E. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00715-8 · Cited by 145 · see citing works
Weitzman, M. L. (2002) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(02)00201-5 · Cited by 134 · see citing works
The relationship of maternal smoking to psychological problems in the offspring
Button, T. M. M., Maughan, B., & McGuffin, P. (2007) · Early Human Development · doi:10.1016/j.earlhumdev.2007.07.006 · Cited by 113 · see citing works
Molecular mechanisms of maternal cannabis and cigarette use on human neurodevelopment
Morris, C. V., DiNieri, J. A., Szutorisz, H., & Hurd, Y. L. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07884.x · Cited by 111 · see citing works
Heath, C. J., & Picciotto, M. R. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.020 · Cited by 99 · see citing works
Prenatal cocaine and/or nicotine exposure produces depression and anxiety in aging rats
Sobrian, S. K., Marr, L., & Ressman, K. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(03)00042-3 · Cited by 92 · see citing works
Falk, L. L., Nordberg, A. K., Seiger, Å., Kjældgaard, A., & Hellström‐Lindahl, E. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.12.049 · Cited by 82 · see citing works
Is There Evidence for Potential Harm of Electronic Cigarette Use in Pregnancy?
Suter, M., Mastrobattista, J. M., Kahr, M. K., & Aagaard, K. M. (2014) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.23333 · Cited by 80 · see citing works
The impact of tobacco chemicals and nicotine on placental development
Suter, M., & Aagaard, K. M. (2020) · Prenatal Diagnosis · doi:10.1002/pd.5660 · Cited by 80 · see citing works
Cigarette Smoking and Brain Regulation of Energy Homeostasis
Chen, H., Saad, S., Sandow, S. L., & Bertrand, P. P. (2012) · Frontiers in Pharmacology · doi:10.3389/fphar.2012.00147 · Cited by 67 · see citing works
Medullary serotonin defects and respiratory dysfunction in sudden infant death syndrome
Paterson, D. S., Hilaire, G., & Weese‐Mayer, D. E. (2009) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2009.05.010 · Cited by 65 · see citing works
Influence of prenatal nicotine exposure on postnatal development of breathing pattern
Huang, Y.-H., Brown, A. R., Costy‐Bennett, S., Luo, Z., & Fregosi, R. F. (2004) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2004.07.002 · Cited by 63 · see citing works
Molecular mechanisms for nicotine intoxication
Alkam, T., & Nabeshima, T. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.02.006 · Cited by 62 · see citing works
Alkam, T., Kim, H., Hiramatsu, M., Mamiya, T., Aoyama, Y., Nitta, A., Yamada, K., & Nabeshima, T. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.10.058 · Cited by 56 · see citing works
Alkam, T., Mamiya, T., Kimura, N., Yoshida, A., Kihara, D., Tsunoda, Y., Aoyama, Y., Hiramatsu, M., Kim, H.-C., & Nabeshima, T. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4591-z · Cited by 50 · see citing works
Respiratory dysfunctions induced by prenatal nicotine exposure
Campos, M., Bravo, E., & Eugenín, J. L. (2009) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2009.05214.x · Cited by 47 · see citing works
Cerpa, V. J., Aylwin, M. D. L. L. O., Beltrán-Castillo, S., Bravo, E. U., Llona, I. R., Richerson, G. B., & Eugenín, J. L. (2015) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2014-0329oc · Cited by 47 · see citing works
Slotkin, T. A., Pinkerton, K. E., Tate, C. A., & Seidler, F. J. (2006) · Brain Research · doi:10.1016/j.brainres.2006.06.094 · Cited by 51 · see citing works
Adult Household Smoking Is Associated With Increased Child Emotional and Behavioral Problems
Salvo, E. P.-D., Liu, Y.-H., Brenner, S., & Weitzman, M. L. (2010) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/dbp.0b013e3181cdaad6 · Cited by 41 · see citing works
Lavezzi, A. M., Casale, V., Oneda, R., Weese‐Mayer, D. E., & Matturri, L. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e3181a7bb73 · Cited by 45 · see citing works
Hill, S. Y., Shen, S., Locke, J., Rickin, E., & Lowers, L. (2005) · Psychiatry Research · doi:10.1016/j.psychres.2005.04.003 · Cited by 36 · see citing works
Suter, M. A., Abramovici, A. R., Griffin, E., Branch, D. W., Lane, R. H., Mastrobattista, J., Rehan, V. K., & Aagaard, K. (2015) · Birth Defects Research Part A: Clinical and Molecular Teratology · doi:10.1002/bdra.23395 · Cited by 35 · see citing works
Nicotine, Serotonin, and Sudden Infant Death Syndrome
Nattie, E., & Kinney, H. C. (2002) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.2210001 · Cited by 32 · see citing works
Environment and autism: current state of the science
Schmidt, R. J., Lyall, K., & Hertz‐Picciotto, I. (2014) · Cutting Edge Psychiatry in Practice · doi:10.65031/ibek1613 · Cited by 24 · see citing works
Exposure to Smoke During Development: Fetal Programming of Adult Disease
Bergen, H. (2006) · Tobacco Induced Diseases · doi:10.1186/1617-9625-3-2-5 · Cited by 19 · see citing works
Awtry, T. L., Frank, J. G., & Werling, L. L. (2006) · Synapse · doi:10.1002/syn.20251 · Cited by 19 · see citing works
Environmental Factors in the Preconception and Prenatal Periods in Relation to Risk for ASD
Lyall, K., Schmidt, R. J., & Hertz‐Picciotto, I. (2014) · Wiley eBooks · doi:10.1002/9781118911389.hautc18 · Cited by 17 · see citing works
Rosenthal, D. G., & Weitzman, M. L. (2011) · International Journal of Mental Health · doi:10.2753/imh0020-7411400103 · Cited by 16 · see citing works
Duko, B., Pereira, G. F., Betts, K. S., Tait, R. J., Newnham, J. P., & Alati, R. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.10.030 · Cited by 14 · see citing works
Gorini, C., Jameson, H. S., Woerman, A. L., Perry, D. C., & Mendelowitz, D. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00552.2013 · Cited by 11 · see citing works
Prenatal nicotine exposure does not cause Purkinje cell loss in the developing rat cerebellar vermis
Chen, W. A., & Edwards, R. B. (2003) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(03)00048-5 · Cited by 10 · see citing works
Perinatal Nicotine Reduces Chemosensitivity of Medullary 5-HT Neurons after Maturation in Culture
Avraam, J., Wu, Y., & Richerson, G. B. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.08.012 · Cited by 7 · see citing works
Czubak, A., Nowakowska, E., Kus, K., Sadowski, C., & Matschay, A. (2008) · Human & Experimental Toxicology · doi:10.1177/0960327108098334 · Cited by 6 · see citing works
The Environment in Autism Spectrum Disorders
Lyall, K., Schmidt, R. J., & Hertz‐Picciotto, I. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-391924-3.00014-4 · Cited by 5 · see citing works
Brain serotonin, oxytocin, and their interaction: Relevance for eating disorders
Ismaylova, E., Nemoda, Z., & Booij, L. (2025) · Journal of Psychopharmacology · doi:10.1177/02698811241309617 · Cited by 4 · see citing works
Sudden death of an infant with cardiac, nervous system and genetic involvement – a case report
Mecchia, D., Casale, V., Oneda, R., Matturri, L., & Lavezzi, A. M. (2013) · Diagnostic Pathology · doi:10.1186/1746-1596-8-159 · Cited by 4 · see citing works
McDonald, F. B., Chandrasekharan, K., Wilson, R. J. A., & Hasan, S. U. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00062.2016 · Cited by 4 · see citing works
A Biological/Genetic Perspective: The Addicted Brain
Kelly, T. H., Kazura, A. N., Lommel, K. M., Babalonis, S. L., & Martin, C. A. (2008) · Springer eBooks · doi:10.1007/978-0-387-09732-9_2 · Cited by 3 · see citing works
Maternal fish consumption during pregnancy and smoking behavioural patterns
Gow, R. V., Heron, J., Hibbeln, J. R., Davis, J. M., & SanGiovanni, J. P. (2018) · British Journal Of Nutrition · doi:10.1017/s0007114517003592 · Cited by 3 · see citing works
Dali, O., Heitz‐Marchaland, C., Kernanec, P.-Y., Carrion-Padilla, J., Godin, B., Tevosian, S. G., Zubcevic, J. A., Hayward, L. F., & Smagulova, F. O. (2025) · BMC Genomics · doi:10.1186/s12864-025-11960-9 · Cited by 1 · see citing works
Lackner, C. L., Thompson, B. A., Santesso, D. L., Wade, T. J., & Segalowitz, S. J. (2023) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2023.107175 · Cited by 2 · see citing works
Weitzman, M. L., Florin, T. A., & Kavanaugh, M. L. (2006) · CRC Press eBooks · doi:10.1201/9781420018523.ch8 · Cited by 1 · see citing works
Influência de fatores genéticos e ambientais nos transtornos do espectro autista
Longo, D. (2009) · Americanae (AECID Library)
Parental Smoking and Children's Behavioral and Cognitive Functioning
Weitzman, M. L., Kavanaugh, M. L., & Florin, T. A. (2005) · International review of research in mental retardation · doi:10.1016/s0074-7750(05)30008-5
Falk, L. L. (2005) · Figshare
Nei, M., & ins, N. (2010) · CRC Press eBooks · doi:10.1201/b10317-14
Prenatal Nicotine Exposure and Impact on the Behaviors of Offspring
Alkam, T., & Nabeshima, T. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813035-3.00024-1
A Biological/Genetic Perspective: The Addicted Brain
Kelly, T. H., Harvanko, A. M., Pierce, M. E., Rayapati, A. O., & Martin, C. A. (2018) · Issues in children's and families' lives · doi:10.1007/978-3-319-90611-9_3
Medullary Serotonergic Abnormalities in Sudden Infant Death Syndrome
Paterson, D. (2010) · CRC Press eBooks · doi:10.1201/b10317-6
Alkam, T., Shota, R., & Nabeshima, T. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-824315-2.00148-2
- Authors
- Muneoka, K., Ogawa, T., Kamei, K., Mimura, Y., Kato, H., & Takigawa, M.
- Affiliations
- Kagoshima University (JP)
- Corresponding author
- Muneoka, Katsumasa
- ORCID
- Muneoka, Katsumasa
- Venue
- European Journal of Pharmacology
- Publisher
- Elsevier BV
- Published
- 2001-01
- Volume
- 411
- Issue
- 3
- Pages
- 279-282
- ISSN
- 0014-2999 (ISSN-L)
- OpenAlex
- W1966750374
- Cited by
- 59
- References
- 27
- Citations by year
- 2025: 2 · 2023: 1 · 2022: 1 · 2020: 3 · 2019: 2 · 2018: 3 · 2017: 1 · 2016: 1 · 2015: 2 · 2014: 4 · 2013: 2 · 2012: 3
- FWCI
- 3.00
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Pharmacology (publishedVersion)
- PubMed (publishedVersion)
- 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
- nicotine, pregnancy, serotonin transporter, prenatal nicotine exposure, forebrain, maternal smoking, developmental neurotoxicity, rat brain
- MeSH terms
- Animals, Brain Chemistry, Carrier Proteins, Female, Infusion Pumps, Injections, Subcutaneous, Male, Membrane Glycoproteins, Nerve Tissue Proteins, Nicotine, Pregnancy, Prenatal Exposure Delayed Effects, Rats, Sprague-Dawley, Selective Serotonin Reuptake Inhibitors, Paroxetine, Nicotinic Agonists, Membrane Transport Proteins, Serotonin Plasma Membrane Transport Proteins, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review