Dopamine and serotonin levels following prenatal viral infection in mouse—implications for psychiatric disorders such as schizophrenia and autism
Open accessAbstract
Prenatal viral infection has been associated with neurodevelopmental disorders such as schizophrenia and autism. It has previously been demonstrated that viral infection causes deleterious effects on brain structure and function in mouse offspring following late first trimester (E9) and middle-late second trimester (E18) administration of influenza virus. Neurochemical analysis following infection on E18 using this model has revealed significantly altered levels of serotonin, 5-hydroxyindoleacetic acid, and taurine, but not dopamine. In order to monitor these different patterns of monoamine expression in exposed offspring in more detail and to see if there are changes in the dopamine system at another time point, pregnant C57BL6J mice were infected with a sublethal dose of human influenza virus or sham-infected using vehicle solution on E16. Male offspring of the infected mice were collected at P0, P14, and P56, their brains removed and cerebellum dissected and flash frozen. Dopamine and serotonin levels were then measured using HPLC-ED technique. When compared to controls, there was a significant decrease in serotonin levels in the cerebella of offspring of virally exposed mice at P14. No differences in levels of dopamine were observed in exposed and control mice, although there was a significant decrease in dopamine at P14 and P56 when compared to P0. The present study shows that the serotonergic system is disrupted following prenatal viral infection, potentially modelling disruptions that occur in patients with schizophrenia and autism.
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Prenatal flu exposure decreased 5-HT and 5-HIAA levels in cerebellum.
“prenatal flu exposure decreased 5-HT and 5-HIAA levels in the cerebellum (Fatemi et al., 2008; Winter et al., 2008).”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Winter et al., 2008
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Cites
A SIMPLE METHOD OF ESTIMATING FIFTY PER CENT ENDPOINTS12
REED, L. J., & Muench, H. (1938) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a118408 · Cited by 20,341 · see citing works
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
A simple method of estimating 50 per cent end points
Muench, H. (1938) · Medical Entomology and Zoology · Cited by 8,377 · see citing works
mouse brain in stereotaxic coordinates
Franklin, K. B. J., & Paxinos, G. (1997) · Cited by 3,258 · see citing works
Adult Schizophrenia Following Prenatal Exposure to an Influenza Epidemic
Mednick, S. A. (1988) · Archives of General Psychiatry · doi:10.1001/archpsyc.1988.01800260109013 · Cited by 1,198 · see citing works
Serologic Evidence of Prenatal Influenza in the Etiology of Schizophrenia
Brown, A. S., Begg, M. D., Gravenstein, S., Schaefer, C. A., Wyatt, R. J., Bresnahan, M. A., Babulas, V. P., & Susser, E. (2004) · Archives of General Psychiatry · doi:10.1001/archpsyc.61.8.774 · Cited by 1,048 · see citing works
Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring
Shi, L., Fatemi, S. H., Sidwell, R. W., & Patterson, P. H. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00297.2003 · Cited by 1,025 · see citing works
Self-citationIncreased baseline occupancy of D <sub>2</sub> receptors by dopamine in schizophrenia
Abi-Dargham, A., Rodenhiser, J., Printz, D., Zea-Ponce, Y., Gil, R., Kegeles, L. S., Weiss, R., Cooper, T. B., Mann, J. J., Van Heertum, R. L., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.14.8104 · Cited by 1,020 · see citing works
Meyer, U., Nyffeler, M., Engler, A., Urwyler, A., Schedlowski, M., Knuesel, I., Yee, B. K., & Feldon, J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0099-06.2006 · Cited by 774 · see citing works
Prefrontal Dopamine D<sub>1</sub>Receptors and Working Memory in Schizophrenia
Abi-Dargham, A., Mawlawi, O., Lombardo, I., Gil, R., Martinez, D., Huang, Y., Hwang, D.-R., Keilp, J., Kochan, L., Van Heertum, R., et al. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03708.2002 · Cited by 724 · see citing works
The role of the cerebellum in schizophrenia
Andreasen, N. C., & Pierson, R. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.01.003 · Cited by 669 · see citing works
DETERMINATION OF CATECHOLAMINES IN RAT BRAIN PARTS BY REVERSE‐PHASE ION‐PAIR LIQUID CHROMATOGRAPHY
Felice, L. J., Felice, J. D., & Kissinger, P. T. (1978) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1978.tb06573.x · Cited by 582 · see citing works
Meyer, U., Nyffeler, M., Yee, B. K., Knuesel, I., & Feldon, J. (2008) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.09.012 · Cited by 457 · see citing works
Neuromotor Precursors of Schizophrenia
Walker, E. F., Savoie, T. M., & Davis, D. (1994) · Schizophrenia Bulletin · doi:10.1093/schbul/20.3.441 · Cited by 445 · see citing works
Activity of Serotonergic Neurons in Behaving Animals
Jacobs, B. L. (1999) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00012-3 · Cited by 318 · see citing works
Meyer, U., Yee, B. K., & Feldon, J. (2007) · The Neuroscientist · doi:10.1177/1073858406296401 · Cited by 303 · see citing works
Fatemi, S. H., Earle, J., Kanodia, R., Kist, D., Emamian, E. S., Patterson, P. H., Shi, L., & Sidwell, R. (2002) · Cellular and Molecular Neurobiology · doi:10.1023/a:1015337611258 · Cited by 261 · see citing works
Self-citationMeyer, U., Feldon, J., Schedlowski, M., & Yee, B. K. (2005) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2005.11.003 · Cited by 260 · see citing works
Fatemi, S. H., Emamian, E. S., Kist, D. A., Sidwell, R. W., Nakajima, K., Akhter, P., Shier, A. C., Sheikh, S. A., & Bailey, K. W. (1999) · Molecular Psychiatry · doi:10.1038/sj.mp.4000520 · Cited by 259 · see citing works
Self-citationFatemi, S. H., Reutiman, T. J., Folsom, T. D., Huang, H., Oishi, K., Mori, S., Smee, D. F., Pearce, D. A., Winter, C., Sohr, R., et al. (2008) · Schizophrenia Research · doi:10.1016/j.schres.2007.11.018 · Cited by 250 · see citing works
Self-citationDalman, C., Allebeck, P., Gunnell, D., Harrison, G. L., Kristensson, K., Lewis, G., Löfving, S., Rasmussen, F. E., Wicks, S., & Karlsson, H. (2007) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.07050740 · Cited by 242 · see citing works
Serum autoantibodies to brain in Landau-Kleffner variant, autism, and other neurologic disorders
Connolly, A. M., Chez, M. G., Pestronk, A., Arnold, S. T., Mehta, S., & Deuel, R. K. (1999) · The Journal of Pediatrics · doi:10.1016/s0022-3476(99)70248-9 · Cited by 236 · see citing works
Serologic Evidence of Prenatal Influenza in the Etiology of Schizophrenia
Brown, A. S., Begg, M. D., Gravenstein, S., Schaefer, C. A., Wyatt, R. J., Bresnahan, M. A., Babulas, V. P., & Susser, E. (2005) · Obstetrical & Gynecological Survey · doi:10.1097/01.ogx.0000151642.60544.d2 · Cited by 216 · see citing works
Review of immunological and immunopathological findings in schizophrenia.
Rothermundt, M., Arolt, V., & Bayer, T. (2001) · Brain, behavior, and immunity · doi:10.1006/brbi.2001.0648 · Cited by 200 · see citing works
Role of altered brain serotonin mechanisms in autism
Chugani, D. C. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001167 · Cited by 166 · see citing works
Fatemi, S. H., Pearce, D. A., Brooks, A. I., & Sidwell, R. W. (2005) · Synapse · doi:10.1002/syn.20162 · Cited by 151 · see citing works
Self-citationSperk, G. (1982) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1982.tb08708.x · Cited by 137 · see citing works
Mittleman, G., Goldowitz, D., Heck, D. H., & Blaha, C. D. (2008) · Synapse · doi:10.1002/syn.20525 · Cited by 111 · see citing works
Serotonin-Dopamine Interaction as a Focus of Novel Antidepressant Drugs
Esposito, E. (2006) · Current Drug Targets · doi:10.2174/138945006775515455 · Cited by 106 · see citing works
Singh, V. K., Singh, E. A., & Warren, R. P. (1997) · Biological Psychiatry · doi:10.1016/s0006-3223(96)00522-7 · Cited by 99 · see citing works
The specificity of neurological signs in schizophrenia: a review
Boks, M. P., Russo, S., Knegtering, R., & van den Bosch, R. J. (2000) · Schizophrenia Research · doi:10.1016/s0920-9964(99)00145-0 · Cited by 99 · see citing works
Sperk, G., Berger, M. M., Hörtnagl, H., et al. (1981) · European Journal of Pharmacology · doi:10.1016/0014-2999(81)90046-7 · Cited by 88 · see citing works
Juckel, G., Gallinat, J., Riedel, M. J., Sokullu, S., Schulz, C. O., Möller, H., Müller, N., & Hegerl, U. (2003) · Schizophrenia Research · doi:10.1016/s0920-9964(03)00016-1 · Cited by 84 · see citing works
Self-citationSeason of birth and autistic disorder in Israel
Barak, Y., Ring, A., Sulkes, J., Gabbay, U., & Elizur, A. (1995) · American Journal of Psychiatry · doi:10.1176/ajp.152.5.798 · Cited by 69 · see citing works
Silver, H. (2004) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.5.10.2053 · Cited by 58 · see citing works
Juckel, G., Gudlowski, Y., Müller, D. K., Özgürdal, S., Brüne, M., Gallinat, J., Frodl, T., Witthaus, H., Uhl, I., Wutzler, A., et al. (2007) · Psychiatry Research · doi:10.1016/j.psychres.2007.08.013 · Cited by 42 · see citing works
Self-citationSchizophrenia as a neurodevelopmental disorder
Bilder, R. M. (2001) · Current Opinion in Psychiatry · doi:10.1097/00001504-200101000-00003 · Cited by 20 · see citing works
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Patterson, P. H. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.016 · Cited by 766 · see citing works
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Brown, A. S. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.09.003 · Cited by 664 · see citing works
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Meyer, U. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.07.011 · Cited by 626 · see citing works
Boksa, P. (2010) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.03.005 · Cited by 603 · see citing works
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Bitanihirwe, B. K., Peleg-Raibstein, D., Mouttet, F., Feldon, J., & Meyer, U. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.129 · Cited by 237 · see citing works
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El-Ansary, A. K., Bacha, A. B., & Kotb, M. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-74 · Cited by 209 · see citing works
Kępińska, A. P., Iyegbe, C. O., Vernon, A. C., Yolken, R., Murray, R. M., & Pollak, T. A. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00072 · Cited by 193 · see citing works
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Meyer, U., & Feldon, J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.022 · Cited by 158 · see citing works
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Kneeland, R. E., & Fatemi, S. H. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.02.001 · Cited by 152 · see citing works
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Piontkewitz, Y., Arad, M., & Weiner, I. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.019 · Cited by 108 · see citing works
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Hanswijk, S. I., Spoelder, M., Shan, L., Verheij, M. M. M., Muilwijk, O. G., Li, W., Liu, C., Kolk, S. M., & Homberg, J. R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165850 · Cited by 86 · see citing works
Goldstein, J. M., Cohen, J. E., Mareckova, K., Holsen, L., Whitfield-Gabrieli, S., Gilman, S. E., Buka, S. L., & Hornig, M. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2014464118 · Cited by 70 · see citing works
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- Authors
- Winter, C., Reutiman, T. J., Folsom, T. D., Sohr, R., Wolf, R. J., Juckel, G., & Fatemi, S. H.
- Affiliations
- Charité – Universitätsmedizin Berlin (DE)
- University of Minnesota (US)
- Ruhr University Bochum (DE)
- Corresponding author
- Juckel, Georg
- Venue
- European Neuropsychopharmacology
- Publisher
- Elsevier BV
- Published
- 2008-10
- Volume
- 18
- Issue
- 10
- Pages
- 712-716
- ISSN
- 0924-977X (ISSN-L)
- PMC
- PMC2714699
- OpenAlex
- W2134700369
- Cited by
- 92
- References
- 37
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 5 · 2020: 2 · 2019: 3 · 2018: 3 · 2017: 4 · 2016: 4 · 2015: 10 · 2014: 4 · 2013: 7 · 2012: 13
- FWCI
- 3.10
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- European Neuropsychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD046589)
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- prenatal viral infection, influenza virus, dopamine, serotonin, serotonergic system, cerebellum, schizophrenia, autism spectrum disorder, neurodevelopmental disorders, monoamines, 5-hydroxyindoleacetic acid, taurine, mouse model
- MeSH terms
- Age Factors, Analysis of Variance, Animals, Animals, Newborn, Cerebellum, Dopamine, Embryo, Mammalian, Female, Male, Mice, Inbred C57BL, Influenza A virus, Pregnancy, Prenatal Exposure Delayed Effects, Serotonin, Time Factors, Central Nervous System Viral Diseases, Mice
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