Maternal infection leads to abnormal gene regulation and brain atrophy in mouse offspring: implications for genesis of neurodevelopmental disorders
Open accessAbstract
Prenatal viral infection has been associated with development of schizophrenia and autism. Our laboratory has previously shown that viral infection causes deleterious effects on brain structure and function in mouse offspring following late first trimester (E9) administration of influenza virus. We hypothesized that late second trimester infection (E18) in mice may lead to a different pattern of brain gene expression and structural defects in the developing offspring. C57BL6J mice were infected on E18 with a sublethal dose of human influenza virus or sham-infected using vehicle solution. Male offsping of the infected mice were collected at P0, P14, P35 and P56, their brains removed and prefrontal cortex, hippocampus and cerebellum dissected and flash frozen. Microarray, qRT-PCR, DTI and MRI scanning, western blotting and neurochemical analysis were performed to detect differences in gene expression and brain atrophy. Expression of several genes associated with schizophrenia or autism including Sema3a, Trfr2 and Vldlr were found to be altered as were protein levels of Foxp2. E18 infection of C57BL6J mice with a sublethal dose of human influenza virus led to significant gene alterations in frontal, hippocampal and cerebellar cortices of developing mouse progeny. Brain imaging revealed significant atrophy in several brain areas and white matter thinning in corpus callosum. Finally, neurochemical analysis revealed significantly altered levels of serotonin (P14, P35), 5-Hydroxyindoleacetic acid (P14) and taurine (P35). We propose that maternal infection in mouse provides an heuristic animal model for studying the environmental contributions to genesis of schizophrenia and autism, two important examples of neurodevelopmental disorders.
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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 Fatemi et al., 2008
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Prenatal maternal immune activation causes epigenetic differences in adolescent mouse brain
Basil, P., Li, Q., Dempster, E. L., Mill, J., Sham, P.-C., Wong, C. C. Y., & McAlonan, G. M. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.80 · Cited by 116 · see citing works
Tracing the development of psychosis and its prevention: what can be learned from animal models
Piontkewitz, Y., Arad, M., & Weiner, I. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.019 · Cited by 108 · see citing works
Winter, C., Reutiman, T. J., Folsom, T. D., Sohr, R., Wolf, R. J., Juckel, G., & Fatemi, S. H. (2008) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2008.06.001 · Cited by 92 · see citing works
Self-citationWeir, R. K., Forghany, R., Smith, S. E. P., Patterson, P. H., McAllister, A. K., Schumann, C. M., & Bauman, M. D. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.03.009 · Cited by 86 · see citing works
Gestational Factors throughout Fetal Neurodevelopment: The Serotonin Link
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
Crum, W. R., Sawiak, S. J., Chege, W., Cooper, J. D., Williams, S. C. R., & Vernon, A. C. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.12.008 · Cited by 76 · see citing works
Decreased Cortical Serotonin in Neonatal Rabbits Exposed to Endotoxin <i>in Utero</i>
Kannan, S., Saadani-Makki, F., Balakrishnan, B., Dai, H., Chakraborty, P. K., Janisse, J., Muzik, O., Romero, R., & Chugani, D. C. (2011) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2010.156 · Cited by 58 · see citing works
- Authors
- Fatemi, S. H., Reutiman, T. J., Folsom, T. D., Huang, H., Oishi, K., Mori, S., Smee, D. F., Pearce, D. A., Winter, C., Sohr, R., & Juckel, G.
- Affiliations
- University of Minnesota (US)
- Johns Hopkins University (US)
- Utah State University (US)
- Charité – Universitätsmedizin Berlin (DE)
- Ruhr University Bochum (DE)
- Corresponding author
- Fatemi, S. Hossein
- ORCID
- Venue
- Schizophrenia Research
- Publisher
- Elsevier BV
- Published
- 2008-02
- Volume
- 99
- Issue
- 1-3
- Pages
- 56-70
- ISSN
- 0920-9964 (ISSN-L)
- PMC
- PMC2312390
- OpenAlex
- W1983141299
- Cited by
- 250
- References
- 79
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 7 · 2023: 7 · 2022: 11 · 2021: 10 · 2020: 13 · 2019: 8 · 2018: 11 · 2017: 10 · 2016: 24 · 2015: 19 · 2014: 13 · 2013: 15 · 2012: 19
- FWCI
- 8.69
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Schizophrenia Research (publishedVersion)
- PubMed (publishedVersion)
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- prenatal viral infection, maternal infection
- MeSH terms
- Animals, Atrophy, Autistic Disorder, Brain, Disease Models, Animal, Female, Gene Expression Regulation, Gestational Age, Humans, Image Processing, Computer-Assisted, Influenza, Human, Magnetic Resonance Imaging, Mice, Inbred C57BL, Pregnancy, Prenatal Exposure Delayed Effects, Receptors, LDL, Receptors, Transferrin, Repressor Proteins, Schizophrenia, Neurotransmitter Agents, Reverse Transcriptase Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, Diffusion Magnetic Resonance Imaging, Semaphorin-3A, Mice, Forkhead Transcription Factors, Influenza A Virus, H1N1 Subtype
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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.
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