Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia

Meyer, Urs; Feldon, Joram; Schedlowski, Manfred; Yee, Benjamin K.

doi:10.1016/j.neubiorev.2004.10.012

Cited by 494Tryptophan and brain disordersSchizophrenia research and treatmentNeuroinflammation and Neurodegeneration Mechanisms

Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia

Meyer, Urs, Feldon, Joram, Schedlowski, Manfred, Yee, Benjamin K.·2005·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2004.10.012

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Abstract

Epidemiological studies have indicated an association between maternal bacterial and viral infections during pregnancy and the higher incidence of schizophrenia in the resultant offspring post-puberty. One hypothesis asserts that the reported epidemiological link is mediated by prenatal activation of the foetal immune system in response to the elevation of maternal cytokine level due to infection. Here, we report that pregnant mouse dams receiving a single exposure to the cytokine-releasing agent, polyriboinosinic-polyribocytidilic acid (PolyI:C; at 2.5, 5.0, or 10.0 mg/kg) on gestation day 9 produced offspring that subsequently exhibited multiple schizophrenia-related behavioural deficits in adulthood, in comparison to offspring from vehicle injected or non-injected control dams. The efficacy of the PolyI:C challenge to induce cytokine responses in naïve non-pregnant adult female mice and in foetal brain tissue when injected to pregnant mice were further ascertained in separate subjects: (i) a dose-dependent elevation of interleukin-10 was detected in the adult female mice at 1 and 6h post-injection, (ii) 12 h following prenatal PolyI:C challenge, the foetal levels of interleukin-1beta were elevated. The spectrum of abnormalities included impairments in exploratory behaviour, prepulse inhibition, latent inhibition, the US-pre-exposure effect, spatial working memory; and enhancement in the locomotor response to systemic amphetamine (2.5 mg/kg, i.p.) as well as in discrimination reversal learning. The neuropsychological parallels between prenatal PolyI:C treatment in mice and psychosis in humans, demonstrated here, leads us to conclude that prenatal PolyI:C treatment represents one of the most powerful environmental-developmental models of schizophrenia to date. The uniqueness of this model lies in its epidemiological and immunological relevance. It is, sui generis, ideally suited for the investigation of the neuropsychoimmunological mechanisms implicated in the developmental aetiology and disease processes of schizophrenia.

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The maternal immune activation model has repeatedly produced consistent results and supports a subset of autism with autism-relevant atypical behaviors.
“Some of the strongest support for maternal infection as a contributor to autism has come from the maternal immune activation (MIA) model, which has repeatedly shown consistent results, helping to establish a subset of autism that is supported by observations of autism-relevant atypical behaviors.”
From The Role of the Immune System in Autism Spectrum Disorder (2017) · cites this paper as Meyer et al, 2005
In the common MIA model, challenging pregnant rodents with infection or poly(I:C) causes significant immunological, neurodevelopmental, and behavioral changes in the offspring.
“The MIA model in its most common design involves challenging pregnant rodents via direct infection (eg, influenza, Escherichia coli) or the dsRNA mimic poly (I:C); significant immunological, neurodevelopmental, and behavioral changes are then observed in the offspring”
From The Role of the Immune System in Autism Spectrum Disorder (2017) · cites this paper as Meyer et al, 2005

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Maternal immune activation and abnormal brain development across CNS disorders
Knuesel, I., Chicha, L., Britschgi, M., Schobel, S. A., Bodmer, M., Hellings, J. A., Toovey, S., & Prinssen, E. P. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.187 · Cited by 880 · see citing works
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Authors: Meyer, U., Feldon, J., Schedlowski, M., & Yee, B. K.
Affiliations: ETH Zurich (CH)
Corresponding author: Yee, Benjamin K.
ORCID: Meyer, Urs
Schedlowski, Manfred
Yee, Benjamin K.
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2005-01
Volume: 29
Issue: 6
Pages: 913-947
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2004.10.012
OpenAlex: W2076644456
Cited by: 494
References: 337
Citations by year: 2026: 9 · 2025: 7 · 2024: 18 · 2023: 16 · 2022: 21 · 2021: 23 · 2020: 19 · 2019: 22 · 2018: 36 · 2017: 20 · 2016: 27 · 2015: 30 · 2014: 20 · 2013: 24 · 2012: 35
FWCI: 8.57
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: schizophrenia, prenatal immune activation, maternal infection, poly(I:C), cytokines, IL-1β, IL-10, prepulse inhibition, latent inhibition, spatial working memory, amphetamine sensitivity, discrimination reversal learning, psychosis
MeSH terms: Animals, Avoidance Learning, Brain Chemistry, Disease Models, Animal, Dose-Response Relationship, Drug, Exploratory Behavior, Female, Humans, Inhibition, Psychological, Male, Memory, Short-Term, Mice, Inbred C57BL, Motor Activity, Polynucleotides, Pregnancy, Prenatal Exposure Delayed Effects, Reflex, Acoustic, Schizophrenia, Schizophrenic Psychology, Cytokines, Mice

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Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia

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