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Cited by 47Neuroinflammation and Neurodegeneration MechanismsAutism Spectrum Disorder ResearchNeuroscience and Neuropharmacology Research

Early postnatal allergic airway inflammation induces dystrophic microglia leading to excitatory postsynaptic surplus and autism-like behavior

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Saitoh, Ban-yu, Tanaka, Eizo, Yamamoto, Norio, Kruining, Daan van, Iinuma, Kyoko, Nakamuta, Yuko, Yamaguchi, Hiroo, Yamasaki, Ryo +2 more·2021·Brain, Behavior, and Immunity
DOI 10.1016/j.bbi.2021.04.008
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Abstract

Microglia play key roles in synaptic pruning, which primarily occurs from the postnatal period to adolescence. Synaptic pruning is essential for normal brain development and its impairment is implicated in neuropsychiatric developmental diseases such as autism spectrum disorders (ASD). Recent epidemiological surveys reported a strong link between ASD and atopic/allergic diseases. However, few studies have experimentally investigated the relationship between allergy and ASD-like manifestations, particularly in the early postnatal period, when allergic disorders occur frequently. Therefore, we aimed to characterize how allergic inflammation in the early postnatal period influences microglia and behavior using mouse models of short- and long-term airway allergy. Male mice were immunized by an intraperitoneal injection of aluminum hydroxide and ovalbumin (OVA) or phosphate-buffered saline (control) on postnatal days (P) 3, 7, and 11, followed by intranasal challenge with OVA or phosphate-buffered saline solution twice a week until P30 or P70. In the hippocampus, Iba-1-positive areas, the size of Iba-1-positive microglial cell bodies, and the ramification index of microglia by Sholl analysis were significantly smaller in the OVA group than in the control group on P30 and P70, although Iba-1-positive microglia numbers did not differ significantly between the two groups. In Iba-1-positive cells, postsynaptic density protein 95 (PSD95)-occupied areas and CD68-occupied areas were significantly decreased on P30 and P70, respectively, in the OVA group compared with the control group. Immunoblotting using hippocampal tissues demonstrated that amounts of PSD95, α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor 2, and N-methyl-D-aspartate (NMDA) receptor 2B were significantly increased in the OVA group compared with the control group on P70, and a similar increasing trend for PSD95 was observed on P30. Neurogenesis was not significantly different between the two groups on P30 or P70 by doublecortin immunohistochemistry. The social preference index was significantly lower in the three chamber test and the number of buried marbles was significantly higher in the OVA group than in the control group on P70 but not on P30, whereas locomotion and anxiety were not different between the two groups. Compared with the control group, serum basal corticosterone levels were significantly elevated and hippocampal glucocorticoid receptor (GR) amounts and nuclear GR translocation in microglia, but not in neurons or astrocytes, were significantly decreased in the OVA group on P70 but not on P30. Gene set enrichment analysis of isolated microglia revealed that genes related to immune responses including Toll-like receptor signaling and chemokine signaling pathways, senescence, and glucocorticoid signaling were significantly upregulated in the OVA group compared with the control group on P30 and P70. These findings suggest that early postnatal allergic airway inflammation induces dystrophic microglia that exhibit defective synaptic pruning upon short- and long-term allergen exposure. Furthermore, long-term allergen exposure induced excitatory postsynaptic surplus and ASD-like behavior. Hypothalamo-pituitary-adrenal axis activation and the compensatory downregulation of microglial GR during long-term allergic airway inflammation may also facilitate these changes.

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  • Microglial changes, including abnormal synaptic pruning and altered surveillance, have been reported in several ASD-related models and may disrupt the normal refinement of hippocampal connectivity.

    “Microglial changes, including abnormal synaptic pruning and altered surveillance, have been reported in several ASD-related models and may disrupt the normal refinement of hippocampal connectivity (Saitoh et al., 2021).”

    From Biological hierarchy from genotype to phenotype in syndromic and non-syndromic autism spectrum disorder (2026) · cites this paper as Saitoh et al., 2021

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Sorted by citations

Authors
Saitoh, B.-Y., Tanaka, E., Yamamoto, N., Kruining, D. V., Iinuma, K., Nakamuta, Y., Yamaguchi, H., Yamasaki, R., Matsumoto, K., & Kira, J.-I.
Affiliations
  • Kyushu University (JP)
  • Maastricht University (NL)
Corresponding author
Kira, Jun-ichi
ORCID
Venue
Brain, Behavior, and Immunity
Publisher
Elsevier BV
Published
2021-07
Volume
95
Pages
362-380
ISSN
0889-1591 (ISSN-L)
DOI
10.1016/j.bbi.2021.04.008
OpenAlex
W3156170096
Cited by
47
References
14
Citations by year
2026: 5 · 2025: 5 · 2024: 10 · 2023: 4 · 2022: 19 · 2021: 3
FWCI
3.57
Type
journal article
Language
en
Open access
Licence
Locations
  • Brain Behavior and Immunity (publishedVersion)
  • PubMed (publishedVersion)
  • Research Publications (Maastricht University) (publishedVersion, other-oa)
  • Kyushu University Institutional Repository (QIR) (Kyushu University) (submittedVersion, other-oa)
  • Research Publications (Maastricht University) (submittedVersion)
Funders
  • Japan Agency for Medical Research and Development (JP20ek019308h0003)
  • Japan Society for the Promotion of Science (JP16H02657, JP19H01045)
Topics
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
allergic airway inflammation, microglia, autism spectrum disorder, synaptic pruning, ovalbumin, postpartum period, hippocampus, PSD-95, AMPA receptors, NMDA receptor, social behavior, neurogenesis, microglial ramification, atopy, neuroinflammation
MeSH terms
Animals, Autistic Disorder, Disease Models, Animal, Hypersensitivity, Inflammation, Male, Ovalbumin, Microglia, Mice

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