Maternal immune activation results in complex microglial transcriptome signature in the adult offspring that is reversed by minocycline treatment
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Maternal immune activation (MIA) during pregnancy has been linked to an increased risk of developing psychiatric pathologies in later life. This link may be bridged by a defective microglial phenotype in the offspring induced by MIA, as microglia have key roles in the development and maintenance of neuronal signaling in the central nervous system. The beneficial effects of the immunomodulatory treatment with minocycline on schizophrenic patients are consistent with this hypothesis. Using the MIA mouse model, we found an altered microglial transcriptome and phagocytic function in the adult offspring accompanied by behavioral abnormalities. The changes in microglial phagocytosis on a functional and transcriptional level were similar to those observed in a mouse model of Alzheimer's disease hinting to a related microglial phenotype in neurodegenerative and psychiatric disorders. Minocycline treatment of adult MIA offspring reverted completely the transcriptional, functional and behavioral deficits, highlighting the potential benefits of therapeutic targeting of microglia in psychiatric disorders.
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Commensal symbiotic bacteria are critical for proper microglial maturation, and induction of infection in pregnant dams can have disruptive effects on the progression of microglial development in offspring.
“While commensal symbiotic bacteria are critical for proper microglial maturation, induction of infection in pregnant dams can have disruptive effects on the progression of microglial development in offspring (Pratt et al., 2013; Matcovitch-Natan et al., 2016; Mattei et al., 2017).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Mattei et al., 2017
Adult MIA offspring exhibit heightened microglial activation, as noted by increased levels of IL-6 and TNF-α.
“Adult MIA offspring exhibit heightened microglial activation, as noted by increased levels of IL-6 and TNF-α (Pratt et al., 2013; Mattei et al., 2017).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Mattei et al., 2017
Maternal immune activation by polyI:C can disrupt pre-microglial development in offspring, leading to a more advanced developmental stage.
“Maternal immune activation (MIA) by administration of polyinosinic:polycytidylic acid (polyI:C), which is a synthetic analog of double-stranded RNA used to simulate viral infections via interaction with TLRs, can disrupt pre-microglial development in offspring, leading to a more advanced developmental stage.”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [59]
Hippocampal microglia from polyI:C offspring show dysregulated genes related to inflammatory response, cell migration, and phagocytosis.
“Hippocampal microglial cells from polyI:C offspring mice showed dysregulation of genes associated with inflammatory response, cell migration and phagocytosis [13, 59, 60].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [59]
Microglia from polyI:C offspring have reduced expression of PU.1 and its target genes, and minocycline restores this expression.
“Microglia from polyI:C offspring had reduced expression of PU.1 and its target genes, which were restored after administration of anti-inflammatory drug minocycline [26, 59].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [59]
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Lampiasi, N., Bonaventura, R., Deidda, I., Zito, F., & Russo, R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032703 · Cited by 39 · see citing works
Microglia sequelae: brain signature of innate immunity in schizophrenia
Rodrigues‐Neves, A. C., Ambrósio, A. F., & Gomes, C. A. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02197-1 · Cited by 34 · see citing works
Maternal viral infection causes global alterations in porcine fetal microglia
Antonson, A. M., Lawson, M. A., Caputo, M. P., Matt, S. M., Leyshon, B. J., & Johnson, R. W. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1817014116 · Cited by 32 · see citing works
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Andoh, M., Ikegaya, Y., & Koyama, R. (2019) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2019.06.012 · Cited by 30 · see citing works
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- Authors
- Mattei, D., Ivanov, A., Ferrai, C., Jordan, P., Guneykaya, D., Buonfiglioli, A., Schaafsma, W., Przanowski, P., Deuther-Conrad, W., Brust, P., Hesse, S., Patt, M., Sabri, O., Ross, T. L., Eggen, B. J. L., Boddeke, E. W. G. M., Kaminska, B., Beule, D., Pombo, A., Kettenmann, H., & Wolf, S. A.
- Affiliations
- Max Delbrück Center (DE)
- Berlin Institute of Health at Charité - Universitätsmedizin Berlin (DE)
- University Medical Center Groningen (NL)
- Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
- Helmholtz-Zentrum Dresden-Rossendorf (DE)
- IFB Adiposity Diseases (DE)
- Leipzig University (DE)
- Medizinische Hochschule Hannover (DE)
- Corresponding author
- Wolf, S A
- ORCID
- Venue
- Translational Psychiatry
- Published
- 2017-05-09
- Volume
- 7
- Issue
- 5
- Pages
- e1120-e1120
- ISSN
- 2158-3188 (ISSN-L)
- PMC
- PMC5534948
- OpenAlex
- W2613880574
- Cited by
- 222
- References
- 86
- Citations by year
- 2026: 16 · 2025: 19 · 2024: 21 · 2023: 26 · 2022: 26 · 2021: 28 · 2020: 37 · 2019: 24 · 2018: 22 · 2017: 3
- FWCI
- 11.73
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Translational Psychiatry (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- Funders
- Deutsche Forschungsgemeinschaft (WO 1418/3-1, SFBTR43)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- maternal immune activation, microglia, microglial transcriptome, minocycline, microglial phagocytosis, adult offspring, mental illness, schizophrenia, brain development, neuroinflammation, behavioral abnormalities, mouse models of Alzheimer's disease
- MeSH terms
- Alzheimer Disease, Animals, Anti-Bacterial Agents, Behavior, Animal, Disease Models, Animal, Female, Humans, Mice, Inbred C57BL, Minocycline, Synaptic Transmission, Phagocytosis, Pregnancy, Schizophrenia, Microglia, Adult Children, Mice, Immune System Phenomena, Transcriptome
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