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Maternal immune activation: Implications for neuropsychiatric disorders
Open accessAbstract
Epidemiological evidence implicates maternal infection as a risk factor for autism spectrum disorder and schizophrenia. Animal models corroborate this link and demonstrate that maternal immune activation (MIA) alone is sufficient to impart lifelong neuropathology and altered behaviors in offspring. This Review describes common principles revealed by these models, highlighting recent findings that strengthen their relevance for schizophrenia and autism and are starting to reveal the molecular mechanisms underlying the effects of MIA on offspring. The role of MIA as a primer for a much wider range of psychiatric and neurologic disorders is also discussed. Finally, the need for more research in this nascent field and the implications for identifying and developing new treatments for individuals at heightened risk for neuroimmune disorders are considered.
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“Current MIA ASD models expose developing rodent pups to bacterial or viral mimetics [126] to elicit strong immune responses.”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [126]
In the citing paper
“MIA can be induced experimentally via immunogens, such as polyinosinic-polycytidylic acid (poly(I:C)) and lipopolysaccharide (LPS).”
From Maternal immune activation dysregulation of the fetal brain transcriptome and relevance to the pathophysiology of autism spectrum disorder (2018) · cites this paper as [29]
In the citing paper
“MIA-induced disruption may work in a manner similar in directionality to rare highly penetrant ASD mutations, and may act as ‘priming’27, 28, 29, 30 or fetal programming21, 22 mechanisms that enhance risk of later developing ASD.”
From Maternal immune activation dysregulation of the fetal brain transcriptome and relevance to the pathophysiology of autism spectrum disorder (2018) · cites this paper as [29]
In the citing paper
“Alterations of the host immune responses by gut microbiota are closely linked to ASD-related symptoms.”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [65]
In the citing paper
“The implicated cytokine pathways include, and not limited to, IL-5, IL-15, IL-17, IL-17a, IL-10, IL-1b, TNF-α, TGF-β1 and IFNγ [12, 18, 65, 66].”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [65]
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Necroptosis: A Novel Pathway in Neuroinflammation
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“Eventually, the effects lead to neuronal and/or axonal degeneration or death (Estes and McAllister, 2016).”
BackgroundLi, N., Yang, J., Zhang, J., Liang, C., Wang, Y., Chen, B., Zhao, C., Wang, J., Zhang, G., Zhao, D., et al. (2019) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2019.01.002 · Cited by 141
“Evidence for the link between ASD and abnormalities in gut microbial function has been accumulating; however, epidemiological and animal studies alone may not be sufficient enough to determine the actual correlations and mechanisms in humans [18].”
BackgroundEmerging role of the host microbiome in neuropsychiatric disorders: overview and future directions
Hashimoto, K. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02287-6 · Cited by 143
“…health issues in women, VMT could emerge as a potential therapeutic option. evidence suggests that maternal immune activation can increase the risk of neuropsychiatric disorders in offspring, including ASD, schizophrenia, and other neurodevelopmental and neuropsychiatric disorders [192, 193].”
BackgroundInflammation of the Embryonic Choroid Plexus Barrier following Maternal Immune Activation
Cui, J., Shipley, F. B., Shannon, M. L., Alturkistani, O., Dani, N., Webb, M. D., Sugden, A. U., Andermann, M. L., & Lehtinen, M. K. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.09.020 · Cited by 128
“Immune system disturbances during development increase the susceptibility of offspring to multiple neurodevelopmental disorders (Ashwood et al., 2006; Estes and McAllister, 2016; Knuesel et al., 2014; Patterson, 2011).”
BackgroundXu, L., Zhang, Y., Li, X., Li, C., Hu, H., Hu, J., Liu, M., Yang, Q. Z., Gu, P., Li, J., et al. (2025) · iMeta · doi:10.1002/imt2.270 · Cited by 143
Purves-Tyson, T. D., Weber‐Stadlbauer, U., Richetto, J., Rothmond, D. A., Labouesse, M. A., Polesel, M., Robinson, K., Weickert, C. S., & Meyer, U. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0434-0 · Cited by 127
“We used the maternal immune activation (MIA) model [2, 34, 35], which was developed based on epidemiological evidence linking MIA with increased risk of schizophrenia and related disorders in the offspring [1, 3].”
Mueller, F. S., Richetto, J., Hayes, L. N., Zambon, A., Pollak, D. D., Sawa, A., Meyer, U., & Weber‐Stadlbauer, U. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.04.019 · Cited by 126
The Impact of Infection in Pregnancy on Placental Vascular Development and Adverse Birth Outcomes
Weckman, A. M., Ngai, M., Wright, J. K., McDonald, C. R., & Kain, K. C. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01924 · Cited by 137
The Role of Microbiome, Dietary Supplements, and Probiotics in Autism Spectrum Disorder
Sivamaruthi, B. S., Suganthy, N., Kesika, P., & Chaiyasut, C. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17082647 · Cited by 133
Jensen, C. S., Bahl, J. M. C., Østergaard, L. B., Høgh, P., Wermuth, L., Heslegrave, A., Zetterberg, H., Heegaard, N. H. H., Hasselbalch, S. G., & Simonsen, A. H. (2019) · Experimental Gerontology · doi:10.1016/j.exger.2019.04.003 · Cited by 125
Mongan, D., Ramesar, M., Föcking, M., Cannon, M., & Cotter, D. (2020) · Early Intervention in Psychiatry · doi:10.1111/eip.12859 · Cited by 123
COVID‐19 in pregnancy: Placental and neonatal involvement
Prochaska, E. C., Jang, M., & Burd, I. D. (2020) · American Journal of Reproductive Immunology · doi:10.1111/aji.13306 · Cited by 119
Acute and chronic neurological consequences of early-life Zika virus infection in mice
Souza, I. N. D. O., Frost, P. S., França, J. V., Nascimento-Viana, J. B., Neris, R. L. S., Oliveira, L. F., Pinheiro, D. J. L. L., Nogueira, C. O., Neves, G. A., Chimelli, L. M. C., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aar2749 · Cited by 117
“Epidemiological and experimental evidence link perinatal infections to the development of neuropsychiatric diseases, including schizophrenia and autism (23), disorders that have, as a common feature, impaired sociability (24).”
BackgroundBacterial Peptidoglycans from Microbiota in Neurodevelopment and Behavior
Gonzalez-Santana, A., & Diaz Heijtz, R. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2020.05.003 · Cited by 118
Cattane, N., Richetto, J., & Cattaneo, A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.001 · Cited by 129
Epigenetic regulation of innate immune memory in microglia
Zhang, X., Kracht, L., Lerário, A. M., Dubbelaar, M. L., Brouwer, N., Wesseling, E. M., Boddeke, E., Eggen, B. J. L., & Kooistra, S. M. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02463-5 · Cited by 116
Fumagalli, M., Lecca, D., Abbracchio, M. P., & Ceruti, S. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00941 · Cited by 125
“…has been indeed reported to cause maternal immune activation (also called mIA) that is associated with later appearance of autism spectrum disorder, and schizophrenia by altering fetal brain development at critical periods of pregnancy (Knuesel et al., 2014; Estes and McAllister, 2016; Table 1).”
BackgroundOxytocin pathways in the intergenerational transmission of maternal early life stress
Töpfer, P., Heim, C. C., Entringer, S., Binder, E. B., Wadhwa, P. D., & Buß, C. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.026 · Cited by 118
Mouse models of maternal immune activation: Mind your caging system!
Mueller, F. S., Polesel, M., Richetto, J., Meyer, U., & Weber‐Stadlbauer, U. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.07.014 · Cited by 111
Gustafsson, H., Sullivan, E. L., Nousen, E. K., Sullivan, C. A., Huang, E., Rincon, M. P., Nigg, J. T., & Loftis, J. M. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.06.011 · Cited by 118
Macrophages on the margin: choroid plexus immune responses
Cui, J., Xu, H., & Lehtinen, M. K. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.07.002 · Cited by 117
Risk of Autism after Prenatal Topiramate, Valproate, or Lamotrigine Exposure
Hernández–Dı́az, S., Straub, L., Bateman, B. T., Zhu, Y., Mogun, H., Wisner, K. L., Gray, K. J., Lester, B. M., McDougle, C. J., DiCesare, E., et al. (2024) · New England Journal of Medicine · doi:10.1056/nejmoa2309359 · Cited by 110
Prenatal environmental risk factors for autism spectrum disorder and their potential mechanisms
Love, C., Sominsky, L., O’Hely, M., Berk, M., Vuillermin, P., & Dawson, S. L. (2024) · BMC Medicine · doi:10.1186/s12916-024-03617-3 · Cited by 110
“It is likely that concurrent risk factors or repeat infections are relevant to ASD susceptibility [57].”
BackgroundThe Major Histocompatibility Complex (MHC) in Schizophrenia: A Review
Mokhtari, R., & Lachman, H. M. (2016) · Journal of Clinical & Cellular Immunology · doi:10.4172/2155-9899.1000479 · Cited by 117
Corradini, I., Focchi, E., Rasile, M., Morini, R., Desiato, G., Tomasoni, R., Lizier, M., Ghirardini, E., Fesce, R., Morone, D., et al. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.09.030 · Cited by 114
Guma, E., Plitman, E., & Chakravarty, M. M. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.06.020 · Cited by 108
Wang, X., Yang, J., Zhang, H., Yu, J., & Yao, Z. (2019) · Autism Research · doi:10.1002/aur.2079 · Cited by 109
“…behavioral phenotypes associated with autism in offspring, has been identified as a vital environmental risk factor for ASD (Choi et al., 2016; Estes & McAllister, 2016; Knuesel et al., 2014; Malkova et al., 2012), in spite of a few clinical epidemiologic studies reporting no association…”
Lammert, C. R., Frost, E. L., Bolte, A. C., Paysour, M. J., Shaw, M. E., Bellinger, C. E., Weigel, T. K., Zunder, E. R., & Lukens, J. R. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701755 · Cited by 105
Hall, M. B., Willis, D. E., Rodriguez, E. L., & Schwarz, J. M. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1135559 · Cited by 117
“Therefore, many important neurodevelopmental processes—neurogenesis, immunogenesis, apoptosis, synaptogenesis— occur during gestation in humans but continue post-birth in rodents (Estes and McAllister, 2016; Guma et al., 2019).”
Background
Metadata
- Authors
- Estes, M. L., & McAllister, A. K.
- Affiliations
- University of California, Davis (US)
- Corresponding author
- McAllister, A. Kimberley
- Venue
- Science
- Published
- 2016-08-19
- Volume
- 353
- Issue
- 6301
- Pages
- 772-777
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC5650490
- OpenAlex
- W2515897135
- Semantic Scholar
- 70e346df06748a0e6435133309a1011e2a43f998
- Cited by
- 1,206
- References
- 86
- Citations by year
- 2026: 109 · 2025: 134 · 2024: 134 · 2023: 128 · 2022: 158 · 2021: 139 · 2020: 119 · 2019: 114 · 2018: 104 · 2017: 54 · 2016: 10
- FWCI
- 5.73
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01-NS060125-05)
- National Institute of Mental Health (P50-MH106438-01)
- Simons Foundation (321998)
- University of California Davis Research Investments in Science and Engineering Program
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- maternal immune activation, maternal infection, autism spectrum disorder, schizophrenia, neuropsychiatric disorders, animal models, neuropathology, neuroimmunological diseases, molecular mechanisms, risk factors
- MeSH terms
- Autism Spectrum Disorder, Adolescent, Animals, Brain, Child, Child, Preschool, Disease Models, Animal, Female, Humans, Immune System, Immune System Diseases, Mothers, Pregnancy, Pregnancy Complications, Infectious, Risk Factors, Schizophrenia, Gastrointestinal Tract, Young Adult
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