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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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In the citing paper
“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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BackgroundExcess hydrogen sulfide and polysulfides production underlies a schizophrenia pathophysiology
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Self-citationAutism Spectrum Disorder from the Womb to Adulthood: Suggestions for a Paradigm Shift
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“Maternal cytokines, particularly IL-6, are central in mediating these effects (5).”
BackgroundSocial impairments in autism spectrum disorder are related to maternal immune history profile
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Alterations in plasma cytokine levels in chinese children with autism spectrum disorder
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“…maternal infection and maternal immune activation (MIA) during pregnancy, immune dysregulation, inflammation and microbial dysbiosis, in the etiology of ASD [Onore, Careaga, & Ashwood, 2012; Rossignol & Frye, 2012; Estes & McAllister, 2016; Matelski & Van de Water, 2016; Vuong & Hsiao, 2017].”
BackgroundPurinergic signalling and brain development
Rodrigues, R. J., Marques, J. M., & Cunha, R. A. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.12.001 · Cited by 72
Kentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64
Bauman, M. D., & de Water, J. V. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104864 · Cited by 65
Cattane, N., Vernon, A. C., Borsini, A., Scassellati, C., Endres, D., Capuron, L., Tamouza, R., Benros, M. E., Leza, J. C., Pariante, C. M., et al. (2022) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2022.02.002 · Cited by 67
“13 exploratory behavior, working memory and cognitive flexibility (Estes and McAllister, 2016; Meyer, 2014).”
BackgroundFoo, S., Cambou, M. C., Mok, T., Fajardo, V. M., Jung, K. L., Fuller, T. L., Chen, W., Kerin, T., Mei, J. Y., Bhattacharya, D., et al. (2021) · Cell Reports Medicine · doi:10.1016/j.xcrm.2021.100453 · Cited by 65
Mitochondrial Dysfunction in Schizophrenia
Ni, P., & Chung, S. (2020) · BioEssays · doi:10.1002/bies.201900202 · Cited by 65
Prins, J. R., Eskandar, S., Eggen, B. J. L., & Scherjon, S. A. (2018) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2018.01.004 · Cited by 66
“The combined influence of prenatal and postnatal influence on microglia cell function has been further elaborated by the two-hit theory (Estes and Mcallister, 2016).”
BackgroundInfluentialMiller, G. E., Borders, A. E., Crockett, A. H., Ross, K. M., Qadir, S., Keenan-Devlin, L., Leigh, A. K., Ham, P., Ma, J., Arevalo, J. M. G., et al. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.04.014 · Cited by 62
Sex differences in neuroimmunity as an inherent risk factor
McCarthy, M. M. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0138-1 · Cited by 63
Thion, M. S., Mosser, C., Férézou, I., Grisel, P., Baptista, S., Low, D., Ginhoux, F., Garel, S., & Audinat, É. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.086 · Cited by 64
Microbiota-gut-brain axis in autism spectrum disorder
Yu, Y., & Zhao, F. (2021) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2021.07.001 · Cited by 64
Loayza, M., Lin, S., Carter, K., Ojeda, N. B., Fan, L., Ramarao, S. M., Bhatt, A., & Pang, Y. (2022) · Pediatric Research · doi:10.1038/s41390-022-02239-w · Cited by 62
Sex-specific Behavioral Features of Rodent Models of Autism Spectrum Disorder
Jeon, S. J., Gonzales, E. L., Mabunga, D. F. N., Valencia, S. T., Kim, D. G., Kim, Y., Adil, K. J., Shin, D., Park, D., & Shin, C. Y. (2018) · Experimental Neurobiology · doi:10.5607/en.2018.27.5.321 · Cited by 67
Needham, B. D., Tang, W., & Wu, W. (2018) · Developmental Neurobiology · doi:10.1002/dneu.22581 · Cited by 60
“As a result of the downstream inflammatory cytokine response, the exposed offspring grow up with comprehensive behavioral abnormalities that are similar to ASD and schizophrenia (Estes and McAllister, 2016; Patterson, 2011).”
BackgroundMaternal immune activation impairs cognitive flexibility and alters transcription in frontal cortex
Amodeo, D. A., Lai, C.-Y., Hassan, O., Mukamel, E. A., Behrens, M. M., & Powell, S. B. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.01.025 · Cited by 61
“Rictor is a crucial component defining distinct function of mTOR complex 2 (mTORC2) (Costa-Mattioli and Monteggia, 2013; Estes and McAllister, 2016).”
BackgroundA Revolutionizing Approach to Autism Spectrum Disorder Using the Microbiome
Johnson, D., Letchumanan, V., Thurairajasingam, S., & Lee, L. (2020) · Nutrients · doi:10.3390/nu12071983 · Cited by 64
Jones, H. F., Han, V. X., Patel, S., Gloss, B., Soler, N., Ho, A. C. C., Sharma, S., Kothur, K., Nosadini, M., Wienholt, L. A., et al. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.12.035 · Cited by 58
“(Estes and McAllister, 2016; Dalsgaard et al., 2015; Mataix-Cols et al., 2018) Animal models and early clinical studies demonstrate that cytokines induced by maternal immune activation correlate with altered brain morphology, neural circuits, microglial functioning, behaviour, and cognition in offspring.”
BackgroundKim, K. H., Kim, S. J., Singha, S., Yang, Y. J., Park, S. K., & Ahn, K. H. (2021) · ACS Sensors · doi:10.1021/acssensors.1c00930 · Cited by 57
Yu, D., Li, T., Delpech, J.-C., Zhu, B., Kishore, P., Koshi, T., Luo, R., Pratt, K. J. B., Popova, G., Nowakowski, T. J., et al. (2022) · Science Advances · doi:10.1126/sciadv.abm2545 · Cited by 60
“Epidemiological studies link maternal inflammation to an increased risk of ASD in offspring ( 8 , 56 – 58 ).”
At the crux of maternal immune activation: Viruses, microglia, microbes, and IL‐17A
Otero, A. M., & Antonson, A. M. (2022) · Immunological Reviews · doi:10.1111/imr.13125 · Cited by 57
Neurodevelopmental Effects of Mercury
Oliveira, C. S., Nogara, P. A., Ardisson-Araújo, D. M. P., Aschner, M., da Rocha, J. B. T., & Dórea, J. G. (2018) · Advances in neurotoxicology · doi:10.1016/bs.ant.2018.03.005 · Cited by 59
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript Table 1: Levels of Hg in ASD patients: examples of case-control studies.”
BackgroundInfluentialSex-dependent neurobiological features of prenatal immune activation via TLR7
Missig, G., Robbins, J. O., Mokler, E. L., McCullough, K. M., Bilbo, S. D., McDougle, C. J., & Carlezon, W. A. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0346-4 · Cited by 60
Kowash, H. M., Potter, H. G., Edye, M. E., Prinssen, E. P. M., Bandinelli, S., Neill, J. C., Hager, R., & Glazier, J. D. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.08.006 · Cited by 58
Yan, J.-J., Du, G., Qin, X., & Gao, L. (2019) · International Immunopharmacology · doi:10.1016/j.intimp.2019.106092 · Cited by 60
Ike, K. G. O., de Boer, S. F., Buwalda, B., & Kas, M. J. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.06.030 · Cited by 64
Dang, D., Wang, L., Zhang, C., Li, Z., & Wu, H. M. (2020) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.14406 · Cited by 58
“Overexpression of IL-17 may activate the IL-17 receptor in fetal neurons, leading to cortical dysplasia and behavioral abnormalities in fetuses(26,27) and increasing the possibility that offspring will develop mental illness in adulthood.(28) Meanwhile, exposure to TNF-α can lead to embryonic development disruption an…”
BackgroundP2X7 receptors drive poly(I:C) induced autism-like behavior in mice
Horváth, G., Otrokocsi, L., Bekő, K., Baranyi, M., Kittel, Á., Fritz-Ruenes, P. A., & Sperlágh, B. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1895-18.2019 · Cited by 58
“, 2017), leading to autism-like behavioral symptoms in offspring (Estes and McAllister, 2016).”
BackgroundUnderstanding microglial diversity and implications for neuronal function in health and disease
Schepper, S. D., Crowley, G., & Hong, S. Y. (2020) · Developmental Neurobiology · doi:10.1002/dneu.22777 · Cited by 54
“Systemic inflammation during pregnancy is associated with defects in synaptic connectivity and maturation later in life (Estes & McAllister, 2016; Meyer et al., 2006; Patterson, 2009).”
BackgroundNeuroendocrine-Immune Crosstalk Shapes Sex-Specific Brain Development
Arambula, S. E., & McCarthy, M. M. (2020) · Endocrinology · doi:10.1210/endocr/bqaa055 · Cited by 55
“Epidemiological studies and animal models of MIA have substantiated a role for early aberrant immune activation in the risk of developmental neuropsychiatric disorders, with evidence being most robust for schizophrenia and growing for autism spectrum disorders (ASDs) (117, 118).”
BackgroundChurch, J. S., Tijerina, P. B., Emerson, F. J., Coburn, M. A., Blum, J. L., Zelikoff, J. T., & Schwartzer, J. J. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2017.10.007 · Cited by 59
Gestational cytokine concentrations and neurocognitive development at 7 years
Ghassabian, A., Albert, P. S., Hornig, M., Yeung, E. H., Cherkerzian, S., Goldstein, R. B., Buka, S. L., Goldstein, J. M., & Gilman, S. E. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0112-z · Cited by 56
Association of Maternal Autoimmune Disease With Attention-Deficit/Hyperactivity Disorder in Children
Nielsen, T. C., Nassar, N., Shand, A., Jones, H. F., Guastella, A. J., Dale, R. C., & Lain, S. J. (2021) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2020.5487 · Cited by 60
Prestwood, T. R., Asgariroozbehani, R., Wu, S., Agarwal, S. M., Logan, R. W., Ballon, J. S., Hahn, M., & Freyberg, Z. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.113101 · Cited by 67
Maternal stressors and the developmental origins of neuropsychiatric risk
Khambadkone, S. G., Cordner, Z. A., & Tamashiro, K. L. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2020.100834 · Cited by 61
“, 2018) and maternal immune activation (Bilbo and Schwarz, 2012; Meyer et al., 2009; Solek et al., 2018; Meyer, 2014; Estes and McAllister, 2016) to offspring neuropsychiatric risk have been extensively reviewed.”
BackgroundInfluentialPozzi, D., Rasile, M., Corradini, I., & Matteoli, M. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-01027-6 · Cited by 57
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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