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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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Citations
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“MIA models vary in regards to species, timing and method of immune activation, with the bacterial cell-wall component lipopolysaccharide (LPS) and the double-stranded RNA mimetic polyinosinic:polycytidylic acid (poly(I:C)) being the most common immunostimulants used [9,12].”
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Baby brains reflect maternal inflammation
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“…perinatal exposure to sex steroids (Baron- Cohen et al., 2019; Geier et al., 2012), perinatal exposure to immunological factors (Depino, 2013, 2018; Estes & McAllister, 2016; Hegvik et al., 2018; Spencer & Meyer, 2017) and altered expression of genes involved in immune and glial…”
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“Both genetic variations and environmental factors in early development have been shown to contribute to the pathogenesis of ASD (Abrahams et al, 2013; Sandin et al, 2012; Estes and McAllister, 2016; Boukhris et al, 2016).”
BackgroundSex-Specific Pathways From Prenatal Maternal Inflammation to Adolescent Depressive Symptoms
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“Maternal immune activation in pregnancy is implicated in the pathogenesis of multiple psychopathologies and insults to neuro-development (Estes and McAllister, 2016), and may operate along iron metabolism pathways.”
Does the kynurenine pathway play a pathogenic role in autism spectrum disorder?
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“The gestational day when an inflammatory insult occurs is key for the development of specific outcomes in the offspring (Estes and McAllister, 2016; Guma et al., 2021, 2022).”
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“However, increasing evidence suggests that environmental and immune-related factors also play a crucial role in shaping cognitive development [3–7].”
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“in the structure and function of the fetal central nervous system by inducing chemical mediators and is a risk factor of autism spectrum disorder (ASD) and schizophrenia.(2) MIA is considered to disrupt the”
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“Intrauterine exposure to various pregnancy complications might be critical environmental factors playing a role in the pathogenesis (Alderete et al., 2018; Estes & McAllister, 2016; Maimburg & Vaeth, 2006).”
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Self-citationAltered proteomic profile in umbilical arterial serum from mothers with schizophrenia
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“It has been also demonstrated that maternal infection can interfere with typical development of the immune system and the brain [55].”
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“DISCUSSION MIA is a relatively well-characterized heuristic model in terms of the behavioral similarities to mental illnesses like schizophrenia, bipolar disorder, and depression [8]; MIA leads to maladaptive changes in locomotor behavior, affect, cognitive flexibility, sensorimotor gating, and social interactions [9,…”
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“Moreover, inflammation 91 and oxidative stress 92 , and particularly fetal exposures to inflammation, stress, and hypoxia 93,94 are indeed associated with schizophrenia risk.”
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“Maternal Immune Activation (MIA) hypothesis postulates a pathogenic mechanism leading to excessive stimulation of the maternal immune system during gestation [3].”
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“In particular, the HSPD1 protein, a constitutive mitochondrial heat shock protein expressed in astrocytes, neurons, and other neuronal cells [75], was recently identified as a long-lived protein associated with synapses [73], and its downregulated expression may thus reflect the long-lasting synaptic maldevelopment li…”
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“…cortisol, and prenatal infection have also been linked with schizophrenia, autism spectrum disorder, and attention deficit/hyperactivity disorders (Estes and McAllister, 2016; Kim et al., 2015), further multidisciplinary research is needed within models of prenatal stress and responses to…”
An Overview of Genetic and Environmental Risk of Autism Spectrum Disorder
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Interleukin-17A stimulation induces alterations in Microglial microRNA expression profiles
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“ASD is known to be associated with both environmental and genetic factors 3 , and MIA is an important environmental factor in utero .”
InfluentialAltered brain metabolites in male nonhuman primate offspring exposed to maternal immune activation
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“…bacterial infections leading to activation of the maternal immune response during pregnancy constitute a significant risk for altered brain development and neuro-developmental disorders (NDD) in the offspring (Smith et al., 2007; Estes and McAllister, 2016; Brown and Meyer, 2018; Han et al., 2021).”
Self-citationАлфимова, М. В., Коровайцева, Г. И., Лежейко, Т. В., & Голимбет, В. Е. (2017) · Schizophrenia Research and Treatment · doi:10.1155/2017/5763094 · Cited by 9
“Accordingly, epidemiological data implicate maternal infection as a risk factor for schizophrenia, and animal models corroborate this link showing the impact of maternal immune activation on lifelong neuropathology in offspring [7, 8].”
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Chemical Modulators for Targeting Autism Spectrum Disorders: From Bench to Clinic
Lim, S., & Lee, S. (2022) · Molecules · doi:10.3390/molecules27165088 · Cited by 9
“In line with the outcome of increased ASD risk in offspring by MIA, maternal infection leads to maternal proinflammatory cytokine release and Th17 cell activation, which can heighten the risk for ASD in offspring, combined with the fetus’ immune state and genetic predisposition [109].”
ResultMum's bacteria linked to baby's behaviour
Powell, C. M. (2017) · Nature · doi:10.1038/nature24139 · Cited by 10
Pancaro, C., Boulanger-Bertolus, J., Segal, S., et al. (2019) · Anesthesia & Analgesia · doi:10.1213/ane.0000000000004051 · Cited by 9
Knutson, A. O., & Watters, J. J. (2019) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2019.103361 · Cited by 10
“While considerable evidence exists regarding the detrimental effects of other maternal exposures to stimuli such as infection or pollution during pregnancy on offspring behaviors such as cognitive function, social interaction, and anxiety (Conway and Brown, 2019; Estes and McAllister, 2016; Scola and Duong, 2017; Sole…”
BackgroundDebs, S. R., Conn, I., Navaneethan, B., Penklis, A. G., Meyer, U., Killcross, S., Weickert, C. S., & Purves-Tyson, T. D. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.02.034 · Cited by 9
“…to psychosis) (Zuckerman et al., 2003, Meyer et al., 2008, Vorhees et al., 2015), and working memory deficits that all typically manifest during young adulthood [~postnatal day (PND)60], which are sometimes sex-specific [reviewed in (Meyer, 2014, Estes and McAllister, 2016, Careaga et al., 2017)].”
BackgroundFan, X., Zang, T., Ni, W., Liu, J., Sun, Y., Slack, J., Bai, J., & Liu, Y. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.07.045 · Cited by 9
Fuma, K., Iitani, Y., Imai, K., Ushida, T., Tano, S., Yoshida, K., Yokoi, A., Miki, R., Kidokoro, H., Sato, Y., et al. (2025) · Communications Biology · doi:10.1038/s42003-025-07511-3 · Cited by 10
“Inaddition,mostexperimentalstudieswereconductedusingpoly(I:C),a Toll-likereceptor-3agonist 1,2 .”
Sun, Y., Huang, X., Guo, W., Hong, C., Ji, J., Zhang, X.-Y., Yang, J., Hu, G., & Sun, X. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03409-3 · Cited by 9
Sex-Specific Behavioral Features of the Prenatal Valproic Acid Rat Model of Autism Spectrum Disorder
Mamali, P. M., Dignon, C., Ngwenya, A., & Maseko, B. C. (2025) · Brain Sciences · doi:10.3390/brainsci15040388 · Cited by 9
Szabó, D., Otrokocsi, L., & Sperlágh, B. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03509-0 · Cited by 10
“Increased maternal immune activation in rodents [87, 100] induced by viral infection at a specific time during CNS development has been shown to increase the prevalence of both ASD-or schizophrenia-like symptoms on the offspring.”
The impact of prenatal inflammation on hematopoietic development
Tseng, N. A., & Beaudin, A. E. (2023) · Current Opinion in Hematology · doi:10.1097/moh.0000000000000770 · Cited by 8
Zeng, X., Fan, L., Li, M., Qin, Q., Pang, X., Shi, S., Zheng, D., Jiang, Y., Wang, H., Wu, L., et al. (2024) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2024.109638 · Cited by 7
Hasegawa‐Ishii, S., Komaki, S., Asano, H., Imai, R., & Osaki, T. (2024) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2024.100848 · Cited by 8
“Maternal and neonatal immune activation leads to neuropsychiatric disorders such as autism spectral disorders and schizophrenia (Estes and McAllister, 2016), although the detailed mechanisms are still being examined.”
Women and schizophrenia: planning for the future
Brzezinski‐Sinai, N. A., & Seeman, M. V. (2017) · Future Neurology · doi:10.2217/fnl-2016-0031 · Cited by 8
Immunological Processes in Schizophrenia Pathology: Potential Biomarkers?
Notter, T. (2018) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_43 · Cited by 9
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Cruz-Carrillo, G., & Camacho‐Morales, A. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-02154-3 · Cited by 7
Maternal multiple sclerosis is not a risk factor for neurodevelopmental disorders in offspring
Carta, A., Zarbo, I. R., Scoppola, C., Pisuttu, G., Conti, M., Melis, M. C., Martino, F. D., Serra, A., Biancu, M. A., Guerini, F. R., et al. (2021) · Multiple Sclerosis Journal - Experimental Translational and Clinical · doi:10.1177/20552173211017301 · Cited by 8
“IL-6, IL-17, IL-4) which, by crossing the placenta and acting directly on the developing fetal brain or altering its epigenetic transcript regulation, have detrimental actions in plasticity, neuronal precursors migration, and synaptic pruning.(16,19)”
BackgroundGuan, X., Dan, G., Yang, Y., Ji, Y., Lai, W., Wang, F., Meng, M., Mo, B., Huang, P., You, T., et al. (2021) · Acta Pharmacologica Sinica · doi:10.1038/s41401-021-00772-8 · Cited by 8
Panisi, C., & Marini, M. (2022) · Brain Sciences · doi:10.3390/brainsci12020250 · Cited by 11
Supplementation of PQQ from pregnancy prevents MK-801-induced schizophrenia-like behaviors in mice
Peng, Y., Xu, D. M., Ding, Y., & Zhou, X. (2022) · Psychopharmacology · doi:10.1007/s00213-022-06113-9 · Cited by 9
“2009; Estes and McAllister 2016).”
Birth triggers an inflammatory response in the neonatal periphery and brain
Castillo‐Ruiz, A., Cisternas, C. D., Sturgeon, H., & Forger, N. G. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.05.021 · Cited by 9
Meningeal regulation of infections: A double‐edged sword
Eme‐Scolan, E., Arnaud, L., Haidar, N., Roussel‐Queval, A., & Rua, R. (2023) · European Journal of Immunology · doi:10.1002/eji.202250267 · Cited by 8
The Contribution of Adult Hippocampal Neurogenesis to the Progression of Psychiatric Disorders
Kohman, R. A., & Rhodes, J. S. (2017) · Modern trends in psychiatry · doi:10.1159/000470812 · Cited by 8
Abelson, N., Meiri, G., Solomon, S., Flusser, H., Michaelovski, A., Dinstein, I., & Menashe, I. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.771232 · Cited by 9
“Other studies, including some on animal models, have suggested that maternal immune activation rather than the infection itself is the cause of the elevated risk of ASD (7, 19, 20).”
BackgroundDetection of abnormal behaviors in prenatal Poly(I:C) exposed mice in a group‐rearing environment
Komada, M., Kiriyama, N., Sugiyama, R., Harada, K., & Kawashita, N. (2024) · Congenital Anomalies · doi:10.1111/cga.12563 · Cited by 7
Zhao, M., Yang, J., & Hashimoto, K. (2024) · Advances in pharmacology · doi:10.1016/bs.apha.2024.10.007 · Cited by 7
Maternal COVID-19 infection associated with offspring neurodevelopmental disorders
Duan, L., Yin, H., Liu, J., Wang, W., Huang, P., Liu, L., Shen, J., & Wang, Z. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02822-z · Cited by 8
Tusa, B. S., Alati, R., Betts, K. S., Ayano, G., & Dachew, B. A. (2025) · Australian & New Zealand Journal of Psychiatry · doi:10.1177/00048674251315641 · Cited by 8
“…stress hormones, inflammatory cytokines or neurotransmitter levels (Christian et al., 2009; Oberlander et al., 2008; Talge et al., 2007), potentially disturbing the development of the foetal brain and increasing the risk of ASD (Estes and McAllister, 2016; Kinney et al., 2008; Talge et al., 2007).”
Gestational autoantibody exposure impacts early brain development in a rat model of MAR autism
McLellan, J., Iosif, A., Cichewicz, K., Canales, C. P., Rahbarian, D., Corea, M., Bauman, M. D., Nord, A. S., & de Water, J. V. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-02907-3 · Cited by 7
Microbiome’s effect on white matter in autism
Canada, K., Evans, T. M., & Pelphrey, K. A. (2025) · Journal of Neurophysiology · doi:10.1152/jn.00607.2024 · Cited by 8
Davis, L. K., Ince, L. M., Gullapalli, S., & Fonken, L. K. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.03.005 · Cited by 7
Neural Circuit Mapping and Neurotherapy-Based Strategies
Marei, H. E. S. (2025) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-025-01595-5 · Cited by 13
Ben‐Shabat, S., Yarmolinsky, L., Sharon, N., Zeadnaa-Aldda, T., Dayan, S., Khalfin, B., & Fleisher‐Berkovich, S. (2026) · Biomolecules · doi:10.3390/biom16020225 · Cited by 7
“Neurodegenerative disorders, such as Alzheimer’s disease and Parkinson’s disease, share a prominent component of chronic neuroinflammation [94,95].”
Effects of iTBS-rTMS on the Behavioral Phenotype of a Rat Model of Maternal Immune Activation
Rittweger, N., Ishorst, T., Barmashenko, G., Aliane, V., Winter, C., & Funke, K. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.670699 · Cited by 7
“…a misbalance of excitatory and inhibitory processes, most strikingly evidenced by a reduced function of the interneurons expressing the calcium-binding protein parvalbumin (PV; for review of knowledge obtained from clinical studies and animal models see Lewis et al., 2012; Ferguson and Gao, 2018).”
BackgroundPrenatal stress dysregulates resting-state functional connectivity and sensory motifs
Rezaei, Z., Jafari, Z., Afrashteh, N., Torabi, R., Singh, S., Kolb, B. E., Davidsen, J., & Mohajerani, M. H. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100345 · Cited by 9
“Both human and nonhuman studies point to altered maternal immune activity in PS, which poses offspring at risk for cognitive and behavioral disorders (Estes and McAllister, 2016; Scheinost et al., 2017).”
An introduction to neuroimmunology
Lukens, J. R., & Williams, J. L. (2022) · Immunological Reviews · doi:10.1111/imr.13133 · Cited by 7
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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