Maternal immune activation: Implications for neuropsychiatric disorders
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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 to elicit strong immune responses.
“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]
MIA can be induced experimentally via immunogens such as polyinosinic-polycytidylic acid (poly(I:C)) and lipopolysaccharide (LPS).
“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]
MIA-induced disruption may work in a manner similar in directionality to rare highly penetrant ASD mutations, and may act as 'priming' or fetal programming mechanisms that enhance risk of later developing ASD.
“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]
Alterations of host immune responses by gut microbiota are closely linked to ASD-related symptoms.
“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]
Implicated cytokine pathways include IL-5, IL-15, IL-17, IL-17a, IL-10, IL-1b, TNF-α, TGF-β1 and IFNγ.
“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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“Remarkably, these procedures are sufficient to induce a set of core behavioral deficits related to neurodevelopmental disorders in the adult offspring ( 36, 37 ) .”
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Rudolph, M. D., Graham, A. M., Feczko, E., Miranda-Dominguez, O., Rasmussen, J. M., Nardos, R., Entringer, S., Wadhwa, P. D., Buss, C., & Fair, D. A. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0128-y · Cited by 374 · see citing works
Maternal immune activation and autism spectrum disorder: From rodents to nonhuman and human primates
Careaga, M., Murai, T., & Bauman, M. D. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.10.020 · Cited by 348 · see citing works
Neuron-glia signaling in synapse elimination
Wilton, D. K., Dissing-Olesen, L., & Stevens, B. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050306 · Cited by 332 · see citing works
The ASD Living Biology: from cell proliferation to clinical phenotype
Courchesne, E., Pramparo, T., Gazestani, V. H., Lombardo, M. V., Pierce, K., & Lewis, N. E. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0056-y · Cited by 333 · see citing works
“Current MIA ASD models expose developing rodent pups to bacterial or viral mimetics 126 to elicit strong immune responses.”
The Impact of Systemic Inflammation on Neurodevelopment
Jiang, N. M., Cowan, M. N., Moonah, S. N., & Petri, W. A. (2018) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2018.06.008 · Cited by 330 · see citing works
“Once cytokines are in the brain, how exactly do they exert their effects? One possibility is that inappropriate activation of cytokines may lead to long-lasting changes in expression of immune molecules that regulate neural connectivity and function [11].”
InfluentialPreterm birth and sustained inflammation: consequences for the neonate
Humberg, A., Fortmann, M. I., Siller, B., Kopp, M., Herting, E., Göpel, W., & Härtel, C. (2020) · Seminars in Immunopathology · doi:10.1007/s00281-020-00803-2 · Cited by 312 · see citing works
Microglia and the brain: Complementary partners in development and disease
Hammond, T. R., Robinton, D., & Stevens, B. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100616-060509 · Cited by 288 · see citing works
Behavioral methods to study anxiety in rodents
Lezak, K. R., Missig, G., & Carlezon Jr, W. A. (2017) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2017.19.2/wcarlezon · Cited by 290 · see citing works
Synaptopathology Involved in Autism Spectrum Disorder
Guang, S., Pang, N., Deng, X., Yang, L., He, F. P., Wu, L., Chen, C., Yin, F., & Peng, J. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00470 · Cited by 283 · see citing works
“, 2012), complications during pregnancy (Brown et al., 2014; Estes and McAllister, 2016) and prenatal exposure to psychotropic drugs like valproic acid (VPA) (Rasalam et al.”
BackgroundMaternal Immune Activation and Neuropsychiatric Illness: A Translational Research Perspective
Brown, A. S., & Meyer, U. (2018) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2018.17121311 · Cited by 285 · see citing works
“Although the latter seem to be crucial contributing factors to many associations(2, 15), it is unlikely that distinct pathogens mediate the negative effects of maternal infection on the offspring through the same immune responses and pathophysiological mechanisms(58).”
BackgroundInfluentialGraham, A. M., Rasmussen, J. M., Rudolph, M. D., Heim, C. M., Gilmore, J. H., Styner, M., Potkin, S. G., Entringer, S., Wadhwa, P. D., Fair, D. A., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.05.027 · Cited by 282 · see citing works
Neurobiological bases of autism–epilepsy comorbidity: a focus on excitation/inhibition imbalance
Bozzi, Y., Provenzano, G., & Casarosa, S. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13595 · Cited by 250 · see citing works
Brain changes in a maternal immune activation model of neurodevelopmental brain disorders
Bergdolt, L., & Dunaevsky, A. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.12.002 · Cited by 266 · see citing works
Signalling pathways in autism spectrum disorder: mechanisms and therapeutic implications
Jiang, C.-C., Lin, L., Long, S., Ke, X., Fukunaga, K., Lu, Y., & Han, F. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01081-0 · Cited by 272 · see citing works
“Most cytokines and their receptors are expressed by neurons and glial cells throughout development, and several studies have revealed that cytokines play important roles in neurogenesis, synapse formation, and plasticity, including IL-1β, IL-6, TNF-α, TGF-β1 and IFNγ Cytokines activate several signal transduction path…”
BackgroundThe fetal origins of mental illness
al-Haddad, B. J. S., Oler, E., Armistead, B., Elsayed, N. A., Weinberger, D. R., Bernier, R., Burd, I. D., Kapur, R. P., Jacobsson, B., Wang, C., et al. (2019) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2019.06.013 · Cited by 265 · see citing works
The Immune System, Cytokines, and Biomarkers in Autism Spectrum Disorder
Masi, A., Glozier, N., Dale, R. C., & Guastella, A. J. (2017) · Neuroscience Bulletin · doi:10.1007/s12264-017-0103-8 · Cited by 260 · see citing works
Buss, C., Entringer, S., Moog, N. K., Toepfer, P., Fair, D. A., Simhan, H. N., Heim, C. M., & Wadhwa, P. D. (2017) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2017.03.001 · Cited by 250 · see citing works
Monoamine Neurotransmitters Control Basic Emotions and Affect Major Depressive Disorders
Jiang, Y., Zou, D., Li, Y., Gu, S., Dong, J., Ma, X., Xu, S., Wang, F., & Huang, J. H. (2022) · Pharmaceuticals · doi:10.3390/ph15101203 · Cited by 272 · see citing works
Kentner, A. C., Bilbo, S. D., Brown, A. S., Hsiao, E. Y., McAllister, A. K., Meyer, U., Pearce, B. D., Pletnikov, M. V., Yolken, R. H., & Bauman, M. D. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0185-7 · Cited by 245 · see citing works
“Rather than being a risk factor for a single disease or disorder, MIA may rather be a primer for a range of psychiatric disorders [34, 35].”
Self-citationPriming Microglia for Innate Immune Memory in the Brain
Neher, J. J., & Cunningham, C. M. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.02.001 · Cited by 255 · see citing works
Innate immunity at the crossroads of healthy brain maturation and neurodevelopmental disorders
Zengeler, K. E., & Lukens, J. R. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-020-00487-7 · Cited by 254 · see citing works
IL-6 and IL-8: An Overview of Their Roles in Healthy and Pathological Pregnancies
Vilotić, A., Nacka-Aleksić, M., Pirković, A., Bojić‐Trbojević, Ž., Dekanski, D., & Krivokuća, M. J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232314574 · Cited by 248 · see citing works
Neuroinflammation and Oxidative Stress in the Pathogenesis of Autism Spectrum Disorder
Usui, N., Kobayashi, H., & Shimada, S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065487 · Cited by 267 · see citing works
“MIA also increases the risk of still‐ birth, miscarriage, and intrauterine gro th retardation [9,11].”
BackgroundInfluentialPaolicelli, R. C., & Ferretti, M. T. (2017) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2017.00009 · Cited by 235 · see citing works
Abnormal mTOR Activation in Autism
Winden, K. D., Ebrahimi‐Fakhari, D., & Şahin, M. (2018) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-080317-061747 · Cited by 222 · see citing works
High intelligence: A risk factor for psychological and physiological overexcitabilities
Karpinski, R. I., Kinase Kolb, A. M., Tetreault, N. A., & Borowski, T. B. (2018) · Intelligence · doi:10.1016/j.intell.2017.09.001 · Cited by 217 · see citing works
Microglia Gone Rogue: Impacts on Psychiatric Disorders across the Lifespan
Tay, T. L., Béchade, C., D’Andrea, I., St‐Pierre, M., Henry, M. S., Roumier, A., & Tremblay, M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00421 · Cited by 211 · see citing works
“…in dopaminergic and GABAergic systems, including increased dopaminergic afferences in the nucleus accumbens (NAc) and decreased inhibition of parvalbumin-positive interneurons on cortical pyramidal neurons were also reported (reviewed in Meyer and Feldon, 2009; Estes and McAllister, 2016).”
BackgroundDuan, L., Zhang, X., Miao, W., Sun, Y., Xiong, G., Wu, Q.-Z., Li, G., Yang, P., Yu, H., Li, H., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.08.030 · Cited by 210 · see citing works
Comer, A. L., Carrier, M., Tremblay, M., & Cruz‐Martín, A. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00274 · Cited by 204 · see citing works
Kępińska, A. P., Iyegbe, C. O., Vernon, A. C., Yolken, R., Murray, R. M., & Pollak, T. A. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00072 · Cited by 193 · see citing works
“org 4 MIA cannot be easily modelled in humans and longitudinal, prospective research on effects of infection during pregnancy on human development is scarce (84).”
BackgroundYou’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
Lombardo, M. V., Moon, H. M., Su, J., Palmer, T. D., Courchesne, E., & Pramparo, T. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.15 · Cited by 201 · see citing works
Khan, A. A., Plana‐Ripoll, O., Antonsen, S., Brandt, J. G., Geels, C., Landecker, H. L., Sullivan, P. F., Pedersen, C. B., & Rzhetsky, A. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000353 · Cited by 199 · see citing works
“Historically, most of the attention to the environment as a causal factor in these studies has focused on home or family environments, with an empirically-justified emphasis on childhood adversity and trauma, [16] and, more recently, on prenatal influences [17].”
BackgroundMicroglial immune checkpoint mechanisms
Deczkowska, A., Amit, I., & Schwartz, M. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0145-x · Cited by 185 · see citing works
Programming Bugs: Microbiota and the Developmental Origins of Brain Health and Disease
Codagnone, M. G., Spichak, S., O’Mahony, S. M., O’Leary, O. F., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.014 · Cited by 198 · see citing works
“infections during pregnancy can impact psychiatric outcomes in the children (103).”
BackgroundPrinciples of plasticity in the developing brain
Kolb, B. E., Harker, A., & Gibb, R. L. (2017) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.13546 · Cited by 197 · see citing works
Haddad, F. L., Patel, S. V., & Schmid, S. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.012 · Cited by 195 · see citing works
Maternal inflammation and its ramifications on fetal neurodevelopment
Kwon, H., Choi, G. B., & Huh, J. R. (2022) · Trends in Immunology · doi:10.1016/j.it.2022.01.007 · Cited by 199 · see citing works
Spann, M. N., Monk, C. E., Scheinost, D., & Peterson, B. S. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2272-17.2018 · Cited by 183 · see citing works
“Two of the most frequently released proteins are as follows: interleukin (IL)-6, a proinflammatory cytokine, and C-reactive protein (CRP), an acute phase reactant (Hunter and Jones, 2015; Estes and McAllister, 2016).”
BackgroundRole of the Immune System in the Development of the Central Nervous System
Morimoto, K., & Nakajima, K. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00916 · Cited by 181 · see citing works
“However, epidemiological studies have demonstrated a link between maternal infection and the onset of neurodevelopmental disorders, such as autism spectrum disorder (ASD), schizophrenia, epilepsy, cerebral palsy, anxiety, and major depressive disorder, pointing to the association between the immune system and neural d…”
BackgroundCircadian rhythms and mood disorders: Time to see the light
Dollish, H. K., Tsyglakova, M., & McClung, C. A. (2023) · Neuron · doi:10.1016/j.neuron.2023.09.023 · Cited by 182 · see citing works
Maternal immune activation in neurodevelopmental disorders
Solek, C. M., Farooqi, N., Verly, M., Lim, T. K., & Ruthazer, E. S. (2018) · Developmental Dynamics · doi:10.1002/dvdy.24612 · Cited by 168 · see citing works
“Interactions of genetic predispositions with MIA are likely to be involved in many cases (Knuesel et al., 2014; Estes and McAllister, 2016).”
BackgroundMicroglia and Neurodevelopmental Disorders
Lukens, J. R., & Eyo, U. B. (2022) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-110920-023056 · Cited by 165 · see citing works
Immune Dysregulation in Autism Spectrum Disorder: What Do We Know about It?
Robinson-Agramonte, M. D. L. A., Noris García, E., Fraga Guerra, J., Vega Hurtado, Y., Antonucci, N., Semprún-Hernández, N., Schultz, S., & Siniscalco, D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23063033 · Cited by 176 · see citing works
“maternal autoantibodies being transferred from mother to the fetal central nervous system (CNS), which could affect fetal brain development [5,6].”
BackgroundInfluentialHui, C. W., St-Pierre, A., Hajj, H. E., Remy, Y., Hébert, S. S., Luheshi, G. N., Srivastava, L. K., & Tremblay, M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00013 · Cited by 158 · see citing works
“Epidemiological studies have implicated prenatal infection and immune genes variations, notably of complement component 4 linked to microglial refinement of neuronal circuits, in the development of schizophrenia (Müller et al., 2015; Estes and McAllister, 2016; Hudson and Miller, 2016; Sekar et al., 2016; Srinivas et…”
BackgroundPu, Y., Yang, J., Chang, L., Qu, Y., Wang, S., Zhang, K., Xiong, Z., Zhang, J., Tan, Y., Wang, X., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1922287117 · Cited by 161 · see citing works
Neuropathobiology of COVID-19: The Role for Glia
Tremblay, M.-E., Madore, C., Bordeleau, M., Tian, L., & Verkhratsky, A. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.592214 · Cited by 159 · see citing works
“MIA and its consequences on the CNS have been documented for diverse pathogens such as influenza or bacterial infections, implicating fevers, cytokine storms, and abnormal immune responses in triggering or sustaining a systemic inflammatory state (Reisinger et al., 2015; Estes and McAllister, 2016).”
BackgroundDevelopmental impact of air pollution on brain function
Costa, L. G., Cole, T. B., Dao, K., Chang, Y. C., & Garrick, J. M. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.104580 · Cited by 170 · see citing works
“Studies in humans and in various animal species have demonstrated that maternal immune activation (MIA), due to viral or bacterial infection, increases neuroinflammation in the placenta and in the fetal brain, leading to offspring that display ASD-like behaviors (Malkova et al. 2012; Xuan and Hampson, 2014; Estes and…”
BackgroundNisar, A., Jagtap, S., Vyavahare, S., Deshpande, M., Harsulkar, A., Ranjekar, P. K., & Prakash, O. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1177050 · Cited by 138 · see citing works
“Thus, obesity-induced or direct inflammation during pregnancy make autism, schizophrenia, attention-deficit hyperactivity disorder and major depressive disorder more prevalent (Patterson, 2009; Knuesel et al., 2014; Estes and McAllister, 2016).”
BackgroundMataix-Cols, D., Frans, E., Pérez-Vigil, A., Kuja-Halkola, R., Gromark, C., Isomura, K., Fernández de la Cruz, L., Serlachius, E., Leckman, J. F., Crowley, J. J., et al. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.215 · Cited by 153 · see citing works
Increasing Role of Maternal Immune Activation in Neurodevelopmental Disorders
Boulanger-Bertolus, J., Pancaro, C., & Mashour, G. A. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00230 · Cited by 158 · see citing works
Prenatal Environment and Neurodevelopmental Disorders
Doi, M., Usui, N., & Shimada, S. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.860110 · Cited by 155 · see citing works
Mirabella, F., Desiato, G., Mancinelli, S., Fossati, G., Rasile, M., Morini, R., Markicevic, M., Grimm, C., Amegandjin, C. A., Termanini, A., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.10.006 · Cited by 148 · see citing works
Structural diversity, functional aspects and future therapeutic applications of human gut microbiome
Ghosh, S., & Pramanik, S. (2021) · Archives of Microbiology · doi:10.1007/s00203-021-02516-y · Cited by 149 · see citing works
Gut microbiota changes in children with autism spectrum disorder: a systematic review
Ho, L. K. H., Tong, V. J. W., Syn, N., Nagarajan, N., Tham, E. H., Tay, S. K., Shorey, S., Tambyah, P. A., & Law, E. C. N. (2020) · Gut Pathogens · doi:10.1186/s13099-020-0346-1 · Cited by 149 · see citing works
Carlezon, W. A., Kim, W., Missig, G., Finger, B. C., Landino, S. M., Alexander, A. J., Mokler, E. L., Robbins, J. O., Li, Y., Bolshakov, V. Y., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-53294-z · Cited by 143 · see citing works
Growth and Neurodevelopment of HIV-Exposed Uninfected Children: a Conceptual Framework
Wedderburn, C. J., Evans, C., Yeung, S., Gibb, D. M., Donald, K. A., & Prendergast, A. J. (2019) · Current HIV/AIDS Reports · doi:10.1007/s11904-019-00459-0 · Cited by 141 · see citing works
Targeting gut microbiome: a novel and potential therapy for autism
Yang, Y., Tian, J., & Yang, B. (2018) · Life Sciences · doi:10.1016/j.lfs.2017.12.027 · Cited by 140 · see citing works
On place and time: microglia in embryonic and perinatal brain development
Thion, M. S., & Garel, S. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.10.004 · Cited by 134 · see citing works
Autism Spectrum Disorder as a Brain-Gut-Microbiome Axis Disorder
Saurman, V. E., Margolis, K. G., & Luna, R. A. (2020) · Digestive Diseases and Sciences · doi:10.1007/s10620-020-06133-5 · Cited by 140 · see citing works
Necroptosis: A Novel Pathway in Neuroinflammation
Yu, Z., Jiang, N., Su, W., & Zhuo, Y. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.701564 · Cited by 133 · see citing works
“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 135 · see citing works
“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 · see citing works
“…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 · see citing works
“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 138 · see citing works
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 125 · see citing works
“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 · see citing works
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 127 · see citing works
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 127 · see citing works
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 120 · see citing works
Mongan, D., Ramesar, M., Föcking, M., Cannon, M., & Cotter, D. (2020) · Early Intervention in Psychiatry · doi:10.1111/eip.12859 · Cited by 123 · see citing works
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 120 · see citing works
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 119 · see citing works
“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 · see citing works
Cattane, N., Richetto, J., & Cattaneo, A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.001 · Cited by 118 · see citing works
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 113 · see citing works
Fumagalli, M., Lecca, D., Abbracchio, M. P., & Ceruti, S. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00941 · Cited by 116 · see citing works
“…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 114 · see citing works
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 107 · see citing works
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 109 · see citing works
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 110 · see citing works
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 · see citing works
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 · see citing works
“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 114 · see citing works
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 108 · see citing works
Guma, E., Plitman, E., & Chakravarty, M. M. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.06.020 · Cited by 108 · see citing works
Wang, X., Yang, J., Zhang, H., Yu, J., & Yao, Z. (2019) · Autism Research · doi:10.1002/aur.2079 · Cited by 107 · see citing works
“…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 · see citing works
Hall, M. B., Willis, D. E., Rodriguez, E. L., & Schwarz, J. M. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1135559 · Cited by 112 · see citing works
“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
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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