The DOI matches its Crossref record; 86 of the 86 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,951
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., Codelli, J. A., Chow, J., Reisman, S. E., Petrosino, J. F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.024 · Cited by 3,283
Schizophrenia risk from complex variation of complement component 4
Sekar, A., Bialas, A. R., de Rivera, H., Davis, A., Hammond, T. R., Kamitaki, N., Tooley, K., Presumey, J., Baum, M., Van Doren, V., et al. (2016) · Nature · doi:10.1038/nature16549 · Cited by 2,394
Genetic relationship between five psychiatric disorders estimated from genome-wide SNPs
Cross-Disorder Group of the Psychiatric Genomics Consortium (2013) · Nature Genetics · doi:10.1038/ng.2711 · Cited by 2,263
Abnormal neural oscillations and synchrony in schizophrenia
Uhlhaas, P. J., & Singer, W. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2774 · Cited by 2,120
Zika Virus and Birth Defects — Reviewing the Evidence for Causality
Rasmussen, S. A., Jamieson, D. J., Honein, M. A., & Petersen, L. R. (2016) · New England Journal of Medicine · doi:10.1056/nejmsr1604338 · Cited by 1,989
Evolution of the immune system in humans from infancy to old age
Simon, A. K., Hollander, G. A., & McMichael, A. (2015) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2014.3085 · Cited by 1,796
Trends in the prevalence of developmental disabilities in US children, 1997-2008
Boyle, C. A., Boulet, S., Schieve, L. A., Cohen, R. A., Blumberg, S. J., Yeargin-Allsopp, M., Visser, S., & Kogan, M. D. (2011) · Pediatrics · doi:10.1542/peds.2010-2989 · Cited by 1,732
Maternal Immune Activation Alters Fetal Brain Development through Interleukin-6
Smith, S. E. P., Li, J., Garbett, K., Mirnics, K., & Patterson, P. H. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2178-07.2007 · Cited by 1,605
The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring
Choi, G. B., Yim, Y. S., Wong, H., Kim, S., Kim, H., Kim, S. V., Hoeffer, C. A., Littman, D. R., & Huh, J. R. (2016) · Science · doi:10.1126/science.aad0314 · Cited by 1,214
Flagged first, then by citations
Cited by
Sorted by citations
Items 201–300 of 1,000
Pulli, E. P., Kumpulainen, V., Kasurinen, J. H., Korja, R., Merisaari, H., Karlsson, L., Parkkola, R. K., Saunavaara, J. P., Lähdesmäki, T., Scheinin, N. M., et al. (2018) · Human Brain Mapping · doi:10.1002/hbm.24480 · Cited by 56
“Maternal inflammation has been linked with increased risk of neuropsychiatric disorders (Estes & McAllister, 2016; Li et al., 2016), however debate exists on what biological mechanisms are included in this process (Van der Burg et al., 2016).”
BackgroundMa, M., Ren, Q., Yang, J., Zhang, K., Xiong, Z., Ishima, T., Pu, Y., Hwang, S. H., Toyoshima, M., Iwayama, Y., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1819234116 · Cited by 54
Gestational diabetes mellitus, prenatal air pollution exposure, and autism spectrum disorder
Jo, H., Eckel, S. P., Chen, J., Cockburn, M., Martinez, M. P., Chow, T., Lurmann, F., Funk, W. E., Xiang, A. H., & McConnell, R. (2019) · Environment International · doi:10.1016/j.envint.2019.105110 · Cited by 54
Estes, M. L., Prendergast, K., MacMahon, J. A., Cameron, S., Aboubechara, J. P., Farrelly, K., Sell, G. L., Haapanen, L. A. D., Schauer, J. D., Horta, A., et al. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.04.061 · Cited by 59
“Recently, attention in the MIA field has started to shift toward studying resilience and susceptibility in large part because of recurring issues of reproducibility stemming from heterogeneous and sometimes opposing findings in MIA offspring (Estes and McAllister, 2016; Harvey and Boksa, 2012; Kentner et al., 2019; Me…”
BackgroundMethodSelf-citationMissig, G., Mokler, E. L., Robbins, J. O., Alexander, A. J., McDougle, C. J., & Carlezon, W. A. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.243 · Cited by 54
Careaga, M., Taylor, S. L., Chang, C., Chiang, A., Ku, K. M., Berman, R. F., de Water, J. V., & Bauman, M. D. (2018) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2018.06.014 · Cited by 53
Su, Z., Frost, E. L., Lammert, C. R., Przanowska, R. K., Lukens, J. R., & Dutta, A. (2020) · RNA Biology · doi:10.1080/15476286.2020.1721047 · Cited by 53
Pregnancy-Related Extracellular Vesicles Revisited
Condrat, C. E., Varlas, V. N., Duică, F., Antoniadis, P., Dănilă, C. A., Crețoiu, D., Suciu, N., Creţoiu, S. M., & Voinea, S. C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22083904 · Cited by 55
“Moreover, factors such as low socioeconomic status, poor diet, high levels of stress can also elicit maternal inflammatory responses expressed by elevated IL-6 levels [143], that do not necessarily culminate in preterm birth [157], but rather in altered neurodevelopment in infants, ascertained by decreased working mem…”
BackgroundMaternal Immune Activation and Schizophrenia–Evidence for an Immune Priming Disorder
Choudhury, Z., & Lennox, B. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.585742 · Cited by 52
Microglial ontogeny, diversity and neurodevelopmental functions
Thion, M. S., & Garel, S. (2020) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.06.013 · Cited by 58
Amegandjin, C. A., Choudhury, M., Jadhav, V., Carriço, J. N., Quintal, A., Berryer, M. H., Snapyan, M., Chattopadhyaya, B., Saghatelyan, A., & Cristo, G. D. (2021) · Nature Communications · doi:10.1038/s41467-021-23939-7 · Cited by 53
Theoharides, T. C., Twahir, A., & Kempuraj, D. (2023) · Annals of Allergy Asthma & Immunology · doi:10.1016/j.anai.2023.10.032 · Cited by 58
Modeling autism in non‐human primates: Opportunities and challenges
Zhao, H., Jiang, Y., & Zhang, Y. (2018) · Autism Research · doi:10.1002/aur.1945 · Cited by 53
“Prenatal MIA has also been linked to altered brain development and behavior abnormalities in humans and animal models [Estes & McAllister, 2016; Kim et al., 2017].”
Autoimmune phenotypes in schizophrenia reveal novel treatment targets
Severance, E. G., Dickerson, F., & Yolken, R. H. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.05.005 · Cited by 52
“The focus of this review is on identifying autoimmune conditions in people with schizophrenia with a direction toward identification of new treatments; however, it should be noted that there is also a large literature base about prenatal exposures to specific microbes and to the infectious disease process as a risk fa…”
Luan, W., Hammond, L. A., Vuillermot, S., Meyer, U., & Eyles, D. W. (2018) · Scientific Reports · doi:10.1038/s41598-018-28090-w · Cited by 55
All Together Now: Modeling the Interaction of Neural With Non-neural Systems Using Organoid Models
Chukwurah, E., Osmundsen, A. M., Davis, S. W., & Lizarraga, S. B. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00582 · Cited by 51
“However, it is not the only example, as several studies have shown that inflammation during pregnancy increases the risk for neuropsychiatric disorders, such as autism and schizophrenia (Estes and McAllister, 2016; Careaga et al., 2017).”
BackgroundRibeiro, V. T., de Souza, L. C., & Silva, A. C. S. E. (2019) · Protein and Peptide Letters · doi:10.2174/0929866527666191230103739 · Cited by 50
Clark, S. M., Notarangelo, F. M., Li, X., Chen, S., Schwarcz, R. M., & Tonelli, L. H. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.09.011 · Cited by 50
Step by step: cells with multiple functions in cortical circuit assembly
Cossart, R., & Garel, S. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00585-6 · Cited by 54
Hadar, R., Dong, L., Del-Valle-Anton, L., Güneykaya, D., Voget, M., Edemann-Callesen, H., Schweibold, R., Djodari-Irani, A., Goetz, T., Ewing, S. G., et al. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.12.003 · Cited by 56
Bacterial peptidoglycans as novel signaling molecules from microbiota to brain
Tosoni, G., Conti, M., & Heijtz, R. D. (2019) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2019.08.003 · Cited by 54
Xia, Y., Zhang, Z.-Q., Lin, W.-P., Yan, J., Zhu, C., Yin, D., He, S., Su, Y., Xu, N., Caldwell, R. W., et al. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0743-7 · Cited by 52
“Studies in animal models have identified that maternal immune activation (MIA) alone is sufficient to induce fetal brain developmental abnormalities and behavior deficits in later life [5].”
BackgroundResultPrenatal origins of neuropsychiatric diseases
Amgalan, A., Andescavage, N. N., & Limperopoulos, C. (2021) · Acta Paediatrica · doi:10.1111/apa.15766 · Cited by 55
Zimmer, A., Youngblood, A., Adnane, A., Miller, B. J., & Goldsmith, D. R. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.10.024 · Cited by 50
Neuroimmunology of the female brain across the lifespan: Plasticity to psychopathology
Barrientos, R. M., Brunton, P. J., Lenz, K. M., Pyter, L. M., & Spencer, S. J. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.03.010 · Cited by 50
“Early life inflammation is a risk factor for neurodevelopmental disorders, such as autism spectrum disorder, schizophrenia, attention deficit hyperactivity disorder (ADHD), and Tourette’s syndrome (Estes and McAllister, 2016).”
BackgroundNovel treatments for autism spectrum disorder based on genomics and systems biology
Baribeau, D. A., & Anagnostou, E. A. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107939 · Cited by 51
Prenatal stress impacts foetal neurodevelopment: Temporal windows of gestational vulnerability
Collins, J. M., Keane, J. M., Deady, C., Khashan, A. S., McCarthy, F. P., O’Keeffe, G. W., Clarke, G. A., Cryan, J. F., Caputi, V., & O’Mahony, S. M. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105793 · Cited by 52
Why are behavioral and immune traits linked?
Lopes, P. C. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.09.008 · Cited by 50
Evaluation and Management of the Child With Autism Spectrum Disorder
Baumer, N., & Spence, S. J. (2018) · CONTINUUM Lifelong Learning in Neurology · doi:10.1212/con.0000000000000578 · Cited by 55
Matsuura, A., Ishima, T., Fujita, Y., Iwayama, Y., Hasegawa, S., Kawahara‐Miki, R., Maekawa, M., Toyoshima, M., Ushida, Y., Suganuma, H., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-20538-3 · Cited by 50
Kuo, H., & Liu, F. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00422 · Cited by 48
Murray, A. L., Kaiser, D. E., Valdebenito, S., Hughes, C. H., Băban, A., Fernando, A. D., Madrid, B. J., Ward, C. L., Osafo, J., Dunne, M. P., et al. (2018) · Trauma Violence & Abuse · doi:10.1177/1524838018813563 · Cited by 54
Advances in Biomarker Studies in Autism Spectrum Disorders
Shen, L., Zhao, Y., Zhang, H., Feng, C., Gao, Y. L., Zhao, D., Xia, S., Qi, H., Iqbal, J., Liu, X., et al. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-05542-4_11 · Cited by 48
Understanding Vulnerability and Adaptation in Early Brain Development using Network Neuroscience
Graham, A. M., Marr, M. C., Buß, C., Sullivan, E. L., & Fair, D. A. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.01.008 · Cited by 50
Maternal effects in mammals: Broadening our understanding of offspring programming
Edwards, P. D., Lavergne, S. G., McCaw, L. K., Wijenayake, S., Boonstra, R., McGowan, P. O., & Holmes, M. M. (2021) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2021.100924 · Cited by 49
Microglia Modulate Neurodevelopment in Autism Spectrum Disorder and Schizophrenia
Fan, G., Ma, J., Ma, R., Suo, M., Chen, Y., Zhang, S., Zeng, Y., & Chen, Y. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242417297 · Cited by 52
“Emerging research underscores the relevance of the complement system in SZ, high-lighting the potential diagnostic and therapeutic power of monitoring and modulating microglial synaptic pruning within this framework.”
BackgroundAlteration of Gut Microbiota in Autism Spectrum Disorder: An Overview
Oh, D., & Cheon, K.-A. A. (2020) · Journal of korean Academy of Child and Adolescent Psychiatry · doi:10.5765/jkacap.190039 · Cited by 53
Eng, M. E., Império, G. E., Bloise, E., & Matthews, S. G. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04432-w · Cited by 49
IL-4 Shapes Microglia-Dependent Pruning of the Cerebellum During Postnatal Development
Guedes, J. R., Ferreira, P. A., Costa, J., Laranjo, M., Pinto, M. J., Reis, T., Cardoso, A. M., Lebre, C., Casquinha, M., Gomes, M. A., et al. (2022) · Neuron · doi:10.1016/j.neuron.2023.09.031 · Cited by 47
Review of Clinical Studies Targeting Inflammatory Pathways for Individuals With Autism
Hafizi, S., Tabatabaei, D., & Lai, M. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00849 · Cited by 47
Interoception and Inflammation in Psychiatric Disorders
Savitz, J., & Harrison, N. A. (2018) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2017.12.011 · Cited by 126
“immune activation leads to changes in synaptic connectivity and neuroplasticity that may manifest as changes in cortical thickness and brain volume (65).”
InfluentialCOVID-19 during pregnancy: Potential risk for neurodevelopmental disorders in neonates?
Martins‐Filho, P. R., Tanajura, D. M., Junior, H. P. D. O. S., et al. (2020) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2020.05.015 · Cited by 45
“Maternal immune activation appears to act as a “neurodevelopmental disease primer” increasing the susceptibility of individuals to the epigenetic alterations and environmental exposures that can interact in triggering disease-related symptoms later in life [4].”
Increased RNA editing in maternal immune activation model of neurodevelopmental disease
Tsivion-Visbord, H., Kopel, E., Feiglin, A., Sofer, T., Barzilay, R., Ben‐Zur, T., Yaron, O., Offen, D., & Levanon, E. Y. (2020) · Nature Communications · doi:10.1038/s41467-020-19048-6 · Cited by 43
Hameete, B. C., Fernández‐Calleja, J. M. S., de Groot, M. W. G. D. M., Oppewal, T. R., Tiemessen, M. M., Hogenkamp, A., de Vries, R. B. M., & Groenink, L. (2020) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2020.100192 · Cited by 50
Between Dysbiosis, Maternal Immune Activation and Autism: Is There a Common Pathway?
Suprunowicz, M., Tomaszek, N., Urbaniak, A., Zackiewicz, K., Modzelewski, S., & Waszkiewicz, N. (2024) · Nutrients · doi:10.3390/nu16040549 · Cited by 44
“Maternal immune activation (MIA) is considered to be a disease primer, making offspring more susceptible to other risk factors, like genetic and environmental ones [10].”
BackgroundMicroglia: Synaptic modulator in autism spectrum disorder
Hu, C., Li, H., Li, J., Luo, X., & Hao, Y. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.958661 · Cited by 50
Sleep as a translationally-relevant endpoint in studies of autism spectrum disorder (ASD)
Missig, G., McDougle, C. J., & Carlezon, W. A. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0409-5 · Cited by 49
Nakahara, K., Michikawa, T., Morokuma, S., Ogawa, M., Kato, K., Sanefuji, M., Shibata, E., Tsuji, M., Shimono, M., Kawamoto, T., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-67852-3 · Cited by 44
The Role of Zebrafish and Laboratory Rodents in Schizophrenia Research
Langová, V., Valeš, K., Horká, P., & Horáček, J. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00703 · Cited by 45
Immune regulation of neurodevelopment at the mother–foetus interface: the case of autism
Sotgiu, S., Manca, S., Gagliano, A., Minutolo, A., Melis, M. C., Pisuttu, G., Scoppola, C., Bolognesi, E., Clerici, M., Guerini, F. R., et al. (2020) · Clinical & Translational Immunology · doi:10.1002/cti2.1211 · Cited by 46
“common infections or a mere cytokine imbalance) may have deleterious consequences on early neurodevelopment.(17,18) The vast majority of women experience at least one infection during gestation, and thus, most”
BackgroundNotaras, M. J., Lodhi, A., Barrio-Alonso, E., Foord, C., Rodrick, T. C., Jones, D. R., Fang, H., Greening, D. W., & Colak, D. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01189-9 · Cited by 45
Pediatric Acute-Onset Neuropsychiatric Syndrome: Current Perspectives
Gagliano, A., Carta, A., Tanca, M. G., & Sotgiu, S. (2023) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s362202 · Cited by 43
“According to this frame, upregulation of genes related to microglial function can sustain inflammatory pathways in response to environmental factors, such as infections, leading to alterations of synaptic pruning, neuronal differentiation, and neural circuit formation in the perinatal and postnatal periods.(103)”
BackgroundPrenatal air pollution, maternal immune activation, and autism spectrum disorder
Yu, X., Rahman, M. M., Carter, S., Lin, J. C., Zhuang, Z., Chow, T., Lurmann, F., Kleeman, M. J., Martinez, M. P., van Donkelaar, A., et al. (2023) · Environment International · doi:10.1016/j.envint.2023.108148 · Cited by 47
Miyaoka, T., Wake, R., Hashioka, S., Hayashida, M., Oh‐Nishi, A., Azis, I. A., Izuhara, M., Tsuchie, K., Araki, T., Arauchi, R., et al. (2017) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2017.00174 · Cited by 46
Camargos, V. N., Foureaux, G., Medeiros, D. D. C., da Silveira, V. T., Queiroz‐Junior, C. M., Matosinhos, A. L. B., Figueiredo, A. F. A., de Sousa, C. D. F., Moreira, T. P., Queiroz, V. F., et al. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.05.014 · Cited by 43
“MIA is considered a risk factor for neurodevelopmental and psychiatric disorders during adulthood, including schizophrenia, depression, and anxiety [4,5].”
BackgroundMaternal immune activation primes deficiencies in adult hippocampal neurogenesis
Couch, A. C. M., Berger, T., Hanger, B., Matulevičiūtė, R., Srivastava, D. P., Thuret, S., & Vernon, A. C. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.07.021 · Cited by 44
Guma, E., Bordeleau, M., Ibáñez, F. G., Picard, K., Snook, E., Desrosiers-Grégoire, G., Spring, S., Lerch, J. P., Nieman, B. J., Devenyi, G. A., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2114545119 · Cited by 42
Jacobsen, H., Gnirß, K., Tekin-Bubenheim, N., Kouassi, N. M., Batalla, I. B., Berenbrok, N., Wolff, M., dos Reis, V. P., Zickler, M., Scholl, L., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25220-3 · Cited by 43
Microglia and Sensitive Periods in Brain Development
Dziabis, J. E., & Bilbo, S. D. (2021) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2021_242 · Cited by 42
Sensorimotor gating deficits in “two-hit” models of schizophrenia risk factors
Khan, A., & Powell, S. B. (2017) · Schizophrenia Research · doi:10.1016/j.schres.2017.10.009 · Cited by 47
Bench to bedside review: Possible role of vitamin D in autism spectrum disorder
Jia, F., Shan, L., Wang, B., Li, H., Miao, C., Xu, Z., Lin, C., & Saad, K. (2017) · Psychiatry Research · doi:10.1016/j.psychres.2017.12.005 · Cited by 44
Zhao, X., Mohammed, R., Tran, H., Erickson, M., & Kentner, A. C. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.03.018 · Cited by 44
Neurodevelopmental delay in children exposed to maternal SARS-CoV-2 in-utero
Fajardo, V. M., Ferreira, F., Fuller, T. L., Cambou, M. C., Kerin, T., Paiola, S. G., Mok, T., Rao, R., Mohole, J., Paravastu, R., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-61918-2 · Cited by 68
“…implicated in the pathogenesis of infant central nervous system disorders, with data suggesting higher risk of future pervasive neurodevelopmental or neuropsychiatric conditions such as autism spectrum disorder, schizophrenia, and cerebral palsy among many neurodevelopmental problems 5,6,32–36 .”
BackgroundBauman, M. D., Lesh, T. A., Rowland, D. J., Schumann, C. M., Smucny, J., Kukis, D. L., Cherry, S. R., McAllister, A. K., & Carter, C. S. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0449-y · Cited by 43
Self-citationDavis, J. M., & Mire, E. (2021) · Brain and Neuroscience Advances · doi:10.1177/23982128211003484 · Cited by 40
“Infection during pregnancy is associated with increased risk for neurodevelopmental and neuropsychiatric disorders including ASD, schizophrenia, childhood depression and bipolar disorders (Brown and Meyer, 2018; Estes and McAllister, 2016).”
BackgroundBach, A., Xie, W., Piazzoli, L., Jensen, S. K. G., Afreen, S., Haque, R., Petri, W. A., & Nelson, C. A. (2021) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2021.101041 · Cited by 45
Rubio, R., Aguilar, R., Bustamante, M., Muñoz, E., Vázquez-Santiago, M., Santano, R., Vidal, M., Melero, N. R., Parras, D., Serra, P., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.999136 · Cited by 38
The Many Faces of Microbiota-Gut-Brain Axis in Autism Spectrum Disorder
Gonçalves, C. L., Doifode, T., Rezende, V. L., Costa, M. A., Rhoads, J. M., & Soutullo, C. A. (2024) · Life Sciences · doi:10.1016/j.lfs.2023.122357 · Cited by 42
Dissecting the Meanings of “Physiology” to Assess the Vitality of the Discipline
Lemoine, M., & Pradeu, T. (2018) · Physiology · doi:10.1152/physiol.00015.2018 · Cited by 41
“An example is provided by studies of interactions between the immune and neurological systems in the onset of mental disorders (26, 33, 38).”
Han, V. X., Jones, H. F., Patel, S., Mohammad, S. S., Hofer, M. J., Alshammery, S., Maple-Brown, E., Gold, W. A., Brilot, F., & Dale, R. C. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.09.009 · Cited by 41
The GABA Developmental Shift Is Abolished by Maternal Immune Activation Already at Birth
Fernandez, A., Dumon, C., Guimond, D., Tyzio, R., Bonifazi, P., Lozovaya, N., Burnashev, N., Ferrari, D. C., & Ben‐Ari, Y. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy279 · Cited by 42
From Infection to the Microbiome: An Evolving Role of Microbes in Schizophrenia
Severance, E. G., & Yolken, R. H. (2019) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_84 · Cited by 40
Hashimoto, K. (2019) · Current Psychiatry Reports · doi:10.1007/s11920-019-1063-7 · Cited by 39
Viral Infections and Schizophrenia: A Comprehensive Review
Kotsiri, I., Resta, P., Spyrantis, A., Panotopoulos, C., Chaniotis, D. I., Beloukas, A. I., & Magiorkinis, E. (2023) · Viruses · doi:10.3390/v15061345 · Cited by 40
Schizophrenia, a disease of impaired dynamic metabolic flexibility: A new mechanistic framework
Sarnyai, Z., & Ben‐Shachar, D. (2024) · Psychiatry Research · doi:10.1016/j.psychres.2024.116220 · Cited by 39
“Maternal viral and bacterial infection, and resulting immune activation, has been identified as an important risk factor for schizophrenia (Brown and Meyer 2018; Estes and McAllister 2016).”
BackgroundCrosstalk between the immune, endocrine, and nervous systems in immunotoxicology
MANLEY, K. M., Han, W., Zelin, G., & Lawrence, D. A. (2017) · Current Opinion in Toxicology · doi:10.1016/j.cotox.2017.12.003 · Cited by 38
Morais, L. H., Felice, D., Golubeva, A. V., Moloney, G. M., Dinan, T. G., & Cryan, J. F. (2018) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000374 · Cited by 40
“Previous research in MIA animal models reproduced many of the core ASD and SZ symptoms showing important construct, face and predictive validity to the model (Meyer, 2014; Estes and McAllister, 2016).”
BackgroundResultInfluentialEndogenous Retroviruses Activity as a Molecular Signature of Neurodevelopmental Disorders
Balestrieri, E., Matteucci, C., Cipriani, C., Grelli, S., Ricceri, L., Calamandrei, G., & Vallebona, P. S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20236050 · Cited by 38
Chen, H., Chen, C., Mandhani, N., Short-Miller, J. C., Smucker, M. R., Sun, Y., & Kuan, C.-Y. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1171-20.2020 · Cited by 40
“Likewise, the pathogenesis of ASD involves complex interactions of genetic, immune, and environmental factors (Geschwind, 2009; De Rubeis et al., 2014; Estes and McAllister, 2016).”
BackgroundAbruzzo, P. M., Panisi, C., & Marini, M. (2021) · Antioxidants · doi:10.3390/antiox10081316 · Cited by 41
“This effect, likely mediated by the pro-inflammatory cytokine IL-1β, which downregulates the transcription of KCC2, is particularly relevant because MIA is one of the more promising murine models of Autistic Spectrum Disorders (ASD) [41], but has also been linked to enhanced risk of schizophrenia in humans [42].”
BackgroundSequential perturbations to mouse corticogenesis following in utero maternal immune activation
Canales, C. P., Estes, M. L., Cichewicz, K., Angara, K., Aboubechara, J. P., Cameron, S., Prendergast, K., Su-Feher, L., Zdilar, I., Kreun, E. J., et al. (2021) · eLife · doi:10.7554/elife.60100 · Cited by 43
Self-citationNour‐Eldine, W., Ltaief, S. M., Manaph, N. P. A., & Al‐Shammari, A. R. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.950275 · Cited by 40
Batorsky, R., Ceasrine, A. M., Shook, L. L., Kışlal, S., Bordt, E. A., Devlin, B. A., Perlis, R. H., Slonim, D. K., Bilbo, S. D., & Edlow, A. G. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114326 · Cited by 38
Consequences of gestational diabetes to the brain and behavior of the offspring
Sousa, R. A. L. D., TORRES, Y. S., Figueiredo, C. P., Passos, G. F., & Clarke, J. R. (2017) · Anais da Academia Brasileira de Ciências · doi:10.1590/0001-3765201720170264 · Cited by 41
T he microglial reaction signature revealed by RNA seq from individual mice
Hirbec, H., Marmai, C., Duroux-Richard, I., Roubert, C., Esclangon, A., Croze, S., Lachuer, J., Peyroutou, R., & Rassendren, F. (2018) · Glia · doi:10.1002/glia.23295 · Cited by 39
“…for which cell surface markers are available and have been used for purification and genome-wide transcriptome profiling (Bennett et al., 2016; Beutner et al., 2013; Butovsky et al., 2014; Chiu et al., 2013; Gautier et al., 2012; Hickman et al., 2013; Srinivasan et al., 2016; Zhang et al., 2014).”
BackgroundMethodThe role of microbiota in autism spectrum disorders
Campion, D., Ponzo, P., Alessandria, C., Saracco, G. M., & Balzola, F. A. (2018) · Minerva Gastroenterologica e Dietologica · doi:10.23736/s1121-421x.18.02493-5 · Cited by 40
“MIA offspring show abnormal communication and sociability, repetitive behaviors and increased anxiety.(20)”
BackgroundDeciphering microbiome and neuroactive immune gene interactions in schizophrenia
Severance, E. G., & Yolken, R. H. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.11.016 · Cited by 41
Openshaw, R. L., Kwon, J., McColl, A., Penninger, J. M., Cavanagh, J., Pratt, J. A., & MORRIS, B. J. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1408-5 · Cited by 36
Gubert, C., Kong, G., Uzungil, V., Zeleznikow-Johnston, A., Burrows, E. L., Renoir, T., & Hannan, A. J. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.582320 · Cited by 38
Golovina, E., Fadason, T., Lints, T., Walker, C. G., Vickers, M. H., & O'Sullivan, J. M. (2021) · Scientific Reports · doi:10.1038/s41598-021-95447-z · Cited by 37
Figueiredo, C. P., Fontes-Dantas, F. L., Poian, A. T. D., & Clarke, J. R. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108841 · Cited by 37
Astrocytes and Microglia in Stress-Induced Neuroinflammation: The African Perspective
Olude, M. A., Mouihate, A., Mustapha, O. A., Farina, C., Quintana, F. J., & Olopade, J. O. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.795089 · Cited by 37
Hsueh, P., Wang, H., Liu, C., Ni, W.-F., Chen, Y., & Liu, J. (2017) · PLoS ONE · doi:10.1371/journal.pone.0179970 · Cited by 37
Maternal Overnutrition Programs Central Inflammation and Addiction-Like Behavior in Offspring
Montalvo-Martínez, L., Maldonado‐Ruiz, R., Cárdenas‐Tueme, M., Reséndez‐Pérez, D., & Camacho‐Morales, A. (2018) · BioMed Research International · doi:10.1155/2018/8061389 · Cited by 42
“Substantial scientific evidence has shown that neuroinflammation commands changes in cerebral plasticity and influences synaptic function andmemory [72].”
BackgroundSaad, K., Abdallah, A. M., Abdelrahman, A. A., Al-Atram, A. A., Abdel-Raheem, Y. F., Gad, E. F., Abo‐Elela, M. G. M., Elserogy, Y., Elhoufey, A. A., Nigm, D. A., et al. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109999 · Cited by 37
Gesù, C. M. D., Matz, L. M., & Buffington, S. A. (2021) · Neuroscience Research · doi:10.1016/j.neures.2021.05.003 · Cited by 47
Breen, M. S., Wingo, A. P., Koen, N., Donald, K. A., Nicol, M., Zar, H. J., Ressler, K. J., Buxbaum, J. D., & Stein, D. J. (2018) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.05.016 · Cited by 35
The impact of (ab)normal maternal environment on cortical development
Vasistha, N. A., & Khodosevich, K. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.102054 · Cited by 38
Hasegawa, Y., Ma, M., Sawa, A., Lane, A. P., & Kamiya, A. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02081-y · Cited by 40
Cipriani, C., Ricceri, L., Matteucci, C., Felice, A. D., Tartaglione, A. M., Argaw-Denboba, A., Pica, F., Grelli, S., Calamandrei, G., Vallebona, P. S., et al. (2018) · Scientific Reports · doi:10.1038/s41598-017-19035-w · Cited by 36
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
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
