The role of IL-6 in neurodevelopment after prenatal stress

Gumusoglu, Serena B.; Fine, Rebecca S.; Murray, Samuel J.; Bittle, Jada L.; Stevens, Hanna E.

doi:10.1016/j.bbi.2017.05.015

Cited by 129Neuroinflammation and Neurodegeneration MechanismsStress Responses and CortisolTryptophan and brain disorders

The role of IL-6 in neurodevelopment after prenatal stress

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Gumusoglu, Serena B., Fine, Rebecca S., Murray, Samuel J., Bittle, Jada L., Stevens, Hanna E.·2017·Brain, Behavior, and Immunity

DOI 10.1016/j.bbi.2017.05.015PMC PMC5537020

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Abstract

Prenatal stress exposure is associated with adverse psychiatric outcomes, including autism and ADHD, as well as locomotor and social inhibition and anxiety-like behaviors in animal offspring. Similarly, maternal immune activation also contributes to psychiatric risk and aberrant offspring behavior. The mechanisms underlying these outcomes are not clear. Offspring microglia and the pro-inflammatory cytokine interleukin-6 (IL-6), known to influence microglia, may serve as common mechanisms between prenatal stress and prenatal immune activation. To evaluate the role of prenatal IL-6 in prenatal stress, microglia morphological analyses were conducted at embryonic days 14 (E14), E15, and in adult mice. Offspring microglia and behavior were evaluated after repetitive maternal restraint stress, repetitive maternal IL-6, or maternal IL-6 blockade during stress from E12 onwards. At E14, novel changes in cortical plate embryonic microglia were documented-a greater density of the mutivacuolated morphology. This resulted from either prenatal stress or IL-6 exposure and was prevented by IL-6 blockade during prenatal stress. Prenatal stress also resulted in increased microglia ramification in adult brain, as has been previously shown. As with embryonic microglia, prenatal IL-6 recapitulated prenatal stress-induced changes in adult microglia. Furthermore, prenatal IL-6 was able to recapitulate the delay in GABAergic progenitor migration caused by prenatal stress. However, IL-6 mechanisms were not necessary for this delay, which persisted after prenatal stress despite IL-6 blockade. As we have previously demonstrated, behavioral effects of prenatal stress in offspring, including increased anxiety-like behavior, decreased sociability, and locomotor inhibition, may be related to these GABAergic delays. While adult microglia changes were ameliorated by IL-6 blockade, these behavioral changes were independent of IL-6 mechanisms, similar to GABAergic delays. This and previous work from our laboratory suggests that multiple mechanisms, including GABAergic delays, may underlie prenatal stress-linked deficits.

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Increased levels of IL-6 alone recapitulate aspects of ASD pathophysiology.
“Importantly, increased levels of IL-6 alone recapitulate aspects of ASD pathophysiology [138, 142, 143].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [142]
Such regulation may also be altered by activation of microglia cells under stress conditions including MIA and/or in response to increased levels of IL-6.
“Such regulation may also be altered by activation of microglia cells under stress conditions including MIA and/or in response to increase levels of IL-6 [142].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [142]

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Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., Mehler, M. F., Conway, S. J., Ng, L. G., Stanley, E. R., et al. (2010) · Science · doi:10.1126/science.1194637 · Cited by 5,175 · see citing works
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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 · see citing works
Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67‐GFP knock‐in mouse
Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J., Obata, K., & Kaneko, T. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10905 · Cited by 1,277 · see citing works
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 · see citing works
Microglia: new roles for the synaptic stripper
Kettenmann, H., Kirchhoff, F., & Verkhratsky, A. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.023 · Cited by 1,173 · see citing works
Microglia Regulate the Number of Neural Precursor Cells in the Developing Cerebral Cortex
Cunningham, C. L., Martínez-Cerdeño, V., & Noctor, S. C. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3441-12.2013 · Cited by 976 · see citing works
Automated apparatus for quantitation of social approach behaviors in mice
Nadler, J. J., Moy, S. S., Dold, G., Trang, D., Simmons, N., Perez, A., Young, N. B., Barbaro, R. P., Piven, J., Magnuson, T. R., et al. (2004) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2004.00071.x · Cited by 775 · see citing works
Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders
Krakowiak, P., Walker, C. K., Bremer, A. A., Baker, A. S., Ozonoff, S., Hansen, R. L., & Hertz-Picciotto, I. (2012) · PEDIATRICS · doi:10.1542/peds.2011-2583 · Cited by 675 · see citing works
Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism
Malkova, N. V., Yu, C. Z., Hsiao, E. Y., Moore, M. J., & Patterson, P. H. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.01.011 · Cited by 662 · see citing works
Microglia Modulate Wiring of the Embryonic Forebrain
Squarzoni, P., Oller, G., Hoeffel, G., Pont‐Lezica, L., Rostaing, P., Low, D., Bessis, A., Ginhoux, F., & Garel, S. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.042 · Cited by 655 · see citing works
Exposure to physical and psychological stressors elevates plasma interleukin 6: Relationship to the activation of hypothalamic-pituitary-adrenal axis
Zhou, D., Kusnecov, A. W., Shurin, M. R., DePaoli, M., & Rabin, B. S. (1993) · Endocrinology · doi:10.1210/endo.133.6.8243274 · Cited by 494 · see citing works
Decreased number of parvalbumin and cholinergic interneurons in the striatum of individuals with Tourette syndrome
Kataoka, Y., Kalanithi, P. S. A., Grantz, H., Schwartz, M. L., Saper, C. B., Leckman, J. F., & Vaccarino, F. M. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22206 · Cited by 457 · see citing works
Prenatal stress and risk for autism
KINNEY, D., MUNIR, K., CROWLEY, D., & MILLER, A. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.06.004 · Cited by 440 · see citing works
The role of inflammatory cytokines as key modulators of neurogenesis
Borsini, A., Zunszain, P. A., Thuret, S., & Pariante, C. M. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2014.12.006 · Cited by 381 · see citing works
Cell Migration from the Ganglionic Eminences Is Required for the Development of Hippocampal GABAergic Interneurons
Pleasure, S. J., Anderson, S. A., Hevner, R. F., Bagri, A., Marín, Ó., Lowenstein, D. H., & Rubenstein, J. L. R. (2000) · Neuron · doi:10.1016/s0896-6273(00)00149-5 · Cited by 356 · see citing works
The neurodevelopmental impact of prenatal infections at different times of pregnancy: the earlier the worse?
Meyer, U., Yee, B. K., & Feldon, J. (2007) · The Neuroscientist · doi:10.1177/1073858406296401 · Cited by 303 · see citing works
Prenatal Maternal Stress Associated with ADHD and Autistic Traits in early Childhood
Ronald, A., Pennell, C. E., & Whitehouse, A. (2011) · Frontiers in Psychology · doi:10.3389/fpsyg.2010.00223 · Cited by 289 · see citing works
Innate Immunity in multiple sclerosis white matter lesions: expression of natural cytotoxicity triggering receptor 1 (NCR1)
Durrenberger, P. F., Ettorre, A., Kamel, F. O., Webb, L. V., Sim, M. J. W., Nicholas, R. S., Malik, O., Reynolds, R., Boyton, R. J., & Altmann, D. M. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-1 · Cited by 286 · see citing works
The placental interleukin-6 signaling controls fetal brain development and behavior
Wu, W.-L., Hsiao, E. Y., Yan, Z., Mazmanian, S. K., & Patterson, P. H. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.11.007 · Cited by 275 · see citing works
Prenatal stress: Role in psychotic and depressive diseases
Markham, J. A., & Koenig, J. I. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2035-0 · Cited by 274 · see citing works
Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice
Matrisciano, F., Tueting, P., Dalal, I., Kadriu, B., Grayson, D. R., Davis, J. M., Nicoletti, F., & Guidotti, A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.04.013 · Cited by 271 · see citing works
Prenatal Social Stress in the Rat Programmes Neuroendocrine and Behavioural Responses to Stress in the Adult Offspring: Sex‐Specific Effects
Brunton, P. J., & Russell, J. A. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.01969.x · Cited by 264 · see citing works
Maternal immune activation by LPS selectively alters specific gene expression profiles of interneuron migration and oxidative stress in the fetus without triggering a fetal immune response
Oskvig, D. B., Elkahloun, A. G., Johnson, K. R., Phillips, T. M., & Herkenham, M. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.01.015 · Cited by 248 · see citing works
Prenatal Infection and Risk for Schizophrenia: IL-1β, IL-6, and TNFα Inhibit Cortical Neuron Dendrite Development
Gilmore, J. H., Jarskog, L. F., Vadlamudi, S., & Lauder, J. M. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300446 · Cited by 246 · see citing works
Prolonged Restraint Stress Increases IL-6, Reduces IL-10, and Causes Persistent Depressive-Like Behavior That Is Reversed by Recombinant IL-10
Voorhees, J. L., Tarr, A. J., Wohleb, E. S., Godbout, J. P., Mo, X., Sheridan, J. F., Eubank, T. D., & Marsh, C. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058488 · Cited by 236 · see citing works
Prenatal stress causes alterations in the morphology of microglia and the inflammatory response of the hippocampus of adult female mice
Diz-Chaves, Y., Pernía, O., Carrero, P., & García‐Segura, L. M. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-71 · Cited by 233 · see citing works
Early prenatal stress impact on coping strategies and learning performance is sex dependent
Mueller, B. R., & Bale, T. L. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.01.017 · Cited by 216 · see citing works
In vitro production of IL-6, IL-1 beta, and tumor necrosis factor-alpha by human embryonic microglial and neural cells
Sébire, G., Émilie, D., Wallon, C., Héry, C., Devergne, O., Delfraissy, J., Galanaud, P., & Tardieu, M. (1993) · The Journal of Immunology · doi:10.4049/jimmunol.150.4.1517 · Cited by 198 · see citing works
Elevated serum levels of interleukin-17A in children with autism
AL-Ayadhi, L. Y., & Mostafa, G. A. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-158 · Cited by 193 · see citing works
Differential Macrophage Responses in the Peripheral and Central Nervous System during Wallerian Degeneration of Axons
Avellino, A. M., Hart, D., Dailey, A. T., Mackinnon, M., Ellegala, D. B., & Kliot, M. (1995) · Experimental Neurology · doi:10.1006/exnr.1995.1095 · Cited by 187 · see citing works
Prenatal stress increases the expression of proinflammatory cytokines and exacerbates the inflammatory response to LPS in the hippocampal formation of adult male mice
Diz-Chaves, Y., Astiz, M., Bellini, M. J., & García‐Segura, L. M. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.11.013 · Cited by 178 · see citing works
Immobilization Stress May Increase Plasma lnterleukin-6 via Central and Peripheral Catecholamines
Takaki, A., Huang, Q.-H., Somogyvári-Vigh, A., & Arimura, A. (1995) · NeuroImmunoModulation · doi:10.1159/000097185 · Cited by 167 · see citing works
Sexually dimorphic responses to early adversity: implications for affective problems and autism spectrum disorder
Davis, E. P., & Pfaff, D. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.06.014 · Cited by 159 · see citing works
Endogenous microglia regulate development of embryonic cortical precursor cells
Antony, J. M., Paquin, A., Nutt, S. L., Kaplan, D. R., & Miller, F. D. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22533 · Cited by 157 · see citing works
Simplex PCR Assay for Sex Determination in Mice
Clapcote, S. J., & Roder, J. (2005) · BioTechniques · doi:10.2144/05385bm05 · Cited by 154 · see citing works
Prenatal immune activation causes hippocampal synaptic deficits in the absence of overt microglia anomalies
Giovanoli, S., Weber‐Stadlbauer, U., Schedlowski, M., Meyer, U., & Engler, H. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.09.015 · Cited by 139 · see citing works
Microglia: Key Elements in Neural Development, Plasticity, and Pathology
Eyo, U. B., & Dailey, M. E. (2013) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-013-9434-z · Cited by 138 · see citing works
Microglia and Macrophages in the Developing CNS
Streit, W. J. (2001) · NeuroToxicology · doi:10.1016/s0161-813x(01)00033-x · Cited by 134 · see citing works
Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring
Ito, H., Smith, S. E. P., Hsiao, E. Y., & Patterson, P. H. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.03.004 · Cited by 133 · see citing works
The effect of chronic psychological stress on corticosterone, plasma metabolites, and immune responsiveness in European starlings
Cyr, N. E., Earle, K. A., Tam, C., & Romero, L. M. (2007) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2007.06.016 · Cited by 129 · see citing works
Prenatal stress induces long term stress vulnerability, compromising stress response systems in the brain and impairing extinction of conditioned fear after adult stress
Green, M. K., Rani, C. S. S., Joshi, A., Soto-Piña, A. E., Martinez, P. A., Frazer, A., Strong, R., & Morilak, D. A. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.06.041 · Cited by 124 · see citing works
Development of microglia in the postnatal rat hippocampus
Dalmau, I., Finsen, B. R., Zimmer, J., Gonz�lez, B., & Castellano, B. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1998)8:5 · Cited by 124 · see citing works
Prenatal Stress Induces Schizophrenia-Like Alterations of Serotonin 2A and Metabotropic Glutamate 2 Receptors in the Adult Offspring: Role of Maternal Immune System
Holloway, T. D., Moreno, J. L., Umali, A., Rayannavar, V., Hodes, G. E., Russo, S. J., & González‐Maeso, J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2331-12.2013 · Cited by 121 · see citing works
Transcriptome analysis of amoeboid and ramified microglia isolated from the corpus callosum of rat brain
Rangarajan, P., Jiang, B., Baby, N., Manivannan, J., Jayapal, M., Lu, J., Tay, S. S. W., Ling, E., & Dheen, S. T. (2012) · BMC Neuroscience · doi:10.1186/1471-2202-13-64 · Cited by 118 · see citing works
Prenatal disturbances of nerve cell migration in the entorhinal region: a common vulnerability factor in functional psychoses?
Beckmann, H., & Jakob, H. (1991) · Journal of Neural Transmission · doi:10.1007/bf01249120 · Cited by 114 · see citing works
Cytokine Levels during Pregnancy Influence Immunological Profiles and Neurobehavioral Patterns of the Offspring
PONZIO, N. M., SERVATIUS, R., BECK, K., MARZOUK, A., & KREIDER, T. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1381.013 · Cited by 114 · see citing works
Increased GAD67 mRNA expression in cerebellar interneurons in autism: Implications for Purkinje cell dysfunction
Yip, J., Soghomonian, J., & Blatt, G. J. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21520 · Cited by 112 · see citing works
The maternal-neonatal neuro-immune interface: Are there long-term implications for inflammatory or stress-related disease?
Shanks, N. M., & Lightman, S. L. (2001) · Journal of Clinical Investigation · doi:10.1172/jci14592 · Cited by 111 · see citing works
A Nationwide Study on the Risk of Autism After Prenatal Stress Exposure to Maternal Bereavement
Li, J., Vestergaard, M., Obel, C., Christensen, J., Precht, D. H., Lu, M., & Olsen, J. (2009) · PEDIATRICS · doi:10.1542/peds.2008-1734 · Cited by 111 · see citing works
The maternal-neonatal neuro-immune interface: Are there long-term implications for inflammatory or stress-related disease?
Shanks, N., & Lightman, S. L. (2001) · Journal of Clinical Investigation · doi:10.1172/jci200114592 · Cited by 111 · see citing works
Restraint stress elevates the plasma interleukin-6 levels in germ-free mice
Nukina, H., Sudo, N., Aiba, Y., Oyama, N., Koga, Y., & Kubo, C. (2001) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(01)00260-0 · Cited by 109 · see citing works
Modulation of behavioral and neurochemical measures of forebrain dopamine function in mice by species-specific interleukin-2
Petitto, J. M., McCarthy, D. B., Rinker, C. M., Huang, Z. L., & Getty, T. (1997) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(96)00196-8 · Cited by 108 · see citing works
Prenatal stress delays inhibitory neuron progenitor migration in the developing neocortex
Stevens, H. E., Su, T., Yanagawa, Y., & Vaccarino, F. M. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.07.011 · Cited by 104 · see citing works
Self-citation
Quantitative Histology Using Confocal Microscopy: Implementation of Unbiased Stereology Procedures
Peterson, D. A. (1999) · Methods · doi:10.1006/meth.1999.0818 · Cited by 98 · see citing works
Neural stem cell regulation, fibroblast growth factors, and the developmental origins of neuropsychiatric disorders
Stevens, H. E. (2010) · Frontiers in Neuroscience · doi:10.3389/fnins.2010.00059 · Cited by 90 · see citing works
Self-citation
Neuroactive steroids in pregnancy: Key regulatory and protective roles in the foetal brain
Hirst, J. J., Kelleher, M. A., Walker, D. W., & Palliser, H. K. (2013) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2013.04.002 · Cited by 90 · see citing works
Delays in GABAergic interneuron development and behavioral inhibition after prenatal stress
Lussier, S. J., & Stevens, H. E. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22376 · Cited by 89 · see citing works
Self-citation
Neuronal migration abnormalities and its possible implications for schizophrenia
Muraki, K., & Tanigaki, K. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00074 · Cited by 83 · see citing works
SDF1 Regulates Leading Process Branching and Speed of Migrating Interneurons
Lysko, D. E., Putt, M. E., & Golden, J. A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3118-10.2011 · Cited by 83 · see citing works
Role of neurosteroids in regulating cell death and proliferation in the late gestation fetal brain
Yawno, T., Hirst, J. J., Castillo-Meléndez, M., & Walker, D. W. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.07.009 · Cited by 79 · see citing works
Maternal inflammation promotes fetal microglial activation and increased cholinergic expression in the fetal basal forebrain: role of interleukin-6
Pratt, L., Ni, L., Ponzio, N. M., & Jonakait, G. M. (2013) · Pediatric Research · doi:10.1038/pr.2013.126 · Cited by 77 · see citing works
Maternal immune activation evoked by polyinosinic:polycytidylic acid does not evoke microglial cell activation in the embryo
Smolders, S., Smolders, S., Swinnen, N., Gärtner, A., Rigo, J., Legendre, P., & Brône, B. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00301 · Cited by 66 · see citing works
Prenatal Exposure to Autism-Specific Maternal Autoantibodies Alters Proliferation of Cortical Neural Precursor Cells, Enlarges Brain, and Increases Neuronal Size in Adult Animals
Martínez-Cerdeño, V., Camacho, J., Fox, E., Miller, E., Ariza, J., Kienzle, D., Plank, K., Noctor, S. C., & Van de Water, J. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhu291 · Cited by 63 · see citing works
Dexamethasone induces apoptosis in the developing rat amygdala in an age-, region-, and sex-specific manner
Zuloaga, D. G., Carbone, D. L., Hiroi, R., Chong, D., & Handa, R. J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.09.052 · Cited by 62 · see citing works
Effects of prenatal stress and neonatal handling on anxiety, spatial learning and serotonergic system of male offspring mice
Akatsu, S., Ishikawa, C., Takemura, K., Ohtani, A., & Shiga, T. (2015) · Neuroscience Research · doi:10.1016/j.neures.2015.07.002 · Cited by 60 · see citing works
The association between prenatal environment and children’s mental health trajectories from 2 to 14 years
Tearne, J. E., Allen, K. L., Herbison, C. E., Lawrence, D. M., Whitehouse, A., SAWYER, M. G., & Robinson, M. (2014) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-014-0651-7 · Cited by 59 · see citing works
Prenatal ontogeny as a susceptibility period for cortical GABA neuron disturbances in schizophrenia
Volk, D. W., & Lewis, D. A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.06.008 · Cited by 56 · see citing works
Prenatal Stress Inhibits Neuronal Maturation through Downregulation of Mineralocorticoid Receptors
Tamura, M., Sajo, M., Kakita, A., Matsuki, N., & Koyama, R. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3447-10.2011 · Cited by 52 · see citing works
Chronic Gestational Exposure to Ethanol Leads to Enduring Aberrances in Cortical Form and Function in the Medial Prefrontal Cortex
Skorput, A. G. J., & Yeh, H. H. (2016) · Alcoholism: Clinical and Experimental Research · doi:10.1111/acer.13107 · Cited by 50 · see citing works
Schizophrenia and reelin: a model based on prenatal stress to study epigenetics, brain development and behavior
Negrón-Oyarzo, I., Lara-Vásquez, A., Palacios-García, I., Fuentealba, P., & Aboitiz, F. (2016) · Biological Research · doi:10.1186/s40659-016-0076-5 · Cited by 46 · see citing works
Maternal viral infection during pregnancy elicits anti-social behavior in neonatal piglet offspring independent of postnatal microglial cell activation
Antonson, A. M., Radlowski, E. C., Lawson, M. A., Rytych, J. L., & Johnson, R. W. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.09.019 · Cited by 44 · see citing works
Biochemical and cognitive impairments observed in animal models of schizophrenia induced by prenatal stress paradigm or methylazoxymethanol acetate administration
Ratajczak, P., Kus, K., Murawiecka, P., Słodzińska, I., Giermaziak, W., & Nowakowska, E. (2015) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-2015-2037 · Cited by 35 · see citing works
A heterozygous deletion in the glutamate decarboxylase 67 gene enhances maternal and fetal stress vulnerability
Uchida, T., Oki, Y., Yanagawa, Y., & Fukuda, A. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.12.010 · Cited by 27 · see citing works
Toll-like receptor 4-mediated immune stress in pregnant rats activates STAT3 in the fetal brain: role of interleukin-6
Mouihate, A., & Mehdawi, H. (2015) · Pediatric Research · doi:10.1038/pr.2015.86 · Cited by 26 · see citing works
The effect of chronic emotional stress on the humoral immune response to Porphyromonas gingivalis in mice
Houri‐Haddad, Y., Itzchaki, O., Ben‐Nathan, D., & Shapira, L. (2003) · Journal of Periodontal Research · doi:10.1034/j.1600-0765.2003.20390.x · Cited by 24 · see citing works
Effects of prenatal stress on anxiety-like behavior and nociceptive response in rats
Said, N., Lakehayli, S., Battas, O., Hakkou, F., & Tazi, A. (2015) · Journal of Integrative Neuroscience · doi:10.1142/s0219635215500107 · Cited by 17 · see citing works
Activation of immature microglia in response to stab wound in embryonic quail retina
Sánchez‐López, A. M., Cuadros, M. Á., Calvente, R., Tassi, M., Marín‐Teva, J. L., & Navascués, J. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20676 · Cited by 11 · see citing works
Introduction to special issue on neuroimmunology in brain development and disease
McAllister, A. K., & Patterson, P. H. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22054 · Cited by 9 · see citing works
Effect of chronic restraint stress on immune status of male Sprague Dawley rats.
Moazzam, S., Hussain, M. M., & Ahmad, T. A. (2013) · PubMed · Cited by 8 · see citing works
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Sandman (1999) · doi:10.1002/(sici)1098-2302(199904)34:3

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McAllister AK Patterson PH 2012 Neuroimmunology in Brain Development and Disease Dev Neurobiol 72 1269 1271 22927111 PMC4357356
Morgan KN Thayer JE Frye CA 1999 Prenatal stress suppresses rat pup ultrasonic vocalization and myoclonic twitching in response to separation Dev Psycho biol 34 205 215 10204096

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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
The Inflamed Brain in Schizophrenia: The Convergence of Genetic and Environmental Risk Factors That Lead to Uncontrolled Neuroinflammation
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
Maternal Inflammation and Neurodevelopmental Programming: A Review of Preclinical Outcomes and Implications for Translational Psychiatry
Gumusoglu, S. B., & Stevens, H. E. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.08.008 · Cited by 207 · see citing works
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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
The Role of Maternal Immune Activation in the Pathogenesis of Autism: A Review of the Evidence, Proposed Mechanisms and Implications for Treatment
Zawadzka, A., Cieślik, M., & Adamczyk, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111516 · Cited by 190 · see citing works
Neuron-Glia Interactions in Neurodevelopmental Disorders
Kim, Y. S., Choi, J., & Yoon, B. (2020) · Cells · doi:10.3390/cells9102176 · Cited by 148 · see citing works
Infant microbes and metabolites point to childhood neurodevelopmental disorders
Ahrens, A. P., Hyötyläinen, T., Petrone, J. R., Igelström, K. M., George, C. D., Garrett, T. J., Orešič, M., Triplett, E. W., & Ludvigsson, J. (2024) · Cell · doi:10.1016/j.cell.2024.02.035 · Cited by 150 · see citing works
Prenatal exposure to environmental insults and enhanced risk of developing Schizophrenia and Autism Spectrum Disorder: focus on biological pathways and epigenetic mechanisms
Cattane, N., Richetto, J., & Cattaneo, A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.001 · Cited by 118 · see citing works
Prenatal stress and genetic risk: How prenatal stress interacts with genetics to alter risk for psychiatric illness
Abbott, P. W., Gumusoglu, S. B., Bittle, J., Beversdorf, D. Q., & Stevens, H. E. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.01.019 · Cited by 109 · see citing works
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Maternal immune activation, central nervous system development and behavioral phenotypes
Minakova, E., & Warner, B. B. (2018) · Birth Defects Research · doi:10.1002/bdr2.1416 · Cited by 108 · see citing works
Altered Intestinal Morphology and Microbiota Composition in the Autism Spectrum Disorders Associated SHANK3 Mouse Model
Sauer, A. K., Bockmann, J., Steinestel, K., Boeckers, T. M., & Grabrucker, A. M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092134 · Cited by 98 · see citing works
Controversies and prospects about microglia in maternal immune activation models for neurodevelopmental disorders
Smolders, S., Notter, T., Smolders, S., Rigo, J., & Brône, B. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.06.001 · Cited by 93 · see citing works
Prenatal Stress, Maternal Immune Dysregulation, and Their Association With Autism Spectrum Disorders
Beversdorf, D. Q., Stevens, H. E., & Jones, K. L. (2018) · Current Psychiatry Reports · doi:10.1007/s11920-018-0945-4 · Cited by 94 · see citing works
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Prenatal stress causes intrauterine inflammation and serotonergic dysfunction, and long-term behavioral deficits through microbe- and CCL2-dependent mechanisms
Chen, H. J., Antonson, A. M., Rajasekera, T. A., Patterson, J. M., Bailey, M. T., & Gur, T. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-00876-5 · Cited by 88 · see citing works
Maternal immune activation and role of placenta in the prenatal programming of neurodevelopmental disorders
Woods, R. M., Lorusso, J. M., Fletcher, J., ElTaher, H., McEwan, F., Harris, I., Kowash, H. M., D'Souza, S. W., Harte, M., Hager, R., et al. (2023) · Neuronal Signaling · doi:10.1042/ns20220064 · Cited by 84 · see citing works
Microbiota-immune-brain interactions: A lifespan perspective
Ratsika, A., Cruz-Pereira, J. S., Lynch, C. M. K., Clarke, G. A., & Cryan, J. F. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102652 · Cited by 78 · see citing works
Preeclampsia and Neurodevelopmental Outcomes: Potential Pathogenic Roles for Inflammation and Oxidative Stress?
Barron, A., McCarthy, C., & O’Keeffe, G. W. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02290-4 · Cited by 72 · see citing works
Intrauterine Microbiota: Missing, or the Missing Link?
Chen, H. J., & Gur, T. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.03.008 · Cited by 70 · see citing works
Consequences of Viral Infection and Cytokine Production During Pregnancy on Brain Development in Offspring
Elgueta, D., Murgas, P., Riquelme, E. M., Yang, G., & Cancino, G. I. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.816619 · Cited by 67 · see citing works
Emerging Role of Neuron‐Glia in Neurological Disorders: At a Glance
Rahman, M. M., Islam, M. R., Yamin, M., Islam, M. R., Islam, M. R., Meem, A. F. K., Akter, A., Emran, T. B., Cavalu, S. D., & Sharma, R. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/3201644 · Cited by 66 · see citing works
Preclinical animal models of mental illnesses to translate findings from the bench to the bedside: Molecular brain mechanisms and peripheral biomarkers associated to early life stress or immune challenges
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 64 · see citing works
What Does Immunology Have to Do With Normal Brain Development and the Pathophysiology Underlying Tourette Syndrome and Related Neuropsychiatric Disorders?
Martino, D., Johnson, I. N. S., & Leckman, J. F. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.567407 · Cited by 59 · see citing works
How do established developmental risk-factors for schizophrenia change the way the brain develops?
Eyles, D. W. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01273-2 · Cited by 55 · see citing works
Prenatal Stress and Maternal Immune Dysregulation in Autism Spectrum Disorders: Potential Points for Intervention
Beversdorf, D. Q., Stevens, H. E., Margolis, K. G., & de Water, J. V. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666191119093335 · Cited by 53 · see citing works
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Diagnostic and Severity-Tracking Biomarkers for Autism Spectrum Disorder
Bjørklund, G., Meguid, N. A., El-Ansary, A. K., El‐Bana, M. A., Dadar, M., Aaseth, J., Hemimi, M., Osredkar, J., & Chirumbolo, S. (2018) · Journal of Molecular Neuroscience · doi:10.1007/s12031-018-1192-1 · Cited by 51 · see citing works
Cellular stress mechanisms of prenatal maternal stress: Heat shock factors and oxidative stress
Dowell, J., Elser, B. A., Schroeder, R. E., & Stevens, H. E. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.134368 · Cited by 50 · see citing works
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Chronic maternal interleukin-17 and autism-related cortical gene expression, neurobiology, and behavior
Gumusoglu, S. B., Hing, B. W. Q., Chilukuri, A. S. S., Dewitt, J. J., Scroggins, S. M., & Stevens, H. E. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0640-0 · Cited by 49 · see citing works
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Maternal immune activation generates anxiety in offspring: A translational meta-analysis
Quagliato, L. A., de Matos, U. M. A., & Nardi, A. E. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01361-3 · Cited by 47 · see citing works
Unique maternal immune and functional microbial profiles during prenatal stress
Antonson, A. M., Evans, M. V., Galley, J. D., Chen, H. J., Rajasekera, T. A., Lammers, S. M., Hale, V. L., Bailey, M. T., & Gur, T. (2020) · Scientific Reports · doi:10.1038/s41598-020-77265-x · Cited by 47 · see citing works
The role of glucocorticoid, interleukin-1β, and antioxidants in prenatal stress effects on embryonic microglia
Bittle, J., & Stevens, H. E. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1079-7 · Cited by 42 · see citing works
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Prenatal stress and increased susceptibility to anxiety-like behaviors: role of neuroinflammation and balance between GABAergic and glutamatergic transmission
Roshan‐Milani, S., Seyyedabadi, B., Saboory, E., Parsamanesh, N., & Mehranfard, N. (2021) · Stress · doi:10.1080/10253890.2021.1942828 · Cited by 41 · see citing works
Influence of Prenatal Drug Exposure, Maternal Inflammation, and Parental Aging on the Development of Autism Spectrum Disorder
Sato, A., Kotajima‐Murakami, H., Tanaka, M., Katoh, Y., & Ikeda, K. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.821455 · Cited by 42 · see citing works
Combined Maternal Exposure to Cypermethrin and Stress Affect Embryonic Brain and Placental Outcomes in Mice
Elser, B. A., Kayali, K., Dhakal, R., O’Hare, B., Wang, K., Lehmler, H., & Stevens, H. E. (2020) · Toxicological Sciences · doi:10.1093/toxsci/kfaa040 · Cited by 40 · see citing works
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Autism spectrum disorder and severe social impairment associated with elevated plasma interleukin-8
Shen, Y., Li, Y., Shi, L., Liu, M., Wu, R., Xia, K., Zhang, F., Ou, J., & Zhao, J. (2020) · Pediatric Research · doi:10.1038/s41390-020-0910-x · Cited by 40 · see citing works
Altered offspring neurodevelopment in an arginine vasopressin preeclampsia model
Gumusoglu, S. B., Chilukuri, A. S. S., Hing, B. W. Q., Scroggins, S. M., Kundu, S., Sandgren, J. A., Santillan, M. K. O., Santillan, D. A., Grobe, J. L., & Stevens, H. E. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01205-0 · Cited by 39 · see citing works
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Maternal Distress and Offspring Neurodevelopment: Challenges and Opportunities for Pre-clinical Research Models
Fitzgerald, E., Parent, C. I., Kee, M. Z. L., & Meaney, M. J. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.635304 · Cited by 39 · see citing works
Modifications of Behavior and Inflammation in Mice Following Transplant with Fecal Microbiota from Children with Autism
Avolio, E., Olivito, I., Rosina, E., Romano, L., Angelone, T., Bartolo, A. D., Scimeca, M., Bellizzi, D., D’Aquila, P., Passarino, G., et al. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.06.038 · Cited by 40 · see citing works
Assessing behavior and cognition in rodents, nonhuman primates, and humans: where are the limits of translation?
Stephan, M., Volkmann, P., & Rossner, M. J. (2019) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2019.21.3/mrossner · Cited by 37 · see citing works
Suppression of the Peripheral Immune System Limits the Central Immune Response Following Cuprizone-Feeding: Relevance to Modelling Multiple Sclerosis
Sen, M. K., Almuslehi, M. S. M., Gyengesi, E., Myers, S. J., Shortland, P. J., Mahns, D. A., & Coorssen, J. R. (2019) · Cells · doi:10.3390/cells8111314 · Cited by 35 · see citing works
Translational models of stress and resilience: An applied neuroscience methodology review
Albayrak, Z. S., Vaz, A., Bordes, J., Ünlü, S., Sep, M. S. C., Vinkers, C. H., Pinto, L., & Eser, H. Y. (2024) · Neuroscience Applied · doi:10.1016/j.nsa.2024.104064 · Cited by 39 · see citing works
The Role of Redox Dysregulation in the Effects of Prenatal Stress on Embryonic Interneuron Migration
Bittle, J., Menezes, E. D. C., McCormick, M. L., Spitz, D. R., Dailey, M. E., & Stevens, H. E. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz052 · Cited by 32 · see citing works
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Effects of a rat model of gestational hypothyroidism on forebrain dopaminergic, GABAergic, and serotonergic systems and related behaviors
Menezes, E. D. C., dos Santos, P. R., Goes, T. C., de Carvalho, V. C. B., Teixeira-Silva, F., Stevens, H. E., & Badauê‐Passos, D. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.03.027 · Cited by 29 · see citing works
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Network and Experimental Pharmacology to Decode the Action of Wendan Decoction Against Generalized Anxiety Disorder
Qi, J., Li, J., Chen, G., Zi-Yu, W., Liu, X., Liu, Y., Chen, L., Wu, X., Liu, Y., Zhao, X., et al. (2022) · Drug Design Development and Therapy · doi:10.2147/dddt.s367871 · Cited by 27 · see citing works
The impact of maternal immune activation on embryonic brain development
McEwan, F., Glazier, J. D., & Hager, R. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1146710 · Cited by 27 · see citing works
From Womb to Mind: Prenatal Epigenetic Influences on Mental Health Disorders
Álvarez-Mejía, D., Rodas, J. A., & León-Rojas, J. E. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26136096 · Cited by 30 · see citing works
Alpha-Synuclein Pre-Formed Fibrils Injected into Prefrontal Cortex Primarily Spread to Cortical and Subcortical Structures
Weber, M. A., Kerr, G., Thangavel, R., Conlon, M. M., Gumusoglu, S. B., Gupta, K., Abdelmotilib, H., Halhouli, O., Zhang, Q., Geerling, J. C., et al. (2023) · Journal of Parkinson s Disease · doi:10.3233/jpd-230129 · Cited by 25 · see citing works
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The role of nutrition and gut microbiome in childhood brain development and behavior
Jiang, Y., & Li, Y. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1590172 · Cited by 33 · see citing works
Maternal Immune Activation Hypotheses for Human Neurodevelopment: Some Outstanding Questions
O’Connor, T. G., & Ciesla, A. A. (2021) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2021.10.006 · Cited by 24 · see citing works
Polybrominated diphenyl ether (PBDE) exposure and adverse maternal and infant health outcomes: Systematic review
Gomes, J., Begum, M., & Kumarathasan, P. (2023) · Chemosphere · doi:10.1016/j.chemosphere.2023.140367 · Cited by 23 · see citing works
Administration of molecular hydrogen during pregnancy improves behavioral abnormalities of offspring in a maternal immune activation model
Imai, K., Kotani, T., Tsuda, H., Nakano, T., Ushida, T., Iwase, A., Nagai, T., Toyokuni, S., Suzumura, A., & Kikkawa, F. (2018) · Scientific Reports · doi:10.1038/s41598-018-27626-4 · Cited by 22 · see citing works
In utero electroporation induces cell death and alters embryonic microglia morphology and expression signatures in the developing hypothalamus
Rosin, J. M., & Kurrasch, D. M. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1213-6 · Cited by 21 · see citing works
Developmental programming of tissue-resident macrophages
Viola, M. F., Taveras, E. F., & Mass, E. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1475369 · Cited by 21 · see citing works
Liposomal Epigallocatechin-3-Gallate for the Treatment of Intestinal Dysbiosis in Children with Autism Spectrum Disorder: A Comprehensive Review
Ortí, J. E. D. L. R., Moneti, C., Serrano-Ballesteros, P., Castellano, G., Bayona-Babiloni, R., Carriquí-Suárez, A. B., Motos-Muñoz, M., Proaño, B., & Benlloch, M. (2023) · Nutrients · doi:10.3390/nu15143265 · Cited by 18 · see citing works
The role of the placenta-brain axis in psychoneuroimmune programming
Gumusoglu, S. B. (2024) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2024.100735 · Cited by 19 · see citing works
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Fetal CCL2 signaling mediates offspring social behavior and recapitulates effects of prenatal stress
Chen, H. J., Galley, J. D., Verosky, B. G., Yang, F. T., Rajasekera, T. A., Bailey, M. T., & Gur, T. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.10.032 · Cited by 18 · see citing works
Stereotypic behaviors are associated with physiology and immunity differences in long-term confined sows
Pan, L., Nian, H., Zhang, R., Liu, H., Li, C., Wei, H., Yi, R., Li, J., Li, X., & Bao, J. (2022) · Physiology & Behavior · doi:10.1016/j.physbeh.2022.113776 · Cited by 17 · see citing works
Maternal P7C3-A20 Treatment Protects Offspring from Neuropsychiatric Sequelae of Prenatal Stress
Schroeder, R. E., Sridharan, P. S., Nguyen, L. T., Loren, A., Williams, N. S., Kettimuthu, K. P., Cintrón-Pérez, C. J., Vázquez‐Rosa, E., Pieper, A. A., & Stevens, H. E. (2021) · Antioxidants and Redox Signaling · doi:10.1089/ars.2020.8227 · Cited by 17 · see citing works
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Maternal Stress during Pregnancy in Mice Induces Sex-Dependent Behavioral Alterations in Offspring along with Impaired Serotonin and Kynurenine Pathways of Tryptophan Metabolism
Moura, C. D. A., Cagni, F. C., Costa, L. R. F., Tiago, P. R. F., Croyal, M., Aguesse, A., Reyes‐Castro, L. A., Zambrano, E., Bolaños, F. J., & Gavioli, E. C. (2022) · Developmental Neuroscience · doi:10.1159/000526647 · Cited by 16 · see citing works
Modelling the Interplay Between Neuron-Glia Cell Dysfunction and Glial Therapy in Autism Spectrum Disorder
Unnisa, A., Greig, N. H., & Kamal, M. A. (2022) · Current Neuropharmacology · doi:10.2174/1570159x21666221221142743 · Cited by 17 · see citing works
Programming of Vascular Dysfunction by Maternal Stress: Immune System Implications
Costa, T. J. D., de Oliveira, J. C., Giachini, F. R. C., Lima, V. V., Tostes, R. C., & Bomfim, G. F. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.787617 · Cited by 16 · see citing works
Effects of Genetic Counseling on Reducing Prenatal Stress and Autism Rates in the Asia-Pacific Region
Bi, Y., & Uludağ, K. (2024) · Advances in healthcare information systems and administration book series · doi:10.4018/979-8-3693-1214-8.ch016 · Cited by 15 · see citing works
Investigating brain–gut microbiota dynamics and inflammatory processes in an autistic-like rat model using MRI biomarkers during childhood and adolescence
Palanivelu, L., Chen, Y., Chang, C., Liang, Y., Tseng, H.-Y., Li, S., Chang, C., & Lo, Y. (2024) · NeuroImage · doi:10.1016/j.neuroimage.2024.120899 · Cited by 15 · see citing works
Interleukin 6 Dependent Synaptic Plasticity in a Social Defeat-Susceptible Prefrontal Cortex Circuit
Esquivel‐Rendon, E., Vargas‐Mireles, J., Cuevas‐Olguin, R., Miranda‐Morales, M., Acosta-Mares, P., García‐Oscos, F., Pineda, J. C., Salgado, H., Rose‐John, S., & Atzori, M. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.07.002 · Cited by 12 · see citing works
A consideration of the increased risk of schizophrenia due to prenatal maternal stress, and the possible role of microglia
Mawson, E. R., & MORRIS, B. J. (2023) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2023.110773 · Cited by 13 · see citing works
Long-term effects of prenatal stress on the development of prefrontal cortex in the adolescent offspring
Suwaluk, A., & Chutabhakdikul, N. (2022) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2022.102169 · Cited by 11 · see citing works
Maternal treatment with P7C3-A20 protects from impaired maternal care after chronic gestational stress
Schroeder, R. E., Nguyen, L. T., Pieper, A. A., & Stevens, H. E. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113558 · Cited by 11 · see citing works
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Prenatal stress and fluoxetine exposure in mice differentially affect repetitive behaviors and synaptic plasticity in adult male and female offspring
Arzuaga, A. L., Edmison, D. D., Mroczek, J., Larson, J., & Ragozzino, M. E. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114114 · Cited by 11 · see citing works
Maternal pre-eclampsia serum increases neurite growth and mitochondrial function through a potential IL-6-dependent mechanism in differentiated SH-SY5Y cells
Barron, A., Manna, S., McElwain, C. J., Musumeci, A. G., McCarthy, F. P., O’Keeffe, G. W., & McCarthy, C. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2022.1043481 · Cited by 11 · see citing works
Effects of immunization with heat-killed Mycobacterium vaccae on autism spectrum disorder-like behavior and epileptogenesis in a rat model of comorbid autism and epilepsy.
Smith, Z., Kubiak, R. A., Arnold, M. R., Loupy, K., Taylor, J. A., Crist, T., Bernier, A. E., D'Angelo, H., Heinze, J. D., Lowry, C., et al. (2020) · Brain, behavior, and immunity · doi:10.1016/j.bbi.2020.05.034 · Cited by 9 · see citing works
Fatores de risco gestacional em mães de crianças diagnosticadas com autismo
dos Santos, H. T., de Souza, L. P., & Passos, A. D. C. F. (2022) · Research Society and Development · doi:10.33448/rsd-v11i15.37837 · Cited by 10 · see citing works
Prenatal stress alters mouse offspring dorsal striatal development and placental function in sex-specific ways
Maurer, S. V., Hing, B. W. Q., Lussier, S. J., Radhakrishna, S., Davis, J. L.-B., Abbott, P. W., Michaelson, J. J., & Stevens, H. E. (2025) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2024.12.048 · Cited by 9 · see citing works
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Maternal high-fat, high-sucrose diet–induced excess adiposity is linked to placental hypoxia and disruption of fetoplacental immune homeostasis in late gestation
Bellissimo, C. J., Ribeiro, T. A., Yeo, E., Jazwiec, P. A., Luo, H., Bains, J., Kennedy, K. M., Bowdish, D. M. E., & Sloboda, D. M. (2025) · Biology of Reproduction · doi:10.1093/biolre/ioaf143 · Cited by 10 · see citing works
Maternal Interleukin-6 Hampers Hippocampal Neurogenesis in Adult Rat Offspring in a Sex-Dependent Manner
Mouihate, A., & Kalakh, S. (2021) · Developmental Neuroscience · doi:10.1159/000516370 · Cited by 9 · see citing works
Holobiont Development: Embryology and Ecological Succession
Gilbert, S. F. (2023) · Human Development · doi:10.1159/000534203 · Cited by 10 · see citing works
Microglia are necessary for probiotics supplementation to improve impaired fear extinction caused by pregnancy stress in adult offspring of rats
Zeng, R., Chen, J., Peng, Y., Xu, W., Tao, Y., Li, M., Zhang, R.-Q., Meng, J., Li, Z., Zeng, L., et al. (2023) · Neurobiology of Stress · doi:10.1016/j.ynstr.2023.100591 · Cited by 8 · see citing works
The Impact of Maternal Antioxidants on Prenatal Stress Effects on Offspring Neurobiology and Behavior.
Davis, J. L.-B., O'Connor, M., Erlbacher, H., Schlichte, S. L., & Stevens, H. E. (2022) · PubMed Central · Cited by 7 · see citing works
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Effect of risperidone on serum IL-6 levels in individuals with schizophrenia: a systematic review and meta-analysis
Ramos-Méndez, M. Á., Tovilla‐Zárate, C. A., Juárez‐Rojop, I. E., Villar-Soto, M., Mendoza, A. D. G., González‐Castro, T. B., López‐Narváez, M. L., Martínez‐Magaña, J. J., Castillo-Ávila, R. G., & Villar-Juárez, G. E. (2022) · International Journal of Psychiatry in Clinical Practice · doi:10.1080/13651501.2022.2100264 · Cited by 7 · see citing works
Altered Development of Prefrontal GABAergic Functions and Anxiety-like Behavior in Adolescent Offspring Induced by Prenatal Stress
Suwaluk, A., & Chutabhakdikul, N. (2022) · Brain Sciences · doi:10.3390/brainsci12081015 · Cited by 7 · see citing works
Assessing in-vitro models for microglial development and fetal programming: a critical review
Schepanski, S. N., Ngoumou, G. B., Buß, C., & Seifert, G. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1538920 · Cited by 6 · see citing works
Exercise, spinogenesis and cognitive functions
Zhang, L., & So, K. (2019) · International review of neurobiology · doi:10.1016/bs.irn.2019.07.005 · Cited by 6 · see citing works
Melatonin Alleviates Behavioral and Neurodevelopmental Abnormalities in Offspring Caused by Prenatal Stress
Wu, D., Du, J., Zhao, T., Li, N., Qiao, X., Peng, F., Wang, D., Shi, J., Zhang, S., Diao, C., et al. (2025) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.70347 · Cited by 5 · see citing works
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Authors: Gumusoglu, S. B., Fine, R. S., Murray, S. J., Bittle, J. L., & Stevens, H. E.
Affiliations: University of Iowa (US)
Yale University (US)
Corresponding author: Stevens, Hanna E.
ORCID: Gumusoglu, Serena B.
Fine, Rebecca S.
Murray, Samuel J.
Stevens, Hanna E.
Venue: Brain, Behavior, and Immunity
Publisher: Elsevier BV
Published: 2017-10
Volume: 65
Pages: 274-283
ISSN: 0889-1591 (ISSN-L)
DOI: 10.1016/j.bbi.2017.05.015
PMC: PMC5537020
OpenAlex: W2617644144
Cited by: 129
References: 79
Citations by year: 2026: 8 · 2025: 18 · 2024: 15 · 2023: 14 · 2022: 22 · 2021: 15 · 2020: 12 · 2019: 11 · 2018: 14
FWCI: 5.05
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Behavior and Immunity (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (K08MH086812, R25MH077823)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: interleukin-6, prenatal stress, maternal restraint stress, microglia, brain development, maternal immune activation, cortical plate, anxiety-like behavior, sociability, locomotor inhibition, autism spectrum disorder, attention deficit hyperactivity disorder, IL-6 inhibition, microglial morphology
MeSH terms: Animals, Anxiety, Behavior, Animal, Brain, Disease Models, Animal, Female, Male, Pregnancy, Prenatal Exposure Delayed Effects, Stress, Psychological, Interleukin-6, Cytokines, Microglia, GABA Agents, Mice, GABAergic Neurons

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The role of IL-6 in neurodevelopment after prenatal stress

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