Effects of early or late prenatal immune activation in mice on behavioral and neuroanatomical abnormalities relevant to schizophrenia in the adulthood
Abstract
Maternal immune activation (MIA) during pregnancy in rodents increases the risk of the offspring to develop schizophrenia-related behaviors, suggesting a relationship between the immune system and the brain development. Here we tested the hypothesis that MIA induced by the viral mimetic polyinosinic-polycytidylic acid (poly I:C) in early or late gestation of mice leads to behavioral and neuroanatomical disorders in the adulthood. On gestational days (GDs) 9 or 17 pregnant dams were treated with poly I:C or saline via intravenous route and the offspring behaviors were measured during adulthood. Considering the progressive structural neuroanatomical alterations in the brain of individuals with schizophrenia, we used magnetic resonance imaging (MRI) to perform brain morphometric analysis of the offspring aged one year. MIA on GD9 or GD17 led to increased basal locomotor activity, enhanced motor responses to ketamine, a psychotomimetic drug, and reduced time spent in the center of the arena, suggesting an increased anxiety-like behavior. In addition, MIA on GD17 reduced glucose preference in the offspring. None of the treatments altered the relative volume of the lateral ventricles. However, a decrease in brain volume, especially for posterior structures, was observed for one-year-old animals treated with poly I:C compared with control groups. Thus, activation of the maternal immune system at different GDs lead to neuroanatomical and behavioral alterations possibly related to the positive and negative symptoms of schizophrenia. These results provide insights on neuroimmunonological and neurodevelopmental aspects of certain psychopathologies, such as schizophrenia.
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Prenatal poly(I:C) exposure decreased overall brain volume in adult mice.
“Decreased overall brain volume was reported with prenatal exposure to poly(I:C) in adult mice (da Silveira et al., 2017).”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as da Silveira et al., 2017
Cites
Diagnostic and Statistical Manual of Mental Disorders
American Psychiatric Association (2013) · doi:10.1176/appi.books.9780890425596 · Cited by 116,369 · see citing works
Diagnostic and Statistical Manual of Mental Disorders(DSM)
Leong, F. T. L. (2008) · Sage eBooks · doi:10.4135/9781412963978.n182 · Cited by 10,858 · see citing works
Implications of Normal Brain Development for the Pathogenesis of Schizophrenia
Weinberger, D. R. (1987) · Archives of General Psychiatry · doi:10.1001/archpsyc.1987.01800190080012 · Cited by 3,724 · see citing works
van Os, J., & Kapur, S. (2009) · The Lancet · doi:10.1016/s0140-6736(09)60995-8 · Cited by 1,971 · see citing works
Meta-Analysis of Cytokine Alterations in Schizophrenia: Clinical Status and Antipsychotic Effects
Miller, B. J., Buckley, P., Seabolt, W., Mellor, A., & Kirkpatrick, B. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.04.013 · Cited by 1,742 · see citing works
Dysregulation of the dopamine system in the pathophysiology of schizophrenia and depression
Grace, A. A. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.57 · Cited by 1,166 · see citing works
Brain Volumes in Schizophrenia: A Meta-Analysis in Over 18 000 Subjects
Haijma, S. V., Van Haren, N., Cahn, W., Koolschijn, P. C. M. P., Hulshoff Pol, H. E., & Kahn, R. S. (2013) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs118 · Cited by 1,012 · see citing works
Modeling transformations of neurodevelopmental sequences across mammalian species
Workman, A. D., Charvet, C. J., Clancy, B., Darlington, R. B., & Finlay, B. L. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.5746-12.2013 · Cited by 833 · see citing works
Steen, R. G., Mull, C., Mcclure, R., Hamer, R. M., & Lieberman, J. A. (2006) · British Journal of Psychiatry · doi:10.1192/bjp.188.6.510 · Cited by 832 · see citing works
Glutamate and dopamine in schizophrenia: An update for the 21 <sup>st</sup> century
Howes, O., McCutcheon, R., & Stone, J. (2015) · Journal of Psychopharmacology · doi:10.1177/0269881114563634 · Cited by 702 · see citing works
Prenatal Poly(I:C) Exposure and Other Developmental Immune Activation Models in Rodent Systems
Meyer, U. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.07.011 · Cited by 626 · see citing works
From neuropathology to neurodevelopment
Weinberger, D. R. (1995) · The Lancet · doi:10.1016/s0140-6736(95)91386-6 · Cited by 568 · see citing works
Achim, A. M., Maziade, M., Raymond, E., Olivier, D. H., Mérette, C., & Roy, M. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbp148 · Cited by 528 · see citing works
Epigenetic and transgenerational reprogramming of brain development
Bale, T. L. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3818 · Cited by 505 · see citing works
Zuckerman, L., Rehavi, M., Nachman, R., & Weiner, I. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300248 · Cited by 501 · see citing works
Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia
Meyer, U., Feldon, J., Schedlowski, M., & Yee, B. K. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.012 · Cited by 494 · see citing works
Olabi, B., Ellison-Wright, I., McIntosh, A. M., Wood, S. J., Bullmore, E. T., & Lawrie, S. M. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.01.032 · Cited by 485 · see citing works
Khandaker, G. M., Zimbron, J., Lewis, G., & Jones, P. B. (2012) · Psychological Medicine · doi:10.1017/s0033291712000736 · Cited by 468 · see citing works
Ozawa, K., Hashimoto, K., Kishimoto, T., Shimizu, E., Ishikura, H., & Iyo, M. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.07.031 · Cited by 467 · see citing works
Meyer, U., Nyffeler, M., Yee, B. K., Knuesel, I., & Feldon, J. (2008) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.09.012 · Cited by 457 · see citing works
Glutamate in Schizophrenia: A Focused Review and Meta-Analysis of 1H-MRS Studies
Marsman, A., van den Heuvel, M. P., Klomp, D. W. J., Kahn, R. S., Luijten, P. R., & Hulshoff Pol, H. E. (2013) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr069 · Cited by 457 · see citing works
Magnetic resonance imaging studies in bipolar disorder and schizophrenia: meta-analysis
Arnone, D., Cavanagh, J., Gerber, D., Lawrie, S. M., Ebmeier, K. P., & McIntosh, A. M. (2009) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.108.059717 · Cited by 441 · see citing works
Activation of the maternal immune system induces endocrine changes in the placenta via IL-6
Hsiao, E. Y., & Patterson, P. H. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.12.017 · Cited by 402 · see citing works
Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring
Zuckerman, L., & Weiner, I. (2004) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2004.08.008 · Cited by 352 · see citing works
van Haren, N. E. M., Pol, H. E. H., Schnack, H. G., Cahn, W., Brans, R. G. H., Carati, I., Rais, M., & Kahn, R. S. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.01.004 · Cited by 278 · see citing works
Childhood infection and adult schizophrenia: A meta-analysis of population-based studies
Khandaker, G. M., Zimbron, J., Dalman, C., Lewis, G., & Jones, P. B. (2012) · Schizophrenia Research · doi:10.1016/j.schres.2012.05.023 · Cited by 257 · see citing works
Meyer, U., & Feldon, J. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.009 · Cited by 247 · see citing works
Bitanihirwe, B. K., Peleg-Raibstein, D., Mouttet, F., Feldon, J., & Meyer, U. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.129 · Cited by 237 · see citing works
Samartzis, L., Dima, D., Fusar‐Poli, P., & Kyriakopoulos, M. (2014) · Journal of Neuroimaging · doi:10.1111/j.1552-6569.2012.00779.x · Cited by 236 · see citing works
Vuillermot, S., Weber, L., Feldon, J., & Meyer, U. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5408-09.2010 · Cited by 217 · see citing works
Canetta, S., Bolkan, S., Padilla-Coreano, N., Song, L. J., Sahn, R., Harrison, N. L., Gordon, J. A., Brown, A., & Kellendonk, C. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.222 · Cited by 201 · see citing works
Microglial activation in a neuroinflammational animal model of schizophrenia – a pilot study
Juckel, G., Manitz, M. P., Brüne, M., Friebe, A., Heneka, M. T., & Wolf, R. J. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.06.018 · Cited by 165 · see citing works
Systematic Review of the Neurobiological Relevance of Chemokines to Psychiatric Disorders
Stuart, M. J., Singhal, G., & Baune, B. T. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00357 · Cited by 163 · see citing works
Li, Q., Cheung, C., Wei, R., Hui, E. S. K., Feldon, J., Meyer, U., Chung, S. K., Chua, S. E., Sham, P. C., Wu, E. X., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006354 · Cited by 149 · see citing works
Piontkewitz, Y., Assaf, Y., & Weiner, I. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.07.005 · Cited by 143 · see citing works
Piontkewitz, Y., Arad, M., & Weiner, I. (2010) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq040 · Cited by 143 · see citing works
Steeds, H., Carhart-Harris, R. L., & Stone, J. M. (2014) · Therapeutic Advances in Psychopharmacology · doi:10.1177/2045125314557797 · Cited by 134 · see citing works
Missault, S., Van den Eynde, K., Vanden Berghe, W., Fransen, E., Weeren, A., Timmermans, J. P., Kumar-Singh, S., & Dedeurwaerdere, S. (2014) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2014.06.013 · Cited by 128 · see citing works
Synaptic changes in the brain of subjects with schizophrenia
Faludi, G., & Mirnics, K. (2011) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.02.013 · Cited by 127 · see citing works
Gogtay, N., Lu, A., Leow, A. D., Klunder, A. D., Lee, A. D., Chavez, A., Greenstein, D., Giedd, J. N., Toga, A. W., Rapoport, J. L., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806485105 · Cited by 125 · see citing works
Ribeiro, B. M. M., do Carmo, M. R. S., Freire, R. S., Rocha, N. F. M., Borella, V., Menezes, A. T., Monte, A. S., Gomes, P. X. L., de Sousa, F. C. F., Vale, M. L., et al. (2013) · Schizophrenia Research · doi:10.1016/j.schres.2013.10.040 · Cited by 123 · see citing works
Arsenault, D., St-Amour, I., Cisbani, G., Rousseau, L.-S., & Cicchetti, F. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.12.016 · Cited by 118 · see citing works
Meehan, C. L., Harms, L. R., Frost, J. D., Barreto, R., Todd, J., Schall, U., Weickert, C. S., Zavitsanou, K., Michie, P. T., & Hodgson, D. M. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.07.144 · Cited by 115 · see citing works
Avramopoulos, D., Pearce, B. D., McGrath, J. A., Wolyniec, P. S., Wang, R., Eckart, N., Hatzimanolis, A., Goes, F. S., Nestadt, G., Mulle, J. G., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0116696 · Cited by 111 · see citing works
Meyer, U., & Feldon, J. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1504-9 · Cited by 109 · see citing works
Tracing the development of psychosis and its prevention: what can be learned from animal models
Piontkewitz, Y., Arad, M., & Weiner, I. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.019 · Cited by 108 · see citing works
Psychosis and brain volume changes during the first five years of schizophrenia
Cahn, W., Rais, M., Stigter, F. P., van Haren, N. E. M., Caspers, E., Pol, H. E. H., Xu, Z., Schnack, H. G., & Kahn, R. S. (2008) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2008.10.006 · Cited by 101 · see citing works
Meyer, U., Knuesel, I., Nyffeler, M., & Feldon, J. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1754-6 · Cited by 94 · see citing works
Piontkewitz, Y., Bernstein, H., Dobrowolny, H., Bogerts, B., Weiner, I., & Keilhoff, G. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.11.004 · Cited by 93 · see citing works
Eyles, D., Feldon, J., & Meyer, U. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.6 · Cited by 92 · see citing works
Fatemi, S. H., Folsom, T. D., Rooney, R. J., Mori, S., Kornfield, T. E., Reutiman, T. J., Kneeland, R. E., Liesch, S. B., Hua, K., Hsu, J., et al. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.011 · Cited by 81 · see citing works
Vorhees, C. V., Graham, D. L., Braun, A. A., Schaefer, T. L., Skelton, M. R., Richtand, N. M., & Williams, M. T. (2014) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2014.10.007 · Cited by 71 · see citing works
Forrest, C. M., Khalil, O. S., Pisar, M., Smith, R. A., Darlington, L. G., & Stone, T. W. (2012) · Molecular Brain · doi:10.1186/1756-6606-5-22 · Cited by 71 · see citing works
Prenatal Infection Affects the Neuronal Architecture and Cognitive Function in Adult Mice
Li, W., Chang, Y.-C., Lee, L. J., & Lee, L. (2014) · Developmental Neuroscience · doi:10.1159/000362383 · Cited by 68 · see citing works
Yee, N., Ribic, A., de Roo, C. C., & Fuchs, E. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.05.040 · Cited by 64 · see citing works
Roenker, N. L., Gudelsky, G. A., Ahlbrand, R. A., Bronson, S. L., Kern, J. R., Waterman, H., & Richtand, N. M. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.06.011 · Cited by 58 · see citing works
Li, Q., Cheung, C., Wei, R., Cheung, V., Hui, E. S. K., You, Y., Wong, P., Chua, S. E., McAlonan, G. M., & Wu, E. X. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.015 · Cited by 55 · see citing works
Age-related brain trajectories in schizophrenia: A systematic review of structural MRI studies
Chiapponi, C., Piras, F., Fagioli, S., Piras, F., Caltagirone, C., & Spalletta, G. (2013) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2013.05.003 · Cited by 52 · see citing works
Lawrie, S. M., Abukmeil, S. S., Chiswick, A., Egan, V., Santosh, C., & Best, J. J. K. (1997) · Schizophrenia Research · doi:10.1016/s0920-9964(97)00019-4 · Cited by 52 · see citing works
Ratnayake, U., Quinn, T., LaRosa, D. A., Dickinson, H., & Walker, D. W. (2014) · Developmental Neuroscience · doi:10.1159/000362205 · Cited by 46 · see citing works
Zavitsanou, K., Lim, C. K., Purves-Tyson, T., Karl, T., Kassiou, M., Banister, S. D., Guillemin, G. J., & Weickert, C. S. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.05.011 · Cited by 46 · see citing works
Association of Interleukin-10 Polymorphisms with Schizophrenia: A Meta-Analysis
Gao, L., Zhao, L., Chang, S., & Wang, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090407 · Cited by 45 · see citing works
Macêdo, D. S., de Araújo, D. P., Sampaio, L. R. L., Vasconcelos, S. M. M., Sales, P. M. G., de Sousa, F. C. F., Hallak, J. E. C., Crippa, J. A., & Carvalho, A. F. (2012) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2012007500031 · Cited by 44 · see citing works
Richtand, N. M., Ahlbrand, R. A., Horn, P. S., Stanford, K. E., Bronson, S. L., & McNamara, R. K. (2011) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2011.02.007 · Cited by 38 · see citing works
Vernon, A. C., So, P., Lythgoe, D. J., Chege, W., Cooper, J. D., Williams, S., & Kapur, S. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.09.022 · Cited by 35 · see citing works
Multivariate analyses applied to fetal, neonatal and pediatric MRI of neurodevelopmental disorders
Levman, J. E. D., & Takahashi, E. (2015) · NeuroImage Clinical · doi:10.1016/j.nicl.2015.09.017 · Cited by 24 · see citing works
Murine model to study brain, behavior and immunity during hepatic encephalopathy
Gomides, L. F. (2014) · World Journal of Hepatology · doi:10.4254/wjh.v6.i4.243 · Cited by 22 · see citing works
Pircher, J., Czermak, T., Merkle, M., Mannell, H., Krötz, F., Ribeiro, A., Vielhauer, V., Nadjiri, J., Gaitzsch, E., Niemeyer, M., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113351 · Cited by 20 · see citing works
Contribution of nonprimate animal models in understanding the etiology of schizophrenia
Lazar, N. L., Neufeld, R. W. J., & Cain, D. P. (2011) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.100054 · Cited by 18 · see citing works
[PolyI:C-induced neurodevelopmental animal model for schizophrenia].
Ibi, D., Nagai, T., Nabeshima, T., & Yamada, K. (2011) · PubMed · Cited by 10 · see citing works
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Neuroinflammation as a risk factor for attention deficit hyperactivity disorder
Dunn, G. A., Nigg, J. T., & Sullivan, E. L. (2019) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2019.05.005 · Cited by 299 · 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
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 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
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
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
Bao, M., Hofsink, N., & Plösch, T. (2021) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00087.2021 · Cited by 91 · see citing works
Chamera, K., Trojan, E., Szuster-Głuszczak, M., & Basta‐Kaim, A. (2019) · Current Neuropharmacology · doi:10.2174/1570159x17666191113101629 · Cited by 80 · see citing works
Aguilar-Valles, A., Rodrigue, B., & Matta-Camacho, E. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00852 · Cited by 62 · see citing works
Active HHV-6 Infection of Cerebellar Purkinje Cells in Mood Disorders
Prusty, B. K., Gulve, N., Govind, S., Krueger, G. R. F., Feichtinger, J., Larcombe, L. D., Aspinall, R., Ablashi, D. V., & Toro, C. T. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01955 · Cited by 63 · see citing works
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
Behavioral Tasks Evaluating Schizophrenia-like Symptoms in Animal Models: A Recent Update
Ang, M. J., Lee, S., Kim, J.-C., Kim, S., & Moon, C. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200814175114 · Cited by 51 · see citing works
Sun, L., Min, L., Zhou, H., Li, M., Shao, F., & Wang, W. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.07.011 · Cited by 51 · see citing works
Graham, A. M., Doyle, O. J., Tilden, E. L., Sullivan, E. L., Gustafsson, H., Marr, M. C., Allen, M. C., & Seghete, K. L. M. (2021) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2021.10.012 · Cited by 54 · see citing works
Kreitz, S., Zambon, A., Ronovsky, M., Budinský, L., Helbich, T. H., Sideromenos, S., Ivan, C., Konerth, L., Wank, I., Berger, A., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.09.011 · Cited by 45 · see citing works
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 · see citing works
Schizophrenia, a disease of impaired dynamic metabolic flexibility: A new mechanistic framework
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Yousif, N. M., de Oliveira, A. C. P., Brioschi, S., Hüell, M., Biber, K. P. H., & Fiebich, B. L. (2017) · Glia · doi:10.1002/glia.23276 · Cited by 39 · see citing works
Stress, depression, and hippocampus: from biochemistry to electrophysiology
Idunkova, A., Lacinová, Ľ., & Hoppanová, L. (2023) · General Physiology and Biophysics · doi:10.4149/gpb_2023001 · Cited by 36 · see citing works
Chamera, K., Szuster-Głuszczak, M., Trojan, E., & Basta-Kaim, A. (2020) · Cells · doi:10.3390/cells9071676 · Cited by 31 · see citing works
Aria, F., Bonini, S. A., Cattaneo, V., Premoli, M., Mastinu, A., Maccarinelli, G., & Memo, M. (2020) · Brain Sciences · doi:10.3390/brainsci10090620 · Cited by 28 · see citing works
Haddad, F. L., Oliveira, C. D., & Schmid, S. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1160243 · Cited by 21 · see citing works
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Mora, S., Martín-González, E., Flores, P., & Moreno, M. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.02.027 · Cited by 15 · see citing works
Missault, S., Anckaerts, C., Ahmadoun, S., Blockx, I., Barbier, M., Bielen, K., Shah, D., Kumar‐Singh, S., Vos, W. H. D., der Linden, A. V., et al. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.02.040 · Cited by 14 · see citing works
Chen, L., Li, Z., & Fan, Y. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1601888 · Cited by 12 · see citing works
Casquero‐Veiga, M., Lamanna‐Rama, N., Romero‐Miguel, D., Márquez, H. R., Alcaide, J., Beltrán, M. A. C. S., Nácher, J., Desco, M., & Soto‐Montenegro, M. L. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1022622 · Cited by 12 · see citing works
Xu, J., Zhao, R., Yan, M., Zhou, M. R., Liu, H., Wang, X., Lu, C. F., Li, Q., Mo, Y., Zhang, P., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25189885 · Cited by 9 · see citing works
Felgel-Farnholz, V., Hlusicka, E. B., Edemann-Callesen, H., Garthe, A., Winter, C., & Hadar, R. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114276 · Cited by 9 · see citing works
Changes in ADAR RNA editing patterns in CMV and ZIKV congenital infections
Wales-McGrath, B. D., Mercer, H., & Piontkivska, H. (2023) · BMC Genomics · doi:10.1186/s12864-023-09778-4 · Cited by 8 · see citing works
Patel, R. T., Gallamoza, B., Kulkarni, P. P., Sherer, M. L., Haas, N. A., Lemanski, E. A., Malik, I., Hekmatyar, K., Parcells, M. S., & Schwarz, J. M. (2021) · Viruses · doi:10.3390/v13061123 · Cited by 7 · see citing works
Yu, S., Lee, C.-W., Li, Y., Chen, T.-H., & Yu, H. (2022) · Dermatologica Sinica · doi:10.4103/ds.ds_6_22 · Cited by 7 · see citing works
Liu, W., Yan, K., Xu, S., Li, L., Zhong, M., Li, G., Li, G., & Yang, J. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.12.018 · Cited by 4 · see citing works
The role of gut-brain axis in mood disorder
Sallem, C. C., Filho, L. B. D. A., da Costa, R. I., Lima, M. P. P., Pimentel, I. D. S., de Figueirêdo, L. R. B., Lima, N. M. P., Galvão, S. L., de Lima, G. M. D. S., Gomes, G. F., et al. (2022) · Journal of Neurology & Stroke · doi:10.15406/jnsk.2022.12.00516 · Cited by 4 · see citing works
Sharma, R., Kearns, M. M., Sarr, F., & Ismail, N. (2019) · Immunology Letters · doi:10.1016/j.imlet.2019.03.005 · Cited by 4 · see citing works
Taşkıran, M., Taskiran, S. Y., Ünal, G., Bozkurt, N. M., & Gölgeli, A. (2024) · Fundamental and Clinical Pharmacology · doi:10.1111/fcp.13028 · Cited by 3 · see citing works
Duarte, R., Ribeiro-Barbosa, É. R., Ferreira, F. R., Espíndola, F. S., & Spini, V. B. M. G. (2024) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2024.111188 · Cited by 3 · see citing works
Deane, A. R., & Ward, R. D. (2022) · Journal of the Experimental Analysis of Behavior · doi:10.1002/jeab.753 · Cited by 1 · see citing works
Systemic inflammation causes microglial dysfunction with a mixed AD-like pathologyPreprint
Bathini, P., Dupanloup, I., Zenaro, E., Terrabuio, E., Fischer, A., Ballabani, E., Doucey, M., & Alberi, L. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.27.223198 · Cited by 1 · see citing works
Inflammation and immune-mediated neurobehavioral alterations : a critical role for microglia
Lacabanne, C. (2018) · theses.fr (ABES) · doi:10.70675/41a4e2a3zdbb7z4aa0z899dz9553bb07954b · Cited by 1 · see citing works
Couture, P. (2019) · uO Research (University of Ottawa) · doi:10.20381/ruor-23143
Systemic Inflammation Causes Microglial Dysfunction with a Mixed AD-Like Pathology.Preprint
Bathini, P., Dupanloup, I., Zenaro, E., Terrabuio, E., Fisher, A., Babaliani, E., Doucey, M., & Alberi, L. A. (2020) · Research Square · doi:10.21203/rs.3.rs-48807/v1
Systemic inflammation causes microglial dysfunction with a mixed AD-like pathologyPreprint
Bathini, P., Dupanloup, I., Zenaro, E., Terrabuio, E., Fischer, A., Ballabani, E., Doucey, M., & Alberi, L. A. (2021) · Research Square · doi:10.21203/rs.3.rs-145868/v1
Systemic Inflammation Causes Microglial Dysfunction With a Mixed Ad-like PathologyPreprint
Bathini, P., Dupanloup, I., Zenaro, E., Terrabuio, E., Fisher, A., Babaliani, E., Doucey, M., & Alberi, L. A. (2020) · Research Square · doi:10.21203/rs.3.rs-80087/v1
Liu, J., Liu, J., & Ke, X. (2024) · PubMed Central · doi:10.7499/j.issn.1008-8830.2309147 · Cited by 1 · see citing works
Understanding schizophrenia through animal models: The role of environmental stressors
Manojlović, M. (2024) · Arhiv za farmaciju · doi:10.5937/arhfarm74-54845
Ohkawara, T., Ida‐Eto, M., & Narita, M. (2025) · Gene · doi:10.1016/j.gene.2025.149780
Animal models of attention-deficit/hyperactivity disorder: Diversity and validity
Nehme, S. B. S., Sánchez‐Sarasúa, S., Medrano, M., Bouchatta, O., Bitar, T., Alameddine, A., Galineau, L., Brunault, P., Kerekes, N., Sánchez‐Pérez, A. M., et al. (2025) · Pharmacological Reviews · doi:10.1016/j.pharmr.2025.100108
- Authors
- da Silveira, V. T., de Castro Medeiros, D., Ropke, J., Guidine, P. A., Rezende, G. H., Moraes, M. F. D., Mendes, E. M. A. M., Macedo, D., Moreira, F. A., & de Oliveira, A. C. P.
- Affiliations
- Department of Pharmacology Institute of Biological Sciences, Universidade Federal de Minas Gerais Brazil
- Center for Technology and Research in Magneto‐Resonance (CTPMAG), Graduate Program in Electrical Engineering – Universidade Federal de Minas Gerais Brazil
- Universidade Federal de Minas Gerais (BR)
- Drug Research and Development Center Department of Physiology and Pharmacology Medical School, Universidade Federal do Ceará Brazil
- Venue
- International Journal of Developmental Neuroscience
- Publisher
- Wiley
- Published
- 2017-01-22
- Volume
- 58
- Issue
- 1
- Pages
- 1-8
- ISSN
- 0736-5748 (ISSN-L)
- 1873-474X
- OpenAlex
- W2581631145
- Cited by
- 51
- References
- 70
- Citations by year
- 2025: 3 · 2024: 9 · 2023: 4 · 2022: 5 · 2021: 4 · 2020: 9 · 2019: 9 · 2018: 4 · 2017: 4
- FWCI
- 2.37
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- International Journal of Developmental Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (publishedVersion)
- Funders
- Fundação de Amparo à Pesquisa do Estado de Minas Gerais
- Conselho Nacional de Desenvolvimento Científico e Tecnológico (479254/2013‐3, 466724/2014‐4)
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- maternal immune activation, schizophrenia, poly(I:C), pregnancy timing, prenatal immune activation, brain morphometry, anxiety-like behavior, locomotor activity, brain volume, brain development, neuroimmunology, positive and negative symptoms
- MeSH terms
- Age Factors, Analysis of Variance, Animals, Animals, Newborn, Mental Disorders, Brain, Disease Models, Animal, Embryo, Mammalian, Female, Food Preferences, Interferon Inducers, Ketamine, Locomotion, Magnetic Resonance Imaging, Mice, Inbred C57BL, Poly I-C, Pregnancy, Prenatal Exposure Delayed Effects, Schizophrenia, Sucrose, Mice
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