Maternal infection during pregnancy aggravates the behavioral response to an immune challenge during adolescence in female rats

Brown, 2011, The environment and susceptibility to schizophrenia, Prog. Neurobiol. [Internet], 93, 23, 10.1016/j.pneurobio.2010.09.003 Herbert, 2010, Contributions of the environment and environmentally vulnerable physiology to autism spectrum disorders, Curr. Opin. Neurol. Engl., 23, 103, 10.1097/WCO.0b013e328336a01f Tsuchiya, 2003, Risk factors in relation to an emergence of bipolar disorder: a systematic review, Bipolar Disord. Den., 5, 231, 10.1034/j.1399-5618.2003.00038.x Pedersen, 2001, Evidence of a dose-response relationship between urbanicity during upbringing and schizophrenia risk, Arch. Gen. Psychiatry. United States, 58, 1039, 10.1001/archpsyc.58.11.1039 Brown, 2006, Prenatal infection as a risk factor for schizophrenia, Schizophr. Bull., 32, 200, 10.1093/schbul/sbj052 Brown, 2001, Prenatal rubella, premorbid abnormalities, and adult schizophrenia, Biol. Psychiatry [Internet], 49, 473, 10.1016/S0006-3223(01)01068-X Blomström, 2016, Associations between maternal infection during pregnancy, childhood infections, and the risk of subsequent psychotic disorder--a swedish cohort study of nearly 2 million individuals, Schizophr. Bull. U. S., 42, 125 Blomström, 2014, Hospital admission with infection during childhood and risk for psychotic illness--a population-based cohort study, Schizophr. Bull. U. S., 40, 1518, 10.1093/schbul/sbt195 Khandaker, 2012, Childhood infection and adult schizophrenia: a meta-analysis of population-based studies, Schizophr. Res., 10.1016/j.schres.2012.05.023 Stilo, 2019, Non-genetic factors in schizophrenia, Curr. Psychiatry Rep., 10.1007/s11920-019-1091-3 Stilo, 2010, The epidemiology of schizophrenia: replacing dogma with knowledge [Internet], Dialog-. Clin. Neurosci., 10.31887/DCNS.2010.12.3/sstilo Selten, 2010, Schizophrenia and 1957 pandemic of influenza: meta-analysis, Schizophr. Bull., 36, 219, 10.1093/schbul/sbp147 Mednick, 1988, Adult schizophrenia following prenatal exposure to an influenza epidemic, Arch. Gen. Psychiatry. United States, 45, 189, 10.1001/archpsyc.1988.01800260109013 Hjorthøj, 2020, Infections as a risk factor forand prognostic factor after substance-induced psychoses, Am. J. Psychiatry [Internet], 177, 335, 10.1176/appi.ajp.2019.19101047 Bayer, 1999, Genetic and non-genetic vulnerability factors in schizophrenia: the basis of the “Two hit hypothesis.”, J. Psychiatr. Res., 33, 543, 10.1016/S0022-3956(99)00039-4 Guerrin, 2021, The dual hit hypothesis of schizophrenia: evidence from animal models, Neurosci. Biobehav Rev. [Internet], 131, 1150, 10.1016/j.neubiorev.2021.10.025 Spear, 2013, Adolescent neurodevelopment, 52, S7 Brenhouse, 2016, Immunoadolescence: neuroimmune development and adolescent behavior, Neurosci. Biobehav. Rev. U. S., 70, 288, 10.1016/j.neubiorev.2016.05.035 Germann, 2021, Abnormal synaptic pruning during adolescence underlying the development of psychotic disorders, Curr. Opin. Psychiatry [Internet]. NLM (Medlin.), 10.1097/YCO.0000000000000696 Koyama, 2015, Microglia in the pathogenesis of autism spectrum disorders, Neurosci. Res. [Internet], 100, 1, 10.1016/j.neures.2015.06.005 Hughes, 2020, Overlapping evidence of innate immune dysfunction in psychotic and affective disorders, Brain, Behav. Immun. - Heal [Internet], 2 Meltzer, 2017, The role of the immune system in Autism spectrum disorder, Neuropsychopharmacol. [Internet], 42, 284, 10.1038/npp.2016.158 Marques, 2019, Neuroinflammation in schizophrenia: meta-analysis of in vivo microglial imaging studies, Psychol. Med., 49, 2186, 10.1017/S0033291718003057 Brown, 2018, Maternal immune activation and neuropsychiatric illness: a translational research perspective, Am. J. Psychiatry, 10.1176/appi.ajp.2018.17121311 Giovanoli, 2015, Late prenatal immune activation causes hippocampal deficits in the absence of persistent inflammation across aging, J. Neuroinflamm., 12, 221, 10.1186/s12974-015-0437-y Giovanoli, 2016, Prenatal immune activation causes hippocampal synaptic deficits in the absence of overt microglia anomalies, Brain Behav. Immun. [Internet], 55, 25, 10.1016/j.bbi.2015.09.015 Garay, 2013, Maternal immune activation causes age- and region-specific changes in brain cytokines in offspring throughout development, Brain Behav. Immun., 10.1016/j.bbi.2012.07.008 Missault, 2014, The risk for behavioural deficits is determined by the maternal immune response to prenatal immune challenge in a neurodevelopmental model, 42, 138 Guerrin, 2022, Immune activation in pregnant rats affects brain glucose consumption, anxiety-like behaviour and recognition memory in their male offspring, Mol. Imaging Biol. [Internet], 10.1007/s11307-022-01723-3 Zhu, 2014, Minocycline alleviates behavioral deficits and inhibits microglial activation in the offspring of pregnant mice after administration of polyriboinosinic–polyribocytidilic acid, Psychiatry Res. [Internet], 219, 680, 10.1016/j.psychres.2014.06.046 Juckel, 2011, Microglial activation in a neuroinflammational animal model of schizophrenia - a pilot study, Schizophr. Res., 10.1016/j.schres.2011.06.018 Mattei, 2014, Minocycline rescues decrease in neurogenesis, increase in microglia cytokines and deficits in sensorimotor gating in an animal model of schizophrenia Li, 2018, Microglia activation in the offspring of prenatal poly I: C exposed rats: A PET imaging and immunohistochemistry study, Gen. Psychiatry, 31, 29 On Wah, 2019, Lipopolysaccharide (LPS) induced sickness in early adolescence alters the behavioral effects of the short-chain fatty acid, propionic acid, in late adolescence and adulthood: examining anxiety and startle reactivity, Behav. Brain Res. [Internet], 360, 312, 10.1016/j.bbr.2018.12.003 Rico, 2010, Neonatal exposure to LPS leads to heightened exploratory activity in adolescent rats, Behav. Brain Res. [Internet], 215, 102, 10.1016/j.bbr.2010.07.001 Spencer, 2006, Early-Life immune challenge: defining a critical window for effects on adult responses to immune challenge, Neuropsychopharmacol. [Internet], 31, 1910, 10.1038/sj.npp.1301004 Clark, 2019, Maternal immune activation in rats blunts brain cytokine and kynurenine pathway responses to a second immune challenge in early adulthood, Prog Neuro-Psychopharmacol. Biol. Psychiatry, 89, 286, 10.1016/j.pnpbp.2018.09.011 Lins, 2019, Maternal immune activation during pregnancy alters the behavior profile of female offspring of Sprague Dawley Rats, eneuro [Internet], 6 Klein, 2002, Seeing the unexpected: how sex differences in stress responses may provide a new perspective on the manifestation of psychiatric disorders, Curr. Psychiatry Rep. U. S., 4, 441, 10.1007/s11920-002-0072-z Riecher-Rössler A. Prospects for the classification of mental disorders in women. Eur Psychiatry [Internet]. 2020/04/16. Cambridge University Press; 2010;25:189–96. Available from: https://www.cambridge.org/core/article/prospects-for-the-classification-of-mental-disorders-in-women/5529E29C335C596ECA5712A4AFD9BF9C. Riecher-Rössler, 2017, Oestrogens, prolactin, hypothalamic-pituitary-gonadal axis, and schizophrenic psychoses, 4, 63 Li, 2017, Why are women so vulnerable to anxiety, trauma-related and stress-related disorders? The potential role of sex hormones, 4, 73 Kuehner, 2017, Why is depression more common among women than among men, 4, 146 Riecher-Rössler, 2017, Sex and gender differences in mental disorders, Lancet Psychiatry [Internet], 4, 8, 10.1016/S2215-0366(16)30348-0 Careaga, 2017, Maternal immune activation and autism spectrum disorder: from rodents to nonhuman and human primates, Biol. Psychiatry, 81, 391, 10.1016/j.biopsych.2016.10.020 Bassi, 2012, Lipopolysaccharide-induced sickness behaviour evaluated in different models of anxiety and innate fear in rats, Basic Clin. Pharm. Toxicol. [Internet]. John Wiley Sons, Ltd, 110, 359, 10.1111/j.1742-7843.2011.00824.x Fullerton JN, Segre E, DeMaeyer RPH, Maini AAN, Gilroy DW. Intravenous Endotoxin Challenge in HealthyHumans: An Experimental Platform to Investigate and Modulate SystemicInflammation. J Vis Exp [Internet]. MyJove Corporation; 2016;53913. Availablefrom: https://pubmed.ncbi.nlm.nih.gov/27213711. Prata, 2019, The Contribution of Inflammation to Autism Spectrum Disorders: Recent Clinical Evidence BT - Psychiatric Disorders: Methods and Protocols, 493 Wohleb, 2017, Dynamic cross-talk between microglia and peripheral monocytes underlies stress-induced neuroinflammation and behavioral consequences, Prog. Neuro-Psychopharmacol. Biol. Psychiatry [Internet], 79, 40, 10.1016/j.pnpbp.2016.04.013 Bayer, 1999, Evidence for activation of microglia in patients with psychiatric illnesses, Neurosci. Lett., 10.1016/S0304-3940(99)00545-5 Tay, 2018, Microglia gone rogue: impacts on psychiatric disorders across the lifespan, [Internet]. Front. Mol. Neurosci., 10.3389/fnmol.2017.00421 Yildiz, 2011, Parietal lobes in schizophrenia: do they matter?, Schizophr Res. Treatment. Egypt, 2011 Teixeira, 2014, Integrative parietal cortex processes: neurological and psychiatric aspects, J. Neurol. Sci. Neth., 338, 12, 10.1016/j.jns.2013.12.025 Gamo, 2011, Molecular modulation of prefrontal cortex: rational development of treatments for psychiatric disorders, Behav. Neurosci. U. S., 125, 282, 10.1037/a0023165 Murray, 2019, Evolution of a maternal immune activation (mIA) model in rats: early developmental effects, Brain Behav. Immun. [Internet], 75, 48, 10.1016/j.bbi.2018.09.005 Dalton, 2012, Synergistic effect between maternal infection and adolescent cannabinoid exposure on serotonin 5HT 1A receptor binding in the hippocampus: testing the “Two Hit” hypothesis for the development of schizophrenia, ISRN Psychiatry, 2012, 1, 10.5402/2012/451865 Kentner, 2019, Maternal immune activation: reporting guidelines to improve the rigor, reproducibility, and transparency of the model, 44, 245 Hao, 2019, Prenatal immune activation induces age-related alterations in rat offspring: effects upon NMDA receptors and behaviors, Behav. Brain Res., 10.1016/j.bbr.2019.111946 Schneider, 2011, A novel elevated plus-maze procedure to avoid the one-trial tolerance problem, [Internet]. Front. Behav. Neurosci., 10.3389/fnbeh.2011.00043 Gould, 2009, 1 Trezza, 2011, Nucleus accumbens μ-opioid receptors mediate social reward, J. Neurosci. [Internet], 31 Houwing, 2019, Subjecting dams to early life stress and perinatal fluoxetine treatment differentially alters social behavior in young and adult rat offspring, [Internet]. Front. Neurosci., 10.3389/fnins.2019.00229 Osborne, 2019, Cannabidiol improves behavioural and neurochemical deficits in adult female offspring of the maternal immune activation (poly I:C) model of neurodevelopmental disorders, Brain Behav. Immun. [Internet], 81, 574, 10.1016/j.bbi.2019.07.018 Osborne, 2017, Improved social interaction, recognition and working memory with cannabidiol treatment in a prenatal infection (poly I:C) rat model, Neuropsychopharmacol. [Internet], 42, 1447, 10.1038/npp.2017.40 Gzielo, 2021, The effect of maternal immune activation on social play-induced ultrasonic vocalization in rats, Brain Sci., 11 Chamera, 2020, The prenatal challenge with lipopolysaccharide and polyinosinic:polycytidylic acid disrupts CX3CL1-CX3CR1 and CD200-CD200R signalling in the brains of male rat offspring: a link to schizophrenia-like behaviours, J. Neuroinflamm. [Internet], 17, 247, 10.1186/s12974-020-01923-0 Goh, 2020, Gestational poly(I:C) attenuates, not exacerbates, the behavioral, cytokine and mTOR changes caused by isolation rearing in a rat ‘dual-hit’ model for neurodevelopmental disorders, 89, 100 Gzieło, 2022, 1 Gray, 2019, Maternal immune activation in mid-late gestation alters amphetamine sensitivity and object recognition, but not other schizophrenia-related behaviours in adult rats, Behav. Brain Res., 10.1016/j.bbr.2018.08.016 Guma, 2020, Early or late gestational exposure to maternal immune activation alters neurodevelopmental trajectories in mice: An integrated neuroimaging, behavioural, and transcriptional study, bioRxiv Mueller, 2021, Behavioral, neuroanatomical, and molecular correlates of resilience and susceptibility to maternal immune activation, Mol. Psychiatry [Internet], 26, 396, 10.1038/s41380-020-00952-8 Richetto, 2013, Prenatal versus postnatal maternal factors in the development of infection-induced working memory impairments in mice, Brain Behav. Immun. [Internet], 33, 190, 10.1016/j.bbi.2013.07.006 Chamera, 2021, Role of polyinosinic:polycytidylic acid-induced maternal immune activation and subsequent immune challenge in the behaviour and microglial cell trajectory in adult offspring: a study of the neurodevelopmental model of schizophrenia, Int. J. Mol. Sci., 10.3390/ijms22041558 Meyer, 2008, Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated anti-inflammatory signaling, Mol. Psychiatry, 13, 208, 10.1038/sj.mp.4002042 Meyer, 2006, The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology, J. Neurosci., 26, 4752, 10.1523/JNEUROSCI.0099-06.2006 Reed, 2020, IL-17a promotes sociability in mouse models of neurodevelopmental disorders, Nature. England, 577, 249, 10.1038/s41586-019-1843-6 Fabricius, 2011, Socially isolated rats exhibit changes in dopamine homeostasis pertinent to schizophrenia, 29, 347 Gunaydin, 2014, Dopaminergic dynamics contributing to social behavior, Cold Spring Harb. Symp. Quant. Biol. U. S., 79, 221, 10.1101/sqb.2014.79.024711 Krach, 2010, The rewarding nature of social interactions [Internet], Front. Behav. Neurosci., 10.3389/fnbeh.2010.00022 Lai, 2019, Prevalence of co-occurring mental health diagnoses in the autism population: a systematic review and meta-analysis, Lancet Psychiatry [Internet], 6, 819, 10.1016/S2215-0366(19)30289-5 Sano, 2012, Enhanced persistency of resting and active periods of locomotor activity in schizophrenia, PLoS One [Internet]. Public Libr. Sci., 7 Van Den Eynde, 2014, Hypolocomotive behaviour associated with increased microglia in a prenatal immune activation model with relevance to schizophrenia, Behav. Brain Res., 10.1016/j.bbr.2013.10.005 Ozaki, 2020, Maternal immune activation induces sustained changes in fetal microglia motility, Sci. Rep. [Internet], 10, 21378, 10.1038/s41598-020-78294-2 Conen, 2020, Neuroinflammation as measured by positron emission tomography in patients with recent onset and established schizophrenia: implications for immune pathogenesis, 1 Reis Marques T., Ashok A.H., Pillinger T., Veronese M., Turkheimer F.E., Dazzan P., et al. Psychological MedicineNeuroinflammation in schizophrenia: meta-analysis of in vivo microglial imagingstudies. 2018 [cited 2020 Jun 24]; Available from:https://doi.org/10.1017/S0033291718003057. Fond, 2020, The role of inflammation in the treatment of schizophrenia, Front. Psychiatry [Internet]. Front. Media S. A., 10.3389/fpsyt.2020.00160 Giovanoli, 2013, Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice, Science (80-), 339, 1100, 10.1126/science.1228261 Kim, 2021, Brain gene co-expression networks link complement signaling with convergent synaptic pathology in schizophrenia, Nat. Neurosci. [Internet], 24, 799, 10.1038/s41593-021-00847-z Cardozo, 2019, Synaptic elimination in neurological disorders, Curr. Neuropharmacol., 17, 1071, 10.2174/1570159X17666190603170511 Paolicelli, 2011, Synaptic pruning by microglia is necessary for normal brain development, Sci. (80-) [Internet]. Am. Assoc. Adv. Sci., 333, 1456 Onwordi, 2020, Synaptic density marker SV2A is reduced in schizophrenia patients and unaffected by antipsychotics in rats, Nat. Commun. [Internet], 11, 246, 10.1038/s41467-019-14122-0 Osimo, 2019, Synaptic loss in schizophrenia: a meta-analysis and systematic review of synaptic protein and mRNA measures, Mol. Psychiatry, 24, 549, 10.1038/s41380-018-0041-5 Corradini, 2009, SNAP-25 in neuropsychiatric disorders, Ann. N. Y Acad. Sci., 1152, 93, 10.1111/j.1749-6632.2008.03995.x Hutsler, 2010, Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders, Brain Res. [Internet], 1309, 83, 10.1016/j.brainres.2009.09.120 Yizhar, 2011, Neocortical excitation/inhibition balance in information processing and social dysfunction, Nat. [Internet], 477, 171, 10.1038/nature10360 Gomot, 2008, Brain hyper-reactivity to auditory novel targets in children with high-functioning autism, Brain [Internet], 131, 2479, 10.1093/brain/awn172