Poly I:C-induced maternal immune challenge reduces perineuronal net area and raises spontaneous network activity of hippocampal neurons in vitro.
extracellular matrix
multielectrode array
neuronal networks
perineuronal nets
schizophrenia
Journal
The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110
Informations de publication
Date de publication:
06 2021
06 2021
Historique:
revised:
08
07
2020
received:
13
01
2020
accepted:
23
07
2020
pubmed:
7
8
2020
medline:
14
8
2021
entrez:
7
8
2020
Statut:
ppublish
Résumé
Activation of the maternal immune system (MIA) during gestation is linked to neuropsychiatric diseases like schizophrenia. While many studies address behavioural aspects, less is known about underlying cellular mechanisms. In the following study, BALB/c mice received intraperitoneal injections of polyinosinic-polycytidylic acid (Poly I:C) (20 µg/ml) or saline (0.9%) at gestation day (GD) 9.5 before hippocampal neurons were isolated and cultured from embryonic mice for further analysis. Interestingly, strongest effects were observed when the perineuronal net (PNN) wearing subpopulation of neurons was analysed. Here, a significant reduction of aggrecan staining intensity, area and soma size could be detected. Alterations of PNNs are often linked to neuropsychiatric diseases, changes in synaptic plasticity and in electrophysiology. Utilizing multielectrode array analysis (MEA), we observed a remarkable increase of the spontaneous network activity in neuronal networks after 21 days in vitro (DIV) when mother mice suffered a prenatal immune challenge. As PNNs are associated with GABAergic interneurons, our data indicate that this neuronal subtype might be stronger affected by a prenatal MIA. Degradation or damage of this subtype might cause the hyperexcitability observed in the whole network. In addition, embryonic neurons of the Poly I:C condition developed significantly shorter axons after five days in culture, while dendritic parameters and apoptosis rate remained unchanged. Structural analysis of synapse numbers revealed an increase of postsynaptic density 95 (PSD-95) puncta after 14 DIV and an increase of presynaptic vesicular glutamate transporter (vGlut) puncta after 21 DIV, while inhibitory synaptic proteins were not altered.
Substances chimiques
Poly I-C
O84C90HH2L
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3920-3941Informations de copyright
© 2020 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
Références
Allswede, D. M., & Cannon, T. D. (2018). Prenatal inflammation and risk for schizophrenia: A role for immune proteins in neurodevelopment. Development and Psychopathology, 30, 1157-1178. https://doi.org/10.1017/S0954579418000317
Ashdown, H., Dumont, Y., Ng, M., Poole, S., Boksa, P., & Luheshi, G. N. (2006). The role of cytokines in mediating effects of prenatal infection on the fetus: Implications for schizophrenia. Molecular Psychiatry, 11, 47-55. https://doi.org/10.1038/sj.mp.4001748
Bartos, M., Vida, I., Frotscher, M., Meyer, A., Monyer, H., Geiger, J. R., & Jonas, P. (2002). Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proceedings of the National Academy of Sciences of the United States of America, 99, 13222-13227. https://doi.org/10.1073/pnas.192233099
Basil, P., Li, Q., Dempster, E. L., Mill, J., Sham, P. C., Wong, C. C., & McAlonan, G. M. (2014). Prenatal maternal immune activation causes epigenetic differences in adolescent mouse brain. Translational Psychiatry, 4, e434. https://doi.org/10.1038/tp.2014.80
Bauman, M. D., Iosif, A. M., Smith, S. E., Bregere, C., Amaral, D. G., & Patterson, P. H. (2014). Activation of the maternal immune system during pregnancy alters behavioral development of rhesus monkey offspring. Biological Psychiatry, 75, 332-341. https://doi.org/10.1016/j.biopsych.2013.06.025
Berretta, S. (2012). Extracellular matrix abnormalities in schizophrenia. Neuropharmacology, 62, 1584-1597. https://doi.org/10.1016/j.neuropharm.2011.08.010
Binder, L. I., Frankfurter, A., & Rebhun, L. I. (1985). The distribution of tau in the mammalian central nervous system. The Journal of Cell Biology, 101, 1371-1378. https://doi.org/10.1083/jcb.101.4.1371
Bitanihirwe, B. K., & Woo, T. U. (2014). Perineuronal nets and schizophrenia: The importance of neuronal coatings. Neuroscience and Biobehavioral Reviews, 45, 85-99. https://doi.org/10.1016/j.neubiorev.2014.03.018
Blomstrom, A., Karlsson, H., Gardner, R., Jorgensen, L., Magnusson, C., & Dalman, C. (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. Schizophrenia Bulletin, 42, 125-133.
Brisch, R., Saniotis, A., Wolf, R., Bielau, H., Bernstein, H. G., Steiner, J., … Gos, T. (2014). The role of dopamine in schizophrenia from a neurobiological and evolutionary perspective: Old fashioned, but still in vogue. Frontiers in Psychiatry, 5, 47.
Brown, A. S., Begg, M. D., Gravenstein, S., Schaefer, C. A., Wyatt, R. J., Bresnahan, M., … Susser, E. S. (2004). Serologic evidence of prenatal influenza in the etiology of schizophrenia. Archives of General Psychiatry, 61, 774-780. https://doi.org/10.1001/archpsyc.61.8.774
Brown, A. S., Cohen, P., Harkavy-Friedman, J., Babulas, V., Malaspina, D., Gorman, J. M., & Susser, E. S. (2001). Prenatal rubella, premorbid abnormalities, and adult schizophrenia. Biological Psychiatry, 49, 473-486. https://doi.org/10.1016/S0006-3223(01)01068-X
Brown, A. S., Schaefer, C. A., Quesenberry, C. P. Jr, Liu, L., Babulas, V. P., & Susser, E. S. (2005). Maternal exposure to toxoplasmosis and risk of schizophrenia in adult offspring. The American Journal of Psychiatry, 162, 767-773. https://doi.org/10.1176/appi.ajp.162.4.767
Bruckner, G., Seeger, G., Brauer, K., Hartig, W., Kacza, J., & Bigl, V. (1994). Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat. Brain Research, 658, 67-86. https://doi.org/10.1016/S0006-8993(09)90012-9
Buka, S. L., Cannon, T. D., Torrey, E. F., & Yolken, R. H. (2008). Maternal exposure to herpes simplex virus and risk of psychosis among adult offspring. Biological Psychiatry, 63, 809-815. https://doi.org/10.1016/j.biopsych.2007.09.022
Buka, S. L., Tsuang, M. T., Torrey, E. F., Klebanoff, M. A., Bernstein, D., & Yolken, R. H. (2001). Maternal infections and subsequent psychosis among offspring. Archives of General Psychiatry, 58, 1032-1037. https://doi.org/10.1001/archpsyc.58.11.1032
Bukalo, O., Schachner, M., & Dityatev, A. (2001). Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience, 104, 359-369. https://doi.org/10.1016/S0306-4522(01)00082-3
Caceres, A., Banker, G., Steward, O., Binder, L., & Payne, M. (1984). MAP2 is localized to the dendrites of hippocampal neurons which develop in culture. Brain Research, 315, 314-318. https://doi.org/10.1016/0165-3806(84)90167-6
Canepari, M., Bove, M., Maeda, E., Cappello, M., & Kawana, A. (1997). Experimental analysis of neuronal dynamics in cultured cortical networks and transitions between different patterns of activity. Biological Cybernetics, 77, 153-162. https://doi.org/10.1007/s004220050376
Cardno, A. G., & Gottesman, I. I. (2000). Twin studies of schizophrenia: From bow-and-arrow concordances to star wars Mx and functional genomics. American Journal of Medical Genetics, 97, 12-17. https://doi.org/10.1002/(SICI)1096-8628(200021)97:1<12:AID-AJMG3>3.0.CO;2-U
Carulli, D., Pizzorusso, T., Kwok, J. C., Putignano, E., Poli, A., Forostyak, S., … Fawcett, J. W. (2010). Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain: A Journal of Neurology, 133, 2331-2347. https://doi.org/10.1093/brain/awq145
Castillo-Gomez, E., Perez-Rando, M., Belles, M., Gilabert-Juan, J., Llorens, J. V., Carceller, H., … Nacher, J. (2017). Early social isolation stress and perinatal NMDA receptor antagonist treatment induce changes in the structure and neurochemistry of inhibitory neurons of the adult amygdala and prefrontal Cortex. Eneuro, 4(2), ENEURO.0034. https://doi.org/10.1523/ENEURO.0034-17.2017
Celio, M. R., Spreafico, R., De Biasi, S., & Vitellaro-Zuccarello, L. (1998). Perineuronal nets: Past and present. Trends in Neurosciences, 21, 510-515. https://doi.org/10.1016/S0166-2236(98)01298-3
Chavez-Valdez, R., Mottahedin, A., Stridh, L., Yellowhair, T. R., Jantzie, L. L., Northington, F. J., & Mallard, C. (2019). Evidence for sexual dimorphism in the response to TLR3 activation in the developing neonatal mouse brain: A pilot study. Frontiers in Physiology, 10, 306. https://doi.org/10.3389/fphys.2019.00306
Chelini, G., Pantazopoulos, H., Durning, P., & Berretta, S. (2018). The tetrapartite synapse: A key concept in the pathophysiology of schizophrenia. European Psychiatry: The Journal of the Association of European Psychiatrists, 50, 60-69. https://doi.org/10.1016/j.eurpsy.2018.02.003
Cunningham, C., Campion, S., Teeling, J., Felton, L., & Perry, V. H. (2007). The sickness behaviour and CNS inflammatory mediator profile induced by systemic challenge of mice with synthetic double-stranded RNA (poly I:C). Brain, Behavior, and Immunity, 21, 490-502. https://doi.org/10.1016/j.bbi.2006.12.007
Dahlgren, J., Samuelsson, A. M., Jansson, T., & Holmang, A. (2006). Interleukin-6 in the maternal circulation reaches the rat fetus in mid-gestation. Pediatric Research, 60, 147-151. https://doi.org/10.1203/01.pdr.0000230026.74139.18
de Souza, D. F., Wartchow, K. M., Lunardi, P. S., Brolese, G., Tortorelli, L. S., Batassini, C., … Goncalves, C. A. (2015). Changes in astroglial markers in a maternal immune activation model of schizophrenia in wistar rats are dependent on sex. Frontiers in Cellular Neuroscience, 9, 489. https://doi.org/10.3389/fncel.2015.00489
Deacon, R. M. (2006). Burrowing in rodents: A sensitive method for detecting behavioral dysfunction. Nature Protocols, 1, 118-121. https://doi.org/10.1038/nprot.2006.19
Dobie, F. A., & Craig, A. M. (2011). Inhibitory synapse dynamics: Coordinated presynaptic and postsynaptic mobility and the major contribution of recycled vesicles to new synapse formation. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 31, 10481-10493.
Drazanova, E., Ruda-Kucerova, J., Kratka, L., Horska, K., Demlova, R., Starcuk, Z. Jr, & Kasparek, T. (2018). Poly(I:C) model of schizophrenia in rats induces sex-dependent functional brain changes detected by MRI that are not reversed by aripiprazole treatment. Brain Research Bulletin, 137, 146-155. https://doi.org/10.1016/j.brainresbull.2017.11.008
Dzyubenko, E., Gottschling, C., & Faissner, A. (2016). Neuron-glia interactions in neural plasticity: Contributions of neural extracellular matrix and perineuronal nets. Neural Plasticity, 2016, 5214961. https://doi.org/10.1155/2016/5214961
Esslinger, M., Wachholz, S., Manitz, M. P., Plumper, J., Sommer, R., Juckel, G., & Friebe, A. (2016). Schizophrenia associated sensory gating deficits develop after adolescent microglia activation. Brain, Behavior, and Immunity, 58, 99-106. https://doi.org/10.1016/j.bbi.2016.05.018
Fischer, M. (1973). Genetic and environmental factors in schizophrenia. A study of schizophrenic twins and their families. Acta Psychiatrica Scandinavica. Supplementum, 238, 9-142.
Frischknecht, R., Heine, M., Perrais, D., Seidenbecher, C. I., Choquet, D., & Gundelfinger, E. D. (2009). Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nature Neuroscience, 12, 897-904. https://doi.org/10.1038/nn.2338
Friston, K. J. (1998). The disconnection hypothesis. Schizophrenia Research, 30, 115-125. https://doi.org/10.1016/S0920-9964(97)00140-0
Geissler, M., & Faissner, A. (2012). A new indirect co-culture set up of mouse hippocampal neurons and cortical astrocytes on microelectrode arrays. Journal of Neuroscience Methods, 204, 262-272. https://doi.org/10.1016/j.jneumeth.2011.11.030
Geissler, M., Gottschling, C., Aguado, A., Rauch, U., Wetzel, C. H., Hatt, H., & Faissner, A. (2013). Primary hippocampal neurons, which lack four crucial extracellular matrix molecules, display abnormalities of synaptic structure and function and severe deficits in perineuronal net formation. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 33, 7742-7755. https://doi.org/10.1523/JNEUROSCI.3275-12.2013
Giamanco, K. A., Morawski, M., & Matthews, R. T. (2010). Perineuronal net formation and structure in aggrecan knockout mice. Neuroscience, 170, 1314-1327. https://doi.org/10.1016/j.neuroscience.2010.08.032
Gilmore, J. H., Fredrik Jarskog, L., Vadlamudi, S., & Lauder, J. M. (2004). Prenatal infection and risk for schizophrenia: IL-1beta, IL-6, and TNFalpha inhibit cortical neuron dendrite development. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 29, 1221-1229.
Gilmore, J. H., & Jarskog, L. F. (1997). Exposure to infection and brain development: Cytokines in the pathogenesis of schizophrenia. Schizophrenia Research, 24, 365-367. https://doi.org/10.1016/S0920-9964(96)00123-5
Gottschling, C., Dzyubenko, E., Geissler, M., & Faissner, A. (2016). The indirect neuron-astrocyte coculture assay: An in vitro set-up for the detailed investigation of neuron-glia interactions. Journal of Visualized Experiments: Jove, (117), 54757. https://doi.org/10.3791/54757
Gottschling, C., Wegrzyn, D., Denecke, B., & Faissner, A. (2019). Elimination of the four extracellular matrix molecules tenascin-C, tenascin-R, brevican and neurocan alters the ratio of excitatory and inhibitory synapses. Scientific Reports, 9, 13939. https://doi.org/10.1038/s41598-019-50404-9
Gyorffy, B. A., Gulyassy, P., Gellen, B., Volgyi, K., Madarasi, D., Kis, V., … Kekesi, K. A. (2016). Widespread alterations in the synaptic proteome of the adolescent cerebral cortex following prenatal immune activation in rats. Brain, Behavior, and Immunity, 56, 289-309. https://doi.org/10.1016/j.bbi.2016.04.002
Haida, O., Al Sagheer, T., Balbous, A., Francheteau, M., Matas, E., Soria, F., … Jaber, M. (2019). Sex-dependent behavioral deficits and neuropathology in a maternal immune activation model of autism. Translational Psychiatry, 9, 124. https://doi.org/10.1038/s41398-019-0457-y
Hartig, W., Brauer, K., Bigl, V., & Bruckner, G. (1994). Chondroitin sulfate proteoglycan-immunoreactivity of lectin-labeled perineuronal nets around parvalbumin-containing neurons. Brain Research, 635, 307-311. https://doi.org/10.1016/0006-8993(94)91452-4
Henriksen, M. G., Nordgaard, J., & Jansson, L. B. (2017). Genetics of Schizophrenia: Overview of methods, findings and limitations. Frontiers in Human Neuroscience, 11, 322. https://doi.org/10.3389/fnhum.2017.00322
Hui, C. W., St-Pierre, A., El Hajj, H., Remy, Y., Hebert, S. S., Luheshi, G. N., … Tremblay, M. E. (2018). Prenatal immune challenge in mice leads to partly sex-dependent behavioral, microglial, and molecular abnormalities associated with schizophrenia. Frontiers in Molecular Neuroscience, 11, 13. https://doi.org/10.3389/fnmol.2018.00013
Inan, M., Petros, T. J., & Anderson, S. A. (2013). Losing your inhibition: Linking cortical GABAergic interneurons to schizophrenia. Neurobiology of Disease, 53, 36-48. https://doi.org/10.1016/j.nbd.2012.11.013
Ito, H. T., Smith, S. E., Hsiao, E., & Patterson, P. H. (2010). Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring. Brain, Behavior, and Immunity, 24, 930-941. https://doi.org/10.1016/j.bbi.2010.03.004
Juckel, G., Manitz, M. P., Brune, M., Friebe, A., Heneka, M. T., & Wolf, R. J. (2011). Microglial activation in a neuroinflammational animal model of schizophrenia-a pilot study. Schizophrenia Research, 131, 96-100. https://doi.org/10.1016/j.schres.2011.06.018
Konat, G. W., Borysiewicz, E., Fil, D., & James, I. (2009). Peripheral challenge with double-stranded RNA elicits global up-regulation of cytokine gene expression in the brain. Journal of Neuroscience Research, 87, 1381-1388. https://doi.org/10.1002/jnr.21958
Labouesse, M. A., Langhans, W., & Meyer, U. (2015). Long-term pathological consequences of prenatal infection: Beyond brain disorders. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 309, R1-R12. https://doi.org/10.1152/ajpregu.00087.2015
Lieberman, J. A., Girgis, R. R., Brucato, G., Moore, H., Provenzano, F., Kegeles, L., … Small, S. A. (2018). Hippocampal dysfunction in the pathophysiology of schizophrenia: A selective review and hypothesis for early detection and intervention. Molecular Psychiatry, 23, 1764-1772. https://doi.org/10.1038/mp.2017.249
Limosin, F., Rouillon, F., Payan, C., Cohen, J. M., & Strub, N. (2003). Prenatal exposure to influenza as a risk factor for adult schizophrenia. Acta Psychiatrica Scandinavica, 107, 331-335. https://doi.org/10.1034/j.1600-0447.2003.00052.x
Lodge, D. J., Behrens, M. M., & Grace, A. A. (2009). A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 29, 2344-2354. https://doi.org/10.1523/JNEUROSCI.5419-08.2009
Lowe, G. C., Luheshi, G. N., & Williams, S. (2008). Maternal infection and fever during late gestation are associated with altered synaptic transmission in the hippocampus of juvenile offspring rats. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 295, R1563-1571. https://doi.org/10.1152/ajpregu.90350.2008
Makinodan, M., Tatsumi, K., Manabe, T., Yamauchi, T., Makinodan, E., Matsuyoshi, H., … Wanaka, A. (2008). Maternal immune activation in mice delays myelination and axonal development in the hippocampus of the offspring. Journal of Neuroscience Research, 86, 2190-2200. https://doi.org/10.1002/jnr.21673
Manitz, M. P., Esslinger, M., Wachholz, S., Plumper, J., Friebe, A., Juckel, G., & Wolf, R. (2013). The role of microglia during life span in neuropsychiatric disease-an animal study. Schizophrenia Research, 143, 221-222. https://doi.org/10.1016/j.schres.2012.10.028
Matuszko, G., Curreli, S., Kaushik, R., Becker, A., & Dityatev, A. (2017). Extracellular matrix alterations in the ketamine model of schizophrenia. Neuroscience, 350, 13-22. https://doi.org/10.1016/j.neuroscience.2017.03.010
Mauney, S. A., Athanas, K. M., Pantazopoulos, H., Shaskan, N., Passeri, E., Berretta, S., & Woo, T. U. (2013). Developmental pattern of perineuronal nets in the human prefrontal cortex and their deficit in schizophrenia. Biological Psychiatry, 74, 427-435. https://doi.org/10.1016/j.biopsych.2013.05.007
McCarthy, K. D., & de Vellis, J. (1980). Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. The Journal of Cell Biology, 85, 890-902. https://doi.org/10.1083/jcb.85.3.890
McCloy, R. A, Rogers, S., Caldon, C. E., Lorca, T., Castro, A., & Burgess, A. (2014). Partial inhibition of Cdk1 in G2phase overrides the SAC and decouples mitotic events. Cell Cycle, 13, 1400-1412. https://doi.org/10.4161/cc.28401
McGrath, J. J., Pemberton, M. R., Welham, J. L., & Murray, R. M. (1994). Schizophrenia and the influenza epidemics of 1954, 1957 and 1959: A southern hemisphere study. Schizophrenia Research, 14, 1-8. https://doi.org/10.1016/0920-9964(94)90002-7
Mednick, S. A., Machon, R. A., Huttunen, M. O., & Bonett, D. (1988). Adult schizophrenia following prenatal exposure to an influenza epidemic. Archives of General Psychiatry, 45, 189-192. https://doi.org/10.1001/archpsyc.1988.01800260109013
Meyer, U. (2013). Developmental neuroinflammation and schizophrenia. Progress in neuro-psychopharmacology & Biological Psychiatry, 42, 20-34. https://doi.org/10.1016/j.pnpbp.2011.11.003
Meyer, U., & Feldon, J. (2012). To poly(I:C) or not to poly(I:C): Advancing preclinical schizophrenia research through the use of prenatal immune activation models. Neuropharmacology, 62, 1308-1321. https://doi.org/10.1016/j.neuropharm.2011.01.009
Meyer, U., Feldon, J., Schedlowski, M., & Yee, B. K. (2005). Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia. Neuroscience and Biobehavioral Reviews, 29, 913-947. https://doi.org/10.1016/j.neubiorev.2004.10.012
Meyer, U., Nyffeler, M., Engler, A., Urwyler, A., Schedlowski, M., Knuesel, I., … Feldon, J. (2006). The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 26, 4752-4762. https://doi.org/10.1523/JNEUROSCI.0099-06.2006
Mortensen, P. B., Norgaard-Pedersen, B., Waltoft, B. L., Sorensen, T. L., Hougaard, D., Torrey, E. F., & Yolken, R. H. (2007). Toxoplasma gondii as a risk factor for early-onset schizophrenia: Analysis of filter paper blood samples obtained at birth. Biological Psychiatry, 61, 688-693. https://doi.org/10.1016/j.biopsych.2006.05.024
Pantazopoulos, H., Boyer-Boiteau, A., Holbrook, E. H., Jang, W., Hahn, C. G., Arnold, S. E., & Berretta, S. (2013). Proteoglycan abnormalities in olfactory epithelium tissue from subjects diagnosed with schizophrenia. Schizophrenia Research, 150, 366-372. https://doi.org/10.1016/j.schres.2013.08.013
Pantazopoulos, H., Woo, T. U., Lim, M. P., Lange, N., & Berretta, S. (2010). Extracellular matrix-glial abnormalities in the amygdala and entorhinal cortex of subjects diagnosed with schizophrenia. Archives of General Psychiatry, 67, 155-166. https://doi.org/10.1001/archgenpsychiatry.2009.196
Patterson, P. H. (2009). Immune involvement in schizophrenia and autism: Etiology, pathology and animal models. Behavioural Brain Research, 204, 313-321. https://doi.org/10.1016/j.bbr.2008.12.016
Paylor, J. W., Lins, B. R., Greba, Q., Moen, N., de Moraes, R. S., Howland, J. G., & Winship, I. R. (2016). Developmental disruption of perineuronal nets in the medial prefrontal cortex after maternal immune activation. Scientific Reports, 6, 37580. https://doi.org/10.1038/srep37580
Pendyala, G., Chou, S., Jung, Y., Coiro, P., Spartz, E., Padmashri, R., … Dunaevsky, A. (2017). Maternal immune activation causes behavioral impairments and altered cerebellar cytokine and synaptic protein expression. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 42, 1435-1446. https://doi.org/10.1038/npp.2017.7
Pietersen, C. Y., Mauney, S. A., Kim, S. S., Passeri, E., Lim, M. P., Rooney, R. J., … Woo, T. U. (2014). Molecular profiles of parvalbumin-immunoreactive neurons in the superior temporal cortex in schizophrenia. Journal of Neurogenetics, 28, 70-85. https://doi.org/10.3109/01677063.2013.878339
Pyka, M., Wetzel, C., Aguado, A., Geissler, M., Hatt, H., & Faissner, A. (2011). Chondroitin sulfate proteoglycans regulate astrocyte-dependent synaptogenesis and modulate synaptic activity in primary embryonic hippocampal neurons. The European Journal of Neuroscience, 33, 2187-2202. https://doi.org/10.1111/j.1460-9568.2011.07690.x
Samuelsson, A. M., Jennische, E., Hansson, H. A., & Holmang, A. (2006). Prenatal exposure to interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABA(A) dysregulation and impaired spatial learning. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 290, R1345-1356.
Segev, R., Shapira, Y., Benveniste, M., & Ben-Jacob, E. (2001). Observations and modeling of synchronized bursting in two-dimensional neural networks. Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics, 64, 011920. https://doi.org/10.1103/PhysRevE.64.011920
Shi, L., Fatemi, S. H., Sidwell, R. W., & Patterson, P. H. (2003). Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 23, 297-302. https://doi.org/10.1523/JNEUROSCI.23-01-00297.2003
Smith, S. E., Li, J., Garbett, K., Mirnics, K., & Patterson, P. H. (2007). Maternal immune activation alters fetal brain development through interleukin-6. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 27, 10695-10702. https://doi.org/10.1523/JNEUROSCI.2178-07.2007
Sofroniew, M. V. (2015). Astrocyte barriers to neurotoxic inflammation. Nature Reviews. Neuroscience, 16, 249-263.
Stan, A. D., & Lewis, D. A. (2012). Altered cortical GABA neurotransmission in schizophrenia: Insights into novel therapeutic strategies. Current Pharmaceutical Biotechnology, 13, 1557-1562.
Steullet, P., Cabungcal, J. H., Coyle, J., Didriksen, M., Gill, K., Grace, A. A., … Do, K. Q. (2017). Oxidative stress-driven parvalbumin interneuron impairment as a common mechanism in models of schizophrenia. Molecular Psychiatry, 22, 936-943. https://doi.org/10.1038/mp.2017.47
Suvisaari, J., Haukka, J., Tanskanen, A., Hovi, T., & Lonnqvist, J. (1999). Association between prenatal exposure to poliovirus infection and adult schizophrenia. The American Journal of Psychiatry, 156, 1100-1102.
Wen, T. H., Binder, D. K., Ethell, I. M., & Razak, K. A. (2018). The perineuronal 'safety' net? perineuronal net abnormalities in neurological disorders. Frontiers in Molecular Neuroscience, 11, 270. https://doi.org/10.3389/fnmol.2018.00270
Winter, C., Djodari-Irani, A., Sohr, R., Morgenstern, R., Feldon, J., Juckel, G., & Meyer, U. (2009). Prenatal immune activation leads to multiple changes in basal neurotransmitter levels in the adult brain: Implications for brain disorders of neurodevelopmental origin such as schizophrenia. The International Journal of Neuropsychopharmacology, 12, 513-524. https://doi.org/10.1017/S1461145708009206
Wintergerst, E. S., Vogt Weisenhorn, D. M., Rathjen, F. G., Riederer, B. M., Lambert, S., & Celio, M. R. (1996). Temporal and spatial appearance of the membrane cytoskeleton and perineuronal nets in the rat neocortex. Neuroscience Letters, 209, 173-176. https://doi.org/10.1016/0304-3940(96)12643-4
Wolff, A. R., & Bilkey, D. K. (2008). Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring. Behavioural Brain Research, 190, 156-159. https://doi.org/10.1016/j.bbr.2008.02.021
Wu, W. L., Hsiao, E. Y., Yan, Z., Mazmanian, S. K., & Patterson, P. H. (2017). The placental interleukin-6 signaling controls fetal brain development and behavior. Brain, Behavior, and Immunity, 62, 11-23. https://doi.org/10.1016/j.bbi.2016.11.007
Yamada, J., Ohgomori, T., & Jinno, S. (2015). Perineuronal nets affect parvalbumin expression in GABAergic neurons of the mouse hippocampus. The European Journal of Neuroscience, 41, 368-378. https://doi.org/10.1111/ejn.12792
Zalesky, A., Fornito, A., Seal, M. L., Cocchi, L., Westin, C. F., Bullmore, E. T., … Pantelis, C. (2011). Disrupted axonal fiber connectivity in schizophrenia. Biological Psychiatry, 69, 80-89. https://doi.org/10.1016/j.biopsych.2010.08.022
Zaretsky, M. V., Alexander, J. M., Byrd, W., & Bawdon, R. E. (2004). Transfer of inflammatory cytokines across the placenta. Obstetrics and Gynecology, 103, 546-550. https://doi.org/10.1097/01.AOG.0000114980.40445.83
Zhang, Z., & van Praag, H. (2015). Maternal immune activation differentially impacts mature and adult-born hippocampal neurons in male mice. Brain, Behavior, and Immunity, 45, 60-70. https://doi.org/10.1016/j.bbi.2014.10.010
Zuckerman, L., Rehavi, M., Nachman, R., & Weiner, I. (2003). Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: A novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 28, 1778-1789.
Zuckerman, L., & Weiner, I. (2005). Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. Journal of Psychiatric Research, 39, 311-323. https://doi.org/10.1016/j.jpsychires.2004.08.008