Effects of prenatal infection on brain development and behavior: A review of findings from animal models

Boksa, Patricia

doi:10.1016/j.bbi.2010.03.005

Cited by 603Tryptophan and brain disordersNeuroinflammation and Neurodegeneration MechanismsStress Responses and Cortisol

Effects of prenatal infection on brain development and behavior: A review of findings from animal models

Boksa, Patricia·2010·Brain, Behavior, and Immunity

DOI 10.1016/j.bbi.2010.03.005

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Abstract

Epidemiological studies with human populations indicate associations between maternal infection during pregnancy and increased risk in offspring for central nervous system (CNS) disorders including schizophrenia, autism and cerebral palsy. Since 2000, a large number of studies have used rodent models of systemic prenatal infection or prenatal immune activation to characterize changes in brain function and behavior caused by the prenatal insult. This review provides a comprehensive summary of these findings, and examines consistencies and trends across studies in an effort to provide a perspective on our current state of understanding from this body of work. Results from these animal modeling studies clearly indicate that prenatal immune activation can cause both acute and lasting changes in behavior and CNS structure and function in offspring. Across laboratories, studies vary with respect to the type, dose and timing of immunogen administration during gestation, species used, postnatal age examined and specific outcome measure quantified. This makes comparison across studies and assessment of replicability difficult. With regard to mechanisms, evidence for roles for several acute mediators of effects of prenatal immune activation has emerged, including circulating interleukin-6, increased placental cytokines and oxidative stress in the fetal brain. However, information required to describe the complete mechanistic pathway responsible for acute effects of prenatal immune activation on fetal brain is lacking, and no studies have yet addressed the issue of how acute prenatal exposure to an immunogen is transduced into a long-term CNS change in the postnatal animal. Directions for further research are discussed.

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Schizophrenia and autism share many immune similarities, including a subset of patients with an etiology based in maternal infection and immune activation.
“Schizophrenia and autism share many immune similarities, including a subset of patients with an etiology based in maternal infection and immune activation (Bauman et al, 2014;Boksa, 2010;Brown et al, 2004a;Meyer et al, 2005Meyer et al, , 2007;;Patterson, 2009;Urakubo et al, 2001).”
From The Role of the Immune System in Autism Spectrum Disorder (2017) · cites this paper as Boksa, 2010

Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
Toll-like receptors in the induction of the innate immune response
Aderem, A. A., & Ulevitch, R. J. (2000) · Nature · doi:10.1038/35021228 · Cited by 3,047 · see citing works
Maternal Immune Activation Alters Fetal Brain Development through Interleukin-6
Smith, S. E. P., Li, J., Garbett, K., Mirnics, K., & Patterson, P. H. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2178-07.2007 · Cited by 1,605 · see citing works
Prenatal Infection and Schizophrenia: A Review of Epidemiologic and Translational Studies
Brown, A. S., & Derkits, E. J. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.09030361 · Cited by 1,269 · see citing works
Adult Schizophrenia Following Prenatal Exposure to an Influenza Epidemic
Mednick, S. A. (1988) · Archives of General Psychiatry · doi:10.1001/archpsyc.1988.01800260109013 · Cited by 1,198 · see citing works
Disorders of Childhood and Adolescence: Gender and Psychopathology
Zahn-Waxler, C., Shirtcliff, E. A., & Marceau, K. (2008) · Annual Review of Clinical Psychology · doi:10.1146/annurev.clinpsy.3.022806.091358 · Cited by 1,072 · see citing works
A systematic review of the incidence of schizophrenia: the distribution of rates and the influence of sex, urbanicity, migrant status and methodology
McGrath, J., Saha, S., Welham, J., El Saadi, O., MacCauley, C., & Chant, D. (2004) · BMC Medicine · doi:10.1186/1741-7015-2-13 · Cited by 1,072 · see citing works
Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges
Swerdlow, N. R., Geyer, M. A., & BRAFF, D. L. (2001) · Psychopharmacology · doi:10.1007/s002130100799 · Cited by 1,053 · see citing works
Serologic Evidence of Prenatal Influenza in the Etiology of Schizophrenia
Brown, A. S., Begg, M. D., Gravenstein, S., Schaefer, C. A., Wyatt, R. J., Bresnahan, M. A., Babulas, V. P., & Susser, E. (2004) · Archives of General Psychiatry · doi:10.1001/archpsyc.61.8.774 · Cited by 1,048 · see citing works
Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring
Shi, L., Fatemi, S. H., Sidwell, R. W., & Patterson, P. H. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00297.2003 · Cited by 1,025 · see citing works
Chorioamnionitis as a Risk Factor for Cerebral Palsy
Wu, T.-W., & Colford, J. M. (2000) · JAMA · doi:10.1001/jama.284.11.1417 · Cited by 954 · see citing works
Cytokines and CNS Development
Deverman, B. E., & Patterson, P. H. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.002 · Cited by 865 · see citing works
Sex Differences in the Risk of Schizophrenia: Evidence From Meta-analysis
Aleman, A., Kahn, R. S., & Selten, J.-P. (2003) · Archives of General Psychiatry · doi:10.1001/archpsyc.60.6.565 · Cited by 818 · see citing works
Extrapolating brain development from experimental species to humans
Clancy, B., Finlay, B. L., Darlington, R. B., & Anand, K. J. S. (2007) · NeuroToxicology · doi:10.1016/j.neuro.2007.01.014 · Cited by 812 · see citing works
The Time of Prenatal Immune Challenge Determines the Specificity of Inflammation-Mediated Brain and Behavioral Pathology
Meyer, U., Nyffeler, M., Engler, A., Urwyler, A., Schedlowski, M., Knuesel, I., Yee, B. K., & Feldon, J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0099-06.2006 · Cited by 774 · see citing works
Half a century of antipsychotics and still a central role for dopamine D2 receptors
Kapur, S., & Mamo, D. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2003.09.004 · Cited by 638 · see citing works
Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response
Liuzzi, J. P., Lichten, L. A., Rivera, S., Blanchard, R. K., Aydemir, T. B., Knutson, M. D., Ganz, T., & Cousins, R. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502257102 · Cited by 594 · see citing works
Epigenetics and the environmental regulation of the genome and its function
Zhang, T.-Y., & Meaney, M. J. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.60.110707.163625 · Cited by 565 · see citing works
At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby?
Romijn, H. J., Hofman, M. A., & Gramsbergen, A. (1991) · Early Human Development · doi:10.1016/0378-3782(91)90044-4 · Cited by 553 · see citing works
Cytokine Induction in Fetal Rat Brains and Brain Injury in Neonatal Rats after Maternal Lipopolysaccharide Administration
Cai, Z., Pan, Z.-L., Pang, Y., Evans, O. B., & Rhodes, P. G. (2000) · Pediatric Research · doi:10.1203/00006450-200001000-00013 · Cited by 507 · see citing works
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
Zuckerman, L., Rehavi, M., Nachman, R., & Weiner, I. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300248 · Cited by 501 · see citing works
Case-control study of antenatal and intrapartum risk factors for cerebral palsy in very preterm singleton babies
Murphy, D. J., Johnson, A. M., Sellers, S. M., & MacKenzie, I. Z. (1995) · The Lancet · doi:10.1016/s0140-6736(95)92471-x · Cited by 495 · see citing works
Maternal Exposure to Toxoplasmosis and Risk of Schizophrenia in Adult Offspring
Brown, A. S., Schaefer, C. A., Quesenberry, C. P., Liu, L., Babulas, V. P., & Susser, E. (2005) · American Journal of Psychiatry · doi:10.1176/appi.ajp.162.4.767 · Cited by 490 · see citing works
Immune activation during pregnancy in mice leads to dopaminergic hyperfunction and cognitive impairment in the offspring: a neurodevelopmental animal model of schizophrenia
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
Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice
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
Cytokine-specific central monoamine alterations induced by interleukin-1, -2 and -6
Zalcman, S., Green-Johnson, J. M., Murray, L., Nance, D. M., Dyck, D., Anisman, H., & Greenberg, A. H. (1994) · Brain Research · doi:10.1016/0006-8993(94)90006-x · Cited by 439 · see citing works
Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain
Urakubo, A., Jarskog, L. F., Lieberman, J. A., & Gilmore, J. H. (2001) · Schizophrenia Research · doi:10.1016/s0920-9964(00)00032-3 · Cited by 405 · see citing works
Schizophrenia after prenatal exposure to 1957 A2 influenza epidemic
O’Callaghan, E., Sham, P. C., Takei, N., Murray, R. M., & Glover, G. R. (1991) · The Lancet · doi:10.1016/0140-6736(91)92919-s · Cited by 402 · see citing works
Stressed-out, or in (utero)?
Avishai‐Eliner, S. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02241-5 · Cited by 397 · see citing works
The role of cytokines in mediating effects of prenatal infection on the fetus: implications for schizophrenia
Ashdown, H. F., Dumont, Y., Ng, M., Poole, S., Boksa, P., & Luheshi, G. N. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001748 · Cited by 387 · see citing works
Self-citation
Follow-up report on autism in congenital rubella
Chess, S. (1977) · Journal of Autism and Childhood Schizophrenia · doi:10.1007/bf01531116 · Cited by 378 · see citing works
Transfer of Inflammatory Cytokines Across the Placenta
Zaretsky, M. V., Alexander, J. M., Byrd, W., & Bawdon, R. E. (2004) · Obstetrics and Gynecology · doi:10.1097/01.aog.0000114980.40445.83 · Cited by 376 · see citing works
In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders
Meyer, U., Feldon, J., & Fatemi, S. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.001 · Cited by 367 · see citing works
The viral mimic, polyinosinic:polycytidylic acid, induces fever in rats via an interleukin-1-dependent mechanism
Fortier, M., Kent, S., Ashdown, H. F., Poole, S., Boksa, P., & Luheshi, G. N. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00293.2004 · Cited by 354 · see citing works
Self-citation
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
Human Tumour Necrosis Factor: Physiological and Pathological Roles in Placenta and Endometrium
Haider, S., & Knöfler, M. (2008) · Placenta · doi:10.1016/j.placenta.2008.10.012 · Cited by 344 · see citing works
Reactive astrogliosis in the neonatal mouse brain and its modulation by cytokines
Balasingam, V, Tejada-Berges, T., Wright, E., Bouckova, R., & Yong, V. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00846.1994 · Cited by 342 · see citing works
Exposure to Influenza Epidemics During Gestation and Adult Schizophrenia
Barr, C. E. (1990) · Archives of General Psychiatry · doi:10.1001/archpsyc.1990.01810210077012 · Cited by 329 · see citing works
Prenatal Immune Challenge Disrupts Sensorimotor Gating in Adult Rats Implications for the Etiopathogenesis of Schizophrenia
Borrell, J. I. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00360-8 · Cited by 307 · see citing works
Differentiation of Mesencephalic Progenitor Cells into Dopaminergic Neurons by Cytokines
Ling, Z. D., Potter, E. D., Lipton, J. W., & Carvey, P. M. (1998) · Experimental Neurology · doi:10.1006/exnr.1998.6715 · Cited by 295 · see citing works
Knockdown of DISC1 by In Utero Gene Transfer Disturbs Postnatal Dopaminergic Maturation in the Frontal Cortex and Leads to Adult Behavioral Deficits
Niwa, M., Kamiya, A., Murai, R., Kubo, K., Gruber, A. J., Tomita, K., Lu, L., Tomisato, S., Jaaro-Peled, H., Seshadri, S., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.019 · Cited by 291 · see citing works
Prenatal exposure to interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABA A dysregulation and impaired spatial learning
Samuelsson, A., Jennische, E., Hansson, H., & Holmäng, A. B. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00268.2005 · Cited by 283 · see citing works
Activation of the maternal immune system alters cerebellar development in the offspring
Shi, L., Smith, S. E. P., Malkova, N., Tse, D., Su, Y., & Patterson, P. H. (2009) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2008.07.012 · Cited by 277 · see citing works
Maternal Exposure to Respiratory Infections and Adult Schizophrenia Spectrum Disorders: A Prospective Birth Cohort Study
Brown, A. S., Schaefer, C. A., Wyatt, R. J., Goetz, R. R., Begg, M. D., Gorman, J. M., & Susser, E. (2000) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a033453 · Cited by 273 · see citing works
Prenatal viral infection leads to pyramidal cell atrophy and macrocephaly in adulthood: implications for genesis of autism and schizophrenia
Fatemi, S. H., Earle, J., Kanodia, R., Kist, D., Emamian, E. S., Patterson, P. H., Shi, L., & Sidwell, R. (2002) · Cellular and Molecular Neurobiology · doi:10.1023/a:1015337611258 · Cited by 261 · see citing works
In utero infection and adult schizophrenia
Brown, A. S., & Susser, E. (2002) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.10004 · Cited by 261 · see citing works
Association Between Prenatal Exposure to Bacterial Infection and Risk of Schizophrenia
Sørensen, H. J., Mortensen, E. L., Reinisch, J. M., & Mednick, S. A. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn121 · Cited by 261 · see citing works
Defective corticogenesis and reduction in Reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice
Fatemi, S. H., Emamian, E. S., Kist, D. A., Sidwell, R. W., Nakajima, K., Akhter, P., Shier, A. C., Sheikh, S. A., & Bailey, K. W. (1999) · Molecular Psychiatry · doi:10.1038/sj.mp.4000520 · Cited by 259 · see citing works
Interleukin-6 in the Maternal Circulation Reaches the Rat Fetus in Mid-gestation
Dahlgren, J., Samuelsson, A., Jansson, T., & Holmäng, A. B. (2006) · Pediatric Research · doi:10.1203/01.pdr.0000230026.74139.18 · Cited by 259 · see citing works
Specific neurodevelopmental damage in mice offspring following maternal inflammation during pregnancy
Golan, H. M., Lev, V., Hallak, M., Sorokin, Y., & Huleihel, M. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.12.023 · Cited by 253 · see citing works
Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated anti-inflammatory signaling
Meyer, U., Murray, P. J., Urwyler, A., Yee, B. K., Schedlowski, M., & Feldon, J. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002042 · Cited by 252 · see citing works
Autistic disorder and viral infections
Libbey, J., Sweeten, T., McMahon, W., & Fujinami, R. (2005) · Journal of NeuroVirology · doi:10.1080/13550280590900553 · Cited by 252 · see citing works
Maternal infection leads to abnormal gene regulation and brain atrophy in mouse offspring: implications for genesis of neurodevelopmental disorders
Fatemi, S. H., Reutiman, T. J., Folsom, T. D., Huang, H., Oishi, K., Mori, S., Smee, D. F., Pearce, D. A., Winter, C., Sohr, R., et al. (2008) · Schizophrenia Research · doi:10.1016/j.schres.2007.11.018 · Cited by 250 · see citing works
Schizophrenia Following Pre-natal Exposure to Influenza Epidemics Between 1939 and 1960
Sham, P. C., O’Callaghan, E., Takei, N., Murray, G. K., Hare, E. H., & Murray, R. M. (1992) · The British Journal of Psychiatry · doi:10.1192/bjp.160.4.461 · Cited by 250 · see citing works
Tumor necrosis factor-alpha potentiates glutamate neurotoxicity in human fetal brain cell cultures.
Chao, C. C., & Hu, S.-X. (1994) · Developmental Neuroscience · doi:10.1159/000112104 · Cited by 249 · see citing works
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
Winter, C., Djodari-Irani, A., Sohr, R., Morgenstern, R., Feldon, J., Juckel, G., & Meyer, U. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708009206 · Cited by 242 · see citing works
In utero bacterial endotoxin exposure causes loss of tyrosine hydroxylase neurons in the postnatal rat midbrain
Ling, Z., Gayle, D. A., Ma, S. Y., Lipton, J. W., Tong, C. W., Hong, J., & Carvey, P. M. (2002) · Movement Disorders · doi:10.1002/mds.10078 · Cited by 241 · see citing works
Maternal Exposure to Herpes Simplex Virus and Risk of Psychosis Among Adult Offspring
Buka, S. L., Cannon, T. D., Torrey, E. F., & Yolken, R. H. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.09.022 · Cited by 233 · see citing works
Prenatal Exposure to Maternal Genital and Reproductive Infections and Adult Schizophrenia
Babulas, V. P., Factor-Litvak, P. R., Goetz, R. R., Schaefer, C. A., & Brown, A. S. (2006) · American Journal of Psychiatry · doi:10.1176/ajp.2006.163.5.927 · Cited by 233 · see citing works
Systematic review of chorioamnionitis and cerebral palsy
Wu, Y. W. (2002) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.10003 · Cited by 230 · see citing works
The host response to endotoxin, antilipopolysaccharide strategies, and the management of severe sepsis
Opal, S. M. (2007) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2007.03.006 · Cited by 230 · see citing works
Effects of prenatal infection on prepulse inhibition in the rat depend on the nature of the infectious agent and the stage of pregnancy
Fortier, M., Luheshi, G. N., & Boksa, P. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.04.016 · Cited by 229 · see citing works
Self-citation
Antipsychotic Drugs: Comparison in Animal Models of Efficacy, Neurotransmitter Regulation, and Neuroprotection
Lieberman, J. A., Bymaster, F. P., Meltzer, H. Y., Deutch, A. Y., Duncan, G. E., Marx, C. E., Aprille, J. R., Dwyer, D. S., Li, X., Mahadik, S. P., et al. (2008) · Pharmacological Reviews · doi:10.1124/pr.107.00107 · Cited by 223 · see citing works
Maternal LPS induces cytokines in the amniotic fluid and corticotropin releasing hormone in the fetal rat brain
Gayle, D. A., Beloosesky, R., Desai, M., Amidi, F., Nuñez, S., & Ross, M. G. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00664.2003 · Cited by 221 · see citing works
IL-1 Receptor Antagonist Protects against Placental and Neurodevelopmental Defects Induced by Maternal Inflammation
Girard, S., Tremblay, L., Lepage, M., & Sébire, G. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903349 · Cited by 220 · see citing works
Evidence for an Interaction Between Familial Liability and Prenatal Exposure to Infection in the Causation of Schizophrenia
Clarke, M. C., Tanskanen, A. J., HUTTUNEN, M. O., Whittaker, J. C., & Cannon, M. D. (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.08010031 · Cited by 216 · see citing works
Relative Prenatal and Postnatal Maternal Contributions to Schizophrenia-Related Neurochemical Dysfunction after In Utero Immune Challenge
Meyer, U., Nyffeler, M., Schwendener, S., Knuesel, I., Yee, B. K., & Feldon, J. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301413 · Cited by 215 · see citing works
Epidemiological Evidence that Maternal Influenza Contributes to the Aetiology of Schizophrenia
Adams, W., Kendell, R. E., Hare, E. H., & Munk‐Jørgensen, P. (1993) · The British Journal of Psychiatry · doi:10.1192/bjp.163.4.522 · Cited by 204 · see citing works
Obstetric conditions and risk of first admission with schizophrenia: A Danish national register based study
Byrne, M., Agerbo, E., Bennedsen, B. E., Eaton, W. W., & Mortensen, P. B. (2007) · Schizophrenia Research · doi:10.1016/j.schres.2007.07.018 · Cited by 201 · see citing works
Maternal influenza infection is likely to alter fetal brain development indirectly: the virus is not detected in the fetus
Shi, L., Tu, N., & Patterson, P. H. (2004) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.05.005 · Cited by 197 · see citing works
Association Between Prenatal Exposure to Poliovirus Infection and Adult Schizophrenia
Suvisaari, J., Haukka, J. K., Tanskanen, A. J., Hovi, T., & Lönnqvist, J. K. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.7.1100 · Cited by 192 · see citing works
Maternal exposure to bacterial endotoxin during pregnancy enhances amphetamine-induced locomotion and startle responses in adult rat offspring.
Fortier, M., Joober, R., Luheshi, G., & Boksa, P. (2004) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2003.10.001 · Cited by 186 · see citing works
Self-citation
Schizophrenic births and viral diseases in two states
Torrey, Ε. F., Rawlings, R. R., & Waldman, I. N. (1988) · Schizophrenia Research · doi:10.1016/0920-9964(88)90043-6 · Cited by 185 · see citing works
The Neurobiology of Infantile Autism
Ciaranello, A. L., & Ciaranello, R. D. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.18.030195.000533 · Cited by 184 · see citing works
Maternal Exposure to LPS Induces Hypomyelination in the Internal Capsule and Programmed Cell Death in the Deep Gray Matter in Newborn Rats
Rousset, C. I., Chalon, S., Cantagrel, S., Bodard, S., Andres, C. R., Gressèns, P., & Saliba, É. (2006) · Pediatric Research · doi:10.1203/01.pdr.0000199905.08848.55 · Cited by 181 · see citing works
Maternal poly I:C exposure during pregnancy regulates TNFα, BDNF, and NGF expression in neonatal brain and the maternal–fetal unit of the rat
Gilmore, J. H., Jarskog, L. F., & Vadlamudi, S. (2005) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2004.10.008 · Cited by 177 · see citing works
Prenatal Exposure to Maternal Infection and Executive Dysfunction in Adult Schizophrenia
Brown, A. S., Vinogradov, S., Kremen, W. S., Poole, J. H., Deicken, R. F., Penner, J. D., McKeague, I. W., Kochetkova, A. S., Kern, D. M., & Schaefer, C. A. (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2008.08010089 · Cited by 177 · see citing works
N‐acetylcysteine prevents endotoxin‐induced degeneration of oligodendrocyte progenitors and hypomyelination in developing rat brain
Paintlia, M. K., Paintlia, A. S., Barbosa, E., Singh, I., & Singh, A. K. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20261 · Cited by 176 · see citing works
Fever and hypothermia: two adaptive thermoregulatory responses to systemic inflammation
Romanovsky, A. A., & Székely, M. (1998) · Medical Hypotheses · doi:10.1016/s0306-9877(98)90022-6 · Cited by 173 · see citing works
Variations of nucleus accumbens dopamine and serotonin following systemic interleukin-1, interleukin-2 or interleukin-6 treatment
Song, C., Merali, Z., & Anisman, H. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00271-1 · Cited by 172 · see citing works
Early Infections of Toxoplasma gondii and the Later Development of Schizophrenia
Mortensen, P. B., Nørgaard‐Pedersen, B., Waltoft, B. L., Sørensen, T. L., HOUGAARD, D. M., & Yolken, R. H. (2007) · Schizophrenia Bulletin · doi:10.1093/schbul/sbm009 · Cited by 171 · see citing works
ORIGINAL ARTICLE: Activation of TLR3 in the Trophoblast is Associated with Preterm Delivery
Koga, K., Cardenas, I., Aldo, P. B., Abrahams, V. M., Peng, B., Malfertheiner, S. F., Romero, R. J., & Mor, G. (2009) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2008.00682.x · Cited by 170 · see citing works
Prenatal Influenza Infections and Adult Schizophrenia
Mednick, S. A., HUTTUNEN, M. O., & Machón, R. A. (1994) · Schizophrenia Bulletin · doi:10.1093/schbul/20.2.263 · Cited by 169 · see citing works
Ontogeny of sensorimotor gating and immune impairment induced by prenatal immune challenge in rats: implications for the etiopathology of schizophrenia
Romero, E., Guaza, C., Castellano, B., & Borrell, J. I. (2008) · Molecular Psychiatry · doi:10.1038/mp.2008.44 · Cited by 165 · see citing works
Progressive dopamine neuron loss following supra-nigral lipopolysaccharide (LPS) infusion into rats exposed to LPS prenatally
Ling, Z., Zhu, Y., Tong, C. W., Snyder, J. A., Lipton, J. W., & Carvey, P. M. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.01.010 · Cited by 160 · see citing works
Chronic Interleukin-6 Alters NMDA Receptor-Mediated Membrane Responses and Enhances Neurotoxicity in Developing CNS Neurons
Qiu, Z. J., Sweeney, D. D., Netzeband, J. G., & Gruol, D. L. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10445.1998 · Cited by 159 · see citing works
Cytokines and Fever: Mechanisms and Sites of Action
Luheshi, G. N. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb08316.x · Cited by 156 · see citing works
Prenatal viral infection in mouse causes differential expression of genes in brains of mouse progeny: A potential animal model for schizophrenia and autism
Fatemi, S. H., Pearce, D. A., Brooks, A. I., & Sidwell, R. W. (2005) · Synapse · doi:10.1002/syn.20162 · Cited by 151 · see citing works
Prenatal Immune Challenge Is an Environmental Risk Factor for Brain and Behavior Change Relevant to Schizophrenia: Evidence from MRI in a Mouse Model
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
Prenatal activation of microglia induces delayed impairment of glutamatergic synaptic function
Roumier, A., Pascual, O., Béchade, C., Wakselman, S., Poncer, J.-C., Réal, E., Triller, A., & Bessis, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002595 · Cited by 146 · see citing works
Alterations in behavior in adult offspring mice following maternal inflammation during pregnancy
Hava, G., Lev, V., Yael, M., Hallak, M., & Mahoud, H. (2006) · Developmental Psychobiology · doi:10.1002/dev.20116 · Cited by 146 · see citing works
Investigating whether adverse prenatal and perinatal events are associated with non-clinical psychotic symptoms at age 12 years in the ALSPAC birth cohort
Zammit, S., Odd, D., Horwood, J., Thompson, A., Thomas, K., Menezes, P., Gunnell, D., Hollis, C., Wolke, D., Lewis, G., et al. (2009) · Psychological Medicine · doi:10.1017/s0033291708005126 · Cited by 142 · see citing works
Prenatal immune challenge alters the hypothalamic-pituitary-adrenocortical axis in adult rats.
Reul, J. M. H. M., Stec, I. S. M., Wiegers, G. J., Labeur, M. S., Linthorst, A. C. E., ARZT, E. S., & Holsboer, F. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117272 · Cited by 142 · see citing works
Neurodevelopmental damage after prenatal infection: role of oxidative stress in the fetal brain
Lanté, F., Meunier, J., Guiramand, J., Maurice, T., Cavalier, M., de Jesus Ferreira, M.-C., Aimar, R., Cohen-Solal, C., Vignes, M., & Barbanel, G. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.01.027 · Cited by 140 · see citing works
Serological pattern consistent with infection with type I Toxoplasma gondii in mothers and risk of psychosis among adult offspring
Xiao, J., Buka, S. L., Cannon, T. D., Suzuki, Y., Viscidi, R. P., Torrey, E. F., & Yolken, R. H. (2009) · Microbes and Infection · doi:10.1016/j.micinf.2009.07.007 · Cited by 140 · see citing works
Maternal immune activation during pregnancy increases limbic GABAA receptor immunoreactivity in the adult offspring: implications for schizophrenia
Nyffeler, M., Meyer, U., Yee, B. K., Feldon, J., & Knuesel, I. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.07.029 · Cited by 139 · see citing works
Neurobehavioral and Immunological Consequences of Prenatal Immune Activation in Rats. Influence of Antipsychotics
Romero, E., Ali, C., Molina‐Holgado, E., Castellano, B., Guaza, C., & Borrell, J. I. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301292 · Cited by 138 · see citing works
Prenatal exposure to influenza as a risk factor for adult schizophrenia
Limosin, F., Rouillon, F., Payan, C., Cohen, J., & Strub, N. (2003) · Acta Psychiatrica Scandinavica · doi:10.1034/j.1600-0447.2003.00052.x · Cited by 137 · see citing works
Preliminary evidence for a modulation of fetal dopaminergic development by maternal immune activation during pregnancy
Meyer, U., Engler, A., Weber, L., Schedlowski, M., & Feldon, J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.031 · Cited by 135 · see citing works
Cytokine effects on cortical neuron MAP-2 immunoreactivity: implications for schizophrenia
Marx, C. E., Jarskog, L. F., Lauder, J. M., Lieberman, J. A., & Gilmore, J. H. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01209-4 · Cited by 134 · see citing works
Rotenone potentiates dopamine neuron loss in animals exposed to lipopolysaccharide prenatally
Ling, Z., Chang, Q. A., Tong, C. W., Leurgans, S. E., Lipton, J. W., & Carvey, P. M. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2004.08.006 · Cited by 131 · see citing works
Maternal immune activation in mice delays myelination and axonal development in the hippocampus of the offspring
Makinodan, M., Tatsumi, K., Manabe, T., Yamauchi, T., Makinodan, E., Matsuyoshi, H., Shimoda, S., Noriyama, Y., Kishimoto, T., & Wanaka, A. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21673 · Cited by 130 · see citing works
Characterization of the action of antipsychotic subtypes on valproate-induced chromatin remodeling
Guidotti, A., Dong, E., Kundakovic, M., Satta, R., Grayson, D. R., & Costa, E. (2009) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2008.10.010 · Cited by 130 · cited 1× · see citing works
“This may be related to any of the multiple actions of anti-psychotic drugs including the ability to block dopamine D2 receptors, provide neuroprotection or enhance demethylation of gene promoters (Kapur and Mamo, 2003; Lieberman et al., 2008; Guidotti et al., 2009).”
Prenatal and postnatal maternal contributions in the infection model of schizophrenia
Meyer, U., Schwendener, S., Feldon, J., & Yee, B. K. (2006) · Experimental Brain Research · doi:10.1007/s00221-006-0419-5 · Cited by 128 · see citing works
Effects of prenatal immune activation on hippocampal neurogenesis in the rat
Cui, K., Ashdown, H. F., Luheshi, G. N., & Boksa, P. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2009.05.003 · Cited by 127 · see citing works
Self-citation
Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring
Wolff, A. R., & Bilkey, D. K. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.02.021 · Cited by 124 · see citing works
Late <i>N</i>‐acetylcysteine treatment prevents the deficits induced in the offspring of dams exposed to an immune stress during gestation
Lanté, F., Meunier, J., Guiramand, J., De Jesus Ferreira, M., Cambonie, G., Aimar, R., Cohen‐Solal, C., Maurice, T., Vignes, M., & Barbanel, G. (2008) · Hippocampus · doi:10.1002/hipo.20421 · Cited by 124 · see citing works
PERINATAL COMPLICATIONS AS PREDICTORS OF INFANTILE AUTISM
WILKERSON, D. S., Volpe, A. G., Dean, R. S., & Titus, J. B. (2002) · International Journal of Neuroscience · doi:10.1080/00207450290026076 · Cited by 121 · see citing works
Post-pubertal emergence of disrupted latent inhibition following prenatal immune activation
Zuckerman, L., & Weiner, I. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1461-7 · Cited by 119 · see citing works
Human influenza viral infection in utero alters glial fibrillary acidic protein immunoreactivity in the developing brains of neonatal mice
Fatemi, S. H., Emamian, E. S., Sidwell, R. W., Kist, D. A., Stary, J. M., Earle, J. A., & THURAS, P. D. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001046 · Cited by 116 · see citing works
Evaluating Early Preventive Antipsychotic and Antidepressant Drug Treatment in an Infection-Based Neurodevelopmental Mouse Model of Schizophrenia
Meyer, U., Spoerri, E., Yee, B. K., Schwarz, M., & Feldon, J. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn131 · Cited by 115 · see citing works
Cognitive Functioning Prior to the Onset of Psychosis: The Role of Fetal Exposure to Serologically Determined Influenza Infection
Ellman, L. M., Yolken, R. H., Buka, S. L., Torrey, E. F., & Cannon, T. D. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.12.015 · Cited by 114 · see citing works
Combined toxicity of prenatal bacterial endotoxin exposure and postnatal 6-hydroxydopamine in the adult rat midbrain
Ling, Z. D., Chang, Q., Lipton, J. W., Tong, C. W., Landers, T. M., & Carvey, P. M. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.12.017 · Cited by 114 · see citing works
Prenatal immune challenge induces developmental changes in the morphology of pyramidal neurons of the prefrontal cortex and hippocampus in rats
Baharnoori, M., Brake, W. G., & Srivastava, L. K. (2008) · Schizophrenia Research · doi:10.1016/j.schres.2008.10.003 · Cited by 113 · see citing works
The Relationship of Schizophrenic Births to 16 Infectious Diseases
O’Callaghan, E., Sham, P. C., Takei, N., Murray, G. K., Glover, G. R., Hare, E. H., & Murray, R. M. (1994) · The British Journal of Psychiatry · doi:10.1192/bjp.165.3.353 · Cited by 110 · see citing works
Relationship between in utero exposure to influenza epidemics and risk of schizophrenia in Denmark
Takei, N., Mortensen, P. B., Kl˦ning, U., Murray, R. M., Sham, P. C., O’Callaghan, E., & Munk‐Jørgensen, P. (1996) · Biological Psychiatry · doi:10.1016/0006-3223(95)00592-7 · Cited by 105 · see citing works
Maternal dietary zinc supplementation prevents aberrant behaviour in an object recognition task in mice offspring exposed to LPS in early pregnancy
Coyle, P. V., TRAN, N., FUNG, J., Summers, B. L., & Rofe, A. M. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.08.022 · Cited by 102 · see citing works
Tumor necrosis factor alpha partially contributes to lipopolysaccharide-induced intra-uterine fetal growth restriction and skeletal development retardation in mice
Xu, D., Chen, Y., Wang, H., Zhao, L., Wang, J., & Wei, W. (2005) · Toxicology Letters · doi:10.1016/j.toxlet.2005.09.009 · Cited by 102 · see citing works
Prostaglandins, endotoxin and lipid A on body temperature in rats.
Feldberg, W. S., & Saxena, P. N. (1975) · The Journal of Physiology · doi:10.1113/jphysiol.1975.sp011033 · Cited by 100 · see citing works
Schizophrenia and 1957 Pandemic of Influenza: Meta-analysis
Selten, J., Frissen, A., Lensvelt‐Mulders, G., & Morgan, V. A. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbp147 · Cited by 97 · see citing works
Developmental motor deficits induced by combined fetal exposure to lipopolysaccharide and early neonatal hypoxia/ischemia: A novel animal model for cerebral palsy in very premature infants
Girard, S., Kadhim, H. J., Beaudet, N., Sarret, P., & Sébire, G. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.10.032 · Cited by 96 · see citing works
The identification of thyrotropin releasing hormone (TRH) in hypothalamic and extrahypothalamic loci of the human nervous system
Kubek, M. J., LORINCZ, M. A., & Wilber, J. F. (1977) · Brain Research · doi:10.1016/0006-8993(77)90230-x · Cited by 96 · see citing works
Erythropoietin Attenuates Lipopolysaccharide-Induced White Matter Injury in the Neonatal Rat Brain
Kumral, A., Baskın, H., Yeşilırmak, D. C., Ergür, B. U., Aykan, S., Genç, Ş., Genç, K., Yılmaz, O., Tuğyan, K., Giray, Ö., et al. (2007) · Neonatology · doi:10.1159/000105493 · Cited by 94 · see citing works
Lipopolysaccharide-induced peroxisomal dysfunction exacerbates cerebral white matter injury: attenuation by N-acetyl cysteine
Paintlia, M. K., Paintlia, A. S., Contreras, M. A., Singh, I., & Singh, A. K. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2007.12.011 · Cited by 93 · see citing works
Dopamine and serotonin levels following prenatal viral infection in mouse—implications for psychiatric disorders such as schizophrenia and autism
Winter, C., Reutiman, T. J., Folsom, T. D., Sohr, R., Wolf, R. J., Juckel, G., & Fatemi, S. H. (2008) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2008.06.001 · Cited by 92 · see citing works
Neuronal Injuries Induced by Perinatal Hypoxic-Ischemic Insults Are Potentiated by Prenatal Exposure to Lipopolysaccharide: Animal Model for Perinatally Acquired Encephalopathy
Larouche, A., Roy, M., Kadhim, H. J., Tsanaclis, A. M. C., Fortin, D., & Sébire, G. (2005) · Developmental Neuroscience · doi:10.1159/000085985 · Cited by 91 · see citing works
Maternal Endotoxemia Results in Obesity and Insulin Resistance in Adult Male Offspring
Nilsson, C., Larsson, B.-M., Jennische, E., Eriksson, E., Björntorp, P. A., York, D. A., & Holmäng, A. B. (2001) · Endocrinology · doi:10.1210/endo.142.6.8191 · Cited by 90 · see citing works
Dopaminergic and serotoninergic deficiencies in young adult rats prenatally exposed to the bacterial lipopolysaccharide
Wang, S. Z., Yan, J.-Y., Lo, Y.-K., Carvey, P. M., & Ling, Z. (2009) · Brain Research · doi:10.1016/j.brainres.2009.02.022 · Cited by 86 · see citing works
Abnormal expression of myelination genes and alterations in white matter fractional anisotropy following prenatal viral influenza infection at E16 in mice
Fatemi, S. H., Folsom, T. D., Reutiman, T. J., Abu-Odeh, D., Mori, S., Huang, H., & Oishi, K. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2009.04.014 · Cited by 86 · see citing works
Prenatal Immune Challenge Affects Growth, Behavior, and Brain Dopamine in Offspring
Bakoš, J., Dunčko, R., Makatsori, A., Pirník, Z., Kiss, A., & Ježová, D. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1296.033 · Cited by 85 · see citing works
Altered glutathione homeostasis in animals prenatally exposed to lipopolysaccharide
ZHU, Y., CARVEY, P., & LING, Z. (2007) · Neurochemistry International · doi:10.1016/j.neuint.2006.12.013 · Cited by 85 · see citing works
Altered expression of pro-inflammatory and developmental genes in the fetal brain in a mouse model of maternal infection
Liverman, C. S., Kaftan, H. A., Cui, L., Hersperger, S. G., Taboada, E. M., Klein, R. M., & Berman, N. E. J. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.01.064 · Cited by 80 · see citing works
Persistence of viral RNA in the brain of offspring to mice infected with influenza A/WSN/33 virus during pregnancy
Aronsson, F. S., Lannebo, C., Paucar, M., Brask, J., Kristensson, K., & Karlsson, H. (2002) · Journal of NeuroVirology · doi:10.1080/13550280290100480 · Cited by 77 · see citing works
Differential expression of cytokines in the brain and serum during endotoxin tolerance
Chen, R., Zhou, H., Beltran, J., Malellari, L., & Chang, S. L. (2005) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2005.02.012 · Cited by 67 · see citing works
NEUROBEHAVIORAL AND IMMUNOLOGICAL CONSEQUENCES OF PRENATAL IMMUNE ACTIVATION IN RATS
Borrell, J. I. (2008) · Schizophrenia Research · doi:10.1016/s0920-9964(08)70050-1 · Cited by 66 · see citing works
Interleukin-6 increases sensitivity to the locomotor-stimulating effects of amphetamine in rats
Zalcman, S., Savina, I., & Wise, R. A. (1999) · Brain Research · doi:10.1016/s0006-8993(99)02063-6 · Cited by 64 · see citing works
Maternal infection and fever during late gestation are associated with altered synaptic transmission in the hippocampus of juvenile offspring rats
Lowe, G. C., Luheshi, G. N., & Williams, S. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90350.2008 · Cited by 64 · see citing works
Epidemiology in neurobiological research: exemplified by the influenza-schizophrenia theory
Munk-J�rgensen, P., & Ewald, H. (2001) · The British Journal of Psychiatry · doi:10.1192/bjp.178.40.s30 · Cited by 64 · see citing works
Hypothermia to endotoxin involves reduced thermogenesis, macrophage-dependent mechanisms, and prostaglandins
DeRijk, R. H., Kampen, M. V., van Rooijen, N., & BERKENBOSCH, F. (1994) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1994.266.1.r1 · Cited by 64 · see citing works
Antenatal Antecedents and the Impact of Obstetric Care in the Etiology of Cerebral Palsy
Clark, S. M., Ghulmiyyah, L., & Hankins, G. D. V. (2008) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181870994 · Cited by 63 · see citing works
Trophoblastic apoptosis in mice with preterm delivery and its suppression by urinary trypsin inhibitor
Kakinuma, C., Kuwayama, C., KAGA, N., Futamura, Y., Katsuki, Y., & Shibutani, Y. (1997) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(97)00176-2 · Cited by 63 · see citing works
Seasonality and infectious disease in schizophrenia: the birth hypothesis revisited
Battle, Y. L., Martin, B. C., Dorfman, J. H., & Miller, L. S. (1999) · Journal of Psychiatric Research · doi:10.1016/s0022-3956(99)00022-9 · Cited by 62 · see citing works
Variability in LPS composition, antigenicity and reactogenicity of phase variants of Bordetella pertussis
Ray, A., Redhead, K., Selkirk, S., & Poole, S. (1991) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1991.tb04531.x · Cited by 62 · see citing works
Interleukin-1 receptor antagonist as a modulator of gender differences in the febrile response to lipopolysaccharide in rats
Ashdown, H. F., Poole, S., Boksa, P., & Luheshi, G. N. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00274.2006 · Cited by 62 · see citing works
Self-citation
The Role of Double-Stranded RNA in Induction of the Acute-Phase Response in an Abortive Influenza Virus Infection Model
Kimura-Takeuchi, M., Majde, J. A., Toth, L. A., & Krueger, J. M. (1992) · The Journal of Infectious Diseases · doi:10.1093/infdis/166.6.1266 · Cited by 61 · see citing works
Age- and gender-dependent impairments of neurobehaviors in mice whose mothers were exposed to lipopolysaccharide during pregnancy
Wang, H., Meng, X., Ning, H., Zhao, X., Wang, Q., Liu, P., Zhang, H., Zhang, C., Chen, G.-H., & Xu, D. (2009) · Toxicology Letters · doi:10.1016/j.toxlet.2009.10.030 · Cited by 58 · see citing works
Effects of Maternal Campylobacter rectus Infection on Murine Placenta, Fetal and Neonatal Survival, and Brain Development
Offenbacher, S., Riché, E. L., Barros, S. P., Bobetsis, Y. A., Lin, D., & Beck, J. D. (2005) · Journal of Periodontology · doi:10.1902/jop.2005.76.11-s.2133 · Cited by 56 · see citing works
Antenatal Bacterial Endotoxin Sensitizes the Immature Rat Brain to Postnatal Excitotoxic Injury
Rousset, C. I., Kassem, J., Olivier, P., Chalon, S., Gressèns, P., & Saliba, É. (2008) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e31818894a1 · Cited by 50 · see citing works
Differential expression of synaptosome-associated protein 25 kDa [SNAP-25] in hippocampi of neonatal mice following exposure to human influenza virus in utero
Fatemi, S. H., Sidwell, R. W., Kist, D. A., Akhter, P., Meltzer, H. Y., Bailey, K. W., THURAS, P. D., & Sedgwick, J. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00450-8 · Cited by 49 · see citing works
Molecular Aspects of Fever and Hyperthermia
Roth, J., Rummel, C. D., Barth, S. W., Gerstberger, R., & Hübschle, T. (2009) · Immunology and Allergy Clinics of North America · doi:10.1016/j.iac.2009.02.005 · Cited by 48 · see citing works
Escherichia coli lipopolysaccharides produce serotype-specific hypothermic response in biotelemetered rats
Akarsu, E. S., & Mamuk, S. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00786.2006 · Cited by 48 · see citing works
The transfer of interleukin-8 across the human placenta perfused in vitro
Reisenberger, K., Egarter, C., Vogl, S., Sternberger, B., Kiss, H., & HUSSLEIN, P. (1996) · Obstetrics and Gynecology · doi:10.1016/0029-7844(95)00473-4 · Cited by 46 · see citing works
Course of fever response to repeated administration of sublethal doses of lipopolysaccharides, polyinosinic: Polycytidylic acid and muramyl dipeptide to rabbits
Soszyński, D., Kozak, W., & Szewczenko, M. (1991) · Cellular and Molecular Life Sciences · doi:10.1007/bf02041248 · Cited by 45 · see citing works
Prenatal viral infection of mice at E16 causes changes in gene expression in hippocampi of the offspring
Fatemi, S. H., Folsom, T. D., Reutiman, T. J., Huang, H., Oishi, K., & Mori, S. (2009) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.03.004 · Cited by 45 · see citing works
Zinc treatment prevents lipopolysaccharide‐induced teratogenicity in mice
Carey, L. C., Berbée, P. L., Coyle, P. V., Philcox, J. C., & Rofe, A. M. (2003) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.10035 · Cited by 45 · see citing works
Prenatal lipopolysaccharide does not accelerate progressive dopamine neuron loss in the rat as a result of normal aging
Ling, Z., Zhu, Y., Tong, C. W., Snyder, J. A., Lipton, J. W., & Carvey, P. M. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2008.12.004 · Cited by 40 · see citing works
Suppression of the Febrile Response in Late Gestation: Evidence, Mechanisms and Outcomes
Mouihate, A., Harré, E. ‐., Martin, S. M., & Pittman, Q. J. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01666.x · Cited by 39 · see citing works
Maternally-administered lipopolysaccharide (LPS) increases tumor necrosis factor alpha in fetal liver and fetal brain: Its suppression by low-dose LPS pretreatment
Ning, H., Wang, H., Zhao, L., Zhang, C., Li, X., Chen, Y., & Xu, D. (2007) · Toxicology Letters · doi:10.1016/j.toxlet.2007.08.002 · Cited by 39 · see citing works
Viral regulation of aquaporin 4, connexin 43, microcephalin and nucleolin
Fatemi, S. H., Folsom, T. D., Reutiman, T. J., & Sidwell, R. W. (2007) · Schizophrenia Research · doi:10.1016/j.schres.2007.09.031 · Cited by 37 · see citing works
Ascorbic acid protects against lipopolysaccharide-induced intra-uterine fetal death and intra-uterine growth retardation in mice
Chen, Y., Xu, D., Zhao, L., Wang, H., Wang, J., & Wei, W. (2005) · Toxicology · doi:10.1016/j.tox.2005.08.010 · Cited by 36 · see citing works
Prenatal exposure to influenza and the risk of subsequent development of schizophrenia.
Ebert, T., & Kotler, M. (2005) · PubMed · Cited by 34 · see citing works
Transplacental murine cytomegalovirus infection in the brain of SCID mice
Woolf, N. K., Jaquish, D. V., & Koehrn, F. J. (2007) · Virology Journal · doi:10.1186/1743-422x-4-26 · Cited by 34 · see citing works
Centrally acting vasopressin contributes to endotoxin tolerance
Wilkinson, M. F., & Kasting, N. W. (1990) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1990.258.2.r443 · Cited by 34 · see citing works
Screening of interleukins for survival-promoting effects on cultured mesencephalic dopaminergic neurons from embryonic rat brain
von Coelln, R., Unsicker, K., & KRIEGLSTEIN, K. G. (1995) · Developmental Brain Research · doi:10.1016/0165-3806(95)00123-u · Cited by 32 · see citing works
Normal aging of offspring mice of mothers with induced inflammation during pregnancy
Golan, H., Stilman, M., Lev, V., & Huleihel, M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.05.045 · Cited by 32 · see citing works
Central and peripheral neuroimmune responses: hyporesponsiveness during pregnancy
Spencer, S. J., Mouihate, A., Galic, M. A., & Pittman, Q. J. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.144006 · Cited by 31 · see citing works
Influence of Pregnancy on Plasma Cytokines and the Febrile Response to Intraperitoneal Administration of Bacterial Endotoxin in Rats
Fofie, A. E., & Fewell, J. E. (2003) · Experimental Physiology · doi:10.1113/eph8802594 · Cited by 31 · see citing works
Activated protein C reduces endotoxin-induced white matter injury in the developing rat brain
Yeşilırmak, D. C., Kumral, A., Baskın, H., Ergür, B. U., Aykan, S., Genç, Ş., Genç, K., Yılmaz, O., Tuğyan, K., Giray, Ö., et al. (2007) · Brain Research · doi:10.1016/j.brainres.2007.04.083 · Cited by 30 · see citing works
Dietary Zinc Supplementation Ameliorates LPS-Induced Teratogenicity in Mice
Chua, J. S. C., Rofe, A. M., & Coyle, P. V. (2006) · Pediatric Research · doi:10.1203/01.pdr.0000199906.37619.9c · Cited by 29 · see citing works
The course of fever following influenza virus infection in children treated with oseltamivir
Suzuki, E., & Ichihara, K. (2008) · Journal of Medical Virology · doi:10.1002/jmv.21144 · Cited by 29 · see citing works
Failure of Endotoxin to Cross the Chorioamniotic Membranes in Vitro
Romero, R. J., Lafreniere, D., Duff, G. W., Kadar, N. R., Durum, S. K., & Hobbins, J. C. (1987) · American Journal of Perinatology · doi:10.1055/s-2007-999808 · Cited by 26 · see citing works
Prenatal infection obliterates glutamate‐related protection against free hydroxyl radicals in neonatal rat brain
Cambonie, G., Hirbec, H., Michaud, M., Kamenka, J. M., & Barbanel, G. (2003) · Journal of Neuroscience Research · doi:10.1002/jnr.10823 · Cited by 25 · see citing works
Gene expression changes in brains of mice exposed to a maternal virus infection
Asp, L., Beraki, S., Aronsson, F. S., Rosvall, L., Ögren, S. O., Kristensson, K., & Karlsson, H. (2005) · Neuroreport · doi:10.1097/00001756-200507130-00016 · Cited by 24 · see citing works
Suppression of endotoxin-induced fever in near-term pregnant rats is mediated by brain nitric oxide
Begg, D. P., Kent, S., McKinley, M. J., & Mathai, M. L. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00032.2007 · Cited by 22 · see citing works
ACTIVATION OF COMMON ANTIVIRAL PATHWAYS CAN POTENTIATE INFLAMMATORY RESPONSES TO SEPTIC SHOCK
Doughty, L., Carlton, S., Galen, B. T., Cooma-Ramberan, I., Chung, C. S., & Ayala, A. (2006) · Shock · doi:10.1097/01.shk.0000223129.79759.74 · Cited by 20 · see citing works
LPS injected into the pregnant rat late in gestation does not induce fetal endotoxemia.
Gotō, M., Yoshioka, T., Ravindranath, T. M., Battelino, T., Young, R., & Zeller, W. P. (1994) · PubMed · Cited by 20 · see citing works
Dose-dependent lipopolysaccharide-induced fetal brain injury in the guinea pig
Harnett, E. L., Dickinson, M. A., & Smith, G. N. (2007) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2007.03.047 · Cited by 19 · see citing works
Natural Course of Fever During Influenza Virus Infection in Children
Suzuki, E., Ichihara, K., & JOHNSON, A. M. (2007) · Clinical Pediatrics · doi:10.1177/0009922806289588 · Cited by 19 · see citing works
Transplacental Effects of Endotoxemia on Fetal Mouse Brain, Bone, and Placental Tissue
Haesaert, B., & Ornoy, A. (1986) · Pediatric Pathology · doi:10.3109/15513818609041199 · Cited by 16 · see citing works
Prenatal inflammatory effects on nigrostriatal development in organotypic cultures
Snyder‐Keller, A., & Stark, P. F. (2008) · Brain Research · doi:10.1016/j.brainres.2008.07.106 · Cited by 13 · see citing works
Lipopolysaccharide (LPS) Up-Regulates the Expression of Haem Oxygenase-1 in Mouse Placenta
Zhang, C., Li, X.-Y., Zhao, L., Wang, H., & Xu, D.-X. (2007) · Placenta · doi:10.1016/j.placenta.2007.04.003 · Cited by 13 · see citing works
Endotoxin exposure in utero increases ethanol consumption in adult male offspring
Liu, X., Lee, J. G., Yee, S. K., Bresee, C. J., Poland, R. E., & Pechnick, R. N. (2003) · Neuroreport · doi:10.1097/00001756-200401190-00039 · Cited by 12 · see citing works
Endotoxin treatment of pregnant rats affects sexual behavior of the male offspring
Wijkstra, S., Valkhof, N., Koolhaas, J. M., & Schuiling, G. A. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90294-x · Cited by 6 · see citing works

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The role of inflammation in perinatal brain injury
Hagberg, H., Mallard, C. E., Ferriero, D. M., Vannucci, S. J., Levison, S. W., Vexler, Z. S., & Gressèns, P. (2015) · Nature Reviews Neurology · doi:10.1038/nrneurol.2015.13 · Cited by 832 · see citing works
Animal models of schizophrenia
Jones, C., Watson, D., & Fone, K. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01386.x · Cited by 771 · 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
Early Adverse Experiences and the Developing Brain
Bick, J., & Nelson, C. A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.252 · Cited by 559 · see citing works
The Role of the Immune System in Autism Spectrum Disorder
Meltzer, A., & Van de Water, J. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.158 · Cited by 533 · see citing works
Toll-like receptor signaling in neural plasticity and disease
Okun, E., Griffioen, K. J. S., & Mattson, M. P. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.02.005 · Cited by 513 · see citing works
HPA Axis in the Pathomechanism of depression and schizophrenia: new therapeutic strategies based on its participation
Mikulska, J., Juszczyk, G., Gawrońska-Grzywacz, M., & Herbet, M. (2021) · Brain Sciences · doi:10.3390/brainsci11101298 · Cited by 450 · 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
Increased midgestational IFN-γ, IL-4 and IL-5 in women bearing a child with autism: A case-control study
Goines, P. E., Croen, L. A., Braunschweig, D., Yoshida, C. K., Grether, J., Hansen, R., Kharrazi, M., Ashwood, P., & Van de Water, J. (2011) · Molecular Autism · doi:10.1186/2040-2392-2-13 · Cited by 351 · see citing works
Maternal immune activation and autism spectrum disorder: From rodents to nonhuman and human primates
Careaga, M., Murai, T., & Bauman, M. D. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.10.020 · Cited by 348 · see citing works
The immune theory of psychiatric diseases: a key role for activated microglia and circulating monocytes
Beumer, W., Gibney, S. M., Drexhage, R. C., Pont-Lezica, L., Doorduin, J., Klein, H. C., Steiner, J., Connor, T. J., Harkin, A., Versnel, M. A., et al. (2012) · Journal of Leukocyte Biology · doi:10.1189/jlb.0212100 · Cited by 347 · see citing works
Prenatal Stress-Induced Increases in Placental Inflammation and Offspring Hyperactivity Are Male-Specific and Ameliorated by Maternal Antiinflammatory Treatment
Bronson, S. L., & Bale, T. L. (2014) · Endocrinology · doi:10.1210/en.2014-1040 · Cited by 299 · see citing works
Inflammation and Schizophrenia
Kirkpatrick, B. W., & Miller, B. J. (2013) · Schizophrenia Bulletin · doi:10.1093/schbul/sbt141 · Cited by 318 · see citing works
Dopamine, Immunity, and Disease
Channer, B., Matt, S. M., Nickoloff-Bybel, E. A., Pappa, V., Agarwal, Y., Wickman, J. R., & Gaskill, P. J. (2022) · Pharmacological Reviews · doi:10.1124/pharmrev.122.000618 · Cited by 319 · see citing works
Developmental neuroinflammation and schizophrenia
Meyer, U. (2011) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2011.11.003 · Cited by 300 · see citing works
Inflammation and the neural diathesis-stress hypothesis of schizophrenia: a reconceptualization
Howes, O. D., & McCutcheon, R. (2017) · Translational Psychiatry · doi:10.1038/tp.2016.278 · Cited by 288 · 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
Microglia and the brain: Complementary partners in development and disease
Hammond, T. R., Robinton, D., & Stevens, B. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100616-060509 · Cited by 288 · see citing works
Inflammation and the two-hit hypothesis of schizophrenia
Feigenson, K. A., Kusnecov, A., & Silverstein, S. M. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.11.006 · Cited by 280 · 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
Autoimmunity, Inflammation, and Psychosis: A Search for Peripheral Markers
Bergink, V., Gibney, S. M., & Drexhage, H. A. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.09.037 · Cited by 269 · see citing works
Microglia in CNS development: Shaping the brain for the future
Mosser, C., Baptista, S., Arnoux, I., & Audinat, É. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.01.002 · Cited by 268 · 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
Microglia in the developing brain: a potential target with lifetime effects
Harry, G. J., & Kraft, A. D. (2012) · NeuroToxicology · doi:10.1016/j.neuro.2012.01.012 · Cited by 250 · see citing works
Maternal immune activation: reporting guidelines to improve the rigor, reproducibility, and transparency of the model
Kentner, A. C., Bilbo, S. D., Brown, A. S., Hsiao, E. Y., McAllister, A. K., Meyer, U., Pearce, B. D., Pletnikov, M. V., Yolken, R. H., & Bauman, M. D. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0185-7 · Cited by 245 · see citing works
Innate immunity at the crossroads of healthy brain maturation and neurodevelopmental disorders
Zengeler, K. E., & Lukens, J. R. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-020-00487-7 · Cited by 254 · see citing works
To poly(I:C) or not to poly(I:C): Advancing preclinical schizophrenia research through the use of prenatal immune activation models
Meyer, U., & Feldon, J. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.009 · Cited by 247 · see citing works
Socio-Emotional Development Following Very Preterm Birth: Pathways to Psychopathology
Montagna, A., & Nosarti, C. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.00080 · Cited by 239 · see citing works
Gliotransmitter Release from Astrocytes: Functional, Developmental, and Pathological Implications in the Brain
Harada, K., Kamiya, T., & Tsuboi, T. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00499 · Cited by 246 · see citing works
Prenatal factors associated with autism spectrum disorder (ASD)
Ornoy, A., Weinstein-Fudim, L., & Ergaz, Z. (2015) · Reproductive Toxicology · doi:10.1016/j.reprotox.2015.05.007 · Cited by 238 · see citing works
Function and Dysfunction of Microglia during Brain Development: Consequences for Synapses and Neural Circuits
Paolicelli, R. C., & Ferretti, M. T. (2017) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2017.00009 · Cited by 235 · see citing works
Evidence for a Dysregulated Immune System in the Etiology of Psychiatric Disorders
Gibney, S. M., & Drexhage, H. A. (2013) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-013-9462-8 · Cited by 237 · see citing works
Oxidative Stress‐Related Mechanisms in Schizophrenia Pathogenesis and New Treatment Perspectives
Ermakov, E. A., Dmitrieva, E. M., Parshukova, D. A., Kazantseva, D. V., Vasilieva, A. R., & Smirnova, L. P. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/8881770 · Cited by 252 · see citing works
The influence of maternal prenatal and early childhood nutrition and maternal prenatal stress on offspring immune system development and neurodevelopmental disorders
Marques, A. H., O'Connor, T. G., Roth, C., Susser, E., & Bjørke-Monsen, A.-L. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00120 · Cited by 226 · see citing works
The Poly(I:C)-induced maternal immune activation model in preclinical neuropsychiatric drug discovery
Reisinger, S. N., Khan, D., Kong, E., Berger, A., Pollak, A. J., & Pollak, D. D. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.01.001 · Cited by 219 · see citing works
Prenatal infection leads to ASD-like behavior and altered synaptic pruning in the mouse offspring
de Cossío, L. F., Guzman, A. S., van der Veldt, S., & Luheshi, G. N. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.09.028 · Cited by 214 · see citing works
Microglia Gone Rogue: Impacts on Psychiatric Disorders across the Lifespan
Tay, T. L., Béchade, C., D’Andrea, I., St‐Pierre, M., Henry, M. S., Roumier, A., & Tremblay, M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00421 · Cited by 211 · see citing works
Elevated Maternal C-Reactive Protein and Increased Risk of Schizophrenia in a National Birth Cohort
Canetta, S., Sourander, A., Surcel, H.-M., Hinkka-Yli-Salomäki, S., Leiviskä, J., Kellendonk, C., McKeague, I. W., & Brown, A. S. (2014) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2014.13121579 · Cited by 203 · see citing works
Sexual Differentiation of the Rodent Brain: Dogma and Beyond
Lenz, K. M., Nugent, B. M., & McCarthy, M. M. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00026 · Cited by 191 · see citing works
Maternal Immune Activation by Poly I:C as a preclinical Model for Neurodevelopmental Disorders: A focus on Autism and Schizophrenia
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
Microglia as modulators of cognition and neuropsychiatric disorders
Blank, T., & Prinz, M. (2012) · Glia · doi:10.1002/glia.22372 · Cited by 185 · see citing works
Immune System Disturbances in Schizophrenia
Horváth, S., & Mirnics, K. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.06.010 · Cited by 177 · see citing works
Sensory Abnormalities in Autism Spectrum Disorders: A Focus on the Tactile Domain, From Genetic Mouse Models to the Clinic
Balasco, L., Provenzano, G., & Bozzi, Y. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.01016 · Cited by 183 · see citing works
Microglia shape corpus callosum axon tract fasciculation: functional impact of prenatal inflammation
Pont‐Lezica, L., Beumer, W., Colasse, S., Drexhage, H. A., Versnel, M. A., & Bessis, A. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12508 · Cited by 174 · 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
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
Maternal stress, nutrition and physical activity: Impact on immune function, CNS development and psychopathology
Marques, A. H., Bjørke-Monsen, A.-L., Teixeira, A. L., & Silverman, M. N. (2015) · Brain Research · doi:10.1016/j.brainres.2014.10.051 · Cited by 166 · see citing works
Prenatal LPS-exposure – a neurodevelopmental rat model of schizophrenia – differentially affects cognitive functions, myelination and parvalbumin expression in male and female offspring
Wischhof, L., Irrsack, E., Osorio, C., & Koch, M. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.10.004 · Cited by 158 · see citing works
Increasing Role of Maternal Immune Activation in Neurodevelopmental Disorders
Boulanger-Bertolus, J., Pancaro, C., & Mashour, G. A. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00230 · Cited by 154 · see citing works
Oligodendroglial alterations and the role of microglia in white matter injury: relevance to schizophrenia
Chew, L.-J., Fusar-Poli, P., & Schmitz, T. (2013) · Developmental Neuroscience · doi:10.1159/000346157 · Cited by 154 · see citing works
Perinatal stress, brain inflammation and risk of autism-Review and proposal
Angelidou, A., Asadi, S., Alysandratos, K., Karagkouni, A., Kourembanas, S., & Theoharides, T. C. (2012) · BMC Pediatrics · doi:10.1186/1471-2431-12-89 · Cited by 153 · see citing works
Association of Maternal Exposure to Childhood Abuse With Elevated Risk for Autism in Offspring
Roberts, A. L., Lyall, K., Rich-Edwards, J. W., Ascherio, A., & Weisskopf, M. G. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.447 · Cited by 152 · see citing works
Prenatal and postnatal animal models of immune activation: Relevance to a range of neurodevelopmental disorders
Harvey, L., & Boksa, P. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22043 · Cited by 149 · see citing works
Self-citation
Maternal infection during late pregnancy increases anxiety- and depression-like behaviors with increasing age in male offspring
Enayati, M., Solati, J., Hosseini, M.-H., Shahi, H.-R., Saki, G., & Salari, A. A. (2011) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2011.08.015 · Cited by 147 · see citing works
Neuroprogression in schizophrenia: Pathways underpinning clinical staging and therapeutic corollaries
Davis, J., Moylan, S., Harvey, B. H., Maes, M. H. J., & Berk, M. (2014) · Australian & New Zealand Journal of Psychiatry · doi:10.1177/0004867414533012 · Cited by 147 · see citing works
Serological Documentation of Maternal Influenza Exposure and Bipolar Disorder in Adult Offspring
Canetta, S., Bao, Y., Co, M. D. T., Ennis, F. A., Cruz, J., Terajima, M., Shen, L., Kellendonk, C., Schaefer, C. A., & Brown, A. S. (2014) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2013.13070943 · Cited by 147 · see citing works
COVID-19 in pregnancy: implications for fetal brain development
Shook, L. L., Sullivan, E. L., Lo, J. O.-T., Perlis, R. H., & Edlow, A. G. (2022) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2022.02.004 · Cited by 145 · see citing works
Maternal immune activation by poly(I:C) induces expression of cytokines IL-1β and IL-13, chemokine MCP-1 and colony stimulating factor VEGF in fetal mouse brain
Arrode-Brusés, G., & Brusés, J. L. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-83 · Cited by 146 · see citing works
Abnormal Trajectories of Neurodevelopment and Behavior Following In Utero Insult in the Rat
Piontkewitz, Y., Arad, M., & Weiner, I. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.06.007 · Cited by 144 · 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
Environmental Enteropathy: Elusive but Significant Subclinical Abnormalities in Developing Countries
Watanabe, K., & Petri, W. A. (2016) · EBioMedicine · doi:10.1016/j.ebiom.2016.07.030 · Cited by 139 · see citing works
Neonatal Behavioral Changes in Rats With Gestational Exposure to Lipopolysaccharide: A Prenatal Infection Model for Developmental Neuropsychiatric Disorders
Baharnoori, M., Bhardwaj, S. K., & Srivastava, L. K. (2010) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq098 · Cited by 134 · see citing works
Prenatal Immune Activation Induces Maturation-Dependent Alterations in the Prefrontal GABAergic Transcriptome
Richetto, J., Calabrese, F., Riva, M. A., & Meyer, U. (2013) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs195 · Cited by 134 · see citing works
Maternal immune activation in nonhuman primates alters social attention in juvenile offspring
Machado, C. J., Whitaker, A. M., Smith, S. E. P., Patterson, P. H., & Bauman, M. D. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.07.035 · Cited by 136 · see citing works
Maternal inflammation induces immune activation of fetal microglia and leads to disrupted microglia immune responses, behavior, and learning performance in adulthood
Schaafsma, W., Bozal‐Basterra, L., Jacobs, S., Brouwer, N., Meerlo, P., Schaafsma, A., Boddeke, E., & Eggen, B. J. L. (2017) · Neurobiology of Disease · doi:10.1016/j.nbd.2017.07.017 · Cited by 135 · see citing works
Inflammation early in life is a vulnerability factor for emotional behavior at adolescence and for lipopolysaccharide-induced spatial memory and neurogenesis alteration at adulthood
Dinel, A., Joffre, C., Trifilieff, P., Aubert, A., Foury, A., Ruyet, P. L., & Layé, S. (2014) · Journal of Neuroinflammation · doi:10.1186/s12974-014-0155-x · Cited by 134 · see citing works
Sex-dependent behavioral deficits and neuropathology in a maternal immune activation model of autism
Haïda, O., Sagheer, T. A., Balbous, A., Francheteau, M., Matas, E., Soria, F. N., Fernagut, P., & Jaber, M. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0457-y · Cited by 131 · see citing works
Acute in utero exposure to lipopolysaccharide induces inflammation in the pre- and postnatal brain and alters the glial cytoarchitecture in the developing amygdala
O’Loughlin, E., Pakan, J. M. P., Yilmazer-Hanke, D., & McDermott, K. W. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0981-8 · Cited by 127 · see citing works
Prenatal inflammation and neurodevelopment in schizophrenia: A review of human studies
Miller, B. J., Culpepper, N. H., Rapaport, M. H., & Buckley, P. F. (2012) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.03.010 · Cited by 124 · see citing works
Hypoactivity of the central dopaminergic system and autistic-like behavior induced by a single early prenatal exposure to lipopolysaccharide
Kirsten, T. B., Chaves‐Kirsten, G. P., Chaible, L. M., Silva, A. C., Martins, D. O., Britto, L. R. G., Dagli, M. L. Z., Torrão, A. S., Palermo‐Neto, J., & Bernardi, M. M. (2012) · Journal of Neuroscience Research · doi:10.1002/jnr.23089 · Cited by 122 · see citing works
Long-term effects of maternal immune activation on depression-like behavior in the mouse
Khan, D., Fernando, P. M., Cicvaric, A., Berger, A., Pollak, A. J., Monje, F. J., & Pollak, D. D. (2014) · Translational Psychiatry · doi:10.1038/tp.2013.132 · Cited by 118 · see citing works
Risk factors in autism: Thinking outside the brain
Matelski, L., & van de Water, J. A. (2015) · Journal of Autoimmunity · doi:10.1016/j.jaut.2015.11.003 · Cited by 127 · see citing works
Associations Between Maternal Infection During Pregnancy, Childhood Infections and the Risk of Subsequent Psychotic Disorder—A Swedish Cohort Study of Nearly 2 Million Individuals
Blomström, Å., Karlsson, H., Gardner, R. M., Jörgensen, L., Magnusson, C., & Dalman, C. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv112 · Cited by 120 · see citing works
Genetic and non-genetic animal models for autism spectrum disorders (ASD)
Ergaz, Z., Weinstein‐Fudim, L., & Ornoy, A. (2016) · Reproductive Toxicology · doi:10.1016/j.reprotox.2016.04.024 · Cited by 116 · see citing works
TLR4 response mediates ethanol-induced neurodevelopment alterations in a model of fetal alcohol spectrum disorders
Pascual, M., Montesinos, J., Montagud‐Romero, S., Forteza, J., Rodríguez‐Arias, M., Miñarro, J., & Guerri, C. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0918-2 · Cited by 119 · 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
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Fumagalli, M., Lecca, D., Abbracchio, M. P., & Ceruti, S. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00941 · Cited by 116 · see citing works
Prenatal lipopolysaccharide exposure increases depression-like behaviors and reduces hippocampal neurogenesis in adult rats
Lin, Y., & Wang, S. Z. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.10.034 · Cited by 115 · see citing works
Effects of immune activation during early or late gestation on schizophrenia-related behaviour in adult rat offspring
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
Linking inflammation, aberrant glutamate-dopamine interaction, and post-synaptic changes: translational relevance for schizophrenia and antipsychotic treatment: a systematic review
de Bartolomeis, A., Barone, A., Vellucci, L., Mazza, B., Austin, M. C., Iasevoli, F., & Ciccarelli, M. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-02976-3 · Cited by 113 · see citing works
Inflammation and the developing brain: Consequences for hippocampal neurogenesis and behavior
Green, H. F., & Nolan, Y. M. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.01.004 · Cited by 111 · see citing works
Maternal prenatal depression predicts infant negative affect via maternal inflammatory cytokine levels
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
Developmental minocycline treatment reverses the effects of neonatal immune activation on anxiety- and depression-like behaviors, hippocampal inflammation, and HPA axis activity in adult mice
Majidi, J., Kosari-Nasab, M., & Salari, A.-A. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2015.10.009 · Cited by 109 · see citing works
Prenatal infection, maternal immune activation, and risk for schizophrenia
Canetta, S., & Brown, A. (2012) · Translational Neuroscience · doi:10.2478/s13380-012-0045-6 · 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
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
The role of maternal immune activation in altering the neurodevelopmental trajectories of offspring: A translational review of neuroimaging studies with implications for autism spectrum disorder and schizophrenia
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
Immune system gene dysregulation in autism and schizophrenia
Michel, M., Schmidt, M. J., & Mirnics, K. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22044 · Cited by 107 · see citing works
Maternal immune activation transgenerationally modulates maternal care and offspring depression-like behavior
Ronovsky, M., Berger, S., Zambon, A., Reisinger, S. N., Horvath, O., Pollak, A. J., Lindtner, C., Berger, A., & Pollak, D. D. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.10.016 · Cited by 108 · see citing works
Hyperoxia and the Immature Brain
Reich, B., Hoeber, D., Bendix, I., & Felderhoff‐Mueser, U. (2016) · Developmental Neuroscience · doi:10.1159/000454917 · Cited by 109 · see citing works
Maternal immune activation as an epidemiological risk factor for neurodevelopmental disorders: Considerations of timing, severity, individual differences, and sex in human and rodent studies
Hall, M. B., Willis, D. E., Rodriguez, E. L., & Schwarz, J. M. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1135559 · Cited by 112 · see citing works
From Maternal Diet to Neurodevelopmental Disorders: A Story of Neuroinflammation
Bordeleau, M., de Cossío, L. F., Chakravarty, M. M., & Tremblay, M. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.612705 · Cited by 108 · see citing works
LPS Exposure Increases Maternal Corticosterone Levels, Causes Placental Injury and Increases IL-1Β Levels in Adult Rat Offspring: Relevance to Autism
Kirsten, T. B., Lippi, L. L., Bevilacqua, E. M. A. F., & Bernardi, M. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082244 · Cited by 103 · see citing works
Postnatal administration of IL-1Ra exerts neuroprotective effects following perinatal inflammation and/or hypoxic-ischemic injuries
Girard, S., Sébire, H., Brochu, M., Briota, S., Sarret, P., & Sébire, G. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.09.001 · Cited by 102 · see citing works
The effects of maternal stress and illness during pregnancy on infant temperament: Project Ice Storm
Laplante, D. P., Brunet, A., & King, S. (2015) · Pediatric Research · doi:10.1038/pr.2015.177 · Cited by 101 · see citing works
Maternal immune activation alters behavior in adult offspring, with subtle changes in the cortical transcriptome and epigenome
Connor, C., Dincer, A., Straubhaar, J., Galler, J. R., Houston, I. B., & Akbarian, S. (2012) · Schizophrenia Research · doi:10.1016/j.schres.2012.06.037 · Cited by 100 · see citing works
A Review of Oxytocin and Arginine-Vasopressin Receptors and Their Modulation of Autism Spectrum Disorder
Cataldo, I., Azhari, A., & Esposito, G. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00027 · Cited by 95 · see citing works
Developmental vitamin D and autism spectrum disorders: findings from the Stockholm Youth Cohort
Lee, B. K., Eyles, D. W., Magnusson, C., Newschaffer, C. J., McGrath, J. J., Kvaskoff, D., Ko, P., Dalman, C., Karlsson, H., & Gardner, R. M. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0578-y · Cited by 101 · see citing works
Epigenomic strategies at the interface of genetic and environmental risk factors for autism
LaSalle, J. M. (2013) · Journal of Human Genetics · doi:10.1038/jhg.2013.49 · Cited by 95 · see citing works
Intravenous administration of AAV2/9 to the fetal and neonatal mouse leads to differential targeting of CNS cell types and extensive transduction of the nervous system
Rahim, A. A., Wong, A. M. S., Hoefer, K., Buckley, S. M. K., Mattar, C. N. Z., Cheng, S. H., Chan, J. K. Y., Cooper, J. D., & Waddington, S. N. (2011) · The FASEB Journal · doi:10.1096/fj.11-182311 · Cited by 95 · see citing works

30.4 PRENATAL INFECTION AND LONG-TERM BRAIN PATHOLOGY: FROM PRECLINICAL MODELS TO MECHANISMS
Richetto, J. (2018) · Schizophrenia Bulletin · doi:10.1093/schbul/sby014.125
Prenatal infection, maternal immune activation, and risk for schizophrenia
Canetta, S., & Brown, A. (2012) · Translational Neuroscience · doi:10.2478/s13380-012-0045-6 · Cited by 109 · see citing works
Maternal immune activation and abnormal brain development across CNS disorders
Knuesel, I., Chicha, L., Britschgi, M., Schobel, S. A., Bodmer, M., Hellings, J. A., Toovey, S., & Prinssen, E. P. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.187 · Cited by 880 · see citing works
Evidence that prenatal infection is a risk factor for brain and behaviour changes relevant to schizophrenia and autism
Edward, W. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/conf.neuro.08.2009.09.228
In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders
Meyer, U., Feldon, J., & Fatemi, S. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.001 · Cited by 367 · see citing works

Authors: Boksa, P.
Affiliations: Douglas Mental Health University Institute (CA)
Corresponding author: Boksa, Patricia
ORCID: Boksa, Patricia
Venue: Brain, Behavior, and Immunity
Publisher: Elsevier BV
Published: 2010-08
Volume: 24
Issue: 6
Pages: 881-897
ISSN: 0889-1591 (ISSN-L)
DOI: 10.1016/j.bbi.2010.03.005
OpenAlex: W2007305673
Cited by: 603
References: 185
Citations by year: 2026: 10 · 2025: 16 · 2024: 22 · 2023: 24 · 2022: 43 · 2021: 33 · 2020: 38 · 2019: 34 · 2018: 48 · 2017: 30 · 2016: 49 · 2015: 48 · 2014: 49 · 2013: 52 · 2012: 48
FWCI: 3.52
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Behavior and Immunity (publishedVersion)
PubMed (publishedVersion)
Funders: Canadian Institutes of Health Research
Topics: Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: prenatal infection, prenatal immune activation, maternal infection, rodent models, brain development, offspring behavior, schizophrenia, autism spectrum disorder, cerebral palsy, interleukin-6, placental cytokines, oxidative stress, fetal brain, central nervous system disorders
MeSH terms: Animals, Behavior, Animal, Brain, Brain Chemistry, Disease Models, Animal, Female, Fetus, Infections, Pregnancy, Prenatal Exposure Delayed Effects, Mice, Rats

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Effects of prenatal infection on brain development and behavior: A review of findings from animal models

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