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Prenatal exposure to interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABA(A) dysregulation and impaired spatial learning

Journal article
Authors Anne-Maj Samuelsson
Eva Jennische
Hans-Arne Hansson
Agneta Holmäng
Published in Am J Physiol Regul Integr Comp Physiol
Volume 290
Issue 5
Pages R1345-56
Publication year 2006
Published at Wallenberg Laboratory
Institute of Neuroscience and Physiology, Department of Physiology
Institute of Biomedicine, Department of Medical Biochemistry and Cell Biology
Pages R1345-56
Language en
Links www.ncbi.nlm.nih.gov/entrez/query.f...
Keywords Adrenocorticotropic Hormone/blood, Aging/metabolism/psychology, Animals, Apoptosis/drug effects, Astrocytes/pathology, Blotting, Western, Body Weight/physiology, Caspase 3, Caspases/metabolism, DNA, Complementary/biosynthesis/genetics, Female, Glial Fibrillary Acidic Protein/metabolism, Gliosis/chemically induced/pathology, Hippocampus/*pathology, Hydrocortisone/blood, Immunohistochemistry, Inflammation/*pathology, Interleukin-6/*pharmacology, Maze Learning/*physiology, Nerve Degeneration/*pathology, Pregnancy, Prenatal Exposure Delayed Effects, Rats, Rats, Wistar, Receptors, GABA-A/*physiology, Receptors, N-Methyl-D-Aspartate/drug effects/*physiology, Reverse Transcriptase Polymerase Chain Reaction
Subject categories Medical and Health Sciences

Abstract

During pregnancy, infection or immune responses induce cytokine release, which might influence fetal neurodevelopment, leading to neurodegenerative disease in adulthood. Because the hippocampus is a key area for learning and memory, we evaluated 4- and 24-wk-old rats for the effects of early and late prenatal exposure to interleukin-6 (IL-6) on hippocampal morphology, expression of mRNA for IL-6, the gamma-aminobutyric acid receptor (GABA(Aalpha5)), the NR1 subunit of the N-methyl-D-aspartate receptor, and glial fibrillary acidic protein (GFAP), caspase-3 protein and mRNA levels, and learning abilities. Late exposure increased serum IL-6 and hippocampal expression of IL-6 mRNA at 4 and 24 wk. All adult rats showed neuronal loss in the hilus and astrogliosis; males had losses mainly in the CA2 and CA3 regions, and females in CA1. Expression of GABA(Aalpha5), NR1, and GFAP mRNA increased in late-exposed males and females at 4 and 24 wk. mRNA and protein levels of the apoptosis marker caspase-3 were increased in all late-exposed rats except males at 4 wk. Evaluation of hippocampus-dependent working memory in the Morris water maze at 20 wk of age showed increases in escape latency and time spent near the pool wall in all IL-6 adult rats, especially females. These findings suggest that fetal IL-6 exposure, especially in late pregnancy, leads to increased IL-6 levels in the circulation and hippocampus, abnormalities of hippocampal structural and morphology, and decreased learning during adulthood.

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