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    Unexpected role of interferon-gamma in regulating neuronal connectivity and social behaviour

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    Authors
    Filiano, Anthony J.
    Xu, Yang
    Tustison, Nicholas J.
    Marsh, Rachel L.
    Baker, Wendy
    Smirnov, Igor
    Overall, Christopher C.
    Gadani, Sachin P.
    Turner, Stephen D.
    Weng, Zhiping
    Peerzade, Sayeda Najamussaha
    Chen, Hao
    Lee, Kevin S.
    Scott, Michael M.
    Beenhakker, Mark P.
    Litvak, Vladimir
    Kipnis, Jonathan
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    UMass Chan Affiliations
    Program in Bioinformatics and Integrative Biology
    Department of Microbiology and Physiological Systems
    Department of Biochemistry and Molecular Pharmacology
    Document Type
    Journal Article
    Publication Date
    2016-07-01
    Keywords
    Bioinformatics
    Computational Biology
    Immunology and Infectious Disease
    Integrative Biology
    Neuroscience and Neurobiology
    
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    Link to Full Text
    https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4961620/
    Abstract
    Immune dysfunction is commonly associated with several neurological and mental disorders. Although the mechanisms by which peripheral immunity may influence neuronal function are largely unknown, recent findings implicate meningeal immunity influencing behaviour, such as spatial learning and memory. Here we show that meningeal immunity is also critical for social behaviour; mice deficient in adaptive immunity exhibit social deficits and hyper-connectivity of fronto-cortical brain regions. Associations between rodent transcriptomes from brain and cellular transcriptomes in response to T-cell-derived cytokines suggest a strong interaction between social behaviour and interferon-gamma (IFN-gamma)-driven responses. Concordantly, we demonstrate that inhibitory neurons respond to IFN-gamma and increase GABAergic (gamma-aminobutyric-acid) currents in projection neurons, suggesting that IFN-gamma is a molecular link between meningeal immunity and neural circuits recruited for social behaviour. Meta-analysis of the transcriptomes of a range of organisms reveals that rodents, fish, and flies elevate IFN-gamma/JAK-STAT-dependent gene signatures in a social context, suggesting that the IFN-gamma signalling pathway could mediate a co-evolutionary link between social/aggregation behaviour and an efficient anti-pathogen response. This study implicates adaptive immune dysfunction, in particular IFN-gamma, in disorders characterized by social dysfunction and suggests a co-evolutionary link between social behaviour and an anti-pathogen immune response driven by IFN-gamma signalling.
    Source
    Nature. 2016 Jul 21;535(7612):425-9. Link to article on publisher's site
    DOI
    10.1038/nature18626
    Permanent Link to this Item
    http://hdl.handle.net/20.500.14038/25816
    PubMed ID
    27409813
    Related Resources
    Link to Article in PubMed
    ae974a485f413a2113503eed53cd6c53
    10.1038/nature18626
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