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

机译：干扰素-γ在调节神经元连接性和社交行为中的意外作用

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摘要

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(1). 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.
机译：免疫功能障碍通常与几种神经系统和精神疾病有关。尽管外围免疫可能影响神经元功能的机制尚不清楚，但最近的发现暗示脑膜免疫影响行为，例如空间学习和记忆（1）。在这里，我们证明脑膜免疫力对于社交行为也至关重要。缺乏适应性免疫的小鼠表现出社交缺陷和额皮质大脑区域的超连通性。来自大脑的啮齿动物转录组与响应T细胞的细胞因子的细胞转录组之间的关联表明，社交行为与干扰素-γ（IFN-γ）驱动的反应之间存在强烈的相互作用。一致地，我们证明抑制性神经元对IFN-γ作出反应并增加投射神经元中的GABA能（γ-氨基丁酸）电流，这表明IFN-γ是脑膜免疫力与为社会行为募集的神经回路之间的分子联系。对一系列生物的转录组进行的荟萃分析显示，啮齿动物，鱼类和苍蝇在社交环境中会升高IFN-γ/ JAK-STAT依赖性基因的特征，这表明IFN-γ信号通路可以介导共同进化。社会/聚集行为与有效的抗病原体反应之间的联系。这项研究牵涉到以社会功能障碍为特征的疾病中的适应性免疫功能障碍，尤其是IFN-γ，并提出了社交行为与IFN-γ信号驱动的抗病原体免疫反应之间的共同进化联系。

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  • 来源
    《Nature》 |2016年第7612期|425-429|共5页
  • 作者

    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 Najamussahar; Chen Hao; Lee Kevin S.; Scott Michael M.; Beenhakker Mark P.; Litvak Vladimir; Kipnis Jonathan;

  • 作者单位

    Univ Virginia, Sch Med, Ctr Brain Immunol & Glia, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Dept Neurosci, Charlottesville, VA 22908 USA;

    Univ Massachusetts, Sch Med, Dept Microbiol & Physiol Syst, Worcester, MA 01655 USA;

    Univ Virginia, Sch Med, Dept Radiol & Med Imaging, Charlottesville, VA 22908 USA;

    Univ Virginia, Sch Med, Ctr Brain Immunol & Glia, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Dept Neurosci, Charlottesville, VA 22908 USA;

    Univ Virginia, Sch Med, Ctr Brain Immunol & Glia, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Dept Neurosci, Charlottesville, VA 22908 USA;

    Univ Virginia, Sch Med, Ctr Brain Immunol & Glia, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Dept Neurosci, Charlottesville, VA 22908 USA;

    Univ Virginia, Sch Med, Ctr Brain Immunol & Glia, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Dept Neurosci, Charlottesville, VA 22908 USA;

    Univ Virginia, Sch Med, Ctr Brain Immunol & Glia, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Dept Neurosci, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Neurosci Grad Program, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Med Scientist Training Program, Charlottesville, VA 22908 USA;

    Univ Virginia, Sch Med, Dept Publ Hlth Sci, Charlottesville, VA 22908 USA;

    Univ Massachusetts, Sch Med, Dept Biochem & Mol Pharmacol, Worcester, MA 01655 USA;

    Univ Massachusetts, Sch Med, Dept Microbiol & Physiol Syst, Worcester, MA 01655 USA;

    Univ Massachusetts, Sch Med, Dept Biochem & Mol Pharmacol, Worcester, MA 01655 USA;

    Univ Virginia, Sch Med, Ctr Brain Immunol & Glia, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Dept Neurosci, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Neurosci Grad Program, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Dept Neurosurg, Charlottesville, VA 22908 USA;

    Univ Virginia, Sch Med, Neurosci Grad Program, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Dept Pharmacol, Charlottesville, VA 22908 USA;

    Univ Virginia, Sch Med, Neurosci Grad Program, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Dept Pharmacol, Charlottesville, VA 22908 USA;

    Univ Massachusetts, Sch Med, Dept Microbiol & Physiol Syst, Worcester, MA 01655 USA;

    Univ Virginia, Sch Med, Ctr Brain Immunol & Glia, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Dept Neurosci, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Neurosci Grad Program, Charlottesville, VA 22908 USA|Univ Virginia, Sch Med, Med Scientist Training Program, Charlottesville, VA 22908 USA;

  • 收录信息 美国《科学引文索引》(SCI);美国《工程索引》(EI);美国《生物学医学文摘》(MEDLINE);美国《化学文摘》(CA);
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