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Natural killer cells and innate lymphoid cells 1 tune anxiety-like behavior and memory in mice via interferon-γ and acetylcholine

Author

Listed:
  • Stefano Garofalo

    (Sapienza University of Rome)

  • Germana Cocozza

    (Sapienza University of Rome
    IRCCS Neuromed)

  • Alessandro Mormino

    (Sapienza University of Rome)

  • Giovanni Bernardini

    (Sapienza University of Rome)

  • Eleonora Russo

    (Sapienza University of Rome)

  • Donald Ielpo

    (Sapienza University of Rome)

  • Diego Andolina

    (Sapienza University of Rome)

  • Rossella Ventura

    (Sapienza University of Rome)

  • Katiuscia Martinello

    (IRCCS Neuromed)

  • Massimiliano Renzi

    (Sapienza University of Rome)

  • Sergio Fucile

    (Sapienza University of Rome
    IRCCS Neuromed)

  • Mattia Laffranchi

    (Sapienza University of Rome)

  • Eva Piano Mortari

    (Bambino Gesù Children’s Hospital, IRCCS)

  • Rita Carsetti

    (Bambino Gesù Children’s Hospital, IRCCS)

  • Giuseppe Sciumè

    (Sapienza University of Rome)

  • Silvano Sozzani

    (IRCCS Neuromed
    Sapienza University of Rome)

  • Angela Santoni

    (IRCCS Neuromed
    Sapienza University of Rome)

  • Marie-Eve Tremblay

    (Centre de Recherche CHU de Quebec-Université Laval)

  • Richard M. Ransohoff

    (Third Rock Ventures)

  • Cristina Limatola

    (IRCCS Neuromed
    Sapienza University, Laboratory affiliated to Istituto Pasteur)

Abstract

The mechanisms of communication between the brain and the immune cells are still largely unclear. Here, we characterize the populations of resident natural killer (NK) cells and innate lymphoid cells (ILC) 1 in the meningeal dura layer of adult mice. We describe that ILC1/NK cell-derived interferon-γ and acetylcholine can contribute to the modulation of brain homeostatic functions, shaping synaptic neuronal transmission and neurotransmitter levels with effects on mice behavior. In detail, the interferon-γ plays a role in the formation of non-spatial memory, tuning the frequency of GABAergic neurotransmission on cortical pyramidal neurons, while the acetylcholine is a mediator involved in the modulation of brain circuitries that regulate anxiety-like behavior. These findings disclose mechanisms of immune-to-brain communication that modulate brain functions under physiological conditions.

Suggested Citation

  • Stefano Garofalo & Germana Cocozza & Alessandro Mormino & Giovanni Bernardini & Eleonora Russo & Donald Ielpo & Diego Andolina & Rossella Ventura & Katiuscia Martinello & Massimiliano Renzi & Sergio F, 2023. "Natural killer cells and innate lymphoid cells 1 tune anxiety-like behavior and memory in mice via interferon-γ and acetylcholine," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38899-3
    DOI: 10.1038/s41467-023-38899-3
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    References listed on IDEAS

    as
    1. Stefano Garofalo & Germana Cocozza & Alessandra Porzia & Maurizio Inghilleri & Marcello Raspa & Ferdinando Scavizzi & Eleonora Aronica & Giovanni Bernardini & Ling Peng & Richard M. Ransohoff & Angela, 2020. "Natural killer cells modulate motor neuron-immune cell cross talk in models of Amyotrophic Lateral Sclerosis," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    2. Shuo Chen & Linmeng He & Arthur J. Y. Huang & Roman Boehringer & Vincent Robert & Marie E. Wintzer & Denis Polygalov & Adam Z. Weitemier & Yanqiu Tao & Mingxiao Gu & Steven J. Middleton & Kana Namiki , 2020. "A hypothalamic novelty signal modulates hippocampal memory," Nature, Nature, vol. 586(7828), pages 270-274, October.
    3. Anthony J. Filiano & Yang Xu & Nicholas J. Tustison & Rachel L. Marsh & Wendy Baker & Igor Smirnov & Christopher C. Overall & Sachin P. Gadani & Stephen D. Turner & Zhiping Weng & Sayeda Najamussahar , 2016. "Unexpected role of interferon-γ in regulating neuronal connectivity and social behaviour," Nature, Nature, vol. 535(7612), pages 425-429, July.
    4. Eoin F. McKinney & Iona Cuthbertson & Kristina M. Harris & Dawn E. Smilek & Christopher Connor & Giulia Manferrari & Edward J. Carr & Scott S. Zamvil & Kenneth G. C. Smith, 2021. "A CD8+ NK cell transcriptomic signature associated with clinical outcome in relapsing remitting multiple sclerosis," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    5. Stefano Garofalo & Giuseppina D’Alessandro & Giuseppina Chece & Frederic Brau & Laura Maggi & Alessandro Rosa & Alessandra Porzia & Fabrizio Mainiero & Vincenzo Esposito & Clotilde Lauro & Giorgia Ben, 2015. "Enriched environment reduces glioma growth through immune and non-immune mechanisms in mice," Nature Communications, Nature, vol. 6(1), pages 1-13, May.
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