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

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 in...

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Main Authors: Stefano Garofalo, Germana Cocozza, Alessandro Mormino, Giovanni Bernardini, Eleonora Russo, Donald Ielpo, Diego Andolina, Rossella Ventura, Katiuscia Martinello, Massimiliano Renzi, Sergio Fucile, Mattia Laffranchi, Eva Piano Mortari, Rita Carsetti, Giuseppe Sciumè, Silvano Sozzani, Angela Santoni, Marie-Eve Tremblay, Richard M. Ransohoff, Cristina Limatola
Format: Article
Language:English
Published: Nature Portfolio 2023-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-38899-3
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author Stefano Garofalo
Germana Cocozza
Alessandro Mormino
Giovanni Bernardini
Eleonora Russo
Donald Ielpo
Diego Andolina
Rossella Ventura
Katiuscia Martinello
Massimiliano Renzi
Sergio Fucile
Mattia Laffranchi
Eva Piano Mortari
Rita Carsetti
Giuseppe Sciumè
Silvano Sozzani
Angela Santoni
Marie-Eve Tremblay
Richard M. Ransohoff
Cristina Limatola
author_facet Stefano Garofalo
Germana Cocozza
Alessandro Mormino
Giovanni Bernardini
Eleonora Russo
Donald Ielpo
Diego Andolina
Rossella Ventura
Katiuscia Martinello
Massimiliano Renzi
Sergio Fucile
Mattia Laffranchi
Eva Piano Mortari
Rita Carsetti
Giuseppe Sciumè
Silvano Sozzani
Angela Santoni
Marie-Eve Tremblay
Richard M. Ransohoff
Cristina Limatola
author_sort Stefano Garofalo
collection DOAJ
description 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.
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spelling doaj.art-0211a315673a47ed8fe4e14ffd46fcd72023-06-04T11:32:53ZengNature PortfolioNature Communications2041-17232023-05-0114111510.1038/s41467-023-38899-3Natural killer cells and innate lymphoid cells 1 tune anxiety-like behavior and memory in mice via interferon-γ and acetylcholineStefano Garofalo0Germana Cocozza1Alessandro Mormino2Giovanni Bernardini3Eleonora Russo4Donald Ielpo5Diego Andolina6Rossella Ventura7Katiuscia Martinello8Massimiliano Renzi9Sergio Fucile10Mattia Laffranchi11Eva Piano Mortari12Rita Carsetti13Giuseppe Sciumè14Silvano Sozzani15Angela Santoni16Marie-Eve Tremblay17Richard M. Ransohoff18Cristina Limatola19Department of Physiology and Pharmacology, Sapienza University of RomeDepartment of Physiology and Pharmacology, Sapienza University of RomeDepartment of Physiology and Pharmacology, Sapienza University of RomeDepartment of Molecular Medicine, Sapienza University of RomeDepartment of Molecular Medicine, Sapienza University of RomeDepartment of Psychology and Centre for Research in Neurobiology D. Bovet, Sapienza University of RomeDepartment of Psychology and Centre for Research in Neurobiology D. Bovet, Sapienza University of RomeDepartment of Psychology and Centre for Research in Neurobiology D. Bovet, Sapienza University of RomeIRCCS NeuromedDepartment of Physiology and Pharmacology, Sapienza University of RomeDepartment of Physiology and Pharmacology, Sapienza University of RomeDepartment of Molecular Medicine, Sapienza University of RomeB Cell Unit, Immunology Research Area, Bambino Gesù Children’s Hospital, IRCCSB Cell Unit, Immunology Research Area, Bambino Gesù Children’s Hospital, IRCCSDepartment of Molecular Medicine, Sapienza University of RomeIRCCS NeuromedIRCCS NeuromedCentre de Recherche CHU de Quebec-Université LavalThird Rock VenturesIRCCS NeuromedAbstract 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.https://doi.org/10.1038/s41467-023-38899-3
spellingShingle Stefano Garofalo
Germana Cocozza
Alessandro Mormino
Giovanni Bernardini
Eleonora Russo
Donald Ielpo
Diego Andolina
Rossella Ventura
Katiuscia Martinello
Massimiliano Renzi
Sergio Fucile
Mattia Laffranchi
Eva Piano Mortari
Rita Carsetti
Giuseppe Sciumè
Silvano Sozzani
Angela Santoni
Marie-Eve Tremblay
Richard M. Ransohoff
Cristina Limatola
Natural killer cells and innate lymphoid cells 1 tune anxiety-like behavior and memory in mice via interferon-γ and acetylcholine
Nature Communications
title Natural killer cells and innate lymphoid cells 1 tune anxiety-like behavior and memory in mice via interferon-γ and acetylcholine
title_full Natural killer cells and innate lymphoid cells 1 tune anxiety-like behavior and memory in mice via interferon-γ and acetylcholine
title_fullStr Natural killer cells and innate lymphoid cells 1 tune anxiety-like behavior and memory in mice via interferon-γ and acetylcholine
title_full_unstemmed Natural killer cells and innate lymphoid cells 1 tune anxiety-like behavior and memory in mice via interferon-γ and acetylcholine
title_short Natural killer cells and innate lymphoid cells 1 tune anxiety-like behavior and memory in mice via interferon-γ and acetylcholine
title_sort natural killer cells and innate lymphoid cells 1 tune anxiety like behavior and memory in mice via interferon γ and acetylcholine
url https://doi.org/10.1038/s41467-023-38899-3
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