Type I Interferon Receptor Signaling of Neurons and Astrocytes Regulates Microglia Activation during Viral Encephalitis

In sterile neuroinflammation, a pathological role is proposed for microglia, whereas in viral encephalitis, their function is not entirely clear. Many viruses exploit the odorant system and enter the CNS via the olfactory bulb (OB). Upon intranasal vesicular stomatitis virus instillation, we show an...

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Published in	Cell reports (Cambridge) Vol. 25; no. 1; pp. 118 - 129.e4
Main Authors	Chhatbar, Chintan, Detje, Claudia N., Grabski, Elena, Borst, Katharina, Spanier, Julia, Ghita, Luca, Elliott, David A., Jordão, Marta Joana Costa, Mueller, Nora, Sutton, James, Prajeeth, Chittappen K., Gudi, Viktoria, Klein, Michael A., Prinz, Marco, Bradke, Frank, Stangel, Martin, Kalinke, Ulrich
Format	Journal Article
Language	English
Published	United States Elsevier Inc 02.10.2018 The Authors Elsevier
Subjects	Animals astrocytes Astrocytes - immunology Astrocytes - pathology Cell Communication - immunology encephalitis Encephalitis, Viral - genetics Encephalitis, Viral - immunology Encephalitis, Viral - pathology Female Humans Male Mice Mice, Inbred C57BL Microglia - immunology Microglia - pathology neurons Neurons - immunology Neurons - pathology Receptor, Interferon alpha-beta - immunology regulation of microglia activation Signal Transduction type I IFN receptor signaling regulation of microglia activation astrocytes type I IFN receptor signaling encephalitis neurons
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Abstract	In sterile neuroinflammation, a pathological role is proposed for microglia, whereas in viral encephalitis, their function is not entirely clear. Many viruses exploit the odorant system and enter the CNS via the olfactory bulb (OB). Upon intranasal vesicular stomatitis virus instillation, we show an accumulation of activated microglia and monocytes in the OB. Depletion of microglia during encephalitis results in enhanced virus spread and increased lethality. Activation, proliferation, and accumulation of microglia are regulated by type I IFN receptor signaling of neurons and astrocytes, but not of microglia. Morphological analysis of myeloid cells shows that type I IFN receptor signaling of neurons has a stronger impact on the activation of myeloid cells than of astrocytes. Thus, in the infected CNS, the cross talk among neurons, astrocytes, and microglia is critical for full microglia activation and protection from lethal encephalitis. [Display omitted] •VSV infection via the olfactory route leads to accumulation of microglia in the OB•Following infection, microglia form an innate immune barrier in the OB•The microglia barrier prevents viral CNS penetration via the olfactory route•IFNAR signaling of neurons and astrocytes regulates microglia barrier formation The mechanisms restricting viral entry into the CNS via the olfactory route were unclear. Chhatbar et al. show that intercellular communication within the olfactory bulb (OB) among neurons, astrocytes, and microglia orchestrates formation of a microglial barrier that restricts the spread of the virus into the CNS.
AbstractList	In sterile neuroinflammation, a pathological role is proposed for microglia, whereas in viral encephalitis, their function is not entirely clear. Many viruses exploit the odorant system and enter the CNS via the olfactory bulb (OB). Upon intranasal vesicular stomatitis virus instillation, we show an accumulation of activated microglia and monocytes in the OB. Depletion of microglia during encephalitis results in enhanced virus spread and increased lethality. Activation, proliferation, and accumulation of microglia are regulated by type I IFN receptor signaling of neurons and astrocytes, but not of microglia. Morphological analysis of myeloid cells shows that type I IFN receptor signaling of neurons has a stronger impact on the activation of myeloid cells than of astrocytes. Thus, in the infected CNS, the cross talk among neurons, astrocytes, and microglia is critical for full microglia activation and protection from lethal encephalitis. In sterile neuroinflammation, a pathological role is proposed for microglia, whereas in viral encephalitis, their function is not entirely clear. Many viruses exploit the odorant system and enter the CNS via the olfactory bulb (OB). Upon intranasal vesicular stomatitis virus instillation, we show an accumulation of activated microglia and monocytes in the OB. Depletion of microglia during encephalitis results in enhanced virus spread and increased lethality. Activation, proliferation, and accumulation of microglia are regulated by type I IFN receptor signaling of neurons and astrocytes, but not of microglia. Morphological analysis of myeloid cells shows that type I IFN receptor signaling of neurons has a stronger impact on the activation of myeloid cells than of astrocytes. Thus, in the infected CNS, the cross talk among neurons, astrocytes, and microglia is critical for full microglia activation and protection from lethal encephalitis. [Display omitted] •VSV infection via the olfactory route leads to accumulation of microglia in the OB•Following infection, microglia form an innate immune barrier in the OB•The microglia barrier prevents viral CNS penetration via the olfactory route•IFNAR signaling of neurons and astrocytes regulates microglia barrier formation The mechanisms restricting viral entry into the CNS via the olfactory route were unclear. Chhatbar et al. show that intercellular communication within the olfactory bulb (OB) among neurons, astrocytes, and microglia orchestrates formation of a microglial barrier that restricts the spread of the virus into the CNS. In sterile neuroinflammation, a pathological role is proposed for microglia, whereas in viral encephalitis, their function is not entirely clear. Many viruses exploit the odorant system and enter the CNS via the olfactory bulb (OB). Upon intranasal vesicular stomatitis virus instillation, we show an accumulation of activated microglia and monocytes in the OB. Depletion of microglia during encephalitis results in enhanced virus spread and increased lethality. Activation, proliferation, and accumulation of microglia are regulated by type I IFN receptor signaling of neurons and astrocytes, but not of microglia. Morphological analysis of myeloid cells shows that type I IFN receptor signaling of neurons has a stronger impact on the activation of myeloid cells than of astrocytes. Thus, in the infected CNS, the cross talk among neurons, astrocytes, and microglia is critical for full microglia activation and protection from lethal encephalitis. : The mechanisms restricting viral entry into the CNS via the olfactory route were unclear. Chhatbar et al. show that intercellular communication within the olfactory bulb (OB) among neurons, astrocytes, and microglia orchestrates formation of a microglial barrier that restricts the spread of the virus into the CNS. Keywords: encephalitis, regulation of microglia activation, neurons, astrocytes, type I IFN receptor signaling In sterile neuroinflammation, a pathological role is proposed for microglia, whereas in viral encephalitis, their function is not entirely clear. Many viruses exploit the odorant system and enter the CNS via the olfactory bulb (OB). Upon intranasal vesicular stomatitis virus instillation, we show an accumulation of activated microglia and monocytes in the OB. Depletion of microglia during encephalitis results in enhanced virus spread and increased lethality. Activation, proliferation, and accumulation of microglia are regulated by type I IFN receptor signaling of neurons and astrocytes, but not of microglia. Morphological analysis of myeloid cells shows that type I IFN receptor signaling of neurons has a stronger impact on the activation of myeloid cells than of astrocytes. Thus, in the infected CNS, the cross talk among neurons, astrocytes, and microglia is critical for full microglia activation and protection from lethal encephalitis. • VSV infection via the olfactory route leads to accumulation of microglia in the OB • Following infection, microglia form an innate immune barrier in the OB • The microglia barrier prevents viral CNS penetration via the olfactory route • IFNAR signaling of neurons and astrocytes regulates microglia barrier formation The mechanisms restricting viral entry into the CNS via the olfactory route were unclear. Chhatbar et al. show that intercellular communication within the olfactory bulb (OB) among neurons, astrocytes, and microglia orchestrates formation of a microglial barrier that restricts the spread of the virus into the CNS. In sterile neuroinflammation, a pathological role is proposed for microglia, whereas in viral encephalitis, their function is not entirely clear. Many viruses exploit the odorant system and enter the CNS via the olfactory bulb (OB). Upon intranasal vesicular stomatitis virus instillation, we show an accumulation of activated microglia and monocytes in the OB. Depletion of microglia during encephalitis results in enhanced virus spread and increased lethality. Activation, proliferation, and accumulation of microglia are regulated by type I IFN receptor signaling of neurons and astrocytes, but not of microglia. Morphological analysis of myeloid cells shows that type I IFN receptor signaling of neurons has a stronger impact on the activation of myeloid cells than of astrocytes. Thus, in the infected CNS, the cross talk among neurons, astrocytes, and microglia is critical for full microglia activation and protection from lethal encephalitis.In sterile neuroinflammation, a pathological role is proposed for microglia, whereas in viral encephalitis, their function is not entirely clear. Many viruses exploit the odorant system and enter the CNS via the olfactory bulb (OB). Upon intranasal vesicular stomatitis virus instillation, we show an accumulation of activated microglia and monocytes in the OB. Depletion of microglia during encephalitis results in enhanced virus spread and increased lethality. Activation, proliferation, and accumulation of microglia are regulated by type I IFN receptor signaling of neurons and astrocytes, but not of microglia. Morphological analysis of myeloid cells shows that type I IFN receptor signaling of neurons has a stronger impact on the activation of myeloid cells than of astrocytes. Thus, in the infected CNS, the cross talk among neurons, astrocytes, and microglia is critical for full microglia activation and protection from lethal encephalitis.
Author	Sutton, James Jordão, Marta Joana Costa Prajeeth, Chittappen K. Ghita, Luca Kalinke, Ulrich Mueller, Nora Borst, Katharina Stangel, Martin Prinz, Marco Elliott, David A. Klein, Michael A. Grabski, Elena Spanier, Julia Bradke, Frank Gudi, Viktoria Chhatbar, Chintan Detje, Claudia N.
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SubjectTerms	Animals astrocytes Astrocytes - immunology Astrocytes - pathology Cell Communication - immunology encephalitis Encephalitis, Viral - genetics Encephalitis, Viral - immunology Encephalitis, Viral - pathology Female Humans Male Mice Mice, Inbred C57BL Microglia - immunology Microglia - pathology neurons Neurons - immunology Neurons - pathology Receptor, Interferon alpha-beta - immunology regulation of microglia activation Signal Transduction type I IFN receptor signaling
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Title	Type I Interferon Receptor Signaling of Neurons and Astrocytes Regulates Microglia Activation during Viral Encephalitis
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