Oligodendrocyte-derived IL-33 functions as a microglial survival factor during neuroinvasive flavivirus infection.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
Nov 2023
Historique:
received: 10 04 2023
accepted: 05 11 2023
revised: 04 12 2023
medline: 6 12 2023
pubmed: 20 11 2023
entrez: 20 11 2023
Statut: epublish

Résumé

In order to recover from infection, organisms must balance robust immune responses to pathogens with the tolerance of immune-mediated pathology. This balance is particularly critical within the central nervous system, whose complex architecture, essential function, and limited capacity for self-renewal render it susceptible to both pathogen- and immune-mediated pathology. Here, we identify the alarmin IL-33 and its receptor ST2 as critical for host survival to neuroinvasive flavivirus infection. We identify oligodendrocytes as the critical source of IL-33, and microglia as the key cellular responders. Notably, we find that the IL-33/ST2 axis does not impact viral control or adaptive immune responses; rather, it is required to promote the activation and survival of microglia. In the absence of intact IL-33/ST2 signaling in the brain, neuroinvasive flavivirus infection triggered aberrant recruitment of monocyte-derived peripheral immune cells, increased neuronal stress, and neuronal cell death, effects that compromised organismal survival. These findings identify IL-33 as a critical mediator of CNS tolerance to pathogen-initiated immunity and inflammation.

Identifiants

pubmed: 37983247
doi: 10.1371/journal.ppat.1011350
pii: PPATHOGENS-D-23-00620
pmc: PMC10695366
doi:

Substances chimiques

Interleukin-33 0
Interleukin-1 Receptor-Like 1 Protein 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1011350

Subventions

Organisme : NIAID NIH HHS
ID : R01 AI132595
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI178512
Pays : United States

Commentaires et corrections

Type : UpdateOf

Informations de copyright

Copyright: © 2023 Norris et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Immunity. 2015 Mar 17;42(3):566-79
pubmed: 25786179
Proc Natl Acad Sci U S A. 2015 Mar 31;112(13):4056-61
pubmed: 25829541
PLoS Pathog. 2017 Apr 27;13(4):e1006345
pubmed: 28448566
Neuron. 2017 Dec 20;96(6):1342-1357.e5
pubmed: 29198757
Annu Rev Immunol. 2019 Apr 26;37:73-95
pubmed: 31026414
Immunity. 2022 Jan 11;55(1):159-173.e9
pubmed: 34982959
Nat Neurosci. 2019 Aug;22(8):1276-1288
pubmed: 31235930
J Exp Med. 2017 Feb;214(2):285-296
pubmed: 27994070
Nature. 2016 Jun 22;534(7608):538-43
pubmed: 27337340
Cell. 2020 Jul 23;182(2):388-403.e15
pubmed: 32615087
Nat Immunol. 2018 Feb;19(2):151-161
pubmed: 29292385
J Neurosci. 2014 Sep 3;34(36):11929-47
pubmed: 25186741
Proc Natl Acad Sci U S A. 2016 Nov 22;113(47):E7572-E7579
pubmed: 27821781
PLoS Pathog. 2017 Apr 27;13(4):e1006322
pubmed: 28448579
Immunity. 2009 Jul 17;31(1):84-98
pubmed: 19559631
Front Pharmacol. 2016 Jan 12;6:321
pubmed: 26793112
Nat Immunol. 2017 Feb;18(2):132-141
pubmed: 28092376
Cell Tissue Res. 2007 Nov;330(2):291-302
pubmed: 17874251
Elife. 2022 Dec 21;11:
pubmed: 36541708
Eur J Immunol. 2015 May;45(5):1354-65
pubmed: 25682948
Viruses. 2021 Jan 11;13(1):
pubmed: 33440758
Annu Rev Physiol. 2017 Feb 10;79:619-643
pubmed: 27959620
J Neuroinflammation. 2019 Jan 31;16(1):22
pubmed: 30704498
Immunity. 2020 Jun 16;52(6):957-970
pubmed: 32553181
J Virol. 2004 Aug;78(15):8312-21
pubmed: 15254203
JAMA. 2013 Jul 17;310(3):308-15
pubmed: 23860989
Cell. 2020 Apr 16;181(2):250-269
pubmed: 32302569
J Neurosci. 2004 Sep 29;24(39):8470-9
pubmed: 15456820
J Exp Med. 2018 Jul 2;215(7):1789-1801
pubmed: 29941548
J Infect Dis. 2000 Oct;182(4):1214-7
pubmed: 10979920
Glia. 2006 Apr 15;53(6):583-92
pubmed: 16419089
Nat Immunol. 2018 Nov;19(11):1189-1198
pubmed: 30333606
Neuron. 2015 Feb 18;85(4):703-9
pubmed: 25661185
Immunity. 2020 May 19;52(5):782-793.e5
pubmed: 32272082
Annu Rev Neurosci. 2012;35:369-89
pubmed: 22715882
Immunity. 2015 Feb 17;42(2):294-308
pubmed: 25692703
Annu Rev Immunol. 2021 Apr 26;39:251-277
pubmed: 33556248
J Neuroinflammation. 2012 Oct 30;9:246
pubmed: 23111065
J Clin Invest. 2009 Nov;119(11):3266-77
pubmed: 19855131
Nat Neurosci. 2022 May;25(5):577-587
pubmed: 35524140
Science. 2018 Mar 16;359(6381):1269-1273
pubmed: 29420261
Clin Ther. 2017 Aug;39(8):1519-1536
pubmed: 28754189
J Exp Med. 2009 Apr 13;206(4):751-60
pubmed: 19332874
Science. 2012 Feb 24;335(6071):984-9
pubmed: 22323740
Lancet. 2008 Feb 9;371(9611):500-9
pubmed: 18262042
Nat Immunol. 2012 Jun 24;13(8):753-60
pubmed: 22729249
PLoS Pathog. 2020 Oct 27;16(10):e1009027
pubmed: 33108405
Glia. 2021 Aug;69(8):2023-2036
pubmed: 33942402
Cell Rep. 2015 Mar 24;10(11):1836-49
pubmed: 25801023
Nat Rev Drug Discov. 2003 Jul;2(7):554-65
pubmed: 12815381
J Neuroinflammation. 2016 Jun 22;13(1):159
pubmed: 27334012
J Exp Med. 2008 Sep 29;205(10):2319-37
pubmed: 18779347
Proc Natl Acad Sci U S A. 2016 Mar 22;113(12):E1738-46
pubmed: 26884166
Nat Neurosci. 2013 Nov;16(11):1618-26
pubmed: 24077561
Immunology. 2018 Dec;155(4):477-490
pubmed: 30098206
Science. 2012 Feb 24;335(6071):936-41
pubmed: 22363001
Nat Commun. 2019 Jan 31;10(1):518
pubmed: 30705270
Neuron Glia Biol. 2011 Feb;7(1):99-108
pubmed: 22613083
J Neuroinflammation. 2012 Dec 17;9:270
pubmed: 23244217

Auteurs

Geoffrey T Norris (GT)

Department of Immunology, University of Washington, Seattle Washington, United States of America.

Joshua M Ames (JM)

Department of Immunology, University of Washington, Seattle Washington, United States of America.

Steven F Ziegler (SF)

Department of Immunology, University of Washington, Seattle Washington, United States of America.
Center for Fundamental Immunology, Benaroya Research Institute, Seattle Washington, United States of America.

Andrew Oberst (A)

Department of Immunology, University of Washington, Seattle Washington, United States of America.

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