The virus-induced cyclic dinucleotide 2'3'-c-di-GMP mediates STING-dependent antiviral immunity in Drosophila.

Animals Antiviral Agents Drosophila Drosophila melanogaster Cyclic GMP Mammals
Drosophila STING c-di-GMP cGAMP cGAS cGLR cyclic dinucleotide evolution pattern recognition receptor virus

Journal

Immunity
ISSN: 1097-4180
Titre abrégé: Immunity
Pays: United States
ID NLM: 9432918

Informations de publication

Date de publication:
12 09 2023
Historique:
received: 26 04 2023
revised: 14 06 2023
accepted: 08 08 2023
medline: 15 9 2023
pubmed: 3 9 2023
entrez: 2 9 2023
Statut: ppublish

Résumé

In mammals, the enzyme cGAS senses the presence of cytosolic DNA and synthesizes the cyclic dinucleotide (CDN) 2'3'-cGAMP, which triggers STING-dependent immunity. In Drosophila melanogaster, two cGAS-like receptors (cGLRs) produce 3'2'-cGAMP and 2'3'-cGAMP to activate STING. We explored CDN-mediated immunity in 14 Drosophila species covering 50 million years of evolution and found that 2'3'-cGAMP and 3'2'-cGAMP failed to control infection by Drosophila C virus in D. serrata and two other species. We discovered diverse CDNs produced in a cGLR-dependent manner in response to viral infection in D. melanogaster, including 2'3'-c-di-GMP. This CDN was a more potent STING agonist than cGAMP in D. melanogaster and it also activated a strong antiviral transcriptional response in D. serrata. Our results shed light on the evolution of cGLRs in flies and provide a basis for understanding the function and regulation of this emerging family of pattern recognition receptors in animal innate immunity.

Identifiants

DOI: 10.1016/j.immuni.2023.08.006 PMID: 37659413
pubmed: 37659413
pii: S1074-7613(23)00362-X
doi: 10.1016/j.immuni.2023.08.006
pii:
doi:

Substances chimiques

Antiviral Agents 0
bis(3',5')-cyclic diguanylic acid 61093-23-0
Cyclic GMP H2D2X058MU

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1991-2005.e9

Subventions

Organisme : NIGMS NIH HHS
ID : DP2 GM146250
Pays : United States
Organisme : NCI NIH HHS
ID : F99 CA274660
Pays : United States

Commentaires et corrections

Type : UpdateOf
Type : CommentIn

Informations de copyright

Copyright © 2023 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Hua Cai (H)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China. Electronic address: chjorbe@hotmail.com.

Lihua Li (L)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China.

Kailey M Slavik (KM)

Department of Microbiology, Harvard Medical School, Boston, MA 02115, USA; Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Boston, MA 02115, USA.

Jingxian Huang (J)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China.

Ting Yin (T)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China.

Xianlong Ai (X)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China.

Léna Hédelin (L)

Université de Strasbourg, CNRS UPR9022, Institut de Biologie Moléculaire et Cellulaire, Strasbourg, France.

Gabrielle Haas (G)

Université de Strasbourg, CNRS UPR9022, Institut de Biologie Moléculaire et Cellulaire, Strasbourg, France.

Zhangmin Xiang (Z)

Guangdong Provincial Engineering Research Center for Ambient Mass Spectrometry, Guangdong Provincial Key Laboratory of Chemical Measurement and Emergency Test Technology, Institute of Analysis, Guangdong Academy of Sciences (China National Analytical Center Guangzhou), Guangzhou, China.

Yunyun Yang (Y)

Guangdong Provincial Engineering Research Center for Ambient Mass Spectrometry, Guangdong Provincial Key Laboratory of Chemical Measurement and Emergency Test Technology, Institute of Analysis, Guangdong Academy of Sciences (China National Analytical Center Guangzhou), Guangzhou, China.

Xiaoyan Li (X)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China.

Yuqiang Chen (Y)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China.

Ziming Wei (Z)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China.

Huimin Deng (H)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China.

Di Chen (D)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China.

Renjie Jiao (R)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China.

Nelson Martins (N)

Université de Strasbourg, CNRS UPR9022, Institut de Biologie Moléculaire et Cellulaire, Strasbourg, France.

Carine Meignin (C)

Université de Strasbourg, CNRS UPR9022, Institut de Biologie Moléculaire et Cellulaire, Strasbourg, France.

Philip J Kranzusch (PJ)

Department of Microbiology, Harvard Medical School, Boston, MA 02115, USA; Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Boston, MA 02115, USA. Electronic address: philip_kranzusch@dfci.harvard.edu.

Jean-Luc Imler (JL)

Sino-French Hoffmann Institute, School of Basic Medical Science, Guangzhou Medical University, Guangzhou, China; Université de Strasbourg, CNRS UPR9022, Institut de Biologie Moléculaire et Cellulaire, Strasbourg, France.

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Classifications MeSH

Recherchemedicale.com › Eucaryotes › Animaux › The virus-induced cyclic dinucleotide...
Recherchemedicale.com › Actions chimiques et utilisations › Actions pharmacologiques › Utilisations thérapeutiques › Anti-infectieux › Antiviraux › The virus-induced cyclic dinucleotide...
Recherchemedicale.com › Eucaryotes › Animaux › Invertébrés › Arthropodes › Insectes › Pterygota › Neoptera › Holometabola › Diptera › Drosophilidae › Drosophila › The virus-induced cyclic dinucleotide...
Recherchemedicale.com › Eucaryotes › Animaux › Invertébrés › Arthropodes › Insectes › Pterygota › Neoptera › Holometabola › Diptera › Drosophilidae › Drosophila › Drosophila melanogaster › The virus-induced cyclic dinucleotide...
Recherchemedicale.com › Acides nucléiques, nucléotides et nucléosides › Nucléotides › Ribonucléotides › Nucléotides guanyliques › GMP cyclique › The virus-induced cyclic dinucleotide...
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