Evidence map›Paper›PMID 35506364›Full record

ArticleThe EMBO journal2022

Host succinate inhibits influenza virus infection through succinylation and nuclear retention of the viral nucleoprotein.

Antoine Guillon, Deborah Brea-Diakite, Adeline Cezard, Alan Wacquiez, Thomas Baranek, Jérôme Bourgeais, Frédéric Picou, Virginie Vasseur, Léa Meyer, Christophe Chevalier and 16 more

Open access · bronzeAbstract read
In one paragraph

Article in The EMBO journal, 2022. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 32 papers.

0numbers the graph read from it
0cells of the map it votes in
32citing papers in PubMed
6.9field-weighted citation impact, top 2% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

32 citing papers in PubMed, 52 citations in OpenAlex.

  1. Review
  2. Article
  3. Host metabolic responses to SARS-CoV-2 and influenza viruses: parallels and contrasts.Metabolomics : Official journal of the Metabolomic Society · 2026
    Review
  4. Article
  5. Article
  6. Review
  7. Review
  8. Emerging microbes & infections · 2025
    Article
  9. Review
  10. Review
  11. Human MX1 orchestrates the cytoplasmic sequestration of neosynthesized influenza A virus vRNPs.Proceedings of the National Academy of Sciences of the United States of America · 2025
    Article
  12. Article
  13. Article
  14. Article
  15. Article
  16. ProbioticJournal of biomedical research · 2025
    Article
  17. Article
  18. Article
  19. Article
  20. Article
4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

26 authors at 8 institutions in 3 countries.

Antoine Guillon *INSERM, Centre d'Etude des Pathologies Respiratoires (CEPR), UMR 1100, Tours, France.
Deborah Brea-Diakite *INSERM, Centre d'Etude des Pathologies Respiratoires (CEPR), UMR 1100, Tours, France.
Adeline Cezard *INSERM, Centre d'Etude des Pathologies Respiratoires (CEPR), UMR 1100, Tours, France.ORCID 0000-0001-8608-701X
Alan WacquiezINSERM, Centre d'Etude des Pathologies Respiratoires (CEPR), UMR 1100, Tours, France.ORCID 0000-0001-5266-5328
Thomas BaranekINSERM, Centre d'Etude des Pathologies Respiratoires (CEPR), UMR 1100, Tours, France.ORCID 0000-0002-5651-0937
Jérôme BourgeaisUniversité de Tours, Tours, France.
Frédéric PicouUniversité de Tours, Tours, France.ORCID 0000-0002-2066-2146
Virginie VasseurINSERM, Centre d'Etude des Pathologies Respiratoires (CEPR), UMR 1100, Tours, France.
Léa MeyerVirologie et Immunologie Moléculaires, INRAe, Université Paris-Saclay, Jouy-en-Josas, France.
Christophe ChevalierVirologie et Immunologie Moléculaires, INRAe, Université Paris-Saclay, Jouy-en-Josas, France.ORCID 0000-0003-3231-9027
Adrien AuvetINSERM, Centre d'Etude des Pathologies Respiratoires (CEPR), UMR 1100, Tours, France.
José M CarballidoNovartis Institutes for BioMedical Research, Basel, Switzerland.ORCID 0000-0001-8465-0665
Lydie Nadal DesbaratsUMR 1253, iBrain, Inserm, Université de Tours, Tours, France.
Florent DingliCentre de Recherche, Laboratoire de Spectrométrie de Masse Protéomique, Institut Curie, PSL Research University, Paris, France.ORCID 0000-0002-7715-2446
Andrei TurtoiTumor Microenvironment Laboratory, Institut de Recherche en Cancérologie de Montpellier, INSERM U1194, Montpellier, France.ORCID 0000-0003-3813-6635
Audrey Le GouellecCNRS, CHU Grenoble Alpes, Grenoble INP, TIMC-IMAG, University Grenoble Alpes, Grenoble, France.ORCID 0000-0002-4905-3854
Florence FauvelleUGA/INSERM U1216, Grenoble Institute of Neurosciences, Grenoble, France.
Amélie DonchetInstitut de Biologie Structurale (IBS), CEA, CNRS, University Grenoble Alpes, Grenoble, France.
Thibaut CrépinInstitut de Biologie Structurale (IBS), CEA, CNRS, University Grenoble Alpes, Grenoble, France.ORCID 0000-0003-2663-1794
Pieter S HiemstraDepartment of Pulmonology, Leiden University Medical Center, Leiden, Netherlands.ORCID 0000-0002-0238-5982
Christophe PagetINSERM, Centre d'Etude des Pathologies Respiratoires (CEPR), UMR 1100, Tours, France.ORCID 0000-0002-5374-5407
Damarys LoewCentre de Recherche, Laboratoire de Spectrométrie de Masse Protéomique, Institut Curie, PSL Research University, Paris, France.ORCID 0000-0002-9111-8842
Olivier Herault *Université de Tours, Tours, France.
Nadia Naffakh *Institut Pasteur, Unité Biologie des ARN et Virus Influenza, CNRS UMR3569, Paris, France.ORCID 0000-0002-0424-0277
Ronan Le Goffic *Virologie et Immunologie Moléculaires, INRAe, Université Paris-Saclay, Jouy-en-Josas, France.ORCID 0000-0002-2012-0064
Mustapha Si-TaharINSERM, Centre d'Etude des Pathologies Respiratoires (CEPR), UMR 1100, Tours, France.ORCID 0000-0002-5792-7742
Université de Tours · FRCentre National de la Recherche Scientifique · FRUniversité Paris-Saclay · FRInserm · FRUniversité Paris Sciences et Lettres · FRInstitut polytechnique de Grenoble · FRLeiden University Medical Center · NLNovartis (Switzerland) · CH

Funding

No grant is acknowledged in the PubMed record.

6 · The paper itself

Abstract

Influenza virus infection causes considerable morbidity and mortality, but current therapies have limited efficacy. We hypothesized that investigating the metabolic signaling during infection may help to design innovative antiviral approaches. Using bronchoalveolar lavages of infected mice, we here demonstrate that influenza virus induces a major reprogramming of lung metabolism. We focused on mitochondria-derived succinate that accumulated both in the respiratory fluids of virus-challenged mice and of patients with influenza pneumonia. Notably, succinate displays a potent antiviral activity in vitro as it inhibits the multiplication of influenza A/H1N1 and A/H3N2 strains and strongly decreases virus-triggered metabolic perturbations and inflammatory responses. Moreover, mice receiving succinate intranasally showed reduced viral loads in lungs and increased survival compared to control animals. The antiviral mechanism involves a succinate-dependent posttranslational modification, that is, succinylation, of the viral nucleoprotein at the highly conserved K87 residue. Succinylation of viral nucleoprotein altered its electrostatic interactions with viral RNA and further impaired the trafficking of viral ribonucleoprotein complexes. The finding that succinate efficiently disrupts the influenza replication cycle opens up new avenues for improved treatment of influenza pneumonia.

Indexed as

Influenza A Virus, H1N1 SubtypeInfluenza, HumanOrthomyxoviridae InfectionsPneumoniaAnimalsAntiviral AgentsHumansInfluenza A Virus, H3N2 SubtypeMiceNucleocapsid ProteinsNucleoproteinsSuccinic AcidVirus ReplicationAntiviral AgentsNucleocapsid ProteinsNucleoproteinsSuccinic Acidantiviralinfluenzametabokinesignalingvirus

Identifiers

PMID35506364
PMCPMC9194747
OpenAlexW4225384899

What OpenQuestion holds

Textmetadata
LicenceCC BY-NC-ND
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.