Frontiers in Immunology (Oct 2023)
The purinergic receptor P2X7 and the NLRP3 inflammasome are druggable host factors required for SARS-CoV-2 infection
- Déborah Lécuyer,
- Déborah Lécuyer,
- Roberta Nardacci,
- Roberta Nardacci,
- Désirée Tannous,
- Désirée Tannous,
- Désirée Tannous,
- Emie Gutierrez-Mateyron,
- Emie Gutierrez-Mateyron,
- Aurélia Deva Nathan,
- Aurélia Deva Nathan,
- Frédéric Subra,
- Cristina Di Primio,
- Cristina Di Primio,
- Paola Quaranta,
- Paola Quaranta,
- Vanessa Petit,
- Clémence Richetta,
- Ali Mostefa-Kara,
- Ali Mostefa-Kara,
- Franca Del Nonno,
- Laura Falasca,
- Romain Marlin,
- Pauline Maisonnasse,
- Julia Delahousse,
- Julia Delahousse,
- Juliette Pascaud,
- Juliette Pascaud,
- Eric Deprez,
- Marie Naigeon,
- Marie Naigeon,
- Marie Naigeon,
- Nathalie Chaput,
- Nathalie Chaput,
- Nathalie Chaput,
- Angelo Paci,
- Angelo Paci,
- Angelo Paci,
- Angelo Paci,
- Véronique Saada,
- David Ghez,
- David Ghez,
- Xavier Mariette,
- Xavier Mariette,
- Xavier Mariette,
- Mario Costa,
- Mario Costa,
- Mario Costa,
- Mauro Pistello,
- Mauro Pistello,
- Awatef Allouch,
- Awatef Allouch,
- Awatef Allouch,
- Olivier Delelis,
- Mauro Piacentini,
- Mauro Piacentini,
- Roger Le Grand,
- Jean-Luc Perfettini,
- Jean-Luc Perfettini
Affiliations
- Déborah Lécuyer
- Université Paris-Saclay, Inserm UMR1030, Laboratory of Molecular Radiotherapy and Therapeutic Innovation, Villejuif, France
- Déborah Lécuyer
- Gustave Roussy Cancer Center, Villejuif, France
- Roberta Nardacci
- National Institute for Infectious Diseases “Lazzaro Spallanzani”, Rome, Italy
- Roberta Nardacci
- UniCamillus - Saint Camillus International University of Health and Medical Sciences, Rome, Italy
- Désirée Tannous
- Université Paris-Saclay, Inserm UMR1030, Laboratory of Molecular Radiotherapy and Therapeutic Innovation, Villejuif, France
- Désirée Tannous
- Gustave Roussy Cancer Center, Villejuif, France
- Désirée Tannous
- NH TherAguix SAS, Meylan, France
- Emie Gutierrez-Mateyron
- Université Paris-Saclay, Inserm UMR1030, Laboratory of Molecular Radiotherapy and Therapeutic Innovation, Villejuif, France
- Emie Gutierrez-Mateyron
- Gustave Roussy Cancer Center, Villejuif, France
- Aurélia Deva Nathan
- Université Paris-Saclay, Inserm UMR1030, Laboratory of Molecular Radiotherapy and Therapeutic Innovation, Villejuif, France
- Aurélia Deva Nathan
- Gustave Roussy Cancer Center, Villejuif, France
- Frédéric Subra
- Université Paris-Saclay, ENS Paris-Saclay, CNRS UMR 8113, IDA FR3242, Laboratory of Biology and Applied Pharmacology (LBPA), Gif-sur-Yvette, France
- Cristina Di Primio
- Institute of Neuroscience, Italian National Research Council, Pisa, Italy
- Cristina Di Primio
- Laboratory of Biology BIO@SNS, Scuola Normale Superiore, Pisa, Italy
- Paola Quaranta
- Institute of Neuroscience, Italian National Research Council, Pisa, Italy
- Paola Quaranta
- Retrovirus Center, Department of Translational Research, Universita of Pisa, Pisa, Italy
- Vanessa Petit
- 0Université Paris-Saclay, Inserm U1274, CEA, Genetic Stability, Stem Cells and Radiation, Fontenay-aux-Roses, France
- Clémence Richetta
- Université Paris-Saclay, ENS Paris-Saclay, CNRS UMR 8113, IDA FR3242, Laboratory of Biology and Applied Pharmacology (LBPA), Gif-sur-Yvette, France
- Ali Mostefa-Kara
- Université Paris-Saclay, Inserm UMR1030, Laboratory of Molecular Radiotherapy and Therapeutic Innovation, Villejuif, France
- Ali Mostefa-Kara
- Gustave Roussy Cancer Center, Villejuif, France
- Franca Del Nonno
- National Institute for Infectious Diseases “Lazzaro Spallanzani”, Rome, Italy
- Laura Falasca
- National Institute for Infectious Diseases “Lazzaro Spallanzani”, Rome, Italy
- Romain Marlin
- 1Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial Diseases (IMVA- HB/IDMIT), Fontenay-aux-Roses, France
- Pauline Maisonnasse
- 1Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial Diseases (IMVA- HB/IDMIT), Fontenay-aux-Roses, France
- Julia Delahousse
- Université Paris-Saclay, Inserm UMR1030, Laboratory of Molecular Radiotherapy and Therapeutic Innovation, Villejuif, France
- Julia Delahousse
- Gustave Roussy Cancer Center, Villejuif, France
- Juliette Pascaud
- 1Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial Diseases (IMVA- HB/IDMIT), Fontenay-aux-Roses, France
- Juliette Pascaud
- 2Assistance Publique, Hôpitaux de Paris (AP-HP), Hôpital Bicêtre, Le Kremlin Bicêtre, France
- Eric Deprez
- Université Paris-Saclay, ENS Paris-Saclay, CNRS UMR 8113, IDA FR3242, Laboratory of Biology and Applied Pharmacology (LBPA), Gif-sur-Yvette, France
- Marie Naigeon
- Gustave Roussy Cancer Center, Villejuif, France
- Marie Naigeon
- 3Université Paris-Saclay, Inserm, CNRS, Analyse Moléculaire, Modélisation et Imagerie de la Maladie Cancéreuse, Laboratoire d’Immunomonitoring en Oncologie, Villejuif, France
- Marie Naigeon
- 4Université Paris-Saclay, Faculté de Pharmacie, Chatenay-Malabry, France
- Nathalie Chaput
- 3Université Paris-Saclay, Inserm, CNRS, Analyse Moléculaire, Modélisation et Imagerie de la Maladie Cancéreuse, Laboratoire d’Immunomonitoring en Oncologie, Villejuif, France
- Nathalie Chaput
- 4Université Paris-Saclay, Faculté de Pharmacie, Chatenay-Malabry, France
- Nathalie Chaput
- 5Université Paris-Saclay, Gustave Roussy Cancer Center, CNRS, Stabilité Génétique et Oncogenèse, Villejuif, France
- Angelo Paci
- Université Paris-Saclay, Inserm UMR1030, Laboratory of Molecular Radiotherapy and Therapeutic Innovation, Villejuif, France
- Angelo Paci
- Gustave Roussy Cancer Center, Villejuif, France
- Angelo Paci
- 4Université Paris-Saclay, Faculté de Pharmacie, Chatenay-Malabry, France
- Angelo Paci
- 6Department of Biology and Pathology, Gustave Roussy Cancer Center, Villejuif, France
- Véronique Saada
- 6Department of Biology and Pathology, Gustave Roussy Cancer Center, Villejuif, France
- David Ghez
- Université Paris-Saclay, Inserm UMR1030, Laboratory of Molecular Radiotherapy and Therapeutic Innovation, Villejuif, France
- David Ghez
- 7Department of Hematology, Gustave Roussy Cancer Center, Villejuif, France
- Xavier Mariette
- 1Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial Diseases (IMVA- HB/IDMIT), Fontenay-aux-Roses, France
- Xavier Mariette
- 2Assistance Publique, Hôpitaux de Paris (AP-HP), Hôpital Bicêtre, Le Kremlin Bicêtre, France
- Xavier Mariette
- 8Université Paris-Saclay, Faculté de Médecine, Le Kremlin Bicêtre, France
- Mario Costa
- Institute of Neuroscience, Italian National Research Council, Pisa, Italy
- Mario Costa
- Laboratory of Biology BIO@SNS, Scuola Normale Superiore, Pisa, Italy
- Mario Costa
- 9Centro Pisano Ricerca e Implementazione Clinical Flash Radiotherapy “CPFR@CISUP“, “S. Chiara” Hospital, Pisa, Italy
- Mauro Pistello
- Retrovirus Center, Department of Translational Research, Universita of Pisa, Pisa, Italy
- Mauro Pistello
- 0Virology Operative Unit, Pisa University Hospital, Pisa, Italy
- Awatef Allouch
- Université Paris-Saclay, Inserm UMR1030, Laboratory of Molecular Radiotherapy and Therapeutic Innovation, Villejuif, France
- Awatef Allouch
- Gustave Roussy Cancer Center, Villejuif, France
- Awatef Allouch
- NH TherAguix SAS, Meylan, France
- Olivier Delelis
- Université Paris-Saclay, ENS Paris-Saclay, CNRS UMR 8113, IDA FR3242, Laboratory of Biology and Applied Pharmacology (LBPA), Gif-sur-Yvette, France
- Mauro Piacentini
- National Institute for Infectious Diseases “Lazzaro Spallanzani”, Rome, Italy
- Mauro Piacentini
- 1Department of Biology, University of Rome “Tor Vergata”, Rome, Italy
- Roger Le Grand
- 1Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial Diseases (IMVA- HB/IDMIT), Fontenay-aux-Roses, France
- Jean-Luc Perfettini
- Université Paris-Saclay, Inserm UMR1030, Laboratory of Molecular Radiotherapy and Therapeutic Innovation, Villejuif, France
- Jean-Luc Perfettini
- Gustave Roussy Cancer Center, Villejuif, France
- DOI
- https://doi.org/10.3389/fimmu.2023.1270081
- Journal volume & issue
-
Vol. 14
Abstract
Purinergic receptors and NOD-like receptor protein 3 (NLRP3) inflammasome regulate inflammation and viral infection, but their effects on severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection remain poorly understood. Here, we report that the purinergic receptor P2X7 and NLRP3 inflammasome are cellular host factors required for SARS-CoV-2 infection. Lung autopsies from patients with severe coronavirus disease 2019 (COVID-19) reveal that NLRP3 expression is increased in host cellular targets of SARS-CoV-2 including alveolar macrophages, type II pneumocytes and syncytia arising from the fusion of infected macrophages, thus suggesting a potential role of NLRP3 and associated signaling pathways to both inflammation and viral replication. In vitro studies demonstrate that NLRP3-dependent inflammasome activation is detected upon macrophage abortive infection. More importantly, a weak activation of NLRP3 inflammasome is also detected during the early steps of SARS-CoV-2 infection of epithelial cells and promotes the viral replication in these cells. Interestingly, the purinergic receptor P2X7, which is known to control NLRP3 inflammasome activation, also favors the replication of D614G and alpha SARS-CoV-2 variants. Altogether, our results reveal an unexpected relationship between the purinergic receptor P2X7, the NLRP3 inflammasome and the permissiveness to SARS-CoV-2 infection that offers novel opportunities for COVID-19 treatment.
Keywords