Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria.

IRF1 Mycobacterium inborn errors of immunity interferon-stimulated gene interferon-γ macrophages viruses

Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
02 02 2023
Historique:
received: 01 04 2022
revised: 22 11 2022
accepted: 19 12 2022
entrez: 3 2 2023
pubmed: 4 2 2023
medline: 8 2 2023
Statut: ppublish

Résumé

Inborn errors of human IFN-γ-dependent macrophagic immunity underlie mycobacterial diseases, whereas inborn errors of IFN-α/β-dependent intrinsic immunity underlie viral diseases. Both types of IFNs induce the transcription factor IRF1. We describe unrelated children with inherited complete IRF1 deficiency and early-onset, multiple, life-threatening diseases caused by weakly virulent mycobacteria and related intramacrophagic pathogens. These children have no history of severe viral disease, despite exposure to many viruses, including SARS-CoV-2, which is life-threatening in individuals with impaired IFN-α/β immunity. In leukocytes or fibroblasts stimulated in vitro, IRF1-dependent responses to IFN-γ are, both quantitatively and qualitatively, much stronger than those to IFN-α/β. Moreover, IRF1-deficient mononuclear phagocytes do not control mycobacteria and related pathogens normally when stimulated with IFN-γ. By contrast, IFN-α/β-dependent intrinsic immunity to nine viruses, including SARS-CoV-2, is almost normal in IRF1-deficient fibroblasts. Human IRF1 is essential for IFN-γ-dependent macrophagic immunity to mycobacteria, but largely redundant for IFN-α/β-dependent antiviral immunity.

Identifiants

pubmed: 36736301
pii: S0092-8674(22)01581-1
doi: 10.1016/j.cell.2022.12.038
pmc: PMC9907019
mid: NIHMS1860716
pii:
doi:

Substances chimiques

Interferon-gamma 82115-62-6
Interferon-alpha 0
IRF1 protein, human 0
Interferon Regulatory Factor-1 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

621-645.e33

Subventions

Organisme : NHGRI NIH HHS
ID : UM1 HG006504
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI091707
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001866
Pays : United States
Organisme : NIH HHS
ID : S10 OD018521
Pays : United States
Organisme : NIAID NIH HHS
ID : U19 AI162568
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI088364
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI163029
Pays : United States
Organisme : NHGRI NIH HHS
ID : U24 HG008956
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI095983
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI103083
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI150095
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Organisme : CIHR
Pays : Canada

Informations de copyright

Crown Copyright © 2022. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests J.-L.C. serves on the scientific advisory boards of ADMA Biologics Inc., Kymera Therapeutics, and Elixiron Immunotherapeutics.

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Auteurs

Jérémie Rosain (J)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France. Electronic address: jeremie.rosain@institutimagine.org.

Anna-Lena Neehus (AL)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; Institute of Experimental Hematology, REBIRTH Center for Regenerative and Translational Medicine, Hannover Medical School, 30625 Hannover, Germany.

Jérémy Manry (J)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

Rui Yang (R)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Jérémie Le Pen (J)

Laboratory of Virology and Infectious Disease, The Rockefeller University, New York, NY 10065, USA.

Wassim Daher (W)

Infectious Disease Research Institute of Montpellier (IRIM), Montpellier University, 34090 Montpellier, France; Inserm, IRIM, CNRS, UMR9004, 34090 Montpellier, France.

Zhiyong Liu (Z)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Yi-Hao Chan (YH)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Natalia Tahuil (N)

Department of Immunology, Del Niño Jesus Hospital, San Miguel de Tucuman, T4000 Tucuman, Argentina.

Özden Türel (Ö)

Department of Pediatric Infectious Disease, Bezmialem Vakif University Faculty of Medicine, 34093 İstanbul, Turkey.

Mathieu Bourgey (M)

Dahdaleh Institute of Genomic Medicine, McGill University, Montreal, QC H3A 0G1, Canada; Canadian Centre for Computation Genomics, Montreal, QC H3A 0G1, Canada.

Masato Ogishi (M)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Jean-Marc Doisne (JM)

Innate Immunity Unit, Institut Pasteur, 75015 Paris, France; Inserm U1223, 75015 Paris, France.

Helena M Izquierdo (HM)

Institut Curie, PSL Research University, Inserm U932, 75005 Paris, France.

Takayoshi Shirasaki (T)

Department of Medicine, Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7292, USA.

Tom Le Voyer (T)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

Antoine Guérin (A)

Garvan Institute of Medical Research, Darlinghurst, NSW 2010, Australia; St. Vincent's Clinical School, Faculty of Medicine, University of NSW, Sydney, NSW 2052, Australia.

Paul Bastard (P)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA; Pediatric Hematology-Immunology and Rheumatology Unit, Necker Hospital for Sick Children, Assistance Publique Hôpitaux de Paris (AP-HP), 75015 Paris, France.

Marcela Moncada-Vélez (M)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Ji Eun Han (JE)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Taushif Khan (T)

Department of Immunology, Sidra Medicine, Doha, Qatar.

Franck Rapaport (F)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Seon-Hui Hong (SH)

Laboratory of Virology and Infectious Disease, The Rockefeller University, New York, NY 10065, USA.

Andrew Cheung (A)

Laboratory of Virology and Infectious Disease, The Rockefeller University, New York, NY 10065, USA.

Kathrin Haake (K)

Institute of Experimental Hematology, REBIRTH Center for Regenerative and Translational Medicine, Hannover Medical School, 30625 Hannover, Germany.

Barbara C Mindt (BC)

Department of Microbiology and Immunology, McGill University, Montreal, QC H3A 0G1, Canada; McGill University Research Centre on Complex Traits, McGill University, Montreal, QC H3A 0G1, Canada; FOCiS Centre of Excellence in Translational Immunology, McGill University, Montreal, QC H3A 0G1, Canada.

Laura Pérez (L)

Department of Immunology and Rheumatology, "J. P. Garrahan" National Hospital of Pediatrics, C1245 CABA Buenos Aires, Argentina.

Quentin Philippot (Q)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

Danyel Lee (D)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Peng Zhang (P)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Darawan Rinchai (D)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Fatima Al Ali (F)

Department of Immunology, Sidra Medicine, Doha, Qatar.

Manar Mahmoud Ahmad Ata (MM)

Department of Immunology, Sidra Medicine, Doha, Qatar.

Mahbuba Rahman (M)

Department of Immunology, Sidra Medicine, Doha, Qatar.

Jessica N Peel (JN)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Søren Heissel (S)

Proteomics Resource Center, The Rockefeller University, New York, NY 10065, USA.

Henrik Molina (H)

Proteomics Resource Center, The Rockefeller University, New York, NY 10065, USA.

Yasemin Kendir-Demirkol (Y)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA; Umraniye Education and Research Hospital, Department of Pediatric Genetics, 34764 İstanbul, Turkey.

Rasheed Bailey (R)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Shuxiang Zhao (S)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Jonathan Bohlen (J)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

Mathieu Mancini (M)

Dahdaleh Institute of Genomic Medicine, McGill University, Montreal, QC H3A 0G1, Canada; Department of Microbiology and Immunology, McGill University, Montreal, QC H3A 0G1, Canada; McGill University Research Centre on Complex Traits, McGill University, Montreal, QC H3A 0G1, Canada.

Yoann Seeleuthner (Y)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

Marie Roelens (M)

Study Center for Primary Immunodeficiencies, Necker Hospital for Sick Children, AP-HP, 75015 Paris, France; Paris Cité University, 75006 Paris, France.

Lazaro Lorenzo (L)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

Camille Soudée (C)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

María Elvira Josefina Paz (MEJ)

Department of Pediatric Pathology, Del Niño Jesus Hospital, San Miguel de Tucuman, T4000 Tucuman, Argentina.

María Laura González (ML)

Central Laboratory, Del Niño Jesus Hospital, San Miguel de Tucuman, T4000 Tucuman, Argentina.

Mohamed Jeljeli (M)

Cochin University Hospital, Biological Immunology Unit, AP-HP, 75014 Paris, France.

Jean Soulier (J)

Inserm/CNRS U944/7212, Paris Cité University, 75006 Paris, France; Hematology Laboratory, Saint-Louis Hospital, AP-HP, 75010 Paris, France; National Reference Center for Bone Marrow Failures, Saint-Louis and Robert Debré Hospitals, 75010 Paris, France.

Serge Romana (S)

Rare Disease Genomic Medicine Department, Paris Cité University, Necker Hospital for Sick Children, 75015 Paris, France.

Anne-Sophie L'Honneur (AS)

Department of Virology, Paris Cité University, Cochin Hospital, 75014 Paris, France.

Marie Materna (M)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

Rubén Martínez-Barricarte (R)

Division of Genetic Medicine, Department of Medicine, Vanderbilt Genetics Institute, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Pathology, Microbiology, and Immunology, Vanderbilt Center for Immunobiology, Vanderbilt Institute for Infection, Immunology, and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA.

Mathieu Pochon (M)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

Carmen Oleaga-Quintas (C)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

Alexandre Michev (A)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

Mélanie Migaud (M)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France.

Romain Lévy (R)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; Pediatric Hematology-Immunology and Rheumatology Unit, Necker Hospital for Sick Children, Assistance Publique Hôpitaux de Paris (AP-HP), 75015 Paris, France.

Marie-Alexandra Alyanakian (MA)

Immunology Laboratory, Necker Hospital for Sick Children, AP-HP, 75015 Paris, France.

Flore Rozenberg (F)

Department of Virology, Paris Cité University, Cochin Hospital, 75014 Paris, France.

Carys A Croft (CA)

Innate Immunity Unit, Institut Pasteur, 75015 Paris, France; Inserm U1223, 75015 Paris, France; Paris Cité University, 75006 Paris, France.

Guillaume Vogt (G)

Inserm UMR1283, CNRS UMR8199, European Genomic Institute for Diabetes, Lille University, Lille Pasteur Institute, Lille University Hospital, 59000 Lille, France; Neglected Human Genetics Laboratory, Paris Cité University, 75006 Paris, France.

Jean-François Emile (JF)

Pathology Department, Ambroise-Paré Hospital, AP-HP, 92100 Boulogne-Billancourt, France.

Laurent Kremer (L)

Infectious Disease Research Institute of Montpellier (IRIM), Montpellier University, 34090 Montpellier, France; Inserm, IRIM, CNRS, UMR9004, 34090 Montpellier, France.

Cindy S Ma (CS)

Garvan Institute of Medical Research, Darlinghurst, NSW 2010, Australia; St. Vincent's Clinical School, Faculty of Medicine, University of NSW, Sydney, NSW 2052, Australia.

Jörg H Fritz (JH)

Department of Microbiology and Immunology, McGill University, Montreal, QC H3A 0G1, Canada; McGill University Research Centre on Complex Traits, McGill University, Montreal, QC H3A 0G1, Canada; FOCiS Centre of Excellence in Translational Immunology, McGill University, Montreal, QC H3A 0G1, Canada; Department of Physiology, McGill University, Montreal, QC H3A 0G1, Canada.

Stanley M Lemon (SM)

Department of Medicine, Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7292, USA.

András N Spaan (AN)

St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA; Department of Medical Microbiology, University Medical Center Utrecht, Utrecht University, 3584CX Utrecht, the Netherlands.

Nicolas Manel (N)

Institut Curie, PSL Research University, Inserm U932, 75005 Paris, France.

Laurent Abel (L)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Margaret R MacDonald (MR)

Laboratory of Virology and Infectious Disease, The Rockefeller University, New York, NY 10065, USA.

Stéphanie Boisson-Dupuis (S)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Nico Marr (N)

Department of Immunology, Sidra Medicine, Doha, Qatar; College of Health and Life Sciences, Hamad Bin Khalifa University, Doha, Qatar.

Stuart G Tangye (SG)

Garvan Institute of Medical Research, Darlinghurst, NSW 2010, Australia; St. Vincent's Clinical School, Faculty of Medicine, University of NSW, Sydney, NSW 2052, Australia.

James P Di Santo (JP)

Innate Immunity Unit, Institut Pasteur, 75015 Paris, France; Inserm U1223, 75015 Paris, France.

Qian Zhang (Q)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Shen-Ying Zhang (SY)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Charles M Rice (CM)

Laboratory of Virology and Infectious Disease, The Rockefeller University, New York, NY 10065, USA.

Vivien Béziat (V)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA.

Nico Lachmann (N)

Institute of Experimental Hematology, REBIRTH Center for Regenerative and Translational Medicine, Hannover Medical School, 30625 Hannover, Germany; Department of Pediatric Pulmonology, Allergology and Neonatology and Biomedical Research in Endstage and Obstructive Lung Disease, German Center for Lung Research, Hannover Medical School, 30625 Hannover, Germany; Cluster of Excellence RESIST (EXC 2155), Hannover Medical School, 30625 Hannover, Germany.

David Langlais (D)

Dahdaleh Institute of Genomic Medicine, McGill University, Montreal, QC H3A 0G1, Canada; Department of Microbiology and Immunology, McGill University, Montreal, QC H3A 0G1, Canada; Department of Human Genetics, McGill University, Montreal, QC H3A 0G1, Canada.

Jean-Laurent Casanova (JL)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA; Department of Pediatrics, Necker Hospital for Sick Children, AP-HP, 75015 Paris, France; Howard Hughes Medical Institute, New York, NY 10065, USA. Electronic address: casanova@rockefeller.edu.

Philippe Gros (P)

Dahdaleh Institute of Genomic Medicine, McGill University, Montreal, QC H3A 0G1, Canada; Department of Biochemistry, McGill University, Montreal, QC H3A 0G1, Canada.

Jacinta Bustamante (J)

Laboratory of Human Genetics of Infectious Diseases, Inserm U1163, 75015 Paris, France; Paris Cité University, Imagine Institute, 75015 Paris, France; St. Giles Laboratory of Human Genetics of Infectious Diseases, The Rockefeller University, New York, NY 10065, USA; Study Center for Primary Immunodeficiencies, Necker Hospital for Sick Children, AP-HP, 75015 Paris, France. Electronic address: jacinta.bustamante@inserm.fr.

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