Human IL-23 is essential for IFN-γ-dependent immunity to mycobacteria.
| Title: | Human IL-23 is essential for IFN-γ-dependent immunity to mycobacteria. |
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| Authors: | Philippot Q; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Ogishi M; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Bohlen J; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Puchan J; Institute of Microbiology, ETH Zürich, Zürich, Switzerland.; Arias AA; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Primary Immunodeficiencies Group, University of Antioquia (UdeA), Medellin, Colombia.; School of Microbiology, University of Antioquia (UdeA), Medellin, Colombia.; Nguyen T; Garvan Institute of Medical Research, Darlinghurst, NSW, Australia.; School of Clinical Medicine, Faculty of Medicine and Health, UNSW Sydney, Sydney, NSW, Australia.; Martin-Fernandez M; Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Conil C; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Rinchai D; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Momenilandi M; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Mahdaviani SA; Pediatric Respiratory Diseases Research Center, National Research Institute of Tuberculosis and Lung Diseases (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran, Iran.; Keramatipour M; Department of Medical Genetics, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran.; Rosain J; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Yang R; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Khan T; Department of Human Immunology, Sidra Medicine, Doha, Qatar.; Neehus AL; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Materna M; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Han JE; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Peel J; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Mele F; Institute for Research in Biomedicine, Università della Svizzera italiana, Bellinzona, Switzerland.; Weisshaar M; Institute of Microbiology, ETH Zürich, Zürich, Switzerland.; Jovic S; Institute for Research in Biomedicine, Università della Svizzera italiana, Bellinzona, Switzerland.; Bastard P; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Pediatric Hematology-Immunology and Rheumatology Unit, Necker Hospital for Sick Children, AP-HP, Paris, France.; Lévy R; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Pediatric Hematology-Immunology and Rheumatology Unit, Necker Hospital for Sick Children, AP-HP, Paris, France.; Le Voyer T; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Zhang P; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Maglorius Renkilaraj MRL; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Arango-Franco CA; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; Primary Immunodeficiencies Group, University of Antioquia (UdeA), Medellin, Colombia.; Pelham S; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Seeleuthner Y; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Pochon M; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Ata MMA; Department of Human Immunology, Sidra Medicine, Doha, Qatar.; Al Ali F; Department of Human Immunology, Sidra Medicine, Doha, Qatar.; Migaud M; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Soudée C; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; Kochetkov T; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Molitor A; Molecular Immuno-Rheumatology Laboratory, INSERM UMR_S1109, GENOMAX Platform, Faculty of Medicine, OMICARE University Hospital Federation, Immunology and Hematology Research Center, Research Center in Biomedicine of Strasbourg (CRBS), Federation of Translational Medicine of Strasbourg (FMTS), University of Strasbourg, Strasbourg, France.; Interdisciplinary Thematic Institute (ITI) of Precision Medicine of Strasbourg, Strasbourg, France.; Carapito R; Molecular Immuno-Rheumatology Laboratory, INSERM UMR_S1109, GENOMAX Platform, Faculty of Medicine, OMICARE University Hospital Federation, Immunology and Hematology Research Center, Research Center in Biomedicine of Strasbourg (CRBS), Federation of Translational Medicine of Strasbourg (FMTS), University of Strasbourg, Strasbourg, France.; Interdisciplinary Thematic Institute (ITI) of Precision Medicine of Strasbourg, Strasbourg, France.; Immunology Laboratory, Biology Technical Platform, Biology Pole, New Civil Hospital, Strasbourg, France.; Bahram S; Molecular Immuno-Rheumatology Laboratory, INSERM UMR_S1109, GENOMAX Platform, Faculty of Medicine, OMICARE University Hospital Federation, Immunology and Hematology Research Center, Research Center in Biomedicine of Strasbourg (CRBS), Federation of Translational Medicine of Strasbourg (FMTS), University of Strasbourg, Strasbourg, France.; Interdisciplinary Thematic Institute (ITI) of Precision Medicine of Strasbourg, Strasbourg, France.; Immunology Laboratory, Biology Technical Platform, Biology Pole, New Civil Hospital, Strasbourg, France.; Boisson B; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Fieschi C; Clinical Immunology Department, Saint Louis Hospital, Paris, France.; Mansouri D; Pediatric Respiratory Diseases Research Center, National Research Institute of Tuberculosis and Lung Diseases (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran, Iran.; Clinical Tuberculosis and Epidemiology Research Centre, NRITLD, Shahid Beheshti University of Medical Sciences, Tehran, Iran.; Marr N; Department of Human Immunology, Sidra Medicine, Doha, Qatar.; College of Health and Life Sciences, Hamad Bin Khalifa University, Doha, Qatar.; Institute of Translational Immunology, Brandenburg Medical School, Brandenburg an der Havel, Germany.; Okada S; Department of Pediatrics, Hiroshima University Graduate School of Biomedical and Health Sciences, 1-2-3 Kasumi, Minami-Ku, Hiroshima-Shi, Hiroshima, Japan.; Shahrooei M; Clinical and Diagnostic Immunology, Department of Microbiology, Immunology, and Transplantation, KU Leuven, Belgium.; Dr. Shahrooei Lab, 22 Bahman St., Ashrafi Esfahni Blvd, Teheran, Iran.; Parvaneh N; Research Center for Immunodeficiencies, Pediatrics Center of Excellence, Children's Medical Center, Tehran University of Medical Sciences, Teheran, Iran.; Chavoshzadeh Z; Pediatric Infections Research Center, Mofid Children's Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran.; Cobat A; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Bogunovic D; Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Pediatric Respiratory Diseases Research Center, National Research Institute of Tuberculosis and Lung Diseases (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran, Iran.; Abel L; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Tangye SG; School of Clinical Medicine, Faculty of Medicine and Health, UNSW Sydney, Sydney, NSW, Australia.; Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Ma CS; School of Clinical Medicine, Faculty of Medicine and Health, UNSW Sydney, Sydney, NSW, Australia.; Center for Inborn Errors of Immunity, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Béziat V; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Sallusto F; Institute of Microbiology, ETH Zürich, Zürich, Switzerland.; Institute for Research in Biomedicine, Università della Svizzera italiana, Bellinzona, Switzerland.; Boisson-Dupuis S; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Bustamante J; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Study Center for Primary Immunodeficiencies, Necker Hospital for Sick Children, AP-HP, Paris, France.; Casanova JL; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA.; Howard Hughes Medical Institute, New York, NY, USA.; Department of Pediatrics, Necker Hospital for Sick Children, Paris, France.; Puel A; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale (INSERM) U1163, Necker Hospital for Sick Children, Paris, France.; University Paris Cité, Imagine Institute, Paris, France.; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York, NY, USA. |
| Source: | Science immunology [Sci Immunol] 2023 Feb 17; Vol. 8 (80), pp. eabq5204. Date of Electronic Publication: 2023 Feb 10. |
| Publication Type: | Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't |
| Language: | English |
| Journal Info: | Publisher: American Association for the Advancement of Science Country of Publication: United States NLM ID: 101688624 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2470-9468 (Electronic) Linking ISSN: 24709468 NLM ISO Abbreviation: Sci Immunol Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: Washington, DC : American Association for the Advancement of Science, [2016]- |
| MeSH Terms: | Interleukin-23*/genetics ; Mycobacterium Infections*/immunology ; Interferon-gamma* ; Mycobacterium*; Interleukin-17/genetics ; Humans ; Genetic Predisposition to Disease |
| Abstract: | Patients with autosomal recessive (AR) IL-12p40 or IL-12Rβ1 deficiency display Mendelian susceptibility to mycobacterial disease (MSMD) due to impaired IFN-γ production and, less commonly, chronic mucocutaneous candidiasis (CMC) due to impaired IL-17A/F production. We report six patients from four kindreds with AR IL-23R deficiency. These patients are homozygous for one of four different loss-of-function IL23R variants. All six patients have a history of MSMD, but only two suffered from CMC. We show that IL-23 induces IL-17A only in MAIT cells, possibly contributing to the incomplete penetrance of CMC in patients unresponsive to IL-23. By contrast, IL-23 is required for both baseline and Mycobacterium-inducible IFN-γ immunity in both Vδ2+ γδ T and MAIT cells, probably contributing to the higher penetrance of MSMD in these patients. Human IL-23 appears to contribute to IL-17A/F-dependent immunity to Candida in a single lymphocyte subset but is required for IFN-γ-dependent immunity to Mycobacterium in at least two lymphocyte subsets. |
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| Grant Information: | R01 AI127372 United States AI NIAID NIH HHS; UL1 TR000043 United States TR NCATS NIH HHS; R01 AI148963 United States AI NIAID NIH HHS; R01 AI095983 United States AI NIAID NIH HHS; UL1 TR001866 United States TR NCATS NIH HHS; F99 CA274708 United States CA NCI NIH HHS; U19 AI162568 United States AI NIAID NIH HHS; United States HHMI Howard Hughes Medical Institute; R01 AI127564 United States AI NIAID NIH HHS |
| Substance Nomenclature: | 82115-62-6 (Interferon-gamma); 0 (Interleukin-17); 0 (Interleukin-23) |
| Entry Date(s): | Date Created: 20230210 Date Completed: 20230223 Latest Revision: 20250530 |
| Update Code: | 20260130 |
| PubMed Central ID: | PMC10069949 |
| DOI: | 10.1126/sciimmunol.abq5204 |
| PMID: | 36763636 |
| Database: | MEDLINE |
Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't