Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria

<p>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...

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Main Author:	Jérémie Rosain (5900399) (author)
Other Authors:	Anna-Lena Neehus (9320912) (author), Jérémy Manry (2160430) (author), Rui Yang (293531) (author), Jérémie Le Pen (18551533) (author), Wassim Daher (240384) (author), Zhiyong Liu (160339) (author), Yi-Hao Chan (7422329) (author), Natalia Tahuil (19483495) (author), Özden Türel (19483498) (author), Mathieu Bourgey (73692) (author), Masato Ogishi (699705) (author), Jean-Marc Doisne (19483501) (author), Helena M. Izquierdo (19483504) (author), Takayoshi Shirasaki (10098660) (author), Tom Le Voyer (18551572) (author), Antoine Guérin (18519939) (author), Paul Bastard (12967485) (author), Marcela Moncada-Vélez (19483408) (author), Ji Eun Han (18519936) (author), Taushif Khan (691254) (author), Franck Rapaport (243876) (author), Seon-Hui Hong (15016838) (author), Andrew Cheung (6485498) (author), Kathrin Haake (15171424) (author), Barbara C. Mindt (11711510) (author), Laura Pérez (234237) (author), Quentin Philippot (558140) (author), Danyel Lee (19483507) (author), Peng Zhang (2071) (author), Darawan Rinchai (742366) (author), Fatima Al Ali (13210926) (author), Manar Mahmoud Ahmad Ata (19483510) (author), Mahbuba Rahman (198499) (author), Jessica N. Peel (19342513) (author), Søren Heissel (5566529) (author), Henrik Molina (1264617) (author), Yasemin Kendir-Demirkol (19342510) (author), Rasheed Bailey (19483513) (author), Shuxiang Zhao (17335719) (author), Jonathan Bohlen (5368448) (author), Mathieu Mancini (11677705) (author), Yoann Seeleuthner (10232517) (author), Marie Roelens (14038091) (author), Lazaro Lorenzo (5155025) (author), Camille Soudée (19342519) (author), María Elvira Josefina Paz (19483516) (author), María Laura González (6238796) (author), Mohamed Jeljeli (5636693) (author), Jean Soulier (15105097) (author), Serge Romana (4260157) (author), Anne-Sophie L’Honneur (5451995) (author), Marie Materna (18387156) (author), Rubén Martínez-Barricarte (19483519) (author), Mathieu Pochon (19483522) (author), Carmen Oleaga-Quintas (19483525) (author), Alexandre Michev (19342507) (author), Mélanie Migaud (5913107) (author), Romain Lévy (18551752) (author), Marie-Alexandra Alyanakian (9518273) (author), Flore Rozenberg (243050) (author), Carys A. Croft (6310997) (author), Guillaume Vogt (64695) (author), Jean-François Emile (64705) (author), Laurent Kremer (37664) (author), Cindy S. Ma (19000769) (author), Jörg H. Fritz (11528196) (author), Stanley M. Lemon (10017699) (author), András N. Spaan (18519927) (author), Nicolas Manel (271967) (author), Laurent Abel (69833) (author), Margaret R. MacDonald (9444081) (author), Stéphanie Boisson-Dupuis (64693) (author), Nico Marr (349853) (author), Stuart G. Tangye (18519960) (author), James P. Di Santo (19483528) (author), Qian Zhang (49333) (author), Shen-Ying Zhang (140174) (author), Charles M. Rice (9110743) (author), Vivien Béziat (204259) (author), Nico Lachmann (3507401) (author), David Langlais (216222) (author), Jean-Laurent Casanova (64712) (author), Philippe Gros (91626) (author), Jacinta Bustamante (64702) (author)
Published:	2023
Subjects:	Biological sciences Genetics Microbiology Biomedical and clinical sciences Immunology inborn errors of immunity Mycobacterium interferon-γ interferon-stimulated geneI RF1 viruses macrophages
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_version_	1864513507061399552
author	Jérémie Rosain (5900399)
author2	Anna-Lena Neehus (9320912) Jérémy Manry (2160430) Rui Yang (293531) Jérémie Le Pen (18551533) Wassim Daher (240384) Zhiyong Liu (160339) Yi-Hao Chan (7422329) Natalia Tahuil (19483495) Özden Türel (19483498) Mathieu Bourgey (73692) Masato Ogishi (699705) Jean-Marc Doisne (19483501) Helena M. Izquierdo (19483504) Takayoshi Shirasaki (10098660) Tom Le Voyer (18551572) Antoine Guérin (18519939) Paul Bastard (12967485) Marcela Moncada-Vélez (19483408) Ji Eun Han (18519936) Taushif Khan (691254) Franck Rapaport (243876) Seon-Hui Hong (15016838) Andrew Cheung (6485498) Kathrin Haake (15171424) Barbara C. Mindt (11711510) Laura Pérez (234237) Quentin Philippot (558140) Danyel Lee (19483507) Peng Zhang (2071) Darawan Rinchai (742366) Fatima Al Ali (13210926) Manar Mahmoud Ahmad Ata (19483510) Mahbuba Rahman (198499) Jessica N. Peel (19342513) Søren Heissel (5566529) Henrik Molina (1264617) Yasemin Kendir-Demirkol (19342510) Rasheed Bailey (19483513) Shuxiang Zhao (17335719) Jonathan Bohlen (5368448) Mathieu Mancini (11677705) Yoann Seeleuthner (10232517) Marie Roelens (14038091) Lazaro Lorenzo (5155025) Camille Soudée (19342519) María Elvira Josefina Paz (19483516) María Laura González (6238796) Mohamed Jeljeli (5636693) Jean Soulier (15105097) Serge Romana (4260157) Anne-Sophie L’Honneur (5451995) Marie Materna (18387156) Rubén Martínez-Barricarte (19483519) Mathieu Pochon (19483522) Carmen Oleaga-Quintas (19483525) Alexandre Michev (19342507) Mélanie Migaud (5913107) Romain Lévy (18551752) Marie-Alexandra Alyanakian (9518273) Flore Rozenberg (243050) Carys A. Croft (6310997) Guillaume Vogt (64695) Jean-François Emile (64705) Laurent Kremer (37664) Cindy S. Ma (19000769) Jörg H. Fritz (11528196) Stanley M. Lemon (10017699) András N. Spaan (18519927) Nicolas Manel (271967) Laurent Abel (69833) Margaret R. MacDonald (9444081) Stéphanie Boisson-Dupuis (64693) Nico Marr (349853) Stuart G. Tangye (18519960) James P. Di Santo (19483528) Qian Zhang (49333) Shen-Ying Zhang (140174) Charles M. Rice (9110743) Vivien Béziat (204259) Nico Lachmann (3507401) David Langlais (216222) Jean-Laurent Casanova (64712) Philippe Gros (91626) Jacinta Bustamante (64702)
author2_role	author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author
author_facet	Jérémie Rosain (5900399) Anna-Lena Neehus (9320912) Jérémy Manry (2160430) Rui Yang (293531) Jérémie Le Pen (18551533) Wassim Daher (240384) Zhiyong Liu (160339) Yi-Hao Chan (7422329) Natalia Tahuil (19483495) Özden Türel (19483498) Mathieu Bourgey (73692) Masato Ogishi (699705) Jean-Marc Doisne (19483501) Helena M. Izquierdo (19483504) Takayoshi Shirasaki (10098660) Tom Le Voyer (18551572) Antoine Guérin (18519939) Paul Bastard (12967485) Marcela Moncada-Vélez (19483408) Ji Eun Han (18519936) Taushif Khan (691254) Franck Rapaport (243876) Seon-Hui Hong (15016838) Andrew Cheung (6485498) Kathrin Haake (15171424) Barbara C. Mindt (11711510) Laura Pérez (234237) Quentin Philippot (558140) Danyel Lee (19483507) Peng Zhang (2071) Darawan Rinchai (742366) Fatima Al Ali (13210926) Manar Mahmoud Ahmad Ata (19483510) Mahbuba Rahman (198499) Jessica N. Peel (19342513) Søren Heissel (5566529) Henrik Molina (1264617) Yasemin Kendir-Demirkol (19342510) Rasheed Bailey (19483513) Shuxiang Zhao (17335719) Jonathan Bohlen (5368448) Mathieu Mancini (11677705) Yoann Seeleuthner (10232517) Marie Roelens (14038091) Lazaro Lorenzo (5155025) Camille Soudée (19342519) María Elvira Josefina Paz (19483516) María Laura González (6238796) Mohamed Jeljeli (5636693) Jean Soulier (15105097) Serge Romana (4260157) Anne-Sophie L’Honneur (5451995) Marie Materna (18387156) Rubén Martínez-Barricarte (19483519) Mathieu Pochon (19483522) Carmen Oleaga-Quintas (19483525) Alexandre Michev (19342507) Mélanie Migaud (5913107) Romain Lévy (18551752) Marie-Alexandra Alyanakian (9518273) Flore Rozenberg (243050) Carys A. Croft (6310997) Guillaume Vogt (64695) Jean-François Emile (64705) Laurent Kremer (37664) Cindy S. Ma (19000769) Jörg H. Fritz (11528196) Stanley M. Lemon (10017699) András N. Spaan (18519927) Nicolas Manel (271967) Laurent Abel (69833) Margaret R. MacDonald (9444081) Stéphanie Boisson-Dupuis (64693) Nico Marr (349853) Stuart G. Tangye (18519960) James P. Di Santo (19483528) Qian Zhang (49333) Shen-Ying Zhang (140174) Charles M. Rice (9110743) Vivien Béziat (204259) Nico Lachmann (3507401) David Langlais (216222) Jean-Laurent Casanova (64712) Philippe Gros (91626) Jacinta Bustamante (64702)
author_role	author
dc.creator.none.fl_str_mv	Jérémie Rosain (5900399) Anna-Lena Neehus (9320912) Jérémy Manry (2160430) Rui Yang (293531) Jérémie Le Pen (18551533) Wassim Daher (240384) Zhiyong Liu (160339) Yi-Hao Chan (7422329) Natalia Tahuil (19483495) Özden Türel (19483498) Mathieu Bourgey (73692) Masato Ogishi (699705) Jean-Marc Doisne (19483501) Helena M. Izquierdo (19483504) Takayoshi Shirasaki (10098660) Tom Le Voyer (18551572) Antoine Guérin (18519939) Paul Bastard (12967485) Marcela Moncada-Vélez (19483408) Ji Eun Han (18519936) Taushif Khan (691254) Franck Rapaport (243876) Seon-Hui Hong (15016838) Andrew Cheung (6485498) Kathrin Haake (15171424) Barbara C. Mindt (11711510) Laura Pérez (234237) Quentin Philippot (558140) Danyel Lee (19483507) Peng Zhang (2071) Darawan Rinchai (742366) Fatima Al Ali (13210926) Manar Mahmoud Ahmad Ata (19483510) Mahbuba Rahman (198499) Jessica N. Peel (19342513) Søren Heissel (5566529) Henrik Molina (1264617) Yasemin Kendir-Demirkol (19342510) Rasheed Bailey (19483513) Shuxiang Zhao (17335719) Jonathan Bohlen (5368448) Mathieu Mancini (11677705) Yoann Seeleuthner (10232517) Marie Roelens (14038091) Lazaro Lorenzo (5155025) Camille Soudée (19342519) María Elvira Josefina Paz (19483516) María Laura González (6238796) Mohamed Jeljeli (5636693) Jean Soulier (15105097) Serge Romana (4260157) Anne-Sophie L’Honneur (5451995) Marie Materna (18387156) Rubén Martínez-Barricarte (19483519) Mathieu Pochon (19483522) Carmen Oleaga-Quintas (19483525) Alexandre Michev (19342507) Mélanie Migaud (5913107) Romain Lévy (18551752) Marie-Alexandra Alyanakian (9518273) Flore Rozenberg (243050) Carys A. Croft (6310997) Guillaume Vogt (64695) Jean-François Emile (64705) Laurent Kremer (37664) Cindy S. Ma (19000769) Jörg H. Fritz (11528196) Stanley M. Lemon (10017699) András N. Spaan (18519927) Nicolas Manel (271967) Laurent Abel (69833) Margaret R. MacDonald (9444081) Stéphanie Boisson-Dupuis (64693) Nico Marr (349853) Stuart G. Tangye (18519960) James P. Di Santo (19483528) Qian Zhang (49333) Shen-Ying Zhang (140174) Charles M. Rice (9110743) Vivien Béziat (204259) Nico Lachmann (3507401) David Langlais (216222) Jean-Laurent Casanova (64712) Philippe Gros (91626) Jacinta Bustamante (64702)
dc.date.none.fl_str_mv	2023-02-02T03:00:00Z
dc.identifier.none.fl_str_mv	10.1016/j.cell.2022.12.038
dc.relation.none.fl_str_mv	https://figshare.com/articles/journal_contribution/Human_IRF1_governs_macrophagic_IFN-_immunity_to_mycobacteria/26831152
dc.rights.none.fl_str_mv	CC BY 4.0 info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv	Biological sciences Genetics Microbiology Biomedical and clinical sciences Immunology inborn errors of immunity Mycobacterium interferon-γ interferon-stimulated geneI RF1 viruses macrophages
dc.title.none.fl_str_mv	Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria
dc.type.none.fl_str_mv	Text Journal contribution info:eu-repo/semantics/publishedVersion text contribution to journal
description	<p>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.</p><h2>Other Information</h2> <p> Published in: Cell<br> License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1016/j.cell.2022.12.038" target="_blank">https://dx.doi.org/10.1016/j.cell.2022.12.038</a></p>
eu_rights_str_mv	openAccess
id	Manara2_c118e43f300d4a81691a34c0f2f64cab
identifier_str_mv	10.1016/j.cell.2022.12.038
network_acronym_str	Manara2
network_name_str	Manara2
oai_identifier_str	oai:figshare.com:article/26831152
publishDate	2023
repository.mail.fl_str_mv
repository.name.fl_str_mv
repository_id_str
rights_invalid_str_mv	CC BY 4.0
spelling	Human IRF1 governs macrophagic IFN-γ immunity to mycobacteriaJérémie Rosain (5900399)Anna-Lena Neehus (9320912)Jérémy Manry (2160430)Rui Yang (293531)Jérémie Le Pen (18551533)Wassim Daher (240384)Zhiyong Liu (160339)Yi-Hao Chan (7422329)Natalia Tahuil (19483495)Özden Türel (19483498)Mathieu Bourgey (73692)Masato Ogishi (699705)Jean-Marc Doisne (19483501)Helena M. Izquierdo (19483504)Takayoshi Shirasaki (10098660)Tom Le Voyer (18551572)Antoine Guérin (18519939)Paul Bastard (12967485)Marcela Moncada-Vélez (19483408)Ji Eun Han (18519936)Taushif Khan (691254)Franck Rapaport (243876)Seon-Hui Hong (15016838)Andrew Cheung (6485498)Kathrin Haake (15171424)Barbara C. Mindt (11711510)Laura Pérez (234237)Quentin Philippot (558140)Danyel Lee (19483507)Peng Zhang (2071)Darawan Rinchai (742366)Fatima Al Ali (13210926)Manar Mahmoud Ahmad Ata (19483510)Mahbuba Rahman (198499)Jessica N. Peel (19342513)Søren Heissel (5566529)Henrik Molina (1264617)Yasemin Kendir-Demirkol (19342510)Rasheed Bailey (19483513)Shuxiang Zhao (17335719)Jonathan Bohlen (5368448)Mathieu Mancini (11677705)Yoann Seeleuthner (10232517)Marie Roelens (14038091)Lazaro Lorenzo (5155025)Camille Soudée (19342519)María Elvira Josefina Paz (19483516)María Laura González (6238796)Mohamed Jeljeli (5636693)Jean Soulier (15105097)Serge Romana (4260157)Anne-Sophie L’Honneur (5451995)Marie Materna (18387156)Rubén Martínez-Barricarte (19483519)Mathieu Pochon (19483522)Carmen Oleaga-Quintas (19483525)Alexandre Michev (19342507)Mélanie Migaud (5913107)Romain Lévy (18551752)Marie-Alexandra Alyanakian (9518273)Flore Rozenberg (243050)Carys A. Croft (6310997)Guillaume Vogt (64695)Jean-François Emile (64705)Laurent Kremer (37664)Cindy S. Ma (19000769)Jörg H. Fritz (11528196)Stanley M. Lemon (10017699)András N. Spaan (18519927)Nicolas Manel (271967)Laurent Abel (69833)Margaret R. MacDonald (9444081)Stéphanie Boisson-Dupuis (64693)Nico Marr (349853)Stuart G. Tangye (18519960)James P. Di Santo (19483528)Qian Zhang (49333)Shen-Ying Zhang (140174)Charles M. Rice (9110743)Vivien Béziat (204259)Nico Lachmann (3507401)David Langlais (216222)Jean-Laurent Casanova (64712)Philippe Gros (91626)Jacinta Bustamante (64702)Biological sciencesGeneticsMicrobiologyBiomedical and clinical sciencesImmunologyinborn errors of immunityMycobacteriuminterferon-γinterferon-stimulated geneIRF1virusesmacrophages<p>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.</p><h2>Other Information</h2> <p> Published in: Cell<br> License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1016/j.cell.2022.12.038" target="_blank">https://dx.doi.org/10.1016/j.cell.2022.12.038</a></p>2023-02-02T03:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1016/j.cell.2022.12.038https://figshare.com/articles/journal_contribution/Human_IRF1_governs_macrophagic_IFN-_immunity_to_mycobacteria/26831152CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/268311522023-02-02T03:00:00Z
spellingShingle	Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria Jérémie Rosain (5900399) Biological sciences Genetics Microbiology Biomedical and clinical sciences Immunology inborn errors of immunity Mycobacterium interferon-γ interferon-stimulated geneI RF1 viruses macrophages
status_str	publishedVersion
title	Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria
title_full	Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria
title_fullStr	Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria
title_full_unstemmed	Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria
title_short	Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria
title_sort	Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria
topic	Biological sciences Genetics Microbiology Biomedical and clinical sciences Immunology inborn errors of immunity Mycobacterium interferon-γ interferon-stimulated geneI RF1 viruses macrophages

Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria

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