Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria

Jérémie Rosain; Anna-Lena Neehus; Jérémy Manry; Rui Yang; Jérémie Le Pen; Wassim Daher; Zhiyong Liu; Yi-Hao Chan; Natalia Tahuil; Özden Türel; Mathieu Bourgey; Masato Ogishi; Jean-Marc Doisne; Helena M Izquierdo; Takayoshi Shirasaki; Tom Le Voyer; Antoine Guérin; Paul Bastard; Marcela Moncada-Vélez; Ji Eun Han; Taushif Khan; Franck Rapaport; Seon-Hui Hong; Andrew Cheung; Kathrin Haake; Barbara C Mindt; Laura Pérez; Quentin Philippot; Danyel Lee; Peng Zhang; Darawan Rinchai; Fatima Al Ali; Manar Mahmoud Ahmad Ata; Mahbuba Rahman; Jessica N Peel; Søren Heissel; Henrik Molina; Yasemin Kendir-Demirkol; Rasheed Bailey; Shuxiang Zhao; Jonathan Bohlen; Yoann Seeleuthner; Marie Roelens; Lazaro Lorenzo; Camille Soudée; María Elvira Josefina Paz; María Laura González; Mohamed Jeljeli; Jean Soulier; Serge Romana; Anne-Sophie L'Honneur; Marie Materna; Rubén Martínez-Barricarte; Mathieu Pochon; Carmen Oleaga-Quintas; Alexandre Michev; Mélanie Migaud; Romain Lévy; Marie-Alexandra Alyanakian; Flore Rozenberg; Carys A Croft; Guillaume Vogt; Jean-François Emile; Laurent Kremer; Cindy S Ma; Jörg H Fritz; Stanley M Lemon; András N Spaan; Nicolas Manel; Laurent Abel; Margaret R MacDonald; Stéphanie Boisson-Dupuis; Nico Marr; Stuart G Tangye; James P Di Santo; Qian Zhang; Shen-Ying Zhang; Charles M Rice; Vivien Béziat; Nico Lachmann; David Langlais; Jean-Laurent Casanova; Philippe Gros; Jacinta Bustamante

doi:10.1016/j.cell.2022.12.038

Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria

Jérémie Rosain, Anna-Lena Neehus, Jérémy Manry, Rui Yang, Jérémie Le Pen, Wassim Daher, Zhiyong Liu, Yi-Hao Chan, Natalia Tahuil, Özden Türel, Mathieu Bourgey, Masato Ogishi, Jean-Marc Doisne, Helena M Izquierdo, Takayoshi Shirasaki, Tom Le Voyer, Antoine Guérin, Paul Bastard, Marcela Moncada-Vélez, Ji Eun HanTaushif Khan, Franck Rapaport, Seon-Hui Hong, Andrew Cheung, Kathrin Haake, Barbara C Mindt, Laura Pérez, Quentin Philippot, Danyel Lee, Peng Zhang, Darawan Rinchai, Fatima Al Ali, Manar Mahmoud Ahmad Ata, Mahbuba Rahman, Jessica N Peel, Søren Heissel, Henrik Molina, Yasemin Kendir-Demirkol, Rasheed Bailey, Shuxiang Zhao, Jonathan Bohlen, Yoann Seeleuthner, Marie Roelens, Lazaro Lorenzo, Camille Soudée, María Elvira Josefina Paz, María Laura González, Mohamed Jeljeli, Jean Soulier, Serge Romana, Anne-Sophie L'Honneur, Marie Materna, Rubén Martínez-Barricarte, Mathieu Pochon, Carmen Oleaga-Quintas, Alexandre Michev, Mélanie Migaud, Romain Lévy, Marie-Alexandra Alyanakian, Flore Rozenberg, Carys A Croft, Guillaume Vogt, Jean-François Emile, Laurent Kremer, Cindy S Ma, Jörg H Fritz, Stanley M Lemon, András N Spaan, Nicolas Manel, Laurent Abel, Margaret R MacDonald, Stéphanie Boisson-Dupuis, Nico Marr, Stuart G Tangye, James P Di Santo, Qian Zhang, Shen-Ying Zhang, Charles M Rice, Vivien Béziat, Nico Lachmann, David Langlais, Jean-Laurent Casanova, Philippe Gros, Jacinta Bustamante

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Abstract

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.

Original language	English
Pages (from-to)	621-645.e33
Journal	Cell
Volume	186
Issue number	3
DOIs	https://doi.org/10.1016/j.cell.2022.12.038
Publication status	Published - 2 Feb 2023

Keywords

COVID-19
Child
Humans
Interferon Regulatory Factor-1
Interferon-alpha
Interferon-gamma
Mycobacterium
SARS-CoV-2

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10.1016/j.cell.2022.12.038Licence: CC BY

1-s2.0-S0092867422015811-mainFinal published version, 14.2 MBLicence: CC BY

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Rosain, J., Neehus, A.-L., Manry, J., Yang, R., Le Pen, J., Daher, W., Liu, Z., Chan, Y.-H., Tahuil, N., Türel, Ö., Bourgey, M., Ogishi, M., Doisne, J.-M., Izquierdo, H. M., Shirasaki, T., Le Voyer, T., Guérin, A., Bastard, P., Moncada-Vélez, M., ... Bustamante, J. (2023). Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria. Cell, 186(3), 621-645.e33. https://doi.org/10.1016/j.cell.2022.12.038

@article{3b15f88e390141f9aec3177f1e9d3191,

title = "Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria",

abstract = "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.",

keywords = "COVID-19, Child, Humans, Interferon Regulatory Factor-1, Interferon-alpha, Interferon-gamma, Mycobacterium, SARS-CoV-2",

author = "J{\'e}r{\'e}mie Rosain and Anna-Lena Neehus and J{\'e}r{\'e}my Manry and Rui Yang and {Le Pen}, J{\'e}r{\'e}mie and Wassim Daher and Zhiyong Liu and Yi-Hao Chan and Natalia Tahuil and {\"O}zden T{\"u}rel and Mathieu Bourgey and Masato Ogishi and Jean-Marc Doisne and Izquierdo, {Helena M} and Takayoshi Shirasaki and {Le Voyer}, Tom and Antoine Gu{\'e}rin and Paul Bastard and Marcela Moncada-V{\'e}lez and Han, {Ji Eun} and Taushif Khan and Franck Rapaport and Seon-Hui Hong and Andrew Cheung and Kathrin Haake and Mindt, {Barbara C} and Laura P{\'e}rez and Quentin Philippot and Danyel Lee and Peng Zhang and Darawan Rinchai and {Al Ali}, Fatima and {Ahmad Ata}, {Manar Mahmoud} and Mahbuba Rahman and Peel, {Jessica N} and S{\o}ren Heissel and Henrik Molina and Yasemin Kendir-Demirkol and Rasheed Bailey and Shuxiang Zhao and Jonathan Bohlen and Yoann Seeleuthner and Marie Roelens and Lazaro Lorenzo and Camille Soud{\'e}e and Paz, {Mar{\'i}a Elvira Josefina} and Gonz{\'a}lez, {Mar{\'i}a Laura} and Mohamed Jeljeli and Jean Soulier and Serge Romana and Anne-Sophie L'Honneur and Marie Materna and Rub{\'e}n Mart{\'i}nez-Barricarte and Mathieu Pochon and Carmen Oleaga-Quintas and Alexandre Michev and M{\'e}lanie Migaud and Romain L{\'e}vy and Marie-Alexandra Alyanakian and Flore Rozenberg and Croft, {Carys A} and Guillaume Vogt and Jean-Fran{\c c}ois Emile and Laurent Kremer and Ma, {Cindy S} and Fritz, {J{\"o}rg H} and Lemon, {Stanley M} and Spaan, {Andr{\'a}s N} and Nicolas Manel and Laurent Abel and MacDonald, {Margaret R} and St{\'e}phanie Boisson-Dupuis and Nico Marr and Tangye, {Stuart G} and {Di Santo}, {James P} and Qian Zhang and Shen-Ying Zhang and Rice, {Charles M} and Vivien B{\'e}ziat and Nico Lachmann and David Langlais and Jean-Laurent Casanova and Philippe Gros and Jacinta Bustamante",

note = "Publisher Copyright: {\textcopyright} 2022",

year = "2023",

month = feb,

day = "2",

doi = "10.1016/j.cell.2022.12.038",

language = "English",

volume = "186",

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Rosain, J, Neehus, A-L, Manry, J, Yang, R, Le Pen, J, Daher, W, Liu, Z, Chan, Y-H, Tahuil, N, Türel, Ö, Bourgey, M, Ogishi, M, Doisne, J-M, Izquierdo, HM, Shirasaki, T, Le Voyer, T, Guérin, A, Bastard, P, Moncada-Vélez, M, Han, JE, Khan, T, Rapaport, F, Hong, S-H, Cheung, A, Haake, K, Mindt, BC, Pérez, L, Philippot, Q, Lee, D, Zhang, P, Rinchai, D, Al Ali, F, Ahmad Ata, MM, Rahman, M, Peel, JN, Heissel, S, Molina, H, Kendir-Demirkol, Y, Bailey, R, Zhao, S, Bohlen, J, Seeleuthner, Y, Roelens, M, Lorenzo, L, Soudée, C, Paz, MEJ, González, ML, Jeljeli, M, Soulier, J, Romana, S, L'Honneur, A-S, Materna, M, Martínez-Barricarte, R, Pochon, M, Oleaga-Quintas, C, Michev, A, Migaud, M, Lévy, R, Alyanakian, M-A, Rozenberg, F, Croft, CA, Vogt, G, Emile, J-F, Kremer, L, Ma, CS, Fritz, JH, Lemon, SM, Spaan, AN, Manel, N, Abel, L, MacDonald, MR, Boisson-Dupuis, S, Marr, N, Tangye, SG, Di Santo, JP, Zhang, Q, Zhang, S-Y, Rice, CM, Béziat, V, Lachmann, N, Langlais, D, Casanova, J-L, Gros, P & Bustamante, J 2023, 'Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria', Cell, vol. 186, no. 3, pp. 621-645.e33. https://doi.org/10.1016/j.cell.2022.12.038

TY - JOUR

T1 - Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria

AU - Rosain, Jérémie

AU - Neehus, Anna-Lena

AU - Manry, Jérémy

AU - Yang, Rui

AU - Le Pen, Jérémie

AU - Daher, Wassim

AU - Liu, Zhiyong

AU - Chan, Yi-Hao

AU - Tahuil, Natalia

AU - Türel, Özden

AU - Bourgey, Mathieu

AU - Ogishi, Masato

AU - Doisne, Jean-Marc

AU - Izquierdo, Helena M

AU - Shirasaki, Takayoshi

AU - Le Voyer, Tom

AU - Guérin, Antoine

AU - Bastard, Paul

AU - Moncada-Vélez, Marcela

AU - Han, Ji Eun

AU - Khan, Taushif

AU - Rapaport, Franck

AU - Hong, Seon-Hui

AU - Cheung, Andrew

AU - Haake, Kathrin

AU - Mindt, Barbara C

AU - Pérez, Laura

AU - Philippot, Quentin

AU - Lee, Danyel

AU - Zhang, Peng

AU - Rinchai, Darawan

AU - Al Ali, Fatima

AU - Ahmad Ata, Manar Mahmoud

AU - Rahman, Mahbuba

AU - Peel, Jessica N

AU - Heissel, Søren

AU - Molina, Henrik

AU - Kendir-Demirkol, Yasemin

AU - Bailey, Rasheed

AU - Zhao, Shuxiang

AU - Bohlen, Jonathan

AU - Seeleuthner, Yoann

AU - Roelens, Marie

AU - Lorenzo, Lazaro

AU - Soudée, Camille

AU - Paz, María Elvira Josefina

AU - González, María Laura

AU - Jeljeli, Mohamed

AU - Soulier, Jean

AU - Romana, Serge

AU - L'Honneur, Anne-Sophie

AU - Materna, Marie

AU - Martínez-Barricarte, Rubén

AU - Pochon, Mathieu

AU - Oleaga-Quintas, Carmen

AU - Michev, Alexandre

AU - Migaud, Mélanie

AU - Lévy, Romain

AU - Alyanakian, Marie-Alexandra

AU - Rozenberg, Flore

AU - Croft, Carys A

AU - Vogt, Guillaume

AU - Emile, Jean-François

AU - Kremer, Laurent

AU - Ma, Cindy S

AU - Fritz, Jörg H

AU - Lemon, Stanley M

AU - Spaan, András N

AU - Manel, Nicolas

AU - Abel, Laurent

AU - MacDonald, Margaret R

AU - Boisson-Dupuis, Stéphanie

AU - Marr, Nico

AU - Tangye, Stuart G

AU - Di Santo, James P

AU - Zhang, Qian

AU - Zhang, Shen-Ying

AU - Rice, Charles M

AU - Béziat, Vivien

AU - Lachmann, Nico

AU - Langlais, David

AU - Casanova, Jean-Laurent

AU - Gros, Philippe

AU - Bustamante, Jacinta

PY - 2023/2/2

Y1 - 2023/2/2

N2 - 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.

AB - 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.

KW - COVID-19

KW - Child

KW - Humans

KW - Interferon Regulatory Factor-1

KW - Interferon-alpha

KW - Interferon-gamma

KW - Mycobacterium

KW - SARS-CoV-2

UR - http://www.scopus.com/inward/record.url?scp=85147121641&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2022.12.038

DO - 10.1016/j.cell.2022.12.038

M3 - Article

C2 - 36736301

SN - 0092-8674

VL - 186

SP - 621-645.e33

JO - Cell

JF - Cell

IS - 3

ER -

Human IRF1 governs macrophagic IFN-γ immunity to mycobacteria

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