Human T-bet Governs Innate and Innate-like Adaptive IFN-γ Immunity against Mycobacteria

Rui Yang; Federico Mele; Lisa Worley; David Langlais; Jérémie Rosain; Ibithal Benhsaien; Houda Elarabi; Carys A. Croft; Jean Marc Doisne; Peng Zhang; Marc Weisshaar; David Jarrossay; Daniela Latorre; Yichao Shen; Jing Han; Masato Ogishi; Conor Gruber; Janet Markle; Fatima Al Ali; Mahbuba Rahman; Taushif Khan; Yoann Seeleuthner; Gaspard Kerner; Lucas T. Husquin; Julia L. Maclsaac; Mohamed Jeljeli; Abderrahmane Errami; Fatima Ailal; Michael S. Kobor; Carmen Oleaga-Quintas; Manon Roynard; Mathieu Bourgey; Jamila El Baghdadi; Stéphanie Boisson-Dupuis; Anne Puel; Fréderic Batteux; Flore Rozenberg; Nico Marr; Qiang Pan-Hammarström; Dusan Bogunovic; Lluis Quintana-Murci; Thomas Carroll; Cindy S. Ma; Laurent Abel; Aziz Bousfiha; James P. Di Santo; Laurie H. Glimcher; Philippe Gros; Stuart G. Tangye; Federica Sallusto; Jacinta Bustamante; Jean Laurent Casanova

doi:10.1016/j.cell.2020.10.046

Human T-bet Governs Innate and Innate-like Adaptive IFN-γ Immunity against Mycobacteria

Rui Yang, Federico Mele, Lisa Worley, David Langlais, Jérémie Rosain, Ibithal Benhsaien, Houda Elarabi, Carys A. Croft, Jean Marc Doisne, Peng Zhang, Marc Weisshaar, David Jarrossay, Daniela Latorre, Yichao Shen, Jing Han, Masato Ogishi, Conor Gruber, Janet Markle, Fatima Al Ali, Mahbuba RahmanTaushif Khan, Yoann Seeleuthner, Gaspard Kerner, Lucas T. Husquin, Julia L. Maclsaac, Mohamed Jeljeli, Abderrahmane Errami, Fatima Ailal, Michael S. Kobor, Carmen Oleaga-Quintas, Manon Roynard, Mathieu Bourgey, Jamila El Baghdadi, Stéphanie Boisson-Dupuis, Anne Puel, Fréderic Batteux, Flore Rozenberg, Nico Marr, Qiang Pan-Hammarström, Dusan Bogunovic, Lluis Quintana-Murci, Thomas Carroll, Cindy S. Ma, Laurent Abel, Aziz Bousfiha, James P. Di Santo, Laurie H. Glimcher, Philippe Gros, Stuart G. Tangye, Federica Sallusto, Jacinta Bustamante, Jean Laurent Casanova

Bloomberg School of Public Health

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

Abstract

Inborn errors of human interferon gamma (IFN-γ) immunity underlie mycobacterial disease. We report a patient with mycobacterial disease due to inherited deficiency of the transcription factor T-bet. The patient has extremely low counts of circulating Mycobacterium-reactive natural killer (NK), invariant NKT (iNKT), mucosal-associated invariant T (MAIT), and Vδ2⁺ γδ T lymphocytes, and of Mycobacterium-non reactive classic T_H1 lymphocytes, with the residual populations of these cells also producing abnormally small amounts of IFN-γ. Other lymphocyte subsets develop normally but produce low levels of IFN-γ, with the exception of CD8⁺ αβ T and non-classic CD4⁺ αβ T_H1^∗ lymphocytes, which produce IFN-γ normally in response to mycobacterial antigens. Human T-bet deficiency thus underlies mycobacterial disease by preventing the development of innate (NK) and innate-like adaptive lymphocytes (iNKT, MAIT, and Vδ2⁺ γδ T cells) and IFN-γ production by them, with mycobacterium-specific, IFN-γ-producing, purely adaptive CD8⁺ αβ T, and CD4⁺ αβ T_H1^∗ cells unable to compensate for this deficit.

Original language	English (US)
Pages (from-to)	1826-1847.e31
Journal	Cell
Volume	183
Issue number	7
DOIs	https://doi.org/10.1016/j.cell.2020.10.046
State	Published - Dec 23 2020

Keywords

IFN-γ
Mendelian susceptibility to mycobacterial disease
T-bet
immunodeficiency
inborn errors of immunity
innate lymphocyte
innate-like adaptive lymphocyte
mycobacterium

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2020.10.046

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Yang, R., Mele, F., Worley, L., Langlais, D., Rosain, J., Benhsaien, I., Elarabi, H., Croft, C. A., Doisne, J. M., Zhang, P., Weisshaar, M., Jarrossay, D., Latorre, D., Shen, Y., Han, J., Ogishi, M., Gruber, C., Markle, J., Al Ali, F., ... Casanova, J. L. (2020). Human T-bet Governs Innate and Innate-like Adaptive IFN-γ Immunity against Mycobacteria. Cell, 183(7), 1826-1847.e31. https://doi.org/10.1016/j.cell.2020.10.046

Yang, R, Mele, F, Worley, L, Langlais, D, Rosain, J, Benhsaien, I, Elarabi, H, Croft, CA, Doisne, JM, Zhang, P, Weisshaar, M, Jarrossay, D, Latorre, D, Shen, Y, Han, J, Ogishi, M, Gruber, C, Markle, J, Al Ali, F, Rahman, M, Khan, T, Seeleuthner, Y, Kerner, G, Husquin, LT, Maclsaac, JL, Jeljeli, M, Errami, A, Ailal, F, Kobor, MS, Oleaga-Quintas, C, Roynard, M, Bourgey, M, El Baghdadi, J, Boisson-Dupuis, S, Puel, A, Batteux, F, Rozenberg, F, Marr, N, Pan-Hammarström, Q, Bogunovic, D, Quintana-Murci, L, Carroll, T, Ma, CS, Abel, L, Bousfiha, A, Di Santo, JP, Glimcher, LH, Gros, P, Tangye, SG, Sallusto, F, Bustamante, J & Casanova, JL 2020, 'Human T-bet Governs Innate and Innate-like Adaptive IFN-γ Immunity against Mycobacteria', Cell, vol. 183, no. 7, pp. 1826-1847.e31. https://doi.org/10.1016/j.cell.2020.10.046

@article{65d4f4ac417a47caa6e5fcd26ba25ea3,

title = "Human T-bet Governs Innate and Innate-like Adaptive IFN-γ Immunity against Mycobacteria",

abstract = "Inborn errors of human interferon gamma (IFN-γ) immunity underlie mycobacterial disease. We report a patient with mycobacterial disease due to inherited deficiency of the transcription factor T-bet. The patient has extremely low counts of circulating Mycobacterium-reactive natural killer (NK), invariant NKT (iNKT), mucosal-associated invariant T (MAIT), and Vδ2+ γδ T lymphocytes, and of Mycobacterium-non reactive classic TH1 lymphocytes, with the residual populations of these cells also producing abnormally small amounts of IFN-γ. Other lymphocyte subsets develop normally but produce low levels of IFN-γ, with the exception of CD8+ αβ T and non-classic CD4+ αβ TH1∗ lymphocytes, which produce IFN-γ normally in response to mycobacterial antigens. Human T-bet deficiency thus underlies mycobacterial disease by preventing the development of innate (NK) and innate-like adaptive lymphocytes (iNKT, MAIT, and Vδ2+ γδ T cells) and IFN-γ production by them, with mycobacterium-specific, IFN-γ-producing, purely adaptive CD8+ αβ T, and CD4+ αβ TH1∗ cells unable to compensate for this deficit.",

keywords = "IFN-γ, Mendelian susceptibility to mycobacterial disease, T-bet, immunodeficiency, inborn errors of immunity, innate lymphocyte, innate-like adaptive lymphocyte, mycobacterium",

author = "Rui Yang and Federico Mele and Lisa Worley and David Langlais and J{\'e}r{\'e}mie Rosain and Ibithal Benhsaien and Houda Elarabi and Croft, {Carys A.} and Doisne, {Jean Marc} and Peng Zhang and Marc Weisshaar and David Jarrossay and Daniela Latorre and Yichao Shen and Jing Han and Masato Ogishi and Conor Gruber and Janet Markle and {Al Ali}, Fatima and Mahbuba Rahman and Taushif Khan and Yoann Seeleuthner and Gaspard Kerner and Husquin, {Lucas T.} and Maclsaac, {Julia L.} and Mohamed Jeljeli and Abderrahmane Errami and Fatima Ailal and Kobor, {Michael S.} and Carmen Oleaga-Quintas and Manon Roynard and Mathieu Bourgey and {El Baghdadi}, Jamila and St{\'e}phanie Boisson-Dupuis and Anne Puel and Fr{\'e}deric Batteux and Flore Rozenberg and Nico Marr and Qiang Pan-Hammarstr{\"o}m and Dusan Bogunovic and Lluis Quintana-Murci and Thomas Carroll and Ma, {Cindy S.} and Laurent Abel and Aziz Bousfiha and {Di Santo}, {James P.} and Glimcher, {Laurie H.} and Philippe Gros and Tangye, {Stuart G.} and Federica Sallusto and Jacinta Bustamante and Casanova, {Jean Laurent}",

note = "Publisher Copyright: {\textcopyright} 2020 Elsevier Inc.",

year = "2020",

month = dec,

day = "23",

doi = "10.1016/j.cell.2020.10.046",

language = "English (US)",

volume = "183",

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T1 - Human T-bet Governs Innate and Innate-like Adaptive IFN-γ Immunity against Mycobacteria

AU - Yang, Rui

AU - Mele, Federico

AU - Worley, Lisa

AU - Langlais, David

AU - Rosain, Jérémie

AU - Benhsaien, Ibithal

AU - Elarabi, Houda

AU - Croft, Carys A.

AU - Doisne, Jean Marc

AU - Zhang, Peng

AU - Weisshaar, Marc

AU - Jarrossay, David

AU - Latorre, Daniela

AU - Shen, Yichao

AU - Han, Jing

AU - Ogishi, Masato

AU - Gruber, Conor

AU - Markle, Janet

AU - Al Ali, Fatima

AU - Rahman, Mahbuba

AU - Khan, Taushif

AU - Seeleuthner, Yoann

AU - Kerner, Gaspard

AU - Husquin, Lucas T.

AU - Maclsaac, Julia L.

AU - Jeljeli, Mohamed

AU - Errami, Abderrahmane

AU - Ailal, Fatima

AU - Kobor, Michael S.

AU - Oleaga-Quintas, Carmen

AU - Roynard, Manon

AU - Bourgey, Mathieu

AU - El Baghdadi, Jamila

AU - Boisson-Dupuis, Stéphanie

AU - Puel, Anne

AU - Batteux, Fréderic

AU - Rozenberg, Flore

AU - Marr, Nico

AU - Pan-Hammarström, Qiang

AU - Bogunovic, Dusan

AU - Quintana-Murci, Lluis

AU - Carroll, Thomas

AU - Ma, Cindy S.

AU - Abel, Laurent

AU - Bousfiha, Aziz

AU - Di Santo, James P.

AU - Glimcher, Laurie H.

AU - Gros, Philippe

AU - Tangye, Stuart G.

AU - Sallusto, Federica

AU - Bustamante, Jacinta

AU - Casanova, Jean Laurent

PY - 2020/12/23

Y1 - 2020/12/23

N2 - Inborn errors of human interferon gamma (IFN-γ) immunity underlie mycobacterial disease. We report a patient with mycobacterial disease due to inherited deficiency of the transcription factor T-bet. The patient has extremely low counts of circulating Mycobacterium-reactive natural killer (NK), invariant NKT (iNKT), mucosal-associated invariant T (MAIT), and Vδ2+ γδ T lymphocytes, and of Mycobacterium-non reactive classic TH1 lymphocytes, with the residual populations of these cells also producing abnormally small amounts of IFN-γ. Other lymphocyte subsets develop normally but produce low levels of IFN-γ, with the exception of CD8+ αβ T and non-classic CD4+ αβ TH1∗ lymphocytes, which produce IFN-γ normally in response to mycobacterial antigens. Human T-bet deficiency thus underlies mycobacterial disease by preventing the development of innate (NK) and innate-like adaptive lymphocytes (iNKT, MAIT, and Vδ2+ γδ T cells) and IFN-γ production by them, with mycobacterium-specific, IFN-γ-producing, purely adaptive CD8+ αβ T, and CD4+ αβ TH1∗ cells unable to compensate for this deficit.

AB - Inborn errors of human interferon gamma (IFN-γ) immunity underlie mycobacterial disease. We report a patient with mycobacterial disease due to inherited deficiency of the transcription factor T-bet. The patient has extremely low counts of circulating Mycobacterium-reactive natural killer (NK), invariant NKT (iNKT), mucosal-associated invariant T (MAIT), and Vδ2+ γδ T lymphocytes, and of Mycobacterium-non reactive classic TH1 lymphocytes, with the residual populations of these cells also producing abnormally small amounts of IFN-γ. Other lymphocyte subsets develop normally but produce low levels of IFN-γ, with the exception of CD8+ αβ T and non-classic CD4+ αβ TH1∗ lymphocytes, which produce IFN-γ normally in response to mycobacterial antigens. Human T-bet deficiency thus underlies mycobacterial disease by preventing the development of innate (NK) and innate-like adaptive lymphocytes (iNKT, MAIT, and Vδ2+ γδ T cells) and IFN-γ production by them, with mycobacterium-specific, IFN-γ-producing, purely adaptive CD8+ αβ T, and CD4+ αβ TH1∗ cells unable to compensate for this deficit.

KW - IFN-γ

KW - Mendelian susceptibility to mycobacterial disease

KW - T-bet

KW - immunodeficiency

KW - inborn errors of immunity

KW - innate lymphocyte

KW - innate-like adaptive lymphocyte

KW - mycobacterium

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DO - 10.1016/j.cell.2020.10.046

M3 - Article

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AN - SCOPUS:85097895677

SN - 0092-8674

VL - 183

SP - 1826-1847.e31

JO - Cell

JF - Cell

IS - 7

ER -

Human T-bet Governs Innate and Innate-like Adaptive IFN-γ Immunity against Mycobacteria

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