Human MCTS1-dependent translation of JAK2 is essential for IFN-γ immunity to mycobacteria

<p>Human inherited disorders of interferon-gamma (IFN-γ) immunity underlie severe mycobacterial diseases. We report X-linked recessive MCTS1 deficiency in men with mycobacterial disease from kindreds of different ancestries (from China, Finland, Iran, and Saudi Arabia). Complete deficiency of...

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Main Author: Jonathan Bohlen (5368448) (author)
Other Authors: Qinhua Zhou (8913419) (author), Quentin Philippot (558140) (author), Masato Ogishi (699705) (author), Darawan Rinchai (742366) (author), Tea Nieminen (19483375) (author), Simin Seyedpour (19342675) (author), Nima Parvaneh (353296) (author), Nima Rezaei (783910) (author), Niloufar Yazdanpanah (16941574) (author), Mana Momenilandi (18602914) (author), Clément Conil (19483378) (author), Anna-Lena Neehus (9320912) (author), Carltin Schmidt (19483381) (author), Carlos A. Arango-Franco (19342654) (author), Tom Le Voyer (19483384) (author), Taushif Khan (691254) (author), Rui Yang (293531) (author), Julia Puchan (19483387) (author), Lucia Erazo (19483390) (author), Mykola Roiuk (19483393) (author), Taja Vatovec (19483396) (author), Zarah Janda (19483399) (author), Ivan Bagarić (19483402) (author), Marie Materna (18387156) (author), Adrian Gervais (12967488) (author), Hailun Li (14896062) (author), Jérémie Rosain (5900399) (author), Jessica N Peel (19483405) (author), Yoann Seeleuthner (10232517) (author), Ji Eun Han (18519936) (author), Anne-Sophie L’Honneur (5451995) (author), Marcela Moncada-Vélez (19483408) (author), Marta Martin-Fernandez (12295293) (author), Michael E. Horesh (19483411) (author), Tatiana Kochetkov (14979483) (author), Monika Schmidt (4475023) (author), Mohammed A. AlShehri (19483414) (author), Eeva Salo (13972749) (author), Harri Saxen (822923) (author), Gehad ElGhazali (9711154) (author), Ahmad Yatim (407443) (author), Camille Soudée (19342519) (author), Federica Sallusto (75054) (author), Armin Ensser (173680) (author), Nico Marr (349853) (author), Peng Zhang (2071) (author), Dusan Bogunovic (9340037) (author), Aurélie Cobat (2160433) (author), Mohammad Shahrooei (847633) (author), Vivien Béziat (204259) (author), Laurent Abel (69833) (author), Xiaochuan Wang (550306) (author), Stéphanie Boisson-Dupuis (64693) (author), Aurelio A. Teleman (12453273) (author), Jacinta Bustamante (64702) (author), Qian Zhang (49333) (author), Jean-Laurent Casanova (64712) (author)
Published: 2023
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_version_ 1864513507046719488
author Jonathan Bohlen (5368448)
author2 Qinhua Zhou (8913419)
Quentin Philippot (558140)
Masato Ogishi (699705)
Darawan Rinchai (742366)
Tea Nieminen (19483375)
Simin Seyedpour (19342675)
Nima Parvaneh (353296)
Nima Rezaei (783910)
Niloufar Yazdanpanah (16941574)
Mana Momenilandi (18602914)
Clément Conil (19483378)
Anna-Lena Neehus (9320912)
Carltin Schmidt (19483381)
Carlos A. Arango-Franco (19342654)
Tom Le Voyer (19483384)
Taushif Khan (691254)
Rui Yang (293531)
Julia Puchan (19483387)
Lucia Erazo (19483390)
Mykola Roiuk (19483393)
Taja Vatovec (19483396)
Zarah Janda (19483399)
Ivan Bagarić (19483402)
Marie Materna (18387156)
Adrian Gervais (12967488)
Hailun Li (14896062)
Jérémie Rosain (5900399)
Jessica N Peel (19483405)
Yoann Seeleuthner (10232517)
Ji Eun Han (18519936)
Anne-Sophie L’Honneur (5451995)
Marcela Moncada-Vélez (19483408)
Marta Martin-Fernandez (12295293)
Michael E. Horesh (19483411)
Tatiana Kochetkov (14979483)
Monika Schmidt (4475023)
Mohammed A. AlShehri (19483414)
Eeva Salo (13972749)
Harri Saxen (822923)
Gehad ElGhazali (9711154)
Ahmad Yatim (407443)
Camille Soudée (19342519)
Federica Sallusto (75054)
Armin Ensser (173680)
Nico Marr (349853)
Peng Zhang (2071)
Dusan Bogunovic (9340037)
Aurélie Cobat (2160433)
Mohammad Shahrooei (847633)
Vivien Béziat (204259)
Laurent Abel (69833)
Xiaochuan Wang (550306)
Stéphanie Boisson-Dupuis (64693)
Aurelio A. Teleman (12453273)
Jacinta Bustamante (64702)
Qian Zhang (49333)
Jean-Laurent Casanova (64712)
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author_facet Jonathan Bohlen (5368448)
Qinhua Zhou (8913419)
Quentin Philippot (558140)
Masato Ogishi (699705)
Darawan Rinchai (742366)
Tea Nieminen (19483375)
Simin Seyedpour (19342675)
Nima Parvaneh (353296)
Nima Rezaei (783910)
Niloufar Yazdanpanah (16941574)
Mana Momenilandi (18602914)
Clément Conil (19483378)
Anna-Lena Neehus (9320912)
Carltin Schmidt (19483381)
Carlos A. Arango-Franco (19342654)
Tom Le Voyer (19483384)
Taushif Khan (691254)
Rui Yang (293531)
Julia Puchan (19483387)
Lucia Erazo (19483390)
Mykola Roiuk (19483393)
Taja Vatovec (19483396)
Zarah Janda (19483399)
Ivan Bagarić (19483402)
Marie Materna (18387156)
Adrian Gervais (12967488)
Hailun Li (14896062)
Jérémie Rosain (5900399)
Jessica N Peel (19483405)
Yoann Seeleuthner (10232517)
Ji Eun Han (18519936)
Anne-Sophie L’Honneur (5451995)
Marcela Moncada-Vélez (19483408)
Marta Martin-Fernandez (12295293)
Michael E. Horesh (19483411)
Tatiana Kochetkov (14979483)
Monika Schmidt (4475023)
Mohammed A. AlShehri (19483414)
Eeva Salo (13972749)
Harri Saxen (822923)
Gehad ElGhazali (9711154)
Ahmad Yatim (407443)
Camille Soudée (19342519)
Federica Sallusto (75054)
Armin Ensser (173680)
Nico Marr (349853)
Peng Zhang (2071)
Dusan Bogunovic (9340037)
Aurélie Cobat (2160433)
Mohammad Shahrooei (847633)
Vivien Béziat (204259)
Laurent Abel (69833)
Xiaochuan Wang (550306)
Stéphanie Boisson-Dupuis (64693)
Aurelio A. Teleman (12453273)
Jacinta Bustamante (64702)
Qian Zhang (49333)
Jean-Laurent Casanova (64712)
author_role author
dc.creator.none.fl_str_mv Jonathan Bohlen (5368448)
Qinhua Zhou (8913419)
Quentin Philippot (558140)
Masato Ogishi (699705)
Darawan Rinchai (742366)
Tea Nieminen (19483375)
Simin Seyedpour (19342675)
Nima Parvaneh (353296)
Nima Rezaei (783910)
Niloufar Yazdanpanah (16941574)
Mana Momenilandi (18602914)
Clément Conil (19483378)
Anna-Lena Neehus (9320912)
Carltin Schmidt (19483381)
Carlos A. Arango-Franco (19342654)
Tom Le Voyer (19483384)
Taushif Khan (691254)
Rui Yang (293531)
Julia Puchan (19483387)
Lucia Erazo (19483390)
Mykola Roiuk (19483393)
Taja Vatovec (19483396)
Zarah Janda (19483399)
Ivan Bagarić (19483402)
Marie Materna (18387156)
Adrian Gervais (12967488)
Hailun Li (14896062)
Jérémie Rosain (5900399)
Jessica N Peel (19483405)
Yoann Seeleuthner (10232517)
Ji Eun Han (18519936)
Anne-Sophie L’Honneur (5451995)
Marcela Moncada-Vélez (19483408)
Marta Martin-Fernandez (12295293)
Michael E. Horesh (19483411)
Tatiana Kochetkov (14979483)
Monika Schmidt (4475023)
Mohammed A. AlShehri (19483414)
Eeva Salo (13972749)
Harri Saxen (822923)
Gehad ElGhazali (9711154)
Ahmad Yatim (407443)
Camille Soudée (19342519)
Federica Sallusto (75054)
Armin Ensser (173680)
Nico Marr (349853)
Peng Zhang (2071)
Dusan Bogunovic (9340037)
Aurélie Cobat (2160433)
Mohammad Shahrooei (847633)
Vivien Béziat (204259)
Laurent Abel (69833)
Xiaochuan Wang (550306)
Stéphanie Boisson-Dupuis (64693)
Aurelio A. Teleman (12453273)
Jacinta Bustamante (64702)
Qian Zhang (49333)
Jean-Laurent Casanova (64712)
dc.date.none.fl_str_mv 2023-10-23T15:00:00Z
dc.identifier.none.fl_str_mv 10.1016/j.cell.2023.09.024
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/Human_MCTS1-dependent_translation_of_JAK2_is_essential_for_IFN-_immunity_to_mycobacteria/26831107
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biological sciences
Biochemistry and cell biology
Genetics
Biomedical and clinical sciences
Clinical sciences
Immunology
MCTS1
translation re-initiation
JAK2IL-23
mycobacterium
MSMD
inborn error of immunity
X-linked disease
dc.title.none.fl_str_mv Human MCTS1-dependent translation of JAK2 is essential for 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>Human inherited disorders of interferon-gamma (IFN-γ) immunity underlie severe mycobacterial diseases. We report X-linked recessive MCTS1 deficiency in men with mycobacterial disease from kindreds of different ancestries (from China, Finland, Iran, and Saudi Arabia). Complete deficiency of this translation re-initiation factor impairs the translation of a subset of proteins, including the kinase JAK2 in all cell types tested, including T lymphocytes and phagocytes. JAK2 expression is sufficiently low to impair cellular responses to interleukin-23 (IL-23) and partially IL-12, but not other JAK2-dependent cytokines. Defective responses to IL-23 preferentially impair the production of IFN-γ by innate-like adaptive mucosal-associated invariant T cells (MAIT) and γδ T lymphocytes upon mycobacterial challenge. Surprisingly, the lack of MCTS1-dependent translation re-initiation and ribosome recycling seems to be otherwise physiologically redundant in these patients. These findings suggest that X-linked recessive human MCTS1 deficiency underlies isolated mycobacterial disease by impairing JAK2 translation in innate-like adaptive T lymphocytes, thereby impairing the IL-23-dependent induction of IFN-γ.</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.2023.09.024" target="_blank">https://dx.doi.org/10.1016/j.cell.2023.09.024</a></p>
eu_rights_str_mv openAccess
id Manara2_018de5fbff4536efca2484cb0ebf7aa1
identifier_str_mv 10.1016/j.cell.2023.09.024
network_acronym_str Manara2
network_name_str Manara2
oai_identifier_str oai:figshare.com:article/26831107
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 MCTS1-dependent translation of JAK2 is essential for IFN-γ immunity to mycobacteriaJonathan Bohlen (5368448)Qinhua Zhou (8913419)Quentin Philippot (558140)Masato Ogishi (699705)Darawan Rinchai (742366)Tea Nieminen (19483375)Simin Seyedpour (19342675)Nima Parvaneh (353296)Nima Rezaei (783910)Niloufar Yazdanpanah (16941574)Mana Momenilandi (18602914)Clément Conil (19483378)Anna-Lena Neehus (9320912)Carltin Schmidt (19483381)Carlos A. Arango-Franco (19342654)Tom Le Voyer (19483384)Taushif Khan (691254)Rui Yang (293531)Julia Puchan (19483387)Lucia Erazo (19483390)Mykola Roiuk (19483393)Taja Vatovec (19483396)Zarah Janda (19483399)Ivan Bagarić (19483402)Marie Materna (18387156)Adrian Gervais (12967488)Hailun Li (14896062)Jérémie Rosain (5900399)Jessica N Peel (19483405)Yoann Seeleuthner (10232517)Ji Eun Han (18519936)Anne-Sophie L’Honneur (5451995)Marcela Moncada-Vélez (19483408)Marta Martin-Fernandez (12295293)Michael E. Horesh (19483411)Tatiana Kochetkov (14979483)Monika Schmidt (4475023)Mohammed A. AlShehri (19483414)Eeva Salo (13972749)Harri Saxen (822923)Gehad ElGhazali (9711154)Ahmad Yatim (407443)Camille Soudée (19342519)Federica Sallusto (75054)Armin Ensser (173680)Nico Marr (349853)Peng Zhang (2071)Dusan Bogunovic (9340037)Aurélie Cobat (2160433)Mohammad Shahrooei (847633)Vivien Béziat (204259)Laurent Abel (69833)Xiaochuan Wang (550306)Stéphanie Boisson-Dupuis (64693)Aurelio A. Teleman (12453273)Jacinta Bustamante (64702)Qian Zhang (49333)Jean-Laurent Casanova (64712)Biological sciencesBiochemistry and cell biologyGeneticsBiomedical and clinical sciencesClinical sciencesImmunologyMCTS1translation re-initiationJAK2IL-23mycobacteriumMSMDinborn error of immunityX-linked disease<p>Human inherited disorders of interferon-gamma (IFN-γ) immunity underlie severe mycobacterial diseases. We report X-linked recessive MCTS1 deficiency in men with mycobacterial disease from kindreds of different ancestries (from China, Finland, Iran, and Saudi Arabia). Complete deficiency of this translation re-initiation factor impairs the translation of a subset of proteins, including the kinase JAK2 in all cell types tested, including T lymphocytes and phagocytes. JAK2 expression is sufficiently low to impair cellular responses to interleukin-23 (IL-23) and partially IL-12, but not other JAK2-dependent cytokines. Defective responses to IL-23 preferentially impair the production of IFN-γ by innate-like adaptive mucosal-associated invariant T cells (MAIT) and γδ T lymphocytes upon mycobacterial challenge. Surprisingly, the lack of MCTS1-dependent translation re-initiation and ribosome recycling seems to be otherwise physiologically redundant in these patients. These findings suggest that X-linked recessive human MCTS1 deficiency underlies isolated mycobacterial disease by impairing JAK2 translation in innate-like adaptive T lymphocytes, thereby impairing the IL-23-dependent induction of IFN-γ.</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.2023.09.024" target="_blank">https://dx.doi.org/10.1016/j.cell.2023.09.024</a></p>2023-10-23T15:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1016/j.cell.2023.09.024https://figshare.com/articles/journal_contribution/Human_MCTS1-dependent_translation_of_JAK2_is_essential_for_IFN-_immunity_to_mycobacteria/26831107CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/268311072023-10-23T15:00:00Z
spellingShingle Human MCTS1-dependent translation of JAK2 is essential for IFN-γ immunity to mycobacteria
Jonathan Bohlen (5368448)
Biological sciences
Biochemistry and cell biology
Genetics
Biomedical and clinical sciences
Clinical sciences
Immunology
MCTS1
translation re-initiation
JAK2IL-23
mycobacterium
MSMD
inborn error of immunity
X-linked disease
status_str publishedVersion
title Human MCTS1-dependent translation of JAK2 is essential for IFN-γ immunity to mycobacteria
title_full Human MCTS1-dependent translation of JAK2 is essential for IFN-γ immunity to mycobacteria
title_fullStr Human MCTS1-dependent translation of JAK2 is essential for IFN-γ immunity to mycobacteria
title_full_unstemmed Human MCTS1-dependent translation of JAK2 is essential for IFN-γ immunity to mycobacteria
title_short Human MCTS1-dependent translation of JAK2 is essential for IFN-γ immunity to mycobacteria
title_sort Human MCTS1-dependent translation of JAK2 is essential for IFN-γ immunity to mycobacteria
topic Biological sciences
Biochemistry and cell biology
Genetics
Biomedical and clinical sciences
Clinical sciences
Immunology
MCTS1
translation re-initiation
JAK2IL-23
mycobacterium
MSMD
inborn error of immunity
X-linked disease