Cargando…

Sequential actions of EOMES and T-BET promote stepwise maturation of natural killer cells

EOMES and T-BET are related T-box transcription factors that control natural killer (NK) cell development. Here we demonstrate that EOMES and T-BET regulate largely distinct gene sets during this process. EOMES is dominantly expressed in immature NK cells and drives early lineage specification by in...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhang, Jiang, Le Gras, Stéphanie, Pouxvielh, Kevin, Faure, Fabrice, Fallone, Lucie, Kern, Nicolas, Moreews, Marion, Mathieu, Anne-Laure, Schneider, Raphaël, Marliac, Quentin, Jung, Mathieu, Berton, Aurore, Hayek, Simon, Vidalain, Pierre-Olivier, Marçais, Antoine, Dodard, Garvin, Dejean, Anne, Brossay, Laurent, Ghavi-Helm, Yad, Walzer, Thierry
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8440589/
https://www.ncbi.nlm.nih.gov/pubmed/34521844
http://dx.doi.org/10.1038/s41467-021-25758-2
_version_ 1783752708132438016
author Zhang, Jiang
Le Gras, Stéphanie
Pouxvielh, Kevin
Faure, Fabrice
Fallone, Lucie
Kern, Nicolas
Moreews, Marion
Mathieu, Anne-Laure
Schneider, Raphaël
Marliac, Quentin
Jung, Mathieu
Berton, Aurore
Hayek, Simon
Vidalain, Pierre-Olivier
Marçais, Antoine
Dodard, Garvin
Dejean, Anne
Brossay, Laurent
Ghavi-Helm, Yad
Walzer, Thierry
author_facet Zhang, Jiang
Le Gras, Stéphanie
Pouxvielh, Kevin
Faure, Fabrice
Fallone, Lucie
Kern, Nicolas
Moreews, Marion
Mathieu, Anne-Laure
Schneider, Raphaël
Marliac, Quentin
Jung, Mathieu
Berton, Aurore
Hayek, Simon
Vidalain, Pierre-Olivier
Marçais, Antoine
Dodard, Garvin
Dejean, Anne
Brossay, Laurent
Ghavi-Helm, Yad
Walzer, Thierry
author_sort Zhang, Jiang
collection PubMed
description EOMES and T-BET are related T-box transcription factors that control natural killer (NK) cell development. Here we demonstrate that EOMES and T-BET regulate largely distinct gene sets during this process. EOMES is dominantly expressed in immature NK cells and drives early lineage specification by inducing hallmark receptors and functions. By contrast, T-BET is dominant in mature NK cells, where it induces responsiveness to IL-12 and represses the cell cycle, likely through transcriptional repressors. Regardless, many genes with distinct functions are co-regulated by the two transcription factors. By generating two gene-modified mice facilitating chromatin immunoprecipitation of endogenous EOMES and T-BET, we show a strong overlap in their DNA binding targets, as well as extensive epigenetic changes during NK cell differentiation. Our data thus suggest that EOMES and T-BET may distinctly govern, via differential expression and co-factors recruitment, NK cell maturation by inserting partially overlapping epigenetic regulations.
format Online
Article
Text
id pubmed-8440589
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-84405892021-10-04 Sequential actions of EOMES and T-BET promote stepwise maturation of natural killer cells Zhang, Jiang Le Gras, Stéphanie Pouxvielh, Kevin Faure, Fabrice Fallone, Lucie Kern, Nicolas Moreews, Marion Mathieu, Anne-Laure Schneider, Raphaël Marliac, Quentin Jung, Mathieu Berton, Aurore Hayek, Simon Vidalain, Pierre-Olivier Marçais, Antoine Dodard, Garvin Dejean, Anne Brossay, Laurent Ghavi-Helm, Yad Walzer, Thierry Nat Commun Article EOMES and T-BET are related T-box transcription factors that control natural killer (NK) cell development. Here we demonstrate that EOMES and T-BET regulate largely distinct gene sets during this process. EOMES is dominantly expressed in immature NK cells and drives early lineage specification by inducing hallmark receptors and functions. By contrast, T-BET is dominant in mature NK cells, where it induces responsiveness to IL-12 and represses the cell cycle, likely through transcriptional repressors. Regardless, many genes with distinct functions are co-regulated by the two transcription factors. By generating two gene-modified mice facilitating chromatin immunoprecipitation of endogenous EOMES and T-BET, we show a strong overlap in their DNA binding targets, as well as extensive epigenetic changes during NK cell differentiation. Our data thus suggest that EOMES and T-BET may distinctly govern, via differential expression and co-factors recruitment, NK cell maturation by inserting partially overlapping epigenetic regulations. Nature Publishing Group UK 2021-09-14 /pmc/articles/PMC8440589/ /pubmed/34521844 http://dx.doi.org/10.1038/s41467-021-25758-2 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Zhang, Jiang
Le Gras, Stéphanie
Pouxvielh, Kevin
Faure, Fabrice
Fallone, Lucie
Kern, Nicolas
Moreews, Marion
Mathieu, Anne-Laure
Schneider, Raphaël
Marliac, Quentin
Jung, Mathieu
Berton, Aurore
Hayek, Simon
Vidalain, Pierre-Olivier
Marçais, Antoine
Dodard, Garvin
Dejean, Anne
Brossay, Laurent
Ghavi-Helm, Yad
Walzer, Thierry
Sequential actions of EOMES and T-BET promote stepwise maturation of natural killer cells
title Sequential actions of EOMES and T-BET promote stepwise maturation of natural killer cells
title_full Sequential actions of EOMES and T-BET promote stepwise maturation of natural killer cells
title_fullStr Sequential actions of EOMES and T-BET promote stepwise maturation of natural killer cells
title_full_unstemmed Sequential actions of EOMES and T-BET promote stepwise maturation of natural killer cells
title_short Sequential actions of EOMES and T-BET promote stepwise maturation of natural killer cells
title_sort sequential actions of eomes and t-bet promote stepwise maturation of natural killer cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8440589/
https://www.ncbi.nlm.nih.gov/pubmed/34521844
http://dx.doi.org/10.1038/s41467-021-25758-2
work_keys_str_mv AT zhangjiang sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT legrasstephanie sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT pouxvielhkevin sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT faurefabrice sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT fallonelucie sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT kernnicolas sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT moreewsmarion sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT mathieuannelaure sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT schneiderraphael sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT marliacquentin sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT jungmathieu sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT bertonaurore sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT hayeksimon sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT vidalainpierreolivier sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT marcaisantoine sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT dodardgarvin sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT dejeananne sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT brossaylaurent sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT ghavihelmyad sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells
AT walzerthierry sequentialactionsofeomesandtbetpromotestepwisematurationofnaturalkillercells