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The RNA editor ADAR2 promotes immune cell trafficking by enhancing endothelial responses to interleukin-6 during sterile inflammation

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The RNA editor ADAR2 promotes immune cell trafficking by enhancing endothelial responses to interleukin-6 during sterile inflammation. / Gatsiou, Aikaterini; Tual-Chalot, Simon; Napoli, Matteo et al.
In: Immunity, Vol. 56, No. 5, 09.05.2023, p. 979-997.e11.

Research output: Contribution to Journal/Magazine › Journal article › peer-review

Harvard

Gatsiou, A, Tual-Chalot, S, Napoli, M, Ortega-Gomez, A, Regen, T, Badolia, R, Cesarini, V, Garcia-Gonzalez, C, Chevre, R, Ciliberti, G, Silvestre-Roig, C, Martini, M, Hoffmann, J, Hamouche, R, Visker, JR, Diakos, N, Wietelmann, A, Silvestris, DA, Georgiopoulos, G, Moshfegh, A, Schneider, A, Chen, W, Guenther, S, Backs, J, Kwak, S, Selzman, CH, Stamatelopoulos, K, Rose-John, S, Trautwein, C, Spyridopoulos, I, Braun, T, Waisman, A, Gallo, A, Drakos, SG, Dimmeler, S, Sperandio, M, Soehnlein, O & Stellos, K 2023, 'The RNA editor ADAR2 promotes immune cell trafficking by enhancing endothelial responses to interleukin-6 during sterile inflammation', Immunity, vol. 56, no. 5, pp. 979-997.e11. https://doi.org/10.1016/j.immuni.2023.03.021

APA

Gatsiou, A., Tual-Chalot, S., Napoli, M., Ortega-Gomez, A., Regen, T., Badolia, R., Cesarini, V., Garcia-Gonzalez, C., Chevre, R., Ciliberti, G., Silvestre-Roig, C., Martini, M., Hoffmann, J., Hamouche, R., Visker, J. R., Diakos, N., Wietelmann, A., Silvestris, D. A., Georgiopoulos, G., ... Stellos, K. (2023). The RNA editor ADAR2 promotes immune cell trafficking by enhancing endothelial responses to interleukin-6 during sterile inflammation. Immunity, 56(5), 979-997.e11. https://doi.org/10.1016/j.immuni.2023.03.021

Vancouver

Gatsiou A, Tual-Chalot S, Napoli M, Ortega-Gomez A, Regen T, Badolia R et al. The RNA editor ADAR2 promotes immune cell trafficking by enhancing endothelial responses to interleukin-6 during sterile inflammation. Immunity. 2023 May 9;56(5):979-997.e11. doi: 10.1016/j.immuni.2023.03.021

Author

Gatsiou, Aikaterini ; Tual-Chalot, Simon ; Napoli, Matteo et al. / The RNA editor ADAR2 promotes immune cell trafficking by enhancing endothelial responses to interleukin-6 during sterile inflammation. In: Immunity. 2023 ; Vol. 56, No. 5. pp. 979-997.e11.

Bibtex

@article{1e060b8ade4345f8bb396be3866ceaae,
title = "The RNA editor ADAR2 promotes immune cell trafficking by enhancing endothelial responses to interleukin-6 during sterile inflammation",
abstract = "Immune cell trafficking constitutes a fundamental component of immunological response to tissue injury, but the contribution of intrinsic RNA nucleotide modifications to this response remains elusive. We report that RNA editor ADAR2 exerts a tissue- and stress-specific regulation of endothelial responses to interleukin-6 (IL-6), which tightly controls leukocyte trafficking in IL-6-inflamed and ischemic tissues. Genetic ablation of ADAR2 from vascular endothelial cells diminished myeloid cell rolling and adhesion on vascular walls and reduced immune cell infiltration within ischemic tissues. ADAR2 was required in the endothelium for the expression of the IL-6 receptor subunit, IL-6 signal transducer (IL6ST; gp130), and subsequently, for IL-6 trans-signaling responses. ADAR2-induced adenosine-to-inosine RNA editing suppressed the Drosha-dependent primary microRNA processing, thereby overwriting the default endothelial transcriptional program to safeguard gp130 expression. This work demonstrates a role for ADAR2 epitranscriptional activity as a checkpoint in IL-6 trans-signaling and immune cell trafficking to sites of tissue injury.",
keywords = "RNA, Interleukin-6, Endothelial Cells/metabolism, Cytokine Receptor gp130, Endothelium/metabolism, Adenosine Deaminase/genetics",
author = "Aikaterini Gatsiou and Simon Tual-Chalot and Matteo Napoli and Almudena Ortega-Gomez and Tommy Regen and Rachit Badolia and Valeriana Cesarini and Claudia Garcia-Gonzalez and Raphael Chevre and Giorgia Ciliberti and Carlos Silvestre-Roig and Maurizio Martini and Jedrzej Hoffmann and Rana Hamouche and Visker, {Joseph R} and Nikolaos Diakos and Astrid Wietelmann and Silvestris, {Domenico Alessandro} and Georgios Georgiopoulos and Ali Moshfegh and Andre Schneider and Wei Chen and Stefan Guenther and Johannes Backs and Shin Kwak and Selzman, {Craig H} and Kimon Stamatelopoulos and Stefan Rose-John and Christian Trautwein and Ioakim Spyridopoulos and Thomas Braun and Ari Waisman and Angela Gallo and Drakos, {Stavros G} and Stefanie Dimmeler and Markus Sperandio and Oliver Soehnlein and Konstantinos Stellos",
year = "2023",
month = may,
day = "9",
doi = "10.1016/j.immuni.2023.03.021",
language = "English",
volume = "56",
pages = "979--997.e11",
journal = "Immunity",
issn = "1074-7613",
publisher = "Cell Press",
number = "5",

}

RIS

TY - JOUR

T1 - The RNA editor ADAR2 promotes immune cell trafficking by enhancing endothelial responses to interleukin-6 during sterile inflammation

AU - Gatsiou, Aikaterini

AU - Tual-Chalot, Simon

AU - Napoli, Matteo

AU - Ortega-Gomez, Almudena

AU - Regen, Tommy

AU - Badolia, Rachit

AU - Cesarini, Valeriana

AU - Garcia-Gonzalez, Claudia

AU - Chevre, Raphael

AU - Ciliberti, Giorgia

AU - Silvestre-Roig, Carlos

AU - Martini, Maurizio

AU - Hoffmann, Jedrzej

AU - Hamouche, Rana

AU - Visker, Joseph R

AU - Diakos, Nikolaos

AU - Wietelmann, Astrid

AU - Silvestris, Domenico Alessandro

AU - Georgiopoulos, Georgios

AU - Moshfegh, Ali

AU - Schneider, Andre

AU - Chen, Wei

AU - Guenther, Stefan

AU - Backs, Johannes

AU - Kwak, Shin

AU - Selzman, Craig H

AU - Stamatelopoulos, Kimon

AU - Rose-John, Stefan

AU - Trautwein, Christian

AU - Spyridopoulos, Ioakim

AU - Braun, Thomas

AU - Waisman, Ari

AU - Gallo, Angela

AU - Drakos, Stavros G

AU - Dimmeler, Stefanie

AU - Sperandio, Markus

AU - Soehnlein, Oliver

AU - Stellos, Konstantinos

PY - 2023/5/9

Y1 - 2023/5/9

N2 - Immune cell trafficking constitutes a fundamental component of immunological response to tissue injury, but the contribution of intrinsic RNA nucleotide modifications to this response remains elusive. We report that RNA editor ADAR2 exerts a tissue- and stress-specific regulation of endothelial responses to interleukin-6 (IL-6), which tightly controls leukocyte trafficking in IL-6-inflamed and ischemic tissues. Genetic ablation of ADAR2 from vascular endothelial cells diminished myeloid cell rolling and adhesion on vascular walls and reduced immune cell infiltration within ischemic tissues. ADAR2 was required in the endothelium for the expression of the IL-6 receptor subunit, IL-6 signal transducer (IL6ST; gp130), and subsequently, for IL-6 trans-signaling responses. ADAR2-induced adenosine-to-inosine RNA editing suppressed the Drosha-dependent primary microRNA processing, thereby overwriting the default endothelial transcriptional program to safeguard gp130 expression. This work demonstrates a role for ADAR2 epitranscriptional activity as a checkpoint in IL-6 trans-signaling and immune cell trafficking to sites of tissue injury.

AB - Immune cell trafficking constitutes a fundamental component of immunological response to tissue injury, but the contribution of intrinsic RNA nucleotide modifications to this response remains elusive. We report that RNA editor ADAR2 exerts a tissue- and stress-specific regulation of endothelial responses to interleukin-6 (IL-6), which tightly controls leukocyte trafficking in IL-6-inflamed and ischemic tissues. Genetic ablation of ADAR2 from vascular endothelial cells diminished myeloid cell rolling and adhesion on vascular walls and reduced immune cell infiltration within ischemic tissues. ADAR2 was required in the endothelium for the expression of the IL-6 receptor subunit, IL-6 signal transducer (IL6ST; gp130), and subsequently, for IL-6 trans-signaling responses. ADAR2-induced adenosine-to-inosine RNA editing suppressed the Drosha-dependent primary microRNA processing, thereby overwriting the default endothelial transcriptional program to safeguard gp130 expression. This work demonstrates a role for ADAR2 epitranscriptional activity as a checkpoint in IL-6 trans-signaling and immune cell trafficking to sites of tissue injury.

KW - RNA

KW - Interleukin-6

KW - Endothelial Cells/metabolism

KW - Cytokine Receptor gp130

KW - Endothelium/metabolism

KW - Adenosine Deaminase/genetics

U2 - 10.1016/j.immuni.2023.03.021

DO - 10.1016/j.immuni.2023.03.021

M3 - Journal article

C2 - 37100060

VL - 56

SP - 979-997.e11

JO - Immunity

JF - Immunity

SN - 1074-7613

IS - 5

ER -