Cargando…

Type 1 interferon suppresses expression and glucocorticoid induction of glucocorticoid-induced leucine zipper (GILZ)

SLE is a systemic multi-organ autoimmune condition associated with reduced life expectancy and quality of life. Glucocorticoids (GC) are heavily relied on for SLE treatment but are associated with detrimental metabolic effects. Type 1 interferons (IFN) are central to SLE pathogenesis and may confer...

Descripción completa

Detalles Bibliográficos
Autores principales: Dankers, Wendy, Northcott, Melissa, Bennett, Taylah, D’Cruz, Akshay, Sherlock, Rochelle, Gearing, Linden J., Hertzog, Paul, Russ, Brendan, Miceli, Iolanda, Scheer, Sebastian, Fujishiro, Maki, Hayakawa, Kunihiro, Ikeda, Keigo, Morand, Eric F., Jones, Sarah A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9727222/
https://www.ncbi.nlm.nih.gov/pubmed/36505447
http://dx.doi.org/10.3389/fimmu.2022.1034880
_version_ 1784844964307402752
author Dankers, Wendy
Northcott, Melissa
Bennett, Taylah
D’Cruz, Akshay
Sherlock, Rochelle
Gearing, Linden J.
Hertzog, Paul
Russ, Brendan
Miceli, Iolanda
Scheer, Sebastian
Fujishiro, Maki
Hayakawa, Kunihiro
Ikeda, Keigo
Morand, Eric F.
Jones, Sarah A.
author_facet Dankers, Wendy
Northcott, Melissa
Bennett, Taylah
D’Cruz, Akshay
Sherlock, Rochelle
Gearing, Linden J.
Hertzog, Paul
Russ, Brendan
Miceli, Iolanda
Scheer, Sebastian
Fujishiro, Maki
Hayakawa, Kunihiro
Ikeda, Keigo
Morand, Eric F.
Jones, Sarah A.
author_sort Dankers, Wendy
collection PubMed
description SLE is a systemic multi-organ autoimmune condition associated with reduced life expectancy and quality of life. Glucocorticoids (GC) are heavily relied on for SLE treatment but are associated with detrimental metabolic effects. Type 1 interferons (IFN) are central to SLE pathogenesis and may confer GC insensitivity. Glucocorticoid-induced leucine zipper (GILZ) mediates many effects of GC relevant to SLE pathogenesis, but the effect of IFN on GC regulation of GILZ is unknown. We performed in vitro experiments using human PBMC to examine the effect of IFN on GILZ expression. JAK inhibitors tofacitinib and tosylate salt were used in vivo and in vitro respectively to investigate JAK-STAT pathway dependence of our observations. ChiP was performed to examine glucocorticoid receptor (GR) binding at the GILZ locus. Several public data sets were mined for correlating clinical data. High IFN was associated with suppressed GILZ and reduced GILZ relevant to GC exposure in a large SLE population. IFN directly reduced GILZ expression and suppressed the induction of GILZ by GC in vitro in human leukocytes. IFN actions on GILZ expression were dependent on the JAK1/Tyk2 pathway, as evidenced by loss of the inhibitory effect of IFN on GILZ in the presence of JAK inhibitors. Activation of this pathway led to reduced GR binding in key regulatory regions of the GILZ locus. IFN directly suppresses GILZ expression and GILZ upregulation by GC, indicating a potential mechanism for IFN-induced GC resistance. This work has important implications for the ongoing development of targeted GC-sparing therapeutics in SLE.
format Online
Article
Text
id pubmed-9727222
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-97272222022-12-08 Type 1 interferon suppresses expression and glucocorticoid induction of glucocorticoid-induced leucine zipper (GILZ) Dankers, Wendy Northcott, Melissa Bennett, Taylah D’Cruz, Akshay Sherlock, Rochelle Gearing, Linden J. Hertzog, Paul Russ, Brendan Miceli, Iolanda Scheer, Sebastian Fujishiro, Maki Hayakawa, Kunihiro Ikeda, Keigo Morand, Eric F. Jones, Sarah A. Front Immunol Immunology SLE is a systemic multi-organ autoimmune condition associated with reduced life expectancy and quality of life. Glucocorticoids (GC) are heavily relied on for SLE treatment but are associated with detrimental metabolic effects. Type 1 interferons (IFN) are central to SLE pathogenesis and may confer GC insensitivity. Glucocorticoid-induced leucine zipper (GILZ) mediates many effects of GC relevant to SLE pathogenesis, but the effect of IFN on GC regulation of GILZ is unknown. We performed in vitro experiments using human PBMC to examine the effect of IFN on GILZ expression. JAK inhibitors tofacitinib and tosylate salt were used in vivo and in vitro respectively to investigate JAK-STAT pathway dependence of our observations. ChiP was performed to examine glucocorticoid receptor (GR) binding at the GILZ locus. Several public data sets were mined for correlating clinical data. High IFN was associated with suppressed GILZ and reduced GILZ relevant to GC exposure in a large SLE population. IFN directly reduced GILZ expression and suppressed the induction of GILZ by GC in vitro in human leukocytes. IFN actions on GILZ expression were dependent on the JAK1/Tyk2 pathway, as evidenced by loss of the inhibitory effect of IFN on GILZ in the presence of JAK inhibitors. Activation of this pathway led to reduced GR binding in key regulatory regions of the GILZ locus. IFN directly suppresses GILZ expression and GILZ upregulation by GC, indicating a potential mechanism for IFN-induced GC resistance. This work has important implications for the ongoing development of targeted GC-sparing therapeutics in SLE. Frontiers Media S.A. 2022-11-23 /pmc/articles/PMC9727222/ /pubmed/36505447 http://dx.doi.org/10.3389/fimmu.2022.1034880 Text en Copyright © 2022 Dankers, Northcott, Bennett, D’Cruz, Sherlock, Gearing, Hertzog, Russ, Miceli, Scheer, Fujishiro, Hayakawa, Ikeda, Morand and Jones https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Dankers, Wendy
Northcott, Melissa
Bennett, Taylah
D’Cruz, Akshay
Sherlock, Rochelle
Gearing, Linden J.
Hertzog, Paul
Russ, Brendan
Miceli, Iolanda
Scheer, Sebastian
Fujishiro, Maki
Hayakawa, Kunihiro
Ikeda, Keigo
Morand, Eric F.
Jones, Sarah A.
Type 1 interferon suppresses expression and glucocorticoid induction of glucocorticoid-induced leucine zipper (GILZ)
title Type 1 interferon suppresses expression and glucocorticoid induction of glucocorticoid-induced leucine zipper (GILZ)
title_full Type 1 interferon suppresses expression and glucocorticoid induction of glucocorticoid-induced leucine zipper (GILZ)
title_fullStr Type 1 interferon suppresses expression and glucocorticoid induction of glucocorticoid-induced leucine zipper (GILZ)
title_full_unstemmed Type 1 interferon suppresses expression and glucocorticoid induction of glucocorticoid-induced leucine zipper (GILZ)
title_short Type 1 interferon suppresses expression and glucocorticoid induction of glucocorticoid-induced leucine zipper (GILZ)
title_sort type 1 interferon suppresses expression and glucocorticoid induction of glucocorticoid-induced leucine zipper (gilz)
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9727222/
https://www.ncbi.nlm.nih.gov/pubmed/36505447
http://dx.doi.org/10.3389/fimmu.2022.1034880
work_keys_str_mv AT dankerswendy type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT northcottmelissa type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT bennetttaylah type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT dcruzakshay type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT sherlockrochelle type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT gearinglindenj type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT hertzogpaul type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT russbrendan type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT miceliiolanda type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT scheersebastian type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT fujishiromaki type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT hayakawakunihiro type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT ikedakeigo type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT morandericf type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz
AT jonessaraha type1interferonsuppressesexpressionandglucocorticoidinductionofglucocorticoidinducedleucinezippergilz