Cargando…

Salmonella effector SopF regulates PANoptosis of intestinal epithelial cells to aggravate systemic infection

SopF, a newly discovered effector secreted by Salmonella pathogenicity island-1 type III secretion system (T3SS1), was reported to target phosphoinositide on host cell membrane and aggravate systemic infection, while its functional relevance and underlying mechanisms have yet to be elucidated. PANop...

Descripción completa

Detalles Bibliográficos
Autores principales: Yuan, Haibo, Zhou, Liting, Chen, Yilin, You, Jiayi, Hu, Hongye, Li, Yuanyuan, Huang, Rui, Wu, Shuyan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Taylor & Francis 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9980482/
https://www.ncbi.nlm.nih.gov/pubmed/36803521
http://dx.doi.org/10.1080/19490976.2023.2180315
_version_ 1784899921849090048
author Yuan, Haibo
Zhou, Liting
Chen, Yilin
You, Jiayi
Hu, Hongye
Li, Yuanyuan
Huang, Rui
Wu, Shuyan
author_facet Yuan, Haibo
Zhou, Liting
Chen, Yilin
You, Jiayi
Hu, Hongye
Li, Yuanyuan
Huang, Rui
Wu, Shuyan
author_sort Yuan, Haibo
collection PubMed
description SopF, a newly discovered effector secreted by Salmonella pathogenicity island-1 type III secretion system (T3SS1), was reported to target phosphoinositide on host cell membrane and aggravate systemic infection, while its functional relevance and underlying mechanisms have yet to be elucidated. PANoptosis (pyroptosis, apoptosis, and necroptosis) of intestinal epithelial cells (IECs) has been characterized as a pivotal host defense to limit the dissemination of foodborne pathogens, whereas the effect of SopF on IECs PANoptosis induced by Salmonella is rather limited. Here, we show that SopF can attenuate intestinal inflammation and suppress IECs expulsion to promote bacterial dissemination in mice infected with Salmonella enterica serovar Typhimurium (S. Typhimurium). We revealed that SopF could activate phosphoinositide-dependent protein kinase-1 (PDK1) to phosphorylate p90 ribosomal S6 kinase (RSK) which down-regulated Caspase-8 activation. Caspase-8 inactivated by SopF resulted in inhibition of pyroptosis and apoptosis, but promotion of necroptosis. The administration of both AR-12 (PDK1 inhibitor) and BI-D1870 (RSK inhibitor) potentially overcame Caspase-8 blockade and subverted PANoptosis challenged by SopF. Collectively, these findings demonstrate that this virulence strategy elicited by SopF aggregates systemic infection via modulating IEC PANoptosis through PDK1-RSK signaling, which throws light on novel functions of bacterial effectors, as well as a mechanism employed by pathogens to counteract host immune defense.
format Online
Article
Text
id pubmed-9980482
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Taylor & Francis
record_format MEDLINE/PubMed
spelling pubmed-99804822023-03-03 Salmonella effector SopF regulates PANoptosis of intestinal epithelial cells to aggravate systemic infection Yuan, Haibo Zhou, Liting Chen, Yilin You, Jiayi Hu, Hongye Li, Yuanyuan Huang, Rui Wu, Shuyan Gut Microbes Research Paper SopF, a newly discovered effector secreted by Salmonella pathogenicity island-1 type III secretion system (T3SS1), was reported to target phosphoinositide on host cell membrane and aggravate systemic infection, while its functional relevance and underlying mechanisms have yet to be elucidated. PANoptosis (pyroptosis, apoptosis, and necroptosis) of intestinal epithelial cells (IECs) has been characterized as a pivotal host defense to limit the dissemination of foodborne pathogens, whereas the effect of SopF on IECs PANoptosis induced by Salmonella is rather limited. Here, we show that SopF can attenuate intestinal inflammation and suppress IECs expulsion to promote bacterial dissemination in mice infected with Salmonella enterica serovar Typhimurium (S. Typhimurium). We revealed that SopF could activate phosphoinositide-dependent protein kinase-1 (PDK1) to phosphorylate p90 ribosomal S6 kinase (RSK) which down-regulated Caspase-8 activation. Caspase-8 inactivated by SopF resulted in inhibition of pyroptosis and apoptosis, but promotion of necroptosis. The administration of both AR-12 (PDK1 inhibitor) and BI-D1870 (RSK inhibitor) potentially overcame Caspase-8 blockade and subverted PANoptosis challenged by SopF. Collectively, these findings demonstrate that this virulence strategy elicited by SopF aggregates systemic infection via modulating IEC PANoptosis through PDK1-RSK signaling, which throws light on novel functions of bacterial effectors, as well as a mechanism employed by pathogens to counteract host immune defense. Taylor & Francis 2023-02-20 /pmc/articles/PMC9980482/ /pubmed/36803521 http://dx.doi.org/10.1080/19490976.2023.2180315 Text en © 2023 The Author(s). Published with license by Taylor & Francis Group, LLC. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Paper
Yuan, Haibo
Zhou, Liting
Chen, Yilin
You, Jiayi
Hu, Hongye
Li, Yuanyuan
Huang, Rui
Wu, Shuyan
Salmonella effector SopF regulates PANoptosis of intestinal epithelial cells to aggravate systemic infection
title Salmonella effector SopF regulates PANoptosis of intestinal epithelial cells to aggravate systemic infection
title_full Salmonella effector SopF regulates PANoptosis of intestinal epithelial cells to aggravate systemic infection
title_fullStr Salmonella effector SopF regulates PANoptosis of intestinal epithelial cells to aggravate systemic infection
title_full_unstemmed Salmonella effector SopF regulates PANoptosis of intestinal epithelial cells to aggravate systemic infection
title_short Salmonella effector SopF regulates PANoptosis of intestinal epithelial cells to aggravate systemic infection
title_sort salmonella effector sopf regulates panoptosis of intestinal epithelial cells to aggravate systemic infection
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9980482/
https://www.ncbi.nlm.nih.gov/pubmed/36803521
http://dx.doi.org/10.1080/19490976.2023.2180315
work_keys_str_mv AT yuanhaibo salmonellaeffectorsopfregulatespanoptosisofintestinalepithelialcellstoaggravatesystemicinfection
AT zhouliting salmonellaeffectorsopfregulatespanoptosisofintestinalepithelialcellstoaggravatesystemicinfection
AT chenyilin salmonellaeffectorsopfregulatespanoptosisofintestinalepithelialcellstoaggravatesystemicinfection
AT youjiayi salmonellaeffectorsopfregulatespanoptosisofintestinalepithelialcellstoaggravatesystemicinfection
AT huhongye salmonellaeffectorsopfregulatespanoptosisofintestinalepithelialcellstoaggravatesystemicinfection
AT liyuanyuan salmonellaeffectorsopfregulatespanoptosisofintestinalepithelialcellstoaggravatesystemicinfection
AT huangrui salmonellaeffectorsopfregulatespanoptosisofintestinalepithelialcellstoaggravatesystemicinfection
AT wushuyan salmonellaeffectorsopfregulatespanoptosisofintestinalepithelialcellstoaggravatesystemicinfection