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inlF Enhances Listeria monocytogenes Early-Stage Infection by Inhibiting the Inflammatory Response

The internalin family proteins, which carry the leucine repeat region structural motif, play diverse roles in Listeria monocytogenes (Lm) infection and pathogenesis. Although Internalin F, encoded by inlF, was identified more than 20 years ago, its role in the Lm anti-inflammatory response remains u...

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Autores principales: Ling, Zhiting, Zhao, Dan, Xie, Xinyu, Yao, Hao, Wang, Yuting, Kong, Suwei, Chen, Xiang, Pan, Zhiming, Jiao, Xin’an, Yin, Yuelan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8866704/
https://www.ncbi.nlm.nih.gov/pubmed/35223532
http://dx.doi.org/10.3389/fcimb.2021.748461
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author Ling, Zhiting
Zhao, Dan
Xie, Xinyu
Yao, Hao
Wang, Yuting
Kong, Suwei
Chen, Xiang
Pan, Zhiming
Jiao, Xin’an
Yin, Yuelan
author_facet Ling, Zhiting
Zhao, Dan
Xie, Xinyu
Yao, Hao
Wang, Yuting
Kong, Suwei
Chen, Xiang
Pan, Zhiming
Jiao, Xin’an
Yin, Yuelan
author_sort Ling, Zhiting
collection PubMed
description The internalin family proteins, which carry the leucine repeat region structural motif, play diverse roles in Listeria monocytogenes (Lm) infection and pathogenesis. Although Internalin F, encoded by inlF, was identified more than 20 years ago, its role in the Lm anti-inflammatory response remains unknown. Lm serotype 4b isolates are associated with the majority of listeriosis outbreaks, but the function of InlF in these strains is not fully understood. In this study, we aimed to elucidate the role of inlF in modulating the inflammatory response and pathogenesis of the 4b strain Lm NTSN. Strikingly, although inlF was highly expressed at the transcriptional level during infection of five non-phagocytic cell types, it was not involved in adherence or invasion. Conversely, inlF did contributed to Lm adhesion and invasion of macrophages, and dramatically suppressed the expression of pro-inflammatory cytokines interleukin (IL)-1β and tumor necrosis factor (TNF-α). Consistent with the in vitro results, during Lm infection mice, inlF significantly inhibited the expression of IL-1β and IL-6 in the spleen, as well as IL-1β, IL-6, and TNF-α in the liver. More importantly, inlF contributed to Lm colonization in the spleen, liver, and ileum during the early stage of mouse infection via intragastric administration, inducing severe inflammatory injury and histopathologic changes in the late stage. To our knowledge, this is the first report to demonstrate that inlF mediates the inhibition of the pro-inflammatory response and contributes to the colonization and survival of Lm during the early stage of infection in mice. Our research partly explains the high pathogenicity of serovar 4b strains and will lead to new insights into the pathogenesis and immune evasion of Lm.
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spelling pubmed-88667042022-02-25 inlF Enhances Listeria monocytogenes Early-Stage Infection by Inhibiting the Inflammatory Response Ling, Zhiting Zhao, Dan Xie, Xinyu Yao, Hao Wang, Yuting Kong, Suwei Chen, Xiang Pan, Zhiming Jiao, Xin’an Yin, Yuelan Front Cell Infect Microbiol Cellular and Infection Microbiology The internalin family proteins, which carry the leucine repeat region structural motif, play diverse roles in Listeria monocytogenes (Lm) infection and pathogenesis. Although Internalin F, encoded by inlF, was identified more than 20 years ago, its role in the Lm anti-inflammatory response remains unknown. Lm serotype 4b isolates are associated with the majority of listeriosis outbreaks, but the function of InlF in these strains is not fully understood. In this study, we aimed to elucidate the role of inlF in modulating the inflammatory response and pathogenesis of the 4b strain Lm NTSN. Strikingly, although inlF was highly expressed at the transcriptional level during infection of five non-phagocytic cell types, it was not involved in adherence or invasion. Conversely, inlF did contributed to Lm adhesion and invasion of macrophages, and dramatically suppressed the expression of pro-inflammatory cytokines interleukin (IL)-1β and tumor necrosis factor (TNF-α). Consistent with the in vitro results, during Lm infection mice, inlF significantly inhibited the expression of IL-1β and IL-6 in the spleen, as well as IL-1β, IL-6, and TNF-α in the liver. More importantly, inlF contributed to Lm colonization in the spleen, liver, and ileum during the early stage of mouse infection via intragastric administration, inducing severe inflammatory injury and histopathologic changes in the late stage. To our knowledge, this is the first report to demonstrate that inlF mediates the inhibition of the pro-inflammatory response and contributes to the colonization and survival of Lm during the early stage of infection in mice. Our research partly explains the high pathogenicity of serovar 4b strains and will lead to new insights into the pathogenesis and immune evasion of Lm. Frontiers Media S.A. 2022-02-10 /pmc/articles/PMC8866704/ /pubmed/35223532 http://dx.doi.org/10.3389/fcimb.2021.748461 Text en Copyright © 2022 Ling, Zhao, Xie, Yao, Wang, Kong, Chen, Pan, Jiao and Yin 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 Cellular and Infection Microbiology
Ling, Zhiting
Zhao, Dan
Xie, Xinyu
Yao, Hao
Wang, Yuting
Kong, Suwei
Chen, Xiang
Pan, Zhiming
Jiao, Xin’an
Yin, Yuelan
inlF Enhances Listeria monocytogenes Early-Stage Infection by Inhibiting the Inflammatory Response
title inlF Enhances Listeria monocytogenes Early-Stage Infection by Inhibiting the Inflammatory Response
title_full inlF Enhances Listeria monocytogenes Early-Stage Infection by Inhibiting the Inflammatory Response
title_fullStr inlF Enhances Listeria monocytogenes Early-Stage Infection by Inhibiting the Inflammatory Response
title_full_unstemmed inlF Enhances Listeria monocytogenes Early-Stage Infection by Inhibiting the Inflammatory Response
title_short inlF Enhances Listeria monocytogenes Early-Stage Infection by Inhibiting the Inflammatory Response
title_sort inlf enhances listeria monocytogenes early-stage infection by inhibiting the inflammatory response
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8866704/
https://www.ncbi.nlm.nih.gov/pubmed/35223532
http://dx.doi.org/10.3389/fcimb.2021.748461
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