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The salmonella effector Hcp modulates infection response, and affects salmonella adhesion and egg contamination incidences in ducks

Salmonella Entertidis (SE) often causes persistent infections and egg contamination in laying ducks. Hcp, the core structural and effector proteins of the Type VI Secretion System (T6SS) in SE, contributes to bacterial invasion, adhesion and virulence. However, little is known about the effect of Hc...

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Autores principales: Song, Lina, Wu, Jia, Weng, Kaiqi, Yao, Fenghua, Vongsangnak, Wanwipa, Zhu, Guoqiang, Chen, Guohong, Zhang, Yu, Xu, Qi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9575552/
https://www.ncbi.nlm.nih.gov/pubmed/36262184
http://dx.doi.org/10.3389/fcimb.2022.948237
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author Song, Lina
Wu, Jia
Weng, Kaiqi
Yao, Fenghua
Vongsangnak, Wanwipa
Zhu, Guoqiang
Chen, Guohong
Zhang, Yu
Xu, Qi
author_facet Song, Lina
Wu, Jia
Weng, Kaiqi
Yao, Fenghua
Vongsangnak, Wanwipa
Zhu, Guoqiang
Chen, Guohong
Zhang, Yu
Xu, Qi
author_sort Song, Lina
collection PubMed
description Salmonella Entertidis (SE) often causes persistent infections and egg contamination in laying ducks. Hcp, the core structural and effector proteins of the Type VI Secretion System (T6SS) in SE, contributes to bacterial invasion, adhesion and virulence. However, little is known about the effect of Hcp on the host’s infection responses and egg contamination incidences in duck. Herein, we generated an hcp deletion mutant SE MY1△hcp and detected its ability to invade duck granulosa cells (dGCs) and contaminate eggs. In comparison with MY1-infected group, the SE adhesion decreased by 15.96% in MY1△hcp-infected dGCs, and the apoptosis in MY1△hcp-infected dGCs decreased by 26.58% and 30.99% at 3 and 6 hours postinfection, respectively. However, the expression levels of immunogenic genes TLR4, NOD1, TNFα, IL-1β and proinflammatory cytokines IL-6, IL-1β, TNF-α release were markedly lower in the dGCs inoculated with MY1△hcp than that of the wild type. Besides, the laying ducks were challenged with MY1 or MY1△hcp in vivo, respectively. The lower egg production and higher egg contamination were observed in MY1-infected ducks in comparison with MY1△hcp-infected birds. Furthermore, the host’s infection response of differentially abundant proteins (DAPs) to Salmonella effector Hcp was identified using quantitative proteomics. A total of 164 DAPs were identified between the MY1- and MY1△hcp-infected cells, which were mainly engaged in the immune, hormone synthesis, cell proliferation and cell apoptotic process. Among them, STAT3, AKT1, MAPK9, MAPK14, and CREBBP were the center of the regulatory network, which might serve as key host response regulators to bacterial Hcp. In conclusion, we demonstrated that effector Hcp contributed to not only SE invasion, induction of dGCs apoptosis, and trigger of immune responses, but also enhanced contamination incidences. Also, the STAT3, AKT1, MAPK9, MAPK14, and CREBBP were identified as host’s infection response regulators of bacterial Hcp in duck. Overall, these results not only offered a novel evidence of SE ovarian transmission but also identified some promising candidate regulators during SE infection.
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spelling pubmed-95755522022-10-18 The salmonella effector Hcp modulates infection response, and affects salmonella adhesion and egg contamination incidences in ducks Song, Lina Wu, Jia Weng, Kaiqi Yao, Fenghua Vongsangnak, Wanwipa Zhu, Guoqiang Chen, Guohong Zhang, Yu Xu, Qi Front Cell Infect Microbiol Cellular and Infection Microbiology Salmonella Entertidis (SE) often causes persistent infections and egg contamination in laying ducks. Hcp, the core structural and effector proteins of the Type VI Secretion System (T6SS) in SE, contributes to bacterial invasion, adhesion and virulence. However, little is known about the effect of Hcp on the host’s infection responses and egg contamination incidences in duck. Herein, we generated an hcp deletion mutant SE MY1△hcp and detected its ability to invade duck granulosa cells (dGCs) and contaminate eggs. In comparison with MY1-infected group, the SE adhesion decreased by 15.96% in MY1△hcp-infected dGCs, and the apoptosis in MY1△hcp-infected dGCs decreased by 26.58% and 30.99% at 3 and 6 hours postinfection, respectively. However, the expression levels of immunogenic genes TLR4, NOD1, TNFα, IL-1β and proinflammatory cytokines IL-6, IL-1β, TNF-α release were markedly lower in the dGCs inoculated with MY1△hcp than that of the wild type. Besides, the laying ducks were challenged with MY1 or MY1△hcp in vivo, respectively. The lower egg production and higher egg contamination were observed in MY1-infected ducks in comparison with MY1△hcp-infected birds. Furthermore, the host’s infection response of differentially abundant proteins (DAPs) to Salmonella effector Hcp was identified using quantitative proteomics. A total of 164 DAPs were identified between the MY1- and MY1△hcp-infected cells, which were mainly engaged in the immune, hormone synthesis, cell proliferation and cell apoptotic process. Among them, STAT3, AKT1, MAPK9, MAPK14, and CREBBP were the center of the regulatory network, which might serve as key host response regulators to bacterial Hcp. In conclusion, we demonstrated that effector Hcp contributed to not only SE invasion, induction of dGCs apoptosis, and trigger of immune responses, but also enhanced contamination incidences. Also, the STAT3, AKT1, MAPK9, MAPK14, and CREBBP were identified as host’s infection response regulators of bacterial Hcp in duck. Overall, these results not only offered a novel evidence of SE ovarian transmission but also identified some promising candidate regulators during SE infection. Frontiers Media S.A. 2022-10-03 /pmc/articles/PMC9575552/ /pubmed/36262184 http://dx.doi.org/10.3389/fcimb.2022.948237 Text en Copyright © 2022 Song, Wu, Weng, Yao, Vongsangnak, Zhu, Chen, Zhang and Xu 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
Song, Lina
Wu, Jia
Weng, Kaiqi
Yao, Fenghua
Vongsangnak, Wanwipa
Zhu, Guoqiang
Chen, Guohong
Zhang, Yu
Xu, Qi
The salmonella effector Hcp modulates infection response, and affects salmonella adhesion and egg contamination incidences in ducks
title The salmonella effector Hcp modulates infection response, and affects salmonella adhesion and egg contamination incidences in ducks
title_full The salmonella effector Hcp modulates infection response, and affects salmonella adhesion and egg contamination incidences in ducks
title_fullStr The salmonella effector Hcp modulates infection response, and affects salmonella adhesion and egg contamination incidences in ducks
title_full_unstemmed The salmonella effector Hcp modulates infection response, and affects salmonella adhesion and egg contamination incidences in ducks
title_short The salmonella effector Hcp modulates infection response, and affects salmonella adhesion and egg contamination incidences in ducks
title_sort salmonella effector hcp modulates infection response, and affects salmonella adhesion and egg contamination incidences in ducks
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9575552/
https://www.ncbi.nlm.nih.gov/pubmed/36262184
http://dx.doi.org/10.3389/fcimb.2022.948237
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