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Salmonella T3SS-elicited inflammatory innate immune response inhibits type I IFN response in macrophages
As a gram-negative intracellular bacterial pathogen, Salmonella enterica serovar Typhimurium (S. Typhimurium) invades different cell types including macrophages. Its infection in macrophages induces robust innate immune responses that are featured by proinflammatory and type I interferon (IFN) respo...
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Published in: | Veterinary microbiology 2024-02, Vol.289, p.109970-109970, Article 109970 |
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creator | Tang, Jingjing Gu, Yanchao Wang, Xiao Luo, Yi Zhang, Fuhua Zheng, Jingcai Wang, Yao Shen, Xihui Xu, Lei |
description | As a gram-negative intracellular bacterial pathogen, Salmonella enterica serovar Typhimurium (S. Typhimurium) invades different cell types including macrophages. Its infection in macrophages induces robust innate immune responses that are featured by proinflammatory and type I interferon (IFN) responses. The type III secretion systems (T3SSs) of S. Typhimurium play a crucial role in activating host inflammasome pathways. It has been recognized that the inflammasome pathways inhibit the type I IFN cascade. However, the potential role of T3SS in regulating the type I IFN response and the underlying mechanisms are largely unknown. In this study, we showed that S. Typhimurium infection activated strong proinflammatory, type I IFN and IFN-stimulated genes (ISGs) expression in macrophages. Furthermore, we showed that T3SS-defective S. Typhimurium mutant ΔinvC elicited attenuated inflammatory response but enhanced type I IFN and ISGs expression. Additionally, the inhibition of caspase-1 by a specific inhibitor VX-765 resulted in increased type I IFN response. Moreover, cell-permeable pan-caspase inhibitor Z-VAD-FMK also enhanced the type I IFN response upon S. Typhimurium infection. Intriguingly, compared with exponential phase S. Typhimurium infection, stationary phase bacteria triggered higher levels of type I IFN responses. Finally, the inhibition of caspase-1 by VX-765 substantially increased the intracellular S. Typhimurium burden. In conclusion, we demonstrated that the proinflammatory response induced by S. Typhimurium T3SS can inhibit the type I IFN response, which provides insight into the role of T3SS in orchestrating innate immunity during S. Typhimurium infection. |
doi_str_mv | 10.1016/j.vetmic.2023.109970 |
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Typhimurium) invades different cell types including macrophages. Its infection in macrophages induces robust innate immune responses that are featured by proinflammatory and type I interferon (IFN) responses. The type III secretion systems (T3SSs) of S. Typhimurium play a crucial role in activating host inflammasome pathways. It has been recognized that the inflammasome pathways inhibit the type I IFN cascade. However, the potential role of T3SS in regulating the type I IFN response and the underlying mechanisms are largely unknown. In this study, we showed that S. Typhimurium infection activated strong proinflammatory, type I IFN and IFN-stimulated genes (ISGs) expression in macrophages. Furthermore, we showed that T3SS-defective S. Typhimurium mutant ΔinvC elicited attenuated inflammatory response but enhanced type I IFN and ISGs expression. Additionally, the inhibition of caspase-1 by a specific inhibitor VX-765 resulted in increased type I IFN response. Moreover, cell-permeable pan-caspase inhibitor Z-VAD-FMK also enhanced the type I IFN response upon S. Typhimurium infection. Intriguingly, compared with exponential phase S. Typhimurium infection, stationary phase bacteria triggered higher levels of type I IFN responses. Finally, the inhibition of caspase-1 by VX-765 substantially increased the intracellular S. Typhimurium burden. In conclusion, we demonstrated that the proinflammatory response induced by S. Typhimurium T3SS can inhibit the type I IFN response, which provides insight into the role of T3SS in orchestrating innate immunity during S. Typhimurium infection.</description><identifier>ISSN: 0378-1135</identifier><identifier>EISSN: 1873-2542</identifier><identifier>DOI: 10.1016/j.vetmic.2023.109970</identifier><identifier>PMID: 38154394</identifier><language>eng</language><publisher>Netherlands</publisher><subject>Animals ; Caspases ; Immunity, Innate ; Inflammasomes ; Interferon Type I ; Macrophages - microbiology ; Salmonella typhimurium - genetics</subject><ispartof>Veterinary microbiology, 2024-02, Vol.289, p.109970-109970, Article 109970</ispartof><rights>Copyright © 2023 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c256t-eb4bd7606b9fcb6b32d394e1c54e68f1c2c6b57b5e783d04405d900e3b4903843</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38154394$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tang, Jingjing</creatorcontrib><creatorcontrib>Gu, Yanchao</creatorcontrib><creatorcontrib>Wang, Xiao</creatorcontrib><creatorcontrib>Luo, Yi</creatorcontrib><creatorcontrib>Zhang, Fuhua</creatorcontrib><creatorcontrib>Zheng, Jingcai</creatorcontrib><creatorcontrib>Wang, Yao</creatorcontrib><creatorcontrib>Shen, Xihui</creatorcontrib><creatorcontrib>Xu, Lei</creatorcontrib><title>Salmonella T3SS-elicited inflammatory innate immune response inhibits type I IFN response in macrophages</title><title>Veterinary microbiology</title><addtitle>Vet Microbiol</addtitle><description>As a gram-negative intracellular bacterial pathogen, Salmonella enterica serovar Typhimurium (S. Typhimurium) invades different cell types including macrophages. Its infection in macrophages induces robust innate immune responses that are featured by proinflammatory and type I interferon (IFN) responses. The type III secretion systems (T3SSs) of S. Typhimurium play a crucial role in activating host inflammasome pathways. It has been recognized that the inflammasome pathways inhibit the type I IFN cascade. However, the potential role of T3SS in regulating the type I IFN response and the underlying mechanisms are largely unknown. In this study, we showed that S. Typhimurium infection activated strong proinflammatory, type I IFN and IFN-stimulated genes (ISGs) expression in macrophages. Furthermore, we showed that T3SS-defective S. Typhimurium mutant ΔinvC elicited attenuated inflammatory response but enhanced type I IFN and ISGs expression. Additionally, the inhibition of caspase-1 by a specific inhibitor VX-765 resulted in increased type I IFN response. Moreover, cell-permeable pan-caspase inhibitor Z-VAD-FMK also enhanced the type I IFN response upon S. Typhimurium infection. Intriguingly, compared with exponential phase S. Typhimurium infection, stationary phase bacteria triggered higher levels of type I IFN responses. Finally, the inhibition of caspase-1 by VX-765 substantially increased the intracellular S. Typhimurium burden. In conclusion, we demonstrated that the proinflammatory response induced by S. Typhimurium T3SS can inhibit the type I IFN response, which provides insight into the role of T3SS in orchestrating innate immunity during S. Typhimurium infection.</description><subject>Animals</subject><subject>Caspases</subject><subject>Immunity, Innate</subject><subject>Inflammasomes</subject><subject>Interferon Type I</subject><subject>Macrophages - microbiology</subject><subject>Salmonella typhimurium - genetics</subject><issn>0378-1135</issn><issn>1873-2542</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNpNkMtOwzAQRS0EoqXwBwhlySZl_MpjiSoKlRAsWtaW7UyoqzgJcYLUvydVC2I1mpl753EIuaUwp0CTh938G3vv7JwB42Mpz1M4I1OapTxmUrBzMgWeZjGlXE7IVQg7ABB5ApdkwjMqBc_FlGzXuvJNjVWlow1fr2OsnHU9FpGry0p7r_um249JrXuMnPdDjVGHoW3qMOb11hnXh6jftxitotXy7X8z8tp2TbvVnxiuyUWpq4A3pzgjH8unzeIlfn1_Xi0eX2PLZNLHaIQp0gQSk5fWJIazYrwTqZUCk6ykltnEyNRITDNegBAgixwAuRE58EzwGbk_zm275mvA0Cvvgj38V2MzBMVyyCjjkqWjVByl45EhdFiqtnNed3tFQR0Yq506MlYHxurIeLTdnTYMxmPxZ_qFyn8Actd6tQ</recordid><startdate>202402</startdate><enddate>202402</enddate><creator>Tang, Jingjing</creator><creator>Gu, Yanchao</creator><creator>Wang, Xiao</creator><creator>Luo, Yi</creator><creator>Zhang, Fuhua</creator><creator>Zheng, Jingcai</creator><creator>Wang, Yao</creator><creator>Shen, Xihui</creator><creator>Xu, Lei</creator><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>202402</creationdate><title>Salmonella T3SS-elicited inflammatory innate immune response inhibits type I IFN response in macrophages</title><author>Tang, Jingjing ; Gu, Yanchao ; Wang, Xiao ; Luo, Yi ; Zhang, Fuhua ; Zheng, Jingcai ; Wang, Yao ; Shen, Xihui ; Xu, Lei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c256t-eb4bd7606b9fcb6b32d394e1c54e68f1c2c6b57b5e783d04405d900e3b4903843</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Caspases</topic><topic>Immunity, Innate</topic><topic>Inflammasomes</topic><topic>Interferon Type I</topic><topic>Macrophages - microbiology</topic><topic>Salmonella typhimurium - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tang, Jingjing</creatorcontrib><creatorcontrib>Gu, Yanchao</creatorcontrib><creatorcontrib>Wang, Xiao</creatorcontrib><creatorcontrib>Luo, Yi</creatorcontrib><creatorcontrib>Zhang, Fuhua</creatorcontrib><creatorcontrib>Zheng, Jingcai</creatorcontrib><creatorcontrib>Wang, Yao</creatorcontrib><creatorcontrib>Shen, Xihui</creatorcontrib><creatorcontrib>Xu, Lei</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Veterinary microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tang, Jingjing</au><au>Gu, Yanchao</au><au>Wang, Xiao</au><au>Luo, Yi</au><au>Zhang, Fuhua</au><au>Zheng, Jingcai</au><au>Wang, Yao</au><au>Shen, Xihui</au><au>Xu, Lei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Salmonella T3SS-elicited inflammatory innate immune response inhibits type I IFN response in macrophages</atitle><jtitle>Veterinary microbiology</jtitle><addtitle>Vet Microbiol</addtitle><date>2024-02</date><risdate>2024</risdate><volume>289</volume><spage>109970</spage><epage>109970</epage><pages>109970-109970</pages><artnum>109970</artnum><issn>0378-1135</issn><eissn>1873-2542</eissn><abstract>As a gram-negative intracellular bacterial pathogen, Salmonella enterica serovar Typhimurium (S. Typhimurium) invades different cell types including macrophages. Its infection in macrophages induces robust innate immune responses that are featured by proinflammatory and type I interferon (IFN) responses. The type III secretion systems (T3SSs) of S. Typhimurium play a crucial role in activating host inflammasome pathways. It has been recognized that the inflammasome pathways inhibit the type I IFN cascade. However, the potential role of T3SS in regulating the type I IFN response and the underlying mechanisms are largely unknown. In this study, we showed that S. Typhimurium infection activated strong proinflammatory, type I IFN and IFN-stimulated genes (ISGs) expression in macrophages. Furthermore, we showed that T3SS-defective S. Typhimurium mutant ΔinvC elicited attenuated inflammatory response but enhanced type I IFN and ISGs expression. Additionally, the inhibition of caspase-1 by a specific inhibitor VX-765 resulted in increased type I IFN response. 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subjects | Animals Caspases Immunity, Innate Inflammasomes Interferon Type I Macrophages - microbiology Salmonella typhimurium - genetics |
title | Salmonella T3SS-elicited inflammatory innate immune response inhibits type I IFN response in macrophages |
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