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Intracellular Staphylococcus aureus triggers pyroptosis and contributes to inhibition of healing due to perforin-2 suppression
Impaired wound healing associated with recurrent Staphylococcus aureus infection and unresolved inflammation are hallmarks of nonhealing diabetic foot ulcers (DFUs). Perforin-2, an innate immunity molecule against intracellular bacteria, limits cutaneous infection and dissemination of S. aureus in m...
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| Published in: | The Journal of clinical investigation 2021-12, Vol.131 (24) |
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| creator | Pastar, Irena Sawaya, Andrew P Marjanovic, Jelena Burgess, Jamie L Strbo, Natasa Rivas, Katelyn E Wikramanayake, Tongyu C Head, Cheyanne R Stone, Rivka C Jozic, Ivan Stojadinovic, Olivera Kornfeld, Eran Y Kirsner, Robert S Lev-Tov, Hadar Tomic-Canic, Marjana |
| description | Impaired wound healing associated with recurrent Staphylococcus aureus infection and unresolved inflammation are hallmarks of nonhealing diabetic foot ulcers (DFUs). Perforin-2, an innate immunity molecule against intracellular bacteria, limits cutaneous infection and dissemination of S. aureus in mice. Here, we report the intracellular accumulation of S. aureus in the epidermis of DFUs with no clinical signs of infection due to marked suppression of perforin-2. S. aureus residing within the epidermis of DFUs triggers AIM2 inflammasome activation and pyroptosis. These findings were corroborated in mice lacking perforin-2. The effects of pyroptosis on DFU clinical outcomes were further elucidated in a 4-week longitudinal clinical study in patients with DFUs receiving standard care. Increased AIM2 inflammasome and ASC-pyroptosome coupled with induction of IL-1β were found in nonhealing DFUs compared with healing DFUs. Our findings revealed that perforin-2 suppression, intracellular S. aureus accumulation, and associated induction of pyroptosis contribute to healing inhibition and prolonged inflammation in patients with DFUs. |
| doi_str_mv | 10.1172/JCI133727 |
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Perforin-2, an innate immunity molecule against intracellular bacteria, limits cutaneous infection and dissemination of S. aureus in mice. Here, we report the intracellular accumulation of S. aureus in the epidermis of DFUs with no clinical signs of infection due to marked suppression of perforin-2. S. aureus residing within the epidermis of DFUs triggers AIM2 inflammasome activation and pyroptosis. These findings were corroborated in mice lacking perforin-2. The effects of pyroptosis on DFU clinical outcomes were further elucidated in a 4-week longitudinal clinical study in patients with DFUs receiving standard care. Increased AIM2 inflammasome and ASC-pyroptosome coupled with induction of IL-1β were found in nonhealing DFUs compared with healing DFUs. Our findings revealed that perforin-2 suppression, intracellular S. aureus accumulation, and associated induction of pyroptosis contribute to healing inhibition and prolonged inflammation in patients with DFUs.</description><identifier>ISSN: 1558-8238</identifier><identifier>ISSN: 0021-9738</identifier><identifier>EISSN: 1558-8238</identifier><identifier>DOI: 10.1172/JCI133727</identifier><identifier>PMID: 34730110</identifier><language>eng</language><publisher>United States: American Society for Clinical Investigation</publisher><subject>Adult ; Aged ; Animals ; Care and treatment ; Cellular proteins ; Complications and side effects ; Diabetic foot ; Diabetic Foot - genetics ; Diabetic Foot - immunology ; Diabetic Foot - microbiology ; DNA-Binding Proteins - genetics ; DNA-Binding Proteins - immunology ; Epidermis - immunology ; Epidermis - microbiology ; Female ; Genetic aspects ; Health aspects ; Humans ; Interleukin-1beta - genetics ; Interleukin-1beta - immunology ; Male ; Membrane Proteins - genetics ; Membrane Proteins - immunology ; Mice ; Mice, Knockout ; Middle Aged ; Physiological aspects ; Pore Forming Cytotoxic Proteins - genetics ; Pore Forming Cytotoxic Proteins - immunology ; Pyroptosis - genetics ; Pyroptosis - immunology ; Staphylococcal Infections - genetics ; Staphylococcal Infections - immunology ; Staphylococcus aureus - immunology ; Staphylococcus aureus infections ; Wound healing ; Wound Healing - genetics ; Wound Healing - immunology</subject><ispartof>The Journal of clinical investigation, 2021-12, Vol.131 (24)</ispartof><rights>COPYRIGHT 2021 American Society for Clinical Investigation</rights><rights>2021 American Society for Clinical Investigation 2021 American Society for Clinical Investigation</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c579t-99853c86539383b17b2796cb64f6e0e86f29298f8dc8e5eb430e2cd033212ed63</citedby><cites>FETCH-LOGICAL-c579t-99853c86539383b17b2796cb64f6e0e86f29298f8dc8e5eb430e2cd033212ed63</cites><orcidid>0000-0002-6824-9844 ; 0000-0002-9341-0193 ; 0000-0003-0197-6198 ; 0000-0001-5114-9524 ; 0000-0001-9527-1337 ; 0000-0003-2152-2433 ; 0000-0002-1137-6850 ; 0000-0002-7489-2123 ; 0000-0001-6307-7986</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8670843/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8670843/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,315,733,786,790,891,27957,27958,53827,53829</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34730110$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Pastar, Irena</creatorcontrib><creatorcontrib>Sawaya, Andrew P</creatorcontrib><creatorcontrib>Marjanovic, Jelena</creatorcontrib><creatorcontrib>Burgess, Jamie L</creatorcontrib><creatorcontrib>Strbo, Natasa</creatorcontrib><creatorcontrib>Rivas, Katelyn E</creatorcontrib><creatorcontrib>Wikramanayake, Tongyu C</creatorcontrib><creatorcontrib>Head, Cheyanne R</creatorcontrib><creatorcontrib>Stone, Rivka C</creatorcontrib><creatorcontrib>Jozic, Ivan</creatorcontrib><creatorcontrib>Stojadinovic, Olivera</creatorcontrib><creatorcontrib>Kornfeld, Eran Y</creatorcontrib><creatorcontrib>Kirsner, Robert S</creatorcontrib><creatorcontrib>Lev-Tov, Hadar</creatorcontrib><creatorcontrib>Tomic-Canic, Marjana</creatorcontrib><title>Intracellular Staphylococcus aureus triggers pyroptosis and contributes to inhibition of healing due to perforin-2 suppression</title><title>The Journal of clinical investigation</title><addtitle>J Clin Invest</addtitle><description>Impaired wound healing associated with recurrent Staphylococcus aureus infection and unresolved inflammation are hallmarks of nonhealing diabetic foot ulcers (DFUs). Perforin-2, an innate immunity molecule against intracellular bacteria, limits cutaneous infection and dissemination of S. aureus in mice. Here, we report the intracellular accumulation of S. aureus in the epidermis of DFUs with no clinical signs of infection due to marked suppression of perforin-2. S. aureus residing within the epidermis of DFUs triggers AIM2 inflammasome activation and pyroptosis. These findings were corroborated in mice lacking perforin-2. The effects of pyroptosis on DFU clinical outcomes were further elucidated in a 4-week longitudinal clinical study in patients with DFUs receiving standard care. Increased AIM2 inflammasome and ASC-pyroptosome coupled with induction of IL-1β were found in nonhealing DFUs compared with healing DFUs. Our findings revealed that perforin-2 suppression, intracellular S. aureus accumulation, and associated induction of pyroptosis contribute to healing inhibition and prolonged inflammation in patients with DFUs.</description><subject>Adult</subject><subject>Aged</subject><subject>Animals</subject><subject>Care and treatment</subject><subject>Cellular proteins</subject><subject>Complications and side effects</subject><subject>Diabetic foot</subject><subject>Diabetic Foot - genetics</subject><subject>Diabetic Foot - immunology</subject><subject>Diabetic Foot - microbiology</subject><subject>DNA-Binding Proteins - genetics</subject><subject>DNA-Binding Proteins - immunology</subject><subject>Epidermis - immunology</subject><subject>Epidermis - microbiology</subject><subject>Female</subject><subject>Genetic aspects</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Interleukin-1beta - genetics</subject><subject>Interleukin-1beta - immunology</subject><subject>Male</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - immunology</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Middle Aged</subject><subject>Physiological aspects</subject><subject>Pore Forming Cytotoxic Proteins - genetics</subject><subject>Pore Forming Cytotoxic Proteins - immunology</subject><subject>Pyroptosis - genetics</subject><subject>Pyroptosis - immunology</subject><subject>Staphylococcal Infections - genetics</subject><subject>Staphylococcal Infections - immunology</subject><subject>Staphylococcus aureus - immunology</subject><subject>Staphylococcus aureus infections</subject><subject>Wound healing</subject><subject>Wound Healing - genetics</subject><subject>Wound Healing - immunology</subject><issn>1558-8238</issn><issn>0021-9738</issn><issn>1558-8238</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNqNkk2LFDEQhhtR3HX14B-QBkH00Gs-ujvJRVgGP0YWFlz1GtLp6p5IT9ImHXEu_nYTdh1mYA6SQ4XUU2-ReqsonmN0iTEjbz-v1phSRtiD4hw3Da84ofzhwf2seBLCD4RwXTf14-KM1owijNF58WdtF680TFOclC9vFzVvdpPTTusYShU9pLB4M47gQznvvJsXF0xK2b7ULhWbLi6QGFcauzGdWYyzpRvKDajJ2LHsI-TkDH5w3tiKlCHOs4cQEvi0eDSoKcCz-3hRfPvw_uvqU3V983G9urqudMPEUgnBG6p521BBOe0w6wgTre7aemgBAW8HIojgA-81hwa6miIgukeUEkygb-lF8e5Od47dFnoN-deTnL3ZKr-TThl5nLFmI0f3S_KWIV7TJPD6XsC7nxHCIrcm5LEpCy4GSRpBERE1wwl9eYeOagJp7ODyhDMur1ouBBOUZMHqBDWChdTeWRhMej7iL0_w6fSwNfpkwZujgmwW_F5GFUOQ69sv_8_efD9mXx2w2eVlE9wUs-_hpKj2LgQPw37cGMm8t3K_t4l9cejPnvy3qPQvBCjncg</recordid><startdate>20211215</startdate><enddate>20211215</enddate><creator>Pastar, Irena</creator><creator>Sawaya, Andrew P</creator><creator>Marjanovic, Jelena</creator><creator>Burgess, Jamie L</creator><creator>Strbo, Natasa</creator><creator>Rivas, Katelyn E</creator><creator>Wikramanayake, Tongyu C</creator><creator>Head, Cheyanne R</creator><creator>Stone, Rivka C</creator><creator>Jozic, Ivan</creator><creator>Stojadinovic, Olivera</creator><creator>Kornfeld, Eran Y</creator><creator>Kirsner, Robert S</creator><creator>Lev-Tov, Hadar</creator><creator>Tomic-Canic, Marjana</creator><general>American Society for Clinical Investigation</general><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>IOV</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6824-9844</orcidid><orcidid>https://orcid.org/0000-0002-9341-0193</orcidid><orcidid>https://orcid.org/0000-0003-0197-6198</orcidid><orcidid>https://orcid.org/0000-0001-5114-9524</orcidid><orcidid>https://orcid.org/0000-0001-9527-1337</orcidid><orcidid>https://orcid.org/0000-0003-2152-2433</orcidid><orcidid>https://orcid.org/0000-0002-1137-6850</orcidid><orcidid>https://orcid.org/0000-0002-7489-2123</orcidid><orcidid>https://orcid.org/0000-0001-6307-7986</orcidid></search><sort><creationdate>20211215</creationdate><title>Intracellular Staphylococcus aureus triggers pyroptosis and contributes to inhibition of healing due to perforin-2 suppression</title><author>Pastar, Irena ; Sawaya, Andrew P ; Marjanovic, Jelena ; Burgess, Jamie L ; Strbo, Natasa ; Rivas, Katelyn E ; Wikramanayake, Tongyu C ; Head, Cheyanne R ; Stone, Rivka C ; Jozic, Ivan ; Stojadinovic, Olivera ; Kornfeld, Eran Y ; Kirsner, Robert S ; Lev-Tov, Hadar ; Tomic-Canic, Marjana</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c579t-99853c86539383b17b2796cb64f6e0e86f29298f8dc8e5eb430e2cd033212ed63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adult</topic><topic>Aged</topic><topic>Animals</topic><topic>Care and treatment</topic><topic>Cellular proteins</topic><topic>Complications and side effects</topic><topic>Diabetic foot</topic><topic>Diabetic Foot - genetics</topic><topic>Diabetic Foot - immunology</topic><topic>Diabetic Foot - microbiology</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - immunology</topic><topic>Epidermis - immunology</topic><topic>Epidermis - microbiology</topic><topic>Female</topic><topic>Genetic aspects</topic><topic>Health aspects</topic><topic>Humans</topic><topic>Interleukin-1beta - genetics</topic><topic>Interleukin-1beta - immunology</topic><topic>Male</topic><topic>Membrane Proteins - genetics</topic><topic>Membrane Proteins - immunology</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Middle Aged</topic><topic>Physiological aspects</topic><topic>Pore Forming Cytotoxic Proteins - genetics</topic><topic>Pore Forming Cytotoxic Proteins - immunology</topic><topic>Pyroptosis - genetics</topic><topic>Pyroptosis - immunology</topic><topic>Staphylococcal Infections - genetics</topic><topic>Staphylococcal Infections - immunology</topic><topic>Staphylococcus aureus - immunology</topic><topic>Staphylococcus aureus infections</topic><topic>Wound healing</topic><topic>Wound Healing - genetics</topic><topic>Wound Healing - immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pastar, Irena</creatorcontrib><creatorcontrib>Sawaya, Andrew P</creatorcontrib><creatorcontrib>Marjanovic, Jelena</creatorcontrib><creatorcontrib>Burgess, Jamie L</creatorcontrib><creatorcontrib>Strbo, Natasa</creatorcontrib><creatorcontrib>Rivas, Katelyn E</creatorcontrib><creatorcontrib>Wikramanayake, Tongyu C</creatorcontrib><creatorcontrib>Head, Cheyanne R</creatorcontrib><creatorcontrib>Stone, Rivka C</creatorcontrib><creatorcontrib>Jozic, Ivan</creatorcontrib><creatorcontrib>Stojadinovic, Olivera</creatorcontrib><creatorcontrib>Kornfeld, Eran Y</creatorcontrib><creatorcontrib>Kirsner, Robert S</creatorcontrib><creatorcontrib>Lev-Tov, Hadar</creatorcontrib><creatorcontrib>Tomic-Canic, Marjana</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of clinical investigation</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pastar, Irena</au><au>Sawaya, Andrew P</au><au>Marjanovic, Jelena</au><au>Burgess, Jamie L</au><au>Strbo, Natasa</au><au>Rivas, Katelyn E</au><au>Wikramanayake, Tongyu C</au><au>Head, Cheyanne R</au><au>Stone, Rivka C</au><au>Jozic, Ivan</au><au>Stojadinovic, Olivera</au><au>Kornfeld, Eran Y</au><au>Kirsner, Robert S</au><au>Lev-Tov, Hadar</au><au>Tomic-Canic, Marjana</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Intracellular Staphylococcus aureus triggers pyroptosis and contributes to inhibition of healing due to perforin-2 suppression</atitle><jtitle>The Journal of clinical investigation</jtitle><addtitle>J Clin Invest</addtitle><date>2021-12-15</date><risdate>2021</risdate><volume>131</volume><issue>24</issue><issn>1558-8238</issn><issn>0021-9738</issn><eissn>1558-8238</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Authorship note: IP and APS contributed equally to this work.</notes><abstract>Impaired wound healing associated with recurrent Staphylococcus aureus infection and unresolved inflammation are hallmarks of nonhealing diabetic foot ulcers (DFUs). Perforin-2, an innate immunity molecule against intracellular bacteria, limits cutaneous infection and dissemination of S. aureus in mice. Here, we report the intracellular accumulation of S. aureus in the epidermis of DFUs with no clinical signs of infection due to marked suppression of perforin-2. S. aureus residing within the epidermis of DFUs triggers AIM2 inflammasome activation and pyroptosis. These findings were corroborated in mice lacking perforin-2. The effects of pyroptosis on DFU clinical outcomes were further elucidated in a 4-week longitudinal clinical study in patients with DFUs receiving standard care. Increased AIM2 inflammasome and ASC-pyroptosome coupled with induction of IL-1β were found in nonhealing DFUs compared with healing DFUs. Our findings revealed that perforin-2 suppression, intracellular S. aureus accumulation, and associated induction of pyroptosis contribute to healing inhibition and prolonged inflammation in patients with DFUs.</abstract><cop>United States</cop><pub>American Society for Clinical Investigation</pub><pmid>34730110</pmid><doi>10.1172/JCI133727</doi><orcidid>https://orcid.org/0000-0002-6824-9844</orcidid><orcidid>https://orcid.org/0000-0002-9341-0193</orcidid><orcidid>https://orcid.org/0000-0003-0197-6198</orcidid><orcidid>https://orcid.org/0000-0001-5114-9524</orcidid><orcidid>https://orcid.org/0000-0001-9527-1337</orcidid><orcidid>https://orcid.org/0000-0003-2152-2433</orcidid><orcidid>https://orcid.org/0000-0002-1137-6850</orcidid><orcidid>https://orcid.org/0000-0002-7489-2123</orcidid><orcidid>https://orcid.org/0000-0001-6307-7986</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Adult Aged Animals Care and treatment Cellular proteins Complications and side effects Diabetic foot Diabetic Foot - genetics Diabetic Foot - immunology Diabetic Foot - microbiology DNA-Binding Proteins - genetics DNA-Binding Proteins - immunology Epidermis - immunology Epidermis - microbiology Female Genetic aspects Health aspects Humans Interleukin-1beta - genetics Interleukin-1beta - immunology Male Membrane Proteins - genetics Membrane Proteins - immunology Mice Mice, Knockout Middle Aged Physiological aspects Pore Forming Cytotoxic Proteins - genetics Pore Forming Cytotoxic Proteins - immunology Pyroptosis - genetics Pyroptosis - immunology Staphylococcal Infections - genetics Staphylococcal Infections - immunology Staphylococcus aureus - immunology Staphylococcus aureus infections Wound healing Wound Healing - genetics Wound Healing - immunology |
| title | Intracellular Staphylococcus aureus triggers pyroptosis and contributes to inhibition of healing due to perforin-2 suppression |
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