Memory Th1 Cells Are Protective in Invasive Staphylococcus aureus Infection
Mechanisms of protective immunity to Staphylococcus aureus infection in humans remain elusive. While the importance of cellular immunity has been shown in mice, T cell responses in humans have not been characterised. Using a murine model of recurrent S. aureus peritonitis, we demonstrated that prior...
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creator | Brown, Aisling F Murphy, Alison G Lalor, Stephen J Leech, John M O'Keeffe, Kate M Mac Aogáin, Micheál O'Halloran, Dara P Lacey, Keenan A Tavakol, Mehri Hearnden, Claire H Fitzgerald-Hughes, Deirdre Humphreys, Hilary Fennell, Jérôme P van Wamel, Willem J Foster, Timothy J Geoghegan, Joan A Lavelle, Ed C Rogers, Thomas R McLoughlin, Rachel M |
description | Mechanisms of protective immunity to Staphylococcus aureus infection in humans remain elusive. While the importance of cellular immunity has been shown in mice, T cell responses in humans have not been characterised. Using a murine model of recurrent S. aureus peritonitis, we demonstrated that prior exposure to S. aureus enhanced IFNγ responses upon subsequent infection, while adoptive transfer of S. aureus antigen-specific Th1 cells was protective in naïve mice. Translating these findings, we found that S. aureus antigen-specific Th1 cells were also significantly expanded during human S. aureus bloodstream infection (BSI). These Th1 cells were CD45RO+, indicative of a memory phenotype. Thus, exposure to S. aureus induces memory Th1 cells in mice and humans, identifying Th1 cells as potential S. aureus vaccine targets. Consequently, we developed a model vaccine comprising staphylococcal clumping factor A, which we demonstrate to be an effective human T cell antigen, combined with the Th1-driving adjuvant CpG. This novel Th1-inducing vaccine conferred significant protection during S. aureus infection in mice. This study notably advances our understanding of S. aureus cellular immunity, and demonstrates for the first time that a correlate of S. aureus protective immunity identified in mice may be relevant in humans. |
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While the importance of cellular immunity has been shown in mice, T cell responses in humans have not been characterised. Using a murine model of recurrent S. aureus peritonitis, we demonstrated that prior exposure to S. aureus enhanced IFNγ responses upon subsequent infection, while adoptive transfer of S. aureus antigen-specific Th1 cells was protective in naïve mice. Translating these findings, we found that S. aureus antigen-specific Th1 cells were also significantly expanded during human S. aureus bloodstream infection (BSI). These Th1 cells were CD45RO+, indicative of a memory phenotype. Thus, exposure to S. aureus induces memory Th1 cells in mice and humans, identifying Th1 cells as potential S. aureus vaccine targets. Consequently, we developed a model vaccine comprising staphylococcal clumping factor A, which we demonstrate to be an effective human T cell antigen, combined with the Th1-driving adjuvant CpG. This novel Th1-inducing vaccine conferred significant protection during S. aureus infection in mice. This study notably advances our understanding of S. aureus cellular immunity, and demonstrates for the first time that a correlate of S. aureus protective immunity identified in mice may be relevant in humans.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1005226</identifier><identifier>PMID: 26539822</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adjuvants, Immunologic - pharmacology ; Adoptive Transfer ; Adult ; Aged ; Animals ; Antigens ; Antigens - immunology ; Bacterial infections ; Bacteriology ; Care and treatment ; Clinical trials ; Complications and side effects ; Experiments ; Female ; Genetic diversity ; Genomes ; Health aspects ; Humans ; Immune system ; Immunologic Memory ; Influence ; Interferon ; Interleukin-17 - metabolism ; Lymphocytes ; Male ; Medical research ; Mice, Inbred C57BL ; Mice, Knockout ; Middle Aged ; Mortality ; Pathogens ; Staphylococcal Infections - immunology ; Staphylococcal Skin Infections - immunology ; Staphylococcal Skin Infections - microbiology ; Staphylococcus aureus - immunology ; Staphylococcus aureus infections ; Staphylococcus infections ; Th1 Cells - drug effects ; Th1 Cells - immunology ; Vaccines</subject><ispartof>PLoS pathogens, 2015-11, Vol.11 (11), p.e1005226</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Brown et al 2015 Brown et al</rights><rights>2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Infection. PLoS Pathog 11(11): e1005226. doi:10.1371/journal.ppat.1005226</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c750t-1a416a27368fb54c35414f5f653f31bd09dc9ac4c299a79ad28e828f757cb77d3</citedby><cites>FETCH-LOGICAL-c750t-1a416a27368fb54c35414f5f653f31bd09dc9ac4c299a79ad28e828f757cb77d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4634925/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4634925/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53770,53772,79347,79348</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26539822$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Miller, Lloyd S</contributor><creatorcontrib>Brown, Aisling F</creatorcontrib><creatorcontrib>Murphy, Alison G</creatorcontrib><creatorcontrib>Lalor, Stephen J</creatorcontrib><creatorcontrib>Leech, John M</creatorcontrib><creatorcontrib>O'Keeffe, Kate M</creatorcontrib><creatorcontrib>Mac Aogáin, Micheál</creatorcontrib><creatorcontrib>O'Halloran, Dara P</creatorcontrib><creatorcontrib>Lacey, Keenan A</creatorcontrib><creatorcontrib>Tavakol, Mehri</creatorcontrib><creatorcontrib>Hearnden, Claire H</creatorcontrib><creatorcontrib>Fitzgerald-Hughes, Deirdre</creatorcontrib><creatorcontrib>Humphreys, Hilary</creatorcontrib><creatorcontrib>Fennell, Jérôme P</creatorcontrib><creatorcontrib>van Wamel, Willem J</creatorcontrib><creatorcontrib>Foster, Timothy J</creatorcontrib><creatorcontrib>Geoghegan, Joan A</creatorcontrib><creatorcontrib>Lavelle, Ed C</creatorcontrib><creatorcontrib>Rogers, Thomas R</creatorcontrib><creatorcontrib>McLoughlin, Rachel M</creatorcontrib><title>Memory Th1 Cells Are Protective in Invasive Staphylococcus aureus Infection</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Mechanisms of protective immunity to Staphylococcus aureus infection in humans remain elusive. While the importance of cellular immunity has been shown in mice, T cell responses in humans have not been characterised. Using a murine model of recurrent S. aureus peritonitis, we demonstrated that prior exposure to S. aureus enhanced IFNγ responses upon subsequent infection, while adoptive transfer of S. aureus antigen-specific Th1 cells was protective in naïve mice. Translating these findings, we found that S. aureus antigen-specific Th1 cells were also significantly expanded during human S. aureus bloodstream infection (BSI). These Th1 cells were CD45RO+, indicative of a memory phenotype. Thus, exposure to S. aureus induces memory Th1 cells in mice and humans, identifying Th1 cells as potential S. aureus vaccine targets. Consequently, we developed a model vaccine comprising staphylococcal clumping factor A, which we demonstrate to be an effective human T cell antigen, combined with the Th1-driving adjuvant CpG. This novel Th1-inducing vaccine conferred significant protection during S. aureus infection in mice. This study notably advances our understanding of S. aureus cellular immunity, and demonstrates for the first time that a correlate of S. aureus protective immunity identified in mice may be relevant in humans.</description><subject>Adjuvants, Immunologic - pharmacology</subject><subject>Adoptive Transfer</subject><subject>Adult</subject><subject>Aged</subject><subject>Animals</subject><subject>Antigens</subject><subject>Antigens - immunology</subject><subject>Bacterial infections</subject><subject>Bacteriology</subject><subject>Care and treatment</subject><subject>Clinical trials</subject><subject>Complications and side effects</subject><subject>Experiments</subject><subject>Female</subject><subject>Genetic diversity</subject><subject>Genomes</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Immune system</subject><subject>Immunologic Memory</subject><subject>Influence</subject><subject>Interferon</subject><subject>Interleukin-17 - metabolism</subject><subject>Lymphocytes</subject><subject>Male</subject><subject>Medical research</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Middle Aged</subject><subject>Mortality</subject><subject>Pathogens</subject><subject>Staphylococcal Infections - immunology</subject><subject>Staphylococcal Skin Infections - immunology</subject><subject>Staphylococcal Skin Infections - microbiology</subject><subject>Staphylococcus aureus - immunology</subject><subject>Staphylococcus aureus infections</subject><subject>Staphylococcus infections</subject><subject>Th1 Cells - drug effects</subject><subject>Th1 Cells - immunology</subject><subject>Vaccines</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVkkuP0zAQxy0EYpeFb4AgEicOLfE7uSBVFY-I5SF2OVsTx25dJXFkJxX99ri0u9pIXJAteTT-zX_G40HoJc6XmEr8buen0EO7HAYYlzjPOSHiEbrEnNOFpJI9fmBfoGcx7vKcYYrFU3RBBKdlQcgl-vLVdD4cststztambWO2Cib7Efxo9Oj2JnN9VvV7iEf7ZoRhe2i99lpPMYMpmHRUvT2yvn-Onlhoo3lxPq_Qr48fbtefF9ffP1Xr1fVCS56PCwwMCyCSisLWnGnKGWaW21STpbhu8rLRJWimSVmCLKEhhSlIYSWXupayoVfo9Ul3aH1U5z5EhSUrBZGiEImoTkTjYaeG4DoIB-XBqb8OHzYKwuh0a5QoaGochsI2lkHatZGpNNkIjbGgkLTen7NNdWcabfoxQDsTnd_0bqs2fq-YoKwkPAm8OQlsIOVzvfUJ052LWq0YFekfJMeJWv6DSqsxndO-N9Yl_yzg7SwgMaP5PW5gilFVNz__g_02Z9mJ1cHHGIy9fyrO1XHy7jqujpOnzpOXwl49bNN90N2o0T8PqNSO</recordid><startdate>20151101</startdate><enddate>20151101</enddate><creator>Brown, Aisling F</creator><creator>Murphy, Alison G</creator><creator>Lalor, Stephen J</creator><creator>Leech, John M</creator><creator>O'Keeffe, Kate M</creator><creator>Mac Aogáin, Micheál</creator><creator>O'Halloran, Dara P</creator><creator>Lacey, Keenan A</creator><creator>Tavakol, Mehri</creator><creator>Hearnden, Claire H</creator><creator>Fitzgerald-Hughes, Deirdre</creator><creator>Humphreys, Hilary</creator><creator>Fennell, Jérôme P</creator><creator>van Wamel, Willem J</creator><creator>Foster, Timothy J</creator><creator>Geoghegan, Joan A</creator><creator>Lavelle, Ed C</creator><creator>Rogers, Thomas R</creator><creator>McLoughlin, Rachel M</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>ISN</scope><scope>ISR</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20151101</creationdate><title>Memory Th1 Cells Are Protective in Invasive Staphylococcus aureus Infection</title><author>Brown, Aisling F ; Murphy, Alison G ; Lalor, Stephen J ; Leech, John M ; O'Keeffe, Kate M ; Mac Aogáin, Micheál ; O'Halloran, Dara P ; Lacey, Keenan A ; Tavakol, Mehri ; Hearnden, Claire H ; Fitzgerald-Hughes, Deirdre ; Humphreys, Hilary ; Fennell, Jérôme P ; van Wamel, Willem J ; Foster, Timothy J ; Geoghegan, Joan A ; Lavelle, Ed C ; Rogers, Thomas R ; McLoughlin, Rachel M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c750t-1a416a27368fb54c35414f5f653f31bd09dc9ac4c299a79ad28e828f757cb77d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Adjuvants, Immunologic - pharmacology</topic><topic>Adoptive Transfer</topic><topic>Adult</topic><topic>Aged</topic><topic>Animals</topic><topic>Antigens</topic><topic>Antigens - immunology</topic><topic>Bacterial infections</topic><topic>Bacteriology</topic><topic>Care and treatment</topic><topic>Clinical trials</topic><topic>Complications and side effects</topic><topic>Experiments</topic><topic>Female</topic><topic>Genetic diversity</topic><topic>Genomes</topic><topic>Health aspects</topic><topic>Humans</topic><topic>Immune system</topic><topic>Immunologic Memory</topic><topic>Influence</topic><topic>Interferon</topic><topic>Interleukin-17 - metabolism</topic><topic>Lymphocytes</topic><topic>Male</topic><topic>Medical research</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Middle Aged</topic><topic>Mortality</topic><topic>Pathogens</topic><topic>Staphylococcal Infections - immunology</topic><topic>Staphylococcal Skin Infections - immunology</topic><topic>Staphylococcal Skin Infections - microbiology</topic><topic>Staphylococcus aureus - immunology</topic><topic>Staphylococcus aureus infections</topic><topic>Staphylococcus infections</topic><topic>Th1 Cells - drug effects</topic><topic>Th1 Cells - immunology</topic><topic>Vaccines</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brown, Aisling F</creatorcontrib><creatorcontrib>Murphy, Alison G</creatorcontrib><creatorcontrib>Lalor, Stephen J</creatorcontrib><creatorcontrib>Leech, John M</creatorcontrib><creatorcontrib>O'Keeffe, Kate M</creatorcontrib><creatorcontrib>Mac Aogáin, Micheál</creatorcontrib><creatorcontrib>O'Halloran, Dara P</creatorcontrib><creatorcontrib>Lacey, Keenan A</creatorcontrib><creatorcontrib>Tavakol, Mehri</creatorcontrib><creatorcontrib>Hearnden, Claire H</creatorcontrib><creatorcontrib>Fitzgerald-Hughes, Deirdre</creatorcontrib><creatorcontrib>Humphreys, Hilary</creatorcontrib><creatorcontrib>Fennell, Jérôme P</creatorcontrib><creatorcontrib>van Wamel, Willem J</creatorcontrib><creatorcontrib>Foster, Timothy J</creatorcontrib><creatorcontrib>Geoghegan, Joan A</creatorcontrib><creatorcontrib>Lavelle, Ed C</creatorcontrib><creatorcontrib>Rogers, Thomas R</creatorcontrib><creatorcontrib>McLoughlin, Rachel M</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: Canada</collection><collection>Gale In Context: Science</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brown, Aisling F</au><au>Murphy, Alison G</au><au>Lalor, Stephen J</au><au>Leech, John M</au><au>O'Keeffe, Kate M</au><au>Mac Aogáin, Micheál</au><au>O'Halloran, Dara P</au><au>Lacey, Keenan A</au><au>Tavakol, Mehri</au><au>Hearnden, Claire H</au><au>Fitzgerald-Hughes, Deirdre</au><au>Humphreys, Hilary</au><au>Fennell, Jérôme P</au><au>van Wamel, Willem J</au><au>Foster, Timothy J</au><au>Geoghegan, Joan A</au><au>Lavelle, Ed C</au><au>Rogers, Thomas R</au><au>McLoughlin, Rachel M</au><au>Miller, Lloyd S</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Memory Th1 Cells Are Protective in Invasive Staphylococcus aureus Infection</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2015-11-01</date><risdate>2015</risdate><volume>11</volume><issue>11</issue><spage>e1005226</spage><pages>e1005226-</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Mechanisms of protective immunity to Staphylococcus aureus infection in humans remain elusive. While the importance of cellular immunity has been shown in mice, T cell responses in humans have not been characterised. Using a murine model of recurrent S. aureus peritonitis, we demonstrated that prior exposure to S. aureus enhanced IFNγ responses upon subsequent infection, while adoptive transfer of S. aureus antigen-specific Th1 cells was protective in naïve mice. Translating these findings, we found that S. aureus antigen-specific Th1 cells were also significantly expanded during human S. aureus bloodstream infection (BSI). These Th1 cells were CD45RO+, indicative of a memory phenotype. Thus, exposure to S. aureus induces memory Th1 cells in mice and humans, identifying Th1 cells as potential S. aureus vaccine targets. Consequently, we developed a model vaccine comprising staphylococcal clumping factor A, which we demonstrate to be an effective human T cell antigen, combined with the Th1-driving adjuvant CpG. This novel Th1-inducing vaccine conferred significant protection during S. aureus infection in mice. This study notably advances our understanding of S. aureus cellular immunity, and demonstrates for the first time that a correlate of S. aureus protective immunity identified in mice may be relevant in humans.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26539822</pmid><doi>10.1371/journal.ppat.1005226</doi><oa>free_for_read</oa></addata></record> |
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subjects | Adjuvants, Immunologic - pharmacology Adoptive Transfer Adult Aged Animals Antigens Antigens - immunology Bacterial infections Bacteriology Care and treatment Clinical trials Complications and side effects Experiments Female Genetic diversity Genomes Health aspects Humans Immune system Immunologic Memory Influence Interferon Interleukin-17 - metabolism Lymphocytes Male Medical research Mice, Inbred C57BL Mice, Knockout Middle Aged Mortality Pathogens Staphylococcal Infections - immunology Staphylococcal Skin Infections - immunology Staphylococcal Skin Infections - microbiology Staphylococcus aureus - immunology Staphylococcus aureus infections Staphylococcus infections Th1 Cells - drug effects Th1 Cells - immunology Vaccines |
title | Memory Th1 Cells Are Protective in Invasive Staphylococcus aureus Infection |
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