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Staphylococcus aureus Targets the Duffy Antigen Receptor for Chemokines (DARC) to Lyse Erythrocytes.

Identifieur interne : 002650 ( PubMed/Checkpoint ); précédent : 002649; suivant : 002651

Staphylococcus aureus Targets the Duffy Antigen Receptor for Chemokines (DARC) to Lyse Erythrocytes.

Auteurs : András N. Spaan [Pays-Bas] ; Tamara Reyes-Robles [États-Unis] ; Cédric Badiou [France] ; Sylvie Cochet [France] ; Kristina M. Boguslawski [États-Unis] ; Pauline Yoong [États-Unis] ; Christopher J. Day [Australie] ; Carla J C. De Haas [Pays-Bas] ; Kok P M. Van Kessel [Pays-Bas] ; François Vandenesch [France] ; Michael P. Jennings [Australie] ; Caroline Le Van Kim [France] ; Yves Colin [France] ; Jos A G. Van Strijp [Pays-Bas] ; Thomas Henry [France] ; Victor J. Torres [États-Unis]

Source :

RBID : pubmed:26320997

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Abstract

In order for Staphylococcus aureus to thrive inside the mammalian host, the bacterium has to overcome iron scarcity. S. aureus is thought to produce toxins that lyse erythrocytes, releasing hemoglobin, the most abundant iron source in mammals. Here we identify the Duffy antigen receptor for chemokines (DARC) as the receptor for the S. aureus hemolytic leukocidins LukED and HlgAB. By assessing human erythrocytes with DARC polymorphisms, we determined that HlgAB- and LukED-mediated lysis directly relates to DARC expression. DARC is required for S. aureus-mediated lysis of human erythrocytes, and DARC overexpression is sufficient to render cells susceptible to toxin-mediated lysis. HlgA and LukE bind directly to DARC through different regions, and by targeting DARC, HlgAB and LukED support S. aureus growth in a hemoglobin-acquisition-dependent manner. These findings elucidate how S. aureus targets and lyses erythrocytes to release one of the scarcest nutrients within the mammalian host.

DOI: 10.1016/j.chom.2015.08.001
PubMed: 26320997


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<name sortKey="Torres, Victor J" sort="Torres, Victor J" uniqKey="Torres V" first="Victor J" last="Torres">Victor J. Torres</name>
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<title xml:lang="en">Staphylococcus aureus Targets the Duffy Antigen Receptor for Chemokines (DARC) to Lyse Erythrocytes.</title>
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<name sortKey="Spaan, Andras N" sort="Spaan, Andras N" uniqKey="Spaan A" first="András N" last="Spaan">András N. Spaan</name>
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<nlm:affiliation>CIRI, Inserm U1111, CNRS UMR 5308, Lyon, France; Université Claude Bernard Lyon-1, Ecole Normale Supérieure, 69007 Lyon, France; Department of Medical Microbiology, University Medical Center Utrecht, 3584CX Utrecht, The Netherlands.</nlm:affiliation>
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<name sortKey="Yoong, Pauline" sort="Yoong, Pauline" uniqKey="Yoong P" first="Pauline" last="Yoong">Pauline Yoong</name>
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<name sortKey="Day, Christopher J" sort="Day, Christopher J" uniqKey="Day C" first="Christopher J" last="Day">Christopher J. Day</name>
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<name sortKey="De Haas, Carla J C" sort="De Haas, Carla J C" uniqKey="De Haas C" first="Carla J C" last="De Haas">Carla J C. De Haas</name>
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<nlm:affiliation>Department of Medical Microbiology, University Medical Center Utrecht, 3584CX Utrecht, The Netherlands.</nlm:affiliation>
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<name sortKey="Vandenesch, Francois" sort="Vandenesch, Francois" uniqKey="Vandenesch F" first="François" last="Vandenesch">François Vandenesch</name>
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<nlm:affiliation>CIRI, Inserm U1111, CNRS UMR 5308, Lyon, France; Université Claude Bernard Lyon-1, Ecole Normale Supérieure, 69007 Lyon, France; Hospices Civils de Lyon, 69007 Lyon, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>CIRI, Inserm U1111, CNRS UMR 5308, Lyon, France; Université Claude Bernard Lyon-1, Ecole Normale Supérieure, 69007 Lyon, France; Hospices Civils de Lyon, 69007 Lyon</wicri:regionArea>
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<name sortKey="Jennings, Michael P" sort="Jennings, Michael P" uniqKey="Jennings M" first="Michael P" last="Jennings">Michael P. Jennings</name>
<affiliation wicri:level="1">
<nlm:affiliation>Institute for Glycomics, Griffith University, Gold Coast, Queensland 4222, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Institute for Glycomics, Griffith University, Gold Coast, Queensland 4222</wicri:regionArea>
<wicri:noRegion>Queensland 4222</wicri:noRegion>
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<name sortKey="Le Van Kim, Caroline" sort="Le Van Kim, Caroline" uniqKey="Le Van Kim C" first="Caroline" last="Le Van Kim">Caroline Le Van Kim</name>
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<nlm:affiliation>Inserm U1134, Paris, France; Université Paris Diderot, Sorbonne Paris Cité, UMR_S1134, Paris, France; Institut National de la Transfusion Sanguine, F-75739 Paris, France; Laboratoire d'Excellence GR-Ex, 75238 Paris, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Inserm U1134, Paris, France; Université Paris Diderot, Sorbonne Paris Cité, UMR_S1134, Paris, France; Institut National de la Transfusion Sanguine, F-75739 Paris, France; Laboratoire d'Excellence GR-Ex, 75238 Paris</wicri:regionArea>
<wicri:noRegion>75238 Paris</wicri:noRegion>
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<name sortKey="Colin, Yves" sort="Colin, Yves" uniqKey="Colin Y" first="Yves" last="Colin">Yves Colin</name>
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<nlm:affiliation>Inserm U1134, Paris, France; Université Paris Diderot, Sorbonne Paris Cité, UMR_S1134, Paris, France; Institut National de la Transfusion Sanguine, F-75739 Paris, France; Laboratoire d'Excellence GR-Ex, 75238 Paris, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Inserm U1134, Paris, France; Université Paris Diderot, Sorbonne Paris Cité, UMR_S1134, Paris, France; Institut National de la Transfusion Sanguine, F-75739 Paris, France; Laboratoire d'Excellence GR-Ex, 75238 Paris</wicri:regionArea>
<wicri:noRegion>75238 Paris</wicri:noRegion>
<placeName>
<settlement type="city">Paris</settlement>
<region type="région" nuts="2">Île-de-France</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Van Strijp, Jos A G" sort="Van Strijp, Jos A G" uniqKey="Van Strijp J" first="Jos A G" last="Van Strijp">Jos A G. Van Strijp</name>
<affiliation wicri:level="1">
<nlm:affiliation>Department of Medical Microbiology, University Medical Center Utrecht, 3584CX Utrecht, The Netherlands.</nlm:affiliation>
<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>Department of Medical Microbiology, University Medical Center Utrecht, 3584CX Utrecht</wicri:regionArea>
<placeName>
<settlement type="city">Utrecht</settlement>
<region nuts="2" type="province">Utrecht (province)</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Henry, Thomas" sort="Henry, Thomas" uniqKey="Henry T" first="Thomas" last="Henry">Thomas Henry</name>
<affiliation wicri:level="1">
<nlm:affiliation>CIRI, Inserm U1111, CNRS UMR 5308, Lyon, France; Université Claude Bernard Lyon-1, Ecole Normale Supérieure, 69007 Lyon, France. Electronic address: thomas.henry@inserm.fr.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>CIRI, Inserm U1111, CNRS UMR 5308, Lyon, France; Université Claude Bernard Lyon-1, Ecole Normale Supérieure, 69007 Lyon</wicri:regionArea>
<wicri:noRegion>69007 Lyon</wicri:noRegion>
<placeName>
<settlement type="city">Lyon</settlement>
<region type="region" nuts="2">Auvergne-Rhône-Alpes</region>
<region type="old region" nuts="2">Rhône-Alpes</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Torres, Victor J" sort="Torres, Victor J" uniqKey="Torres V" first="Victor J" last="Torres">Victor J. Torres</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Microbiology, New York University School of Medicine, NY 10016, USA. Electronic address: victor.torres@nyumc.org.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology, New York University School of Medicine, NY 10016</wicri:regionArea>
<placeName>
<region type="state">État de New York</region>
</placeName>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Cell host & microbe</title>
<idno type="eISSN">1934-6069</idno>
<imprint>
<date when="2015" type="published">2015</date>
</imprint>
</series>
</biblStruct>
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<profileDesc>
<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>Duffy Blood-Group System (metabolism)</term>
<term>Erythrocytes (drug effects)</term>
<term>Hemolysis</term>
<term>Host-Pathogen Interactions</term>
<term>Humans</term>
<term>Leukocidins (metabolism)</term>
<term>Protein Binding</term>
<term>Receptors, Cell Surface (metabolism)</term>
<term>Staphylococcus aureus (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Humains</term>
<term>Hémolyse</term>
<term>Interactions hôte-pathogène</term>
<term>Leucocidine (métabolisme)</term>
<term>Liaison aux protéines</term>
<term>Récepteurs de surface cellulaire (métabolisme)</term>
<term>Staphylococcus aureus (métabolisme)</term>
<term>Système Duffy (métabolisme)</term>
<term>Érythrocytes ()</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Duffy Blood-Group System</term>
<term>Leukocidins</term>
<term>Receptors, Cell Surface</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Erythrocytes</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Staphylococcus aureus</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Leucocidine</term>
<term>Récepteurs de surface cellulaire</term>
<term>Staphylococcus aureus</term>
<term>Système Duffy</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Hemolysis</term>
<term>Host-Pathogen Interactions</term>
<term>Humans</term>
<term>Protein Binding</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Humains</term>
<term>Hémolyse</term>
<term>Interactions hôte-pathogène</term>
<term>Liaison aux protéines</term>
<term>Érythrocytes</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">In order for Staphylococcus aureus to thrive inside the mammalian host, the bacterium has to overcome iron scarcity. S. aureus is thought to produce toxins that lyse erythrocytes, releasing hemoglobin, the most abundant iron source in mammals. Here we identify the Duffy antigen receptor for chemokines (DARC) as the receptor for the S. aureus hemolytic leukocidins LukED and HlgAB. By assessing human erythrocytes with DARC polymorphisms, we determined that HlgAB- and LukED-mediated lysis directly relates to DARC expression. DARC is required for S. aureus-mediated lysis of human erythrocytes, and DARC overexpression is sufficient to render cells susceptible to toxin-mediated lysis. HlgA and LukE bind directly to DARC through different regions, and by targeting DARC, HlgAB and LukED support S. aureus growth in a hemoglobin-acquisition-dependent manner. These findings elucidate how S. aureus targets and lyses erythrocytes to release one of the scarcest nutrients within the mammalian host.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">26320997</PMID>
<DateCreated>
<Year>2015</Year>
<Month>09</Month>
<Day>11</Day>
</DateCreated>
<DateCompleted>
<Year>2016</Year>
<Month>05</Month>
<Day>31</Day>
</DateCompleted>
<DateRevised>
<Year>2016</Year>
<Month>10</Month>
<Day>25</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1934-6069</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>18</Volume>
<Issue>3</Issue>
<PubDate>
<Year>2015</Year>
<Month>Sep</Month>
<Day>09</Day>
</PubDate>
</JournalIssue>
<Title>Cell host & microbe</Title>
<ISOAbbreviation>Cell Host Microbe</ISOAbbreviation>
</Journal>
<ArticleTitle>Staphylococcus aureus Targets the Duffy Antigen Receptor for Chemokines (DARC) to Lyse Erythrocytes.</ArticleTitle>
<Pagination>
<MedlinePgn>363-70</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1016/j.chom.2015.08.001</ELocationID>
<ELocationID EIdType="pii" ValidYN="Y">S1931-3128(15)00309-1</ELocationID>
<Abstract>
<AbstractText>In order for Staphylococcus aureus to thrive inside the mammalian host, the bacterium has to overcome iron scarcity. S. aureus is thought to produce toxins that lyse erythrocytes, releasing hemoglobin, the most abundant iron source in mammals. Here we identify the Duffy antigen receptor for chemokines (DARC) as the receptor for the S. aureus hemolytic leukocidins LukED and HlgAB. By assessing human erythrocytes with DARC polymorphisms, we determined that HlgAB- and LukED-mediated lysis directly relates to DARC expression. DARC is required for S. aureus-mediated lysis of human erythrocytes, and DARC overexpression is sufficient to render cells susceptible to toxin-mediated lysis. HlgA and LukE bind directly to DARC through different regions, and by targeting DARC, HlgAB and LukED support S. aureus growth in a hemoglobin-acquisition-dependent manner. These findings elucidate how S. aureus targets and lyses erythrocytes to release one of the scarcest nutrients within the mammalian host.</AbstractText>
<CopyrightInformation>Copyright © 2015 Elsevier Inc. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Spaan</LastName>
<ForeName>András N</ForeName>
<Initials>AN</Initials>
<AffiliationInfo>
<Affiliation>CIRI, Inserm U1111, CNRS UMR 5308, Lyon, France; Université Claude Bernard Lyon-1, Ecole Normale Supérieure, 69007 Lyon, France; Department of Medical Microbiology, University Medical Center Utrecht, 3584CX Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Reyes-Robles</LastName>
<ForeName>Tamara</ForeName>
<Initials>T</Initials>
<AffiliationInfo>
<Affiliation>Department of Microbiology, New York University School of Medicine, NY 10016, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Badiou</LastName>
<ForeName>Cédric</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>CIRI, Inserm U1111, CNRS UMR 5308, Lyon, France; Université Claude Bernard Lyon-1, Ecole Normale Supérieure, 69007 Lyon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Cochet</LastName>
<ForeName>Sylvie</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Inserm U1134, Paris, France; Université Paris Diderot, Sorbonne Paris Cité, UMR_S1134, Paris, France; Institut National de la Transfusion Sanguine, F-75739 Paris, France; Laboratoire d'Excellence GR-Ex, 75238 Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Boguslawski</LastName>
<ForeName>Kristina M</ForeName>
<Initials>KM</Initials>
<AffiliationInfo>
<Affiliation>Department of Microbiology, New York University School of Medicine, NY 10016, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Yoong</LastName>
<ForeName>Pauline</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>Department of Microbiology, New York University School of Medicine, NY 10016, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Day</LastName>
<ForeName>Christopher J</ForeName>
<Initials>CJ</Initials>
<AffiliationInfo>
<Affiliation>Institute for Glycomics, Griffith University, Gold Coast, Queensland 4222, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>de Haas</LastName>
<ForeName>Carla J C</ForeName>
<Initials>CJ</Initials>
<AffiliationInfo>
<Affiliation>Department of Medical Microbiology, University Medical Center Utrecht, 3584CX Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>van Kessel</LastName>
<ForeName>Kok P M</ForeName>
<Initials>KP</Initials>
<AffiliationInfo>
<Affiliation>Department of Medical Microbiology, University Medical Center Utrecht, 3584CX Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Vandenesch</LastName>
<ForeName>François</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>CIRI, Inserm U1111, CNRS UMR 5308, Lyon, France; Université Claude Bernard Lyon-1, Ecole Normale Supérieure, 69007 Lyon, France; Hospices Civils de Lyon, 69007 Lyon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Jennings</LastName>
<ForeName>Michael P</ForeName>
<Initials>MP</Initials>
<AffiliationInfo>
<Affiliation>Institute for Glycomics, Griffith University, Gold Coast, Queensland 4222, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Le Van Kim</LastName>
<ForeName>Caroline</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Inserm U1134, Paris, France; Université Paris Diderot, Sorbonne Paris Cité, UMR_S1134, Paris, France; Institut National de la Transfusion Sanguine, F-75739 Paris, France; Laboratoire d'Excellence GR-Ex, 75238 Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Colin</LastName>
<ForeName>Yves</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Inserm U1134, Paris, France; Université Paris Diderot, Sorbonne Paris Cité, UMR_S1134, Paris, France; Institut National de la Transfusion Sanguine, F-75739 Paris, France; Laboratoire d'Excellence GR-Ex, 75238 Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>van Strijp</LastName>
<ForeName>Jos A G</ForeName>
<Initials>JA</Initials>
<AffiliationInfo>
<Affiliation>Department of Medical Microbiology, University Medical Center Utrecht, 3584CX Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Henry</LastName>
<ForeName>Thomas</ForeName>
<Initials>T</Initials>
<AffiliationInfo>
<Affiliation>CIRI, Inserm U1111, CNRS UMR 5308, Lyon, France; Université Claude Bernard Lyon-1, Ecole Normale Supérieure, 69007 Lyon, France. Electronic address: thomas.henry@inserm.fr.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Torres</LastName>
<ForeName>Victor J</ForeName>
<Initials>VJ</Initials>
<AffiliationInfo>
<Affiliation>Department of Microbiology, New York University School of Medicine, NY 10016, USA. Electronic address: victor.torres@nyumc.org.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<GrantID>R01 AI099394</GrantID>
<Acronym>AI</Acronym>
<Agency>NIAID NIH HHS</Agency>
<Country>United States</Country>
</Grant>
<Grant>
<GrantID>T32 GM007308</GrantID>
<Acronym>GM</Acronym>
<Agency>NIGMS NIH HHS</Agency>
<Country>United States</Country>
</Grant>
<Grant>
<GrantID>R01 AI105129</GrantID>
<Acronym>AI</Acronym>
<Agency>NIAID NIH HHS</Agency>
<Country>United States</Country>
</Grant>
<Grant>
<GrantID>F31 AI112290</GrantID>
<Acronym>AI</Acronym>
<Agency>NIAID NIH HHS</Agency>
<Country>United States</Country>
</Grant>
<Grant>
<GrantID>T32 AI007180</GrantID>
<Acronym>AI</Acronym>
<Agency>NIAID NIH HHS</Agency>
<Country>United States</Country>
</Grant>
<Grant>
<GrantID>F32 AI098395</GrantID>
<Acronym>AI</Acronym>
<Agency>NIAID NIH HHS</Agency>
<Country>United States</Country>
</Grant>
</GrantList>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2015</Year>
<Month>08</Month>
<Day>27</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Cell Host Microbe</MedlineTA>
<NlmUniqueID>101302316</NlmUniqueID>
<ISSNLinking>1931-3128</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C473745">DARC protein, human</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D004375">Duffy Blood-Group System</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D007956">Leukocidins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011956">Receptors, Cell Surface</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
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<CommentsCorrections RefType="Cites">
<RefSource>Nat Genet. 1995 Jun;10(2):224-8</RefSource>
<PMID Version="1">7663520</PMID>
</CommentsCorrections>
<CommentsCorrections RefType="CommentIn">
<RefSource>Cell Host Microbe. 2015 Sep 9;18(3):272-4</RefSource>
<PMID Version="1">26355213</PMID>
</CommentsCorrections>
</CommentsCorrectionsList>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D004375" MajorTopicYN="N">Duffy Blood-Group System</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D004912" MajorTopicYN="N">Erythrocytes</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006461" MajorTopicYN="Y">Hemolysis</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D054884" MajorTopicYN="Y">Host-Pathogen Interactions</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D007956" MajorTopicYN="N">Leukocidins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011485" MajorTopicYN="N">Protein Binding</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011956" MajorTopicYN="N">Receptors, Cell Surface</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013211" MajorTopicYN="N">Staphylococcus aureus</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
<OtherID Source="NLM">NIHMS713749</OtherID>
<OtherID Source="NLM">PMC4578157</OtherID>
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<Year>2015</Year>
<Month>04</Month>
<Day>10</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised">
<Year>2015</Year>
<Month>07</Month>
<Day>02</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2015</Year>
<Month>08</Month>
<Day>03</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2015</Year>
<Month>9</Month>
<Day>1</Day>
<Hour>6</Hour>
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<PubMedPubDate PubStatus="pubmed">
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<PubMedPubDate PubStatus="medline">
<Year>2016</Year>
<Month>6</Month>
<Day>1</Day>
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<PublicationStatus>ppublish</PublicationStatus>
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<ArticleId IdType="pii">S1931-3128(15)00309-1</ArticleId>
<ArticleId IdType="doi">10.1016/j.chom.2015.08.001</ArticleId>
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<li>Australie</li>
<li>France</li>
<li>Pays-Bas</li>
<li>États-Unis</li>
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<region>
<li>Auvergne-Rhône-Alpes</li>
<li>Rhône-Alpes</li>
<li>Utrecht (province)</li>
<li>État de New York</li>
<li>Île-de-France</li>
</region>
<settlement>
<li>Lyon</li>
<li>Paris</li>
<li>Utrecht</li>
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<country name="Pays-Bas">
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<name sortKey="De Haas, Carla J C" sort="De Haas, Carla J C" uniqKey="De Haas C" first="Carla J C" last="De Haas">Carla J C. De Haas</name>
<name sortKey="Van Kessel, Kok P M" sort="Van Kessel, Kok P M" uniqKey="Van Kessel K" first="Kok P M" last="Van Kessel">Kok P M. Van Kessel</name>
<name sortKey="Van Strijp, Jos A G" sort="Van Strijp, Jos A G" uniqKey="Van Strijp J" first="Jos A G" last="Van Strijp">Jos A G. Van Strijp</name>
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<region name="État de New York">
<name sortKey="Reyes Robles, Tamara" sort="Reyes Robles, Tamara" uniqKey="Reyes Robles T" first="Tamara" last="Reyes-Robles">Tamara Reyes-Robles</name>
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<name sortKey="Boguslawski, Kristina M" sort="Boguslawski, Kristina M" uniqKey="Boguslawski K" first="Kristina M" last="Boguslawski">Kristina M. Boguslawski</name>
<name sortKey="Torres, Victor J" sort="Torres, Victor J" uniqKey="Torres V" first="Victor J" last="Torres">Victor J. Torres</name>
<name sortKey="Yoong, Pauline" sort="Yoong, Pauline" uniqKey="Yoong P" first="Pauline" last="Yoong">Pauline Yoong</name>
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<country name="France">
<region name="Auvergne-Rhône-Alpes">
<name sortKey="Badiou, Cedric" sort="Badiou, Cedric" uniqKey="Badiou C" first="Cédric" last="Badiou">Cédric Badiou</name>
</region>
<name sortKey="Cochet, Sylvie" sort="Cochet, Sylvie" uniqKey="Cochet S" first="Sylvie" last="Cochet">Sylvie Cochet</name>
<name sortKey="Colin, Yves" sort="Colin, Yves" uniqKey="Colin Y" first="Yves" last="Colin">Yves Colin</name>
<name sortKey="Henry, Thomas" sort="Henry, Thomas" uniqKey="Henry T" first="Thomas" last="Henry">Thomas Henry</name>
<name sortKey="Le Van Kim, Caroline" sort="Le Van Kim, Caroline" uniqKey="Le Van Kim C" first="Caroline" last="Le Van Kim">Caroline Le Van Kim</name>
<name sortKey="Vandenesch, Francois" sort="Vandenesch, Francois" uniqKey="Vandenesch F" first="François" last="Vandenesch">François Vandenesch</name>
</country>
<country name="Australie">
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<name sortKey="Day, Christopher J" sort="Day, Christopher J" uniqKey="Day C" first="Christopher J" last="Day">Christopher J. Day</name>
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<name sortKey="Jennings, Michael P" sort="Jennings, Michael P" uniqKey="Jennings M" first="Michael P" last="Jennings">Michael P. Jennings</name>
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