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Legionella pneumophila Strain 130b Evades Macrophage Cell Death Independent of the Effector SidF in the Absence of Flagellin.

Identifieur interne : 001126 ( PubMed/Curation ); précédent : 001125; suivant : 001127

Legionella pneumophila Strain 130b Evades Macrophage Cell Death Independent of the Effector SidF in the Absence of Flagellin.

Auteurs : Mary Speir [Australie] ; Adam Vogrin [Australie] ; Azadeh Seidi [Australie] ; Gilu Abraham [Australie] ; Stéphane Hunot [France] ; Qingqing Han [États-Unis] ; Gerald W. Dorn [États-Unis] ; Seth L. Masters [Australie] ; Richard A. Flavell [États-Unis] ; James E. Vince [Australie] ; Thomas Naderer [Australie]

Source :

Frontiers in cellular and infection microbiology [ 2235-2988 ] ; 2017.

RBID : pubmed:28261564

Descripteurs français

KwdFr :
- Animaux, Apoptose, Délétion de gène, Facteurs de virulence (génétique), Femelle, Flagelline (génétique), Flagelline (métabolisme), Interactions hôte-pathogène, Legionella pneumophila (physiologie), Macrophages (microbiologie), Macrophages (métabolisme), Maladie des légionnaires (microbiologie), Maladie des légionnaires (métabolisme), Mitochondries (génétique), Mitochondries (métabolisme), Mort cellulaire, Protéines bactériennes (génétique), Protéines bactériennes (métabolisme), Protéines membranaires (métabolisme), Protéines mitochondriales (métabolisme), Protéines régulatrices de l'apoptose (métabolisme), Souris, Survie cellulaire.
MESH :
- génétique : Facteurs de virulence, Flagelline, Mitochondries, Protéines bactériennes.
- microbiologie : Macrophages, Maladie des légionnaires.
- métabolisme : Flagelline, Macrophages, Maladie des légionnaires, Mitochondries, Protéines bactériennes, Protéines membranaires, Protéines mitochondriales, Protéines régulatrices de l'apoptose.
- physiologie : Legionella pneumophila.
- Animaux, Apoptose, Délétion de gène, Femelle, Interactions hôte-pathogène, Mort cellulaire, Souris, Survie cellulaire.

English descriptors

KwdEn :
- Animals, Apoptosis, Apoptosis Regulatory Proteins (metabolism), Bacterial Proteins (genetics), Bacterial Proteins (metabolism), Cell Death, Cell Survival, Female, Flagellin (genetics), Flagellin (metabolism), Gene Deletion, Host-Pathogen Interactions, Legionella pneumophila (physiology), Legionnaires' Disease (metabolism), Legionnaires' Disease (microbiology), Macrophages (metabolism), Macrophages (microbiology), Membrane Proteins (metabolism), Mice, Mitochondria (genetics), Mitochondria (metabolism), Mitochondrial Proteins (metabolism), Virulence Factors (genetics).
MESH :
- chemical , genetics : Bacterial Proteins, Flagellin, Virulence Factors.
- chemical , metabolism : Apoptosis Regulatory Proteins, Bacterial Proteins, Flagellin, Membrane Proteins, Mitochondrial Proteins.
- genetics : Mitochondria.
- metabolism : Legionnaires' Disease, Macrophages, Mitochondria.
- microbiology : Legionnaires' Disease, Macrophages.
- physiology : Legionella pneumophila.
- Animals, Apoptosis, Cell Death, Cell Survival, Female, Gene Deletion, Host-Pathogen Interactions, Mice.

Abstract

The human pathogen Legionella pneumophila must evade host cell death signaling to enable replication in lung macrophages and to cause disease. After bacterial growth, however, L. pneumophila is thought to induce apoptosis during egress from macrophages. The bacterial effector protein, SidF, has been shown to control host cell survival and death by inhibiting pro-apoptotic BNIP3 and BCL-RAMBO signaling. Using live-cell imaging to follow the L. pneumophila-macrophage interaction, we now demonstrate that L. pneumophila evades host cell apoptosis independent of SidF. In the absence of SidF, L. pneumophila was able to replicate, cause loss of mitochondria membrane potential, kill macrophages, and establish infections in lungs of mice. Consistent with this, deletion of BNIP3 and BCL-RAMBO did not affect intracellular L. pneumophila replication, macrophage death rates, and in vivo bacterial virulence. Abrogating mitochondrial cell death by genetic deletion of the effectors of intrinsic apoptosis, BAX, and BAK, or the regulator of mitochondrial permeability transition pore formation, cyclophilin-D, did not affect bacterial growth or the initial killing of macrophages. Loss of BAX and BAK only marginally limited the ability of L. pneumophila to efficiently kill all macrophages over extended periods. L. pneumophila induced killing of macrophages was delayed in the absence of capsase-11 mediated pyroptosis. Together, our data demonstrate that L. pneumophila evades host cell death responses independently of SidF during replication and can induce pyroptosis to kill macrophages in a timely manner.

DOI: 10.3389/fcimb.2017.00035
PubMed: 28261564

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<term>Apoptosis</term>
<term>Apoptosis Regulatory Proteins (metabolism)</term>
<term>Bacterial Proteins (genetics)</term>
<term>Bacterial Proteins (metabolism)</term>
<term>Cell Death</term>
<term>Cell Survival</term>
<term>Female</term>
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<term>Flagellin (metabolism)</term>
<term>Gene Deletion</term>
<term>Host-Pathogen Interactions</term>
<term>Legionella pneumophila (physiology)</term>
<term>Legionnaires' Disease (metabolism)</term>
<term>Legionnaires' Disease (microbiology)</term>
<term>Macrophages (metabolism)</term>
<term>Macrophages (microbiology)</term>
<term>Membrane Proteins (metabolism)</term>
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<term>Mitochondria (genetics)</term>
<term>Mitochondria (metabolism)</term>
<term>Mitochondrial Proteins (metabolism)</term>
<term>Virulence Factors (genetics)</term>
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<term>Apoptose</term>
<term>Délétion de gène</term>
<term>Facteurs de virulence (génétique)</term>
<term>Femelle</term>
<term>Flagelline (génétique)</term>
<term>Flagelline (métabolisme)</term>
<term>Interactions hôte-pathogène</term>
<term>Legionella pneumophila (physiologie)</term>
<term>Macrophages (microbiologie)</term>
<term>Macrophages (métabolisme)</term>
<term>Maladie des légionnaires (microbiologie)</term>
<term>Maladie des légionnaires (métabolisme)</term>
<term>Mitochondries (génétique)</term>
<term>Mitochondries (métabolisme)</term>
<term>Mort cellulaire</term>
<term>Protéines bactériennes (génétique)</term>
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<term>Souris</term>
<term>Survie cellulaire</term>
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<term>Flagellin</term>
<term>Virulence Factors</term>
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<term>Bacterial Proteins</term>
<term>Flagellin</term>
<term>Membrane Proteins</term>
<term>Mitochondrial Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Mitochondria</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Facteurs de virulence</term>
<term>Flagelline</term>
<term>Mitochondries</term>
<term>Protéines bactériennes</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Legionnaires' Disease</term>
<term>Macrophages</term>
<term>Mitochondria</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Macrophages</term>
<term>Maladie des légionnaires</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Legionnaires' Disease</term>
<term>Macrophages</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Flagelline</term>
<term>Macrophages</term>
<term>Maladie des légionnaires</term>
<term>Mitochondries</term>
<term>Protéines bactériennes</term>
<term>Protéines membranaires</term>
<term>Protéines mitochondriales</term>
<term>Protéines régulatrices de l'apoptose</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Legionella pneumophila</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Legionella pneumophila</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Animals</term>
<term>Apoptosis</term>
<term>Cell Death</term>
<term>Cell Survival</term>
<term>Female</term>
<term>Gene Deletion</term>
<term>Host-Pathogen Interactions</term>
<term>Mice</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Animaux</term>
<term>Apoptose</term>
<term>Délétion de gène</term>
<term>Femelle</term>
<term>Interactions hôte-pathogène</term>
<term>Mort cellulaire</term>
<term>Souris</term>
<term>Survie cellulaire</term>
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<front><div type="abstract" xml:lang="en">The human pathogen Legionella pneumophila must evade host cell death signaling to enable replication in lung macrophages and to cause disease. After bacterial growth, however, L. pneumophila is thought to induce apoptosis during egress from macrophages. The bacterial effector protein, SidF, has been shown to control host cell survival and death by inhibiting pro-apoptotic BNIP3 and BCL-RAMBO signaling. Using live-cell imaging to follow the L. pneumophila-macrophage interaction, we now demonstrate that L. pneumophila evades host cell apoptosis independent of SidF. In the absence of SidF, L. pneumophila was able to replicate, cause loss of mitochondria membrane potential, kill macrophages, and establish infections in lungs of mice. Consistent with this, deletion of BNIP3 and BCL-RAMBO did not affect intracellular L. pneumophila replication, macrophage death rates, and in vivo bacterial virulence. Abrogating mitochondrial cell death by genetic deletion of the effectors of intrinsic apoptosis, BAX, and BAK, or the regulator of mitochondrial permeability transition pore formation, cyclophilin-D, did not affect bacterial growth or the initial killing of macrophages. Loss of BAX and BAK only marginally limited the ability of L. pneumophila to efficiently kill all macrophages over extended periods. L. pneumophila induced killing of macrophages was delayed in the absence of capsase-11 mediated pyroptosis. Together, our data demonstrate that L. pneumophila evades host cell death responses independently of SidF during replication and can induce pyroptosis to kill macrophages in a timely manner.</div>
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<Abstract><AbstractText>The human pathogen Legionella pneumophila must evade host cell death signaling to enable replication in lung macrophages and to cause disease. After bacterial growth, however, L. pneumophila is thought to induce apoptosis during egress from macrophages. The bacterial effector protein, SidF, has been shown to control host cell survival and death by inhibiting pro-apoptotic BNIP3 and BCL-RAMBO signaling. Using live-cell imaging to follow the L. pneumophila-macrophage interaction, we now demonstrate that L. pneumophila evades host cell apoptosis independent of SidF. In the absence of SidF, L. pneumophila was able to replicate, cause loss of mitochondria membrane potential, kill macrophages, and establish infections in lungs of mice. Consistent with this, deletion of BNIP3 and BCL-RAMBO did not affect intracellular L. pneumophila replication, macrophage death rates, and in vivo bacterial virulence. Abrogating mitochondrial cell death by genetic deletion of the effectors of intrinsic apoptosis, BAX, and BAK, or the regulator of mitochondrial permeability transition pore formation, cyclophilin-D, did not affect bacterial growth or the initial killing of macrophages. Loss of BAX and BAK only marginally limited the ability of L. pneumophila to efficiently kill all macrophages over extended periods. L. pneumophila induced killing of macrophages was delayed in the absence of capsase-11 mediated pyroptosis. Together, our data demonstrate that L. pneumophila evades host cell death responses independently of SidF during replication and can induce pyroptosis to kill macrophages in a timely manner.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Speir</LastName>
<ForeName>Mary</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University Clayton, VIC, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Vogrin</LastName>
<ForeName>Adam</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University Clayton, VIC, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Seidi</LastName>
<ForeName>Azadeh</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University Clayton, VIC, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Abraham</LastName>
<ForeName>Gilu</ForeName>
<Initials>G</Initials>
<AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University Clayton, VIC, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Hunot</LastName>
<ForeName>Stéphane</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Department of Immunobiology, Howard Hughes Medical Institute, Yale University School of MedicineNew Haven, CT, USA; Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale, Institut du Cerveau et la Moelle - Hôpital Pitié-Salpêtrière, Boulevard de l'hôpital, Sorbonne Universités, UPMC Univ Paris 06Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Han</LastName>
<ForeName>Qingqing</ForeName>
<Initials>Q</Initials>
<AffiliationInfo><Affiliation>Department of Immunobiology, Howard Hughes Medical Institute, Yale University School of Medicine New Haven, CT, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Dorn</LastName>
<ForeName>Gerald W</ForeName>
<Initials>GW</Initials>
<Suffix>2nd</Suffix>
<AffiliationInfo><Affiliation>Department of Medicine, Center for Pharmacogenomics, Washington University School of Medicine St. Louis, MO, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Masters</LastName>
<ForeName>Seth L</ForeName>
<Initials>SL</Initials>
<AffiliationInfo><Affiliation>Walter and Eliza Hall Institute of Medical ResearchParkville, VIC, Australia; Department of Medical Biology, University of MelbourneParkville, VIC, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Flavell</LastName>
<ForeName>Richard A</ForeName>
<Initials>RA</Initials>
<AffiliationInfo><Affiliation>Department of Immunobiology, Howard Hughes Medical Institute, Yale University School of Medicine New Haven, CT, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Vince</LastName>
<ForeName>James E</ForeName>
<Initials>JE</Initials>
<AffiliationInfo><Affiliation>Walter and Eliza Hall Institute of Medical ResearchParkville, VIC, Australia; Department of Medical Biology, University of MelbourneParkville, VIC, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Naderer</LastName>
<ForeName>Thomas</ForeName>
<Initials>T</Initials>
<AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University Clayton, VIC, Australia.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2017</Year>
<Month>02</Month>
<Day>16</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>Switzerland</Country>
<MedlineTA>Front Cell Infect Microbiol</MedlineTA>
<NlmUniqueID>101585359</NlmUniqueID>
<ISSNLinking>2235-2988</ISSNLinking>
</MedlineJournalInfo>
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<NameOfSubstance UI="D051017">Apoptosis Regulatory Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C508686">BNip3 protein, mouse</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
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<Chemical><RegistryNumber>12777-81-0</RegistryNumber>
<NameOfSubstance UI="D005408">Flagellin</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
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<MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D017209" MajorTopicYN="N">Apoptosis</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D051017" MajorTopicYN="N">Apoptosis Regulatory Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D001426" MajorTopicYN="N">Bacterial Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D016923" MajorTopicYN="N">Cell Death</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002470" MajorTopicYN="N">Cell Survival</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005260" MajorTopicYN="N">Female</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005408" MajorTopicYN="N">Flagellin</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D017353" MajorTopicYN="N">Gene Deletion</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D054884" MajorTopicYN="N">Host-Pathogen Interactions</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D016952" MajorTopicYN="N">Legionella pneumophila</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D007877" MajorTopicYN="N">Legionnaires' Disease</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008264" MajorTopicYN="N">Macrophages</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008565" MajorTopicYN="N">Membrane Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008928" MajorTopicYN="N">Mitochondria</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D024101" MajorTopicYN="N">Mitochondrial Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D037521" MajorTopicYN="N">Virulence Factors</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">bacteria</Keyword>
<Keyword MajorTopicYN="N">caspases</Keyword>
<Keyword MajorTopicYN="N">infection</Keyword>
<Keyword MajorTopicYN="N">live-cell imaging</Keyword>
<Keyword MajorTopicYN="N">mitochondria</Keyword>
<Keyword MajorTopicYN="N">pneumonia</Keyword>
<Keyword MajorTopicYN="N">pyroptosis</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2016</Year>
<Month>09</Month>
<Day>29</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted"><Year>2017</Year>
<Month>01</Month>
<Day>30</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez"><Year>2017</Year>
<Month>3</Month>
<Day>7</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="pubmed"><Year>2017</Year>
<Month>3</Month>
<Day>7</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline"><Year>2017</Year>
<Month>7</Month>
<Day>1</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>epublish</PublicationStatus>
<ArticleIdList><ArticleId IdType="pubmed">28261564</ArticleId>
<ArticleId IdType="doi">10.3389/fcimb.2017.00035</ArticleId>
<ArticleId IdType="pmc">PMC5311068</ArticleId>
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Legionella pneumophila Strain 130b Evades Macrophage Cell Death Independent of the Effector SidF in the Absence of Flagellin.

Legionella pneumophila Strain 130b Evades Macrophage Cell Death Independent of the Effector SidF in the Absence of Flagellin.

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