Serveur d'exploration sur la glutarédoxine

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Deletion of glutaredoxin promotes oxidative tolerance and intracellular infection in Listeria monocytogenes.

Identifieur interne : 000179 ( Main/Exploration ); précédent : 000178; suivant : 000180

Deletion of glutaredoxin promotes oxidative tolerance and intracellular infection in Listeria monocytogenes.

Auteurs : Jing Sun [République populaire de Chine] ; Yi Hang [République populaire de Chine] ; Yue Han [République populaire de Chine] ; Xian Zhang [République populaire de Chine] ; Li Gan [République populaire de Chine] ; Chang Cai [République populaire de Chine, Australie] ; Zhongwei Chen [République populaire de Chine] ; Yang Yang [République populaire de Chine] ; Quanjiang Song [République populaire de Chine] ; Chunyan Shao [République populaire de Chine] ; Yongchun Yang [République populaire de Chine] ; Yingshan Zhou [République populaire de Chine] ; Xiaodu Wang [République populaire de Chine] ; Changyong Cheng [République populaire de Chine] ; Houhui Song [République populaire de Chine]

Source :

RBID : pubmed:31680614

Descripteurs français

English descriptors

Abstract

Thiol-disulfide glutaredoxin systems of bacterial cytoplasm favor reducing conditions for the correct disulfide bonding of functional proteins, and therefore were employed by bacteria to defend against oxidative stress. Listeria monocytogenes has been shown to encode a putative glutaredoxin, Grx (encoded by lmo2344), while the underlying roles remain unknown. Here we suggest an unexpected role of L. monocytogenes Grx in oxidative tolerance and intracellular infection. The recombinant Grx was able to efficiently catalyze the thiol-disulfide oxidoreduction of insulin in the presence of DTT as an election donor. Unexpectedly, the deletion of grx resulted in a remarkably increased tolerance and survival ability of this bacteria when exposed to various oxidizing agents, including diamide, and copper and cadmium ions. Furthermore, loss of grx significantly promoted bacterial invasion and proliferation in human epithelial Caco-2 cells and murine macrophages, as well as a notably increasing invasion but not cell-to-cell spread in the murine fibroblasts L929 cells. More importantly, L. monocytogenes lacking the glutaredoxin exhibited more efficient proliferation and recovery in the spleens and livers of the infected mice, and hence became more virulent by upregulating the virulence factors, InlA and InlB. In summary, we here for the first time demonstrated that L. monocytogenes glutaredoxin plays a counterintuitive role in bacterial oxidative resistance and intracellular infection, which is the first report to provide valuable evidence for the role of glutaredoxins in bacterial infection, and more importantly suggests a favorable model to illustrate the functional diversity of bacterial Grx systems during environmental adaption and host infection.

DOI: 10.1080/21505594.2019.1685640
PubMed: 31680614
PubMed Central: PMC6844310


Affiliations:


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<name sortKey="Gan, Li" sort="Gan, Li" uniqKey="Gan L" first="Li" last="Gan">Li Gan</name>
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<nlm:affiliation>Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, China-Australian Joint Laboratory for Animal Health Big Data Analytics, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University, Hangzhou, P. R. China.</nlm:affiliation>
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<nlm:affiliation>Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, China-Australian Joint Laboratory for Animal Health Big Data Analytics, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University, Hangzhou, P. R. China.</nlm:affiliation>
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<name sortKey="Zhou, Yingshan" sort="Zhou, Yingshan" uniqKey="Zhou Y" first="Yingshan" last="Zhou">Yingshan Zhou</name>
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<nlm:affiliation>Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, China-Australian Joint Laboratory for Animal Health Big Data Analytics, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University, Hangzhou, P. R. China.</nlm:affiliation>
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<name sortKey="Wang, Xiaodu" sort="Wang, Xiaodu" uniqKey="Wang X" first="Xiaodu" last="Wang">Xiaodu Wang</name>
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<nlm:affiliation>Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, China-Australian Joint Laboratory for Animal Health Big Data Analytics, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University, Hangzhou, P. R. China.</nlm:affiliation>
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<name sortKey="Cheng, Changyong" sort="Cheng, Changyong" uniqKey="Cheng C" first="Changyong" last="Cheng">Changyong Cheng</name>
<affiliation wicri:level="3">
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<author>
<name sortKey="Song, Houhui" sort="Song, Houhui" uniqKey="Song H" first="Houhui" last="Song">Houhui Song</name>
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<series>
<title level="j">Virulence</title>
<idno type="eISSN">2150-5608</idno>
<imprint>
<date when="2019" type="published">2019</date>
</imprint>
</series>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Animals (MeSH)</term>
<term>Bacterial Proteins (genetics)</term>
<term>Caco-2 Cells (MeSH)</term>
<term>Cell Line (MeSH)</term>
<term>Cytoplasm (microbiology)</term>
<term>Epithelial Cells (microbiology)</term>
<term>Female (MeSH)</term>
<term>Fibroblasts (microbiology)</term>
<term>Gene Deletion (MeSH)</term>
<term>Glutaredoxins (genetics)</term>
<term>Humans (MeSH)</term>
<term>Insulin (metabolism)</term>
<term>Listeria monocytogenes (drug effects)</term>
<term>Listeria monocytogenes (genetics)</term>
<term>Listeria monocytogenes (pathogenicity)</term>
<term>Listeriosis (microbiology)</term>
<term>Macrophages (microbiology)</term>
<term>Mice (MeSH)</term>
<term>Mice, Inbred ICR (MeSH)</term>
<term>Oxidants (pharmacology)</term>
<term>Oxidative Stress (MeSH)</term>
<term>Virulence Factors (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Animaux (MeSH)</term>
<term>Cellules Caco-2 (MeSH)</term>
<term>Cellules épithéliales (microbiologie)</term>
<term>Cytoplasme (microbiologie)</term>
<term>Délétion de gène (MeSH)</term>
<term>Facteurs de virulence (MeSH)</term>
<term>Femelle (MeSH)</term>
<term>Fibroblastes (microbiologie)</term>
<term>Glutarédoxines (génétique)</term>
<term>Humains (MeSH)</term>
<term>Infections à Listeria (microbiologie)</term>
<term>Insuline (métabolisme)</term>
<term>Lignée cellulaire (MeSH)</term>
<term>Listeria monocytogenes (effets des médicaments et des substances chimiques)</term>
<term>Listeria monocytogenes (génétique)</term>
<term>Listeria monocytogenes (pathogénicité)</term>
<term>Macrophages (microbiologie)</term>
<term>Oxydants (pharmacologie)</term>
<term>Protéines bactériennes (génétique)</term>
<term>Souris (MeSH)</term>
<term>Souris de lignée ICR (MeSH)</term>
<term>Stress oxydatif (MeSH)</term>
</keywords>
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<term>Bacterial Proteins</term>
<term>Glutaredoxins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Insulin</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Listeria monocytogenes</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr">
<term>Listeria monocytogenes</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Listeria monocytogenes</term>
</keywords>
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<term>Glutarédoxines</term>
<term>Listeria monocytogenes</term>
<term>Protéines bactériennes</term>
</keywords>
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<term>Cellules épithéliales</term>
<term>Cytoplasme</term>
<term>Fibroblastes</term>
<term>Infections à Listeria</term>
<term>Macrophages</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Cytoplasm</term>
<term>Epithelial Cells</term>
<term>Fibroblasts</term>
<term>Listeriosis</term>
<term>Macrophages</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Insuline</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en">
<term>Listeria monocytogenes</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr">
<term>Listeria monocytogenes</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Oxydants</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Oxidants</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>Caco-2 Cells</term>
<term>Cell Line</term>
<term>Female</term>
<term>Gene Deletion</term>
<term>Humans</term>
<term>Mice</term>
<term>Mice, Inbred ICR</term>
<term>Oxidative Stress</term>
<term>Virulence Factors</term>
</keywords>
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<term>Animaux</term>
<term>Cellules Caco-2</term>
<term>Délétion de gène</term>
<term>Facteurs de virulence</term>
<term>Femelle</term>
<term>Humains</term>
<term>Lignée cellulaire</term>
<term>Souris</term>
<term>Souris de lignée ICR</term>
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<front>
<div type="abstract" xml:lang="en">Thiol-disulfide glutaredoxin systems of bacterial cytoplasm favor reducing conditions for the correct disulfide bonding of functional proteins, and therefore were employed by bacteria to defend against oxidative stress.
<i>Listeria monocytogenes</i>
has been shown to encode a putative glutaredoxin, Grx (encoded by
<i>lmo2344</i>
), while the underlying roles remain unknown. Here we suggest an unexpected role of
<i>L. monocytogenes</i>
Grx in oxidative tolerance and intracellular infection. The recombinant Grx was able to efficiently catalyze the thiol-disulfide oxidoreduction of insulin in the presence of DTT as an election donor. Unexpectedly, the deletion of
<i>grx</i>
resulted in a remarkably increased tolerance and survival ability of this bacteria when exposed to various oxidizing agents, including diamide, and copper and cadmium ions. Furthermore, loss of
<i>grx</i>
significantly promoted bacterial invasion and proliferation in human epithelial Caco-2 cells and murine macrophages, as well as a notably increasing invasion but not cell-to-cell spread in the murine fibroblasts L929 cells. More importantly,
<i>L. monocytogenes</i>
lacking the glutaredoxin exhibited more efficient proliferation and recovery in the spleens and livers of the infected mice, and hence became more virulent by upregulating the virulence factors, InlA and InlB. In summary, we here for the first time demonstrated that
<i>L. monocytogenes</i>
glutaredoxin plays a counterintuitive role in bacterial oxidative resistance and intracellular infection, which is the first report to provide valuable evidence for the role of glutaredoxins in bacterial infection, and more importantly suggests a favorable model to illustrate the functional diversity of bacterial Grx systems during environmental adaption and host infection.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">31680614</PMID>
<DateCompleted>
<Year>2020</Year>
<Month>08</Month>
<Day>03</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>08</Month>
<Day>03</Day>
</DateRevised>
<Article PubModel="Print">
<Journal>
<ISSN IssnType="Electronic">2150-5608</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>10</Volume>
<Issue>1</Issue>
<PubDate>
<Year>2019</Year>
<Month>12</Month>
</PubDate>
</JournalIssue>
<Title>Virulence</Title>
<ISOAbbreviation>Virulence</ISOAbbreviation>
</Journal>
<ArticleTitle>Deletion of glutaredoxin promotes oxidative tolerance and intracellular infection in
<i>Listeria monocytogenes</i>
.</ArticleTitle>
<Pagination>
<MedlinePgn>910-924</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1080/21505594.2019.1685640</ELocationID>
<Abstract>
<AbstractText>Thiol-disulfide glutaredoxin systems of bacterial cytoplasm favor reducing conditions for the correct disulfide bonding of functional proteins, and therefore were employed by bacteria to defend against oxidative stress.
<i>Listeria monocytogenes</i>
has been shown to encode a putative glutaredoxin, Grx (encoded by
<i>lmo2344</i>
), while the underlying roles remain unknown. Here we suggest an unexpected role of
<i>L. monocytogenes</i>
Grx in oxidative tolerance and intracellular infection. The recombinant Grx was able to efficiently catalyze the thiol-disulfide oxidoreduction of insulin in the presence of DTT as an election donor. Unexpectedly, the deletion of
<i>grx</i>
resulted in a remarkably increased tolerance and survival ability of this bacteria when exposed to various oxidizing agents, including diamide, and copper and cadmium ions. Furthermore, loss of
<i>grx</i>
significantly promoted bacterial invasion and proliferation in human epithelial Caco-2 cells and murine macrophages, as well as a notably increasing invasion but not cell-to-cell spread in the murine fibroblasts L929 cells. More importantly,
<i>L. monocytogenes</i>
lacking the glutaredoxin exhibited more efficient proliferation and recovery in the spleens and livers of the infected mice, and hence became more virulent by upregulating the virulence factors, InlA and InlB. In summary, we here for the first time demonstrated that
<i>L. monocytogenes</i>
glutaredoxin plays a counterintuitive role in bacterial oxidative resistance and intracellular infection, which is the first report to provide valuable evidence for the role of glutaredoxins in bacterial infection, and more importantly suggests a favorable model to illustrate the functional diversity of bacterial Grx systems during environmental adaption and host infection.</AbstractText>
</Abstract>
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<Author ValidYN="Y">
<LastName>Sun</LastName>
<ForeName>Jing</ForeName>
<Initials>J</Initials>
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<Affiliation>Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, China-Australian Joint Laboratory for Animal Health Big Data Analytics, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University, Hangzhou, P. R. China.</Affiliation>
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<LastName>Hang</LastName>
<ForeName>Yi</ForeName>
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<Affiliation>Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, China-Australian Joint Laboratory for Animal Health Big Data Analytics, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University, Hangzhou, P. R. China.</Affiliation>
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<LastName>Han</LastName>
<ForeName>Yue</ForeName>
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</AffiliationInfo>
<AffiliationInfo>
<Affiliation>School of Veterinary and Life Sciences, Murdoch University, Murdoch, Australia.</Affiliation>
</AffiliationInfo>
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