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A Novel Virus Alters Gene Expression and Vacuolar Morphology in Malassezia Cells and Induces a TLR3-Mediated Inflammatory Immune Response.

Identifieur interne : 000236 ( Main/Exploration ); précédent : 000235; suivant : 000237

A Novel Virus Alters Gene Expression and Vacuolar Morphology in Malassezia Cells and Induces a TLR3-Mediated Inflammatory Immune Response.

Auteurs : Minji Park [Corée du Sud] ; Yong-Joon Cho [Corée du Sud] ; Donggyu Kim [Corée du Sud] ; Chul-Su Yang [Corée du Sud] ; Shi Mun Lee [Singapour] ; Thomas L. Dawson [Singapour, États-Unis] ; Satoshi Nakamizo [Singapour] ; Kenji Kabashima [Singapour, Japon] ; Yang Won Lee [Corée du Sud] ; Won Hee Jung [Corée du Sud]

Source :

RBID : pubmed:32873759

Abstract

Most fungal viruses have been identified in plant pathogens, whereas the presence of viral particles in human-pathogenic fungi is less well studied. In the present study, we observed extrachromosomal double-stranded RNA (dsRNA) segments in various clinical isolates of Malassezia species. Malassezia is the most dominant fungal genus on the human skin surface, and species in this group are considered etiological factors of various skin diseases including dandruff, seborrheic dermatitis, and atopic dermatitis. We identified novel dsRNA segments, and our sequencing results revealed that the virus, named MrV40, belongs to the Totiviridae family and contains an additional satellite dsRNA segment encoding a novel protein. The transcriptome of virus-infected Malassezia restricta cells was compared to that of virus-cured cells, and the results showed that transcripts involved in ribosomal biosynthesis were downregulated and those involved in energy production and programmed cell death were upregulated. Moreover, transmission electron microscopy revealed significantly larger vacuoles in virus-infected M. restricta cells, indicating that MrV40 infection dramatically altered M. restricta physiology. Our analysis also revealed that viral nucleic acid from MrV40 induced a TLR3 (Toll-like receptor 3)-mediated inflammatory immune response in bone marrow-derived dendritic cells, suggesting that a viral element contributes to the pathogenicity of MalasseziaIMPORTANCEMalassezia is the most dominant fungal genus on the human skin surface and is associated with various skin diseases including dandruff and seborrheic dermatitis. Among Malassezia species, Malassezia restricta is the most widely observed species on the human skin. In the current study, we identified a novel dsRNA virus, named MrV40, in M. restricta and characterized the sequence and structure of the viral genome along with an independent satellite dsRNA viral segment. Moreover, expression of genes involved in ribosomal synthesis and programmed cell death was altered, indicating that virus infection affected the physiology of the fungal host cells. Our data also showed that the viral nucleic acid from MrV40 induces a TLR3-mediated inflammatory immune response in bone marrow-derived dendritic cells, indicating that a viral element likely contributes to the pathogenicity of Malassezia This is the first study to identify and characterize a novel mycovirus in Malassezia.

DOI: 10.1128/mBio.01521-20
PubMed: 32873759
PubMed Central: PMC7468201


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<name sortKey="Lee, Yang Won" sort="Lee, Yang Won" uniqKey="Lee Y" first="Yang Won" last="Lee">Yang Won Lee</name>
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<div type="abstract" xml:lang="en">Most fungal viruses have been identified in plant pathogens, whereas the presence of viral particles in human-pathogenic fungi is less well studied. In the present study, we observed extrachromosomal double-stranded RNA (dsRNA) segments in various clinical isolates of
<i>Malassezia</i>
species.
<i>Malassezia</i>
is the most dominant fungal genus on the human skin surface, and species in this group are considered etiological factors of various skin diseases including dandruff, seborrheic dermatitis, and atopic dermatitis. We identified novel dsRNA segments, and our sequencing results revealed that the virus, named MrV40, belongs to the
<i>Totiviridae</i>
family and contains an additional satellite dsRNA segment encoding a novel protein. The transcriptome of virus-infected
<i>Malassezia restricta</i>
cells was compared to that of virus-cured cells, and the results showed that transcripts involved in ribosomal biosynthesis were downregulated and those involved in energy production and programmed cell death were upregulated. Moreover, transmission electron microscopy revealed significantly larger vacuoles in virus-infected
<i>M. restricta</i>
cells, indicating that MrV40 infection dramatically altered
<i>M. restricta</i>
physiology. Our analysis also revealed that viral nucleic acid from MrV40 induced a TLR3 (Toll-like receptor 3)-mediated inflammatory immune response in bone marrow-derived dendritic cells, suggesting that a viral element contributes to the pathogenicity of
<i>Malassezia</i>
<b>IMPORTANCE</b>
<i>Malassezia</i>
is the most dominant fungal genus on the human skin surface and is associated with various skin diseases including dandruff and seborrheic dermatitis. Among
<i>Malassezia</i>
species,
<i>Malassezia restricta</i>
is the most widely observed species on the human skin. In the current study, we identified a novel dsRNA virus, named MrV40, in
<i>M. restricta</i>
and characterized the sequence and structure of the viral genome along with an independent satellite dsRNA viral segment. Moreover, expression of genes involved in ribosomal synthesis and programmed cell death was altered, indicating that virus infection affected the physiology of the fungal host cells. Our data also showed that the viral nucleic acid from MrV40 induces a TLR3-mediated inflammatory immune response in bone marrow-derived dendritic cells, indicating that a viral element likely contributes to the pathogenicity of
<i>Malassezia</i>
This is the first study to identify and characterize a novel mycovirus in
<i>Malassezia</i>
.</div>
</front>
</TEI>
<pubmed>
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<DateRevised>
<Year>2020</Year>
<Month>11</Month>
<Day>14</Day>
</DateRevised>
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<Journal>
<ISSN IssnType="Electronic">2150-7511</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>11</Volume>
<Issue>5</Issue>
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<Year>2020</Year>
<Month>09</Month>
<Day>01</Day>
</PubDate>
</JournalIssue>
<Title>mBio</Title>
<ISOAbbreviation>mBio</ISOAbbreviation>
</Journal>
<ArticleTitle>A Novel Virus Alters Gene Expression and Vacuolar Morphology in
<i>Malassezia</i>
Cells and Induces a TLR3-Mediated Inflammatory Immune Response.</ArticleTitle>
<ELocationID EIdType="pii" ValidYN="Y">e01521-20</ELocationID>
<ELocationID EIdType="doi" ValidYN="Y">10.1128/mBio.01521-20</ELocationID>
<Abstract>
<AbstractText>Most fungal viruses have been identified in plant pathogens, whereas the presence of viral particles in human-pathogenic fungi is less well studied. In the present study, we observed extrachromosomal double-stranded RNA (dsRNA) segments in various clinical isolates of
<i>Malassezia</i>
species.
<i>Malassezia</i>
is the most dominant fungal genus on the human skin surface, and species in this group are considered etiological factors of various skin diseases including dandruff, seborrheic dermatitis, and atopic dermatitis. We identified novel dsRNA segments, and our sequencing results revealed that the virus, named MrV40, belongs to the
<i>Totiviridae</i>
family and contains an additional satellite dsRNA segment encoding a novel protein. The transcriptome of virus-infected
<i>Malassezia restricta</i>
cells was compared to that of virus-cured cells, and the results showed that transcripts involved in ribosomal biosynthesis were downregulated and those involved in energy production and programmed cell death were upregulated. Moreover, transmission electron microscopy revealed significantly larger vacuoles in virus-infected
<i>M. restricta</i>
cells, indicating that MrV40 infection dramatically altered
<i>M. restricta</i>
physiology. Our analysis also revealed that viral nucleic acid from MrV40 induced a TLR3 (Toll-like receptor 3)-mediated inflammatory immune response in bone marrow-derived dendritic cells, suggesting that a viral element contributes to the pathogenicity of
<i>Malassezia</i>
<b>IMPORTANCE</b>
<i>Malassezia</i>
is the most dominant fungal genus on the human skin surface and is associated with various skin diseases including dandruff and seborrheic dermatitis. Among
<i>Malassezia</i>
species,
<i>Malassezia restricta</i>
is the most widely observed species on the human skin. In the current study, we identified a novel dsRNA virus, named MrV40, in
<i>M. restricta</i>
and characterized the sequence and structure of the viral genome along with an independent satellite dsRNA viral segment. Moreover, expression of genes involved in ribosomal synthesis and programmed cell death was altered, indicating that virus infection affected the physiology of the fungal host cells. Our data also showed that the viral nucleic acid from MrV40 induces a TLR3-mediated inflammatory immune response in bone marrow-derived dendritic cells, indicating that a viral element likely contributes to the pathogenicity of
<i>Malassezia</i>
This is the first study to identify and characterize a novel mycovirus in
<i>Malassezia</i>
.</AbstractText>
<CopyrightInformation>Copyright © 2020 Park et al.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Park</LastName>
<ForeName>Minji</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Department of Systems Biotechnology, Chung-Ang University, Anseong, South Korea.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Cho</LastName>
<ForeName>Yong-Joon</ForeName>
<Initials>YJ</Initials>
<AffiliationInfo>
<Affiliation>The Research Institute of Basic Sciences, Seoul National University, Seoul, South Korea.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kim</LastName>
<ForeName>Donggyu</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular and Life Science, Hanyang University, Ansan, South Korea.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Yang</LastName>
<ForeName>Chul-Su</ForeName>
<Initials>CS</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular and Life Science, Hanyang University, Ansan, South Korea.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Bionano Technology, Hanyang University, Seoul, South Korea.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lee</LastName>
<ForeName>Shi Mun</ForeName>
<Initials>SM</Initials>
<AffiliationInfo>
<Affiliation>Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Skin Research Institute of Singapore (SRIS), Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore.</Affiliation>
</AffiliationInfo>
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<LastName>Dawson</LastName>
<ForeName>Thomas L</ForeName>
<Initials>TL</Initials>
<Suffix>Jr</Suffix>
<AffiliationInfo>
<Affiliation>Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Center for Cell Death, Injury & Regeneration, Medical University of South Carolina, Charleston, South Carolina, USA.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Skin Research Institute of Singapore (SRIS), Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Drug Discovery & Biomedical Sciences, Medical University of South Carolina, Charleston, South Carolina, USA.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Biochemistry & Molecular Biology, Medical University of South Carolina, Charleston, South Carolina, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Nakamizo</LastName>
<ForeName>Satoshi</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Skin Research Institute of Singapore (SRIS), Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore.</Affiliation>
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<Author ValidYN="Y">
<LastName>Kabashima</LastName>
<ForeName>Kenji</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Dermatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Skin Research Institute of Singapore (SRIS), Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lee</LastName>
<ForeName>Yang Won</ForeName>
<Initials>YW</Initials>
<AffiliationInfo>
<Affiliation>Department of Dermatology, School of Medicine, Konkuk University, Seoul, South Korea.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Research Institute of Medicine, Konkuk University, Seoul, South Korea.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Jung</LastName>
<ForeName>Won Hee</ForeName>
<Initials>WH</Initials>
<Identifier Source="ORCID">0000-0002-6920-0233</Identifier>
<AffiliationInfo>
<Affiliation>Department of Systems Biotechnology, Chung-Ang University, Anseong, South Korea whjung@cau.ac.kr.</Affiliation>
</AffiliationInfo>
</Author>
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<Language>eng</Language>
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<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
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<ArticleDate DateType="Electronic">
<Year>2020</Year>
<Month>09</Month>
<Day>01</Day>
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<Country>United States</Country>
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<Keyword MajorTopicYN="Y">Malassezia </Keyword>
<Keyword MajorTopicYN="Y">Malassezia restricta </Keyword>
<Keyword MajorTopicYN="Y">TLR3</Keyword>
<Keyword MajorTopicYN="Y">cytokine</Keyword>
<Keyword MajorTopicYN="Y">double-stranded RNA virus</Keyword>
<Keyword MajorTopicYN="Y">mycovirus</Keyword>
<Keyword MajorTopicYN="Y">virus</Keyword>
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