Interaction with Tsg101 Is Necessary for the Efficient Transport and Release of Nucleocapsids in Marburg Virus-Infected Cells

Endosomal sorting complex required for transport (ESCRT) machinery supports the efficient budding of Marburg virus (MARV) and many other enveloped viruses. Interaction between components of the ESCRT machinery and viral proteins is predominantly mediated by short tetrapeptide motifs, known as late d...

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Vydáno v:	PLoS pathogens Ročník 10; číslo 10; s. e1004463
Hlavní autoři:	Dolnik, Olga, Kolesnikova, Larissa, Welsch, Sonja, Strecker, Thomas, Schudt, Gordian, Becker, Stephan
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	United States Public Library of Science 01.10.2014 Public Library of Science (PLoS)
Témata:	Actin Cytoskeleton - metabolism Animals Biology and Life Sciences Cytoskeleton DNA-Binding Proteins - metabolism Endosomal Sorting Complexes Required for Transport - metabolism Fever Health aspects Host-parasite relationships Humans Marburgvirus Medicine and Health Sciences Microscopy Mortality Nucleocapsid - metabolism Plasma Plasmids Protein Transport - physiology Proteins Ribonucleoproteins - metabolism RNA viruses Transcription Factors - metabolism Viral Proteins - metabolism Virus Release - physiology Virus research Viruses
ISSN:	1553-7374, 1553-7366, 1553-7374
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Abstract	Endosomal sorting complex required for transport (ESCRT) machinery supports the efficient budding of Marburg virus (MARV) and many other enveloped viruses. Interaction between components of the ESCRT machinery and viral proteins is predominantly mediated by short tetrapeptide motifs, known as late domains. MARV contains late domain motifs in the matrix protein VP40 and in the genome-encapsidating nucleoprotein (NP). The PSAP late domain motif of NP recruits the ESCRT-I protein tumor susceptibility gene 101 (Tsg101). Here, we generated a recombinant MARV encoding NP with a mutated PSAP late domain (rMARV(PSAPmut)). rMARV(PSAPmut) was attenuated by up to one log compared with recombinant wild-type MARV (rMARV(wt)), formed smaller plaques and exhibited delayed virus release. Nucleocapsids in rMARV(PSAPmut)-infected cells were more densely packed inside viral inclusions and more abundant in the cytoplasm than in rMARV(wt)-infected cells. A similar phenotype was detected when MARV-infected cells were depleted of Tsg101. Live-cell imaging analyses revealed that Tsg101 accumulated in inclusions of rMARV(wt)-infected cells and was co-transported together with nucleocapsids. In contrast, rMARV(PSAPmut) nucleocapsids did not display co-localization with Tsg101, had significantly shorter transport trajectories, and migration close to the plasma membrane was severely impaired, resulting in reduced recruitment into filopodia, the major budding sites of MARV. We further show that the Tsg101 interacting protein IQGAP1, an actin cytoskeleton regulator, was recruited into inclusions and to individual nucleocapsids together with Tsg101. Moreover, IQGAP1 was detected in a contrail-like structure at the rear end of migrating nucleocapsids. Down regulation of IQGAP1 impaired release of MARV. These results indicate that the PSAP motif in NP, which enables binding to Tsg101, is important for the efficient actin-dependent transport of nucleocapsids to the sites of budding. Thus, the interaction between NP and Tsg101 supports several steps of MARV assembly before virus fission.
AbstractList	Endosomal sorting complex required for transport (ESCRT) machinery supports the efficient budding of Marburg virus (MARV) and many other enveloped viruses. Interaction between components of the ESCRT machinery and viral proteins is predominantly mediated by short tetrapeptide motifs, known as late domains. MARV contains late domain motifs in the matrix protein VP40 and in the genome-encapsidating nucleoprotein (NP). The PSAP late domain motif of NP recruits the ESCRT-I protein tumor susceptibility gene 101 (Tsg101). Here, we generated a recombinant MARV encoding NP with a mutated PSAP late domain (rMARV(PSAPmut)). rMARV(PSAPmut) was attenuated by up to one log compared with recombinant wild-type MARV (rMARV(wt)), formed smaller plaques and exhibited delayed virus release. Nucleocapsids in rMARV(PSAPmut)-infected cells were more densely packed inside viral inclusions and more abundant in the cytoplasm than in rMARV(wt)-infected cells. A similar phenotype was detected when MARV-infected cells were depleted of Tsg101. Live-cell imaging analyses revealed that Tsg101 accumulated in inclusions of rMARV(wt)-infected cells and was co-transported together with nucleocapsids. In contrast, rMARV(PSAPmut) nucleocapsids did not display co-localization with Tsg101, had significantly shorter transport trajectories, and migration close to the plasma membrane was severely impaired, resulting in reduced recruitment into filopodia, the major budding sites of MARV. We further show that the Tsg101 interacting protein IQGAP1, an actin cytoskeleton regulator, was recruited into inclusions and to individual nucleocapsids together with Tsg101. Moreover, IQGAP1 was detected in a contrail-like structure at the rear end of migrating nucleocapsids. Down regulation of IQGAP1 impaired release of MARV. These results indicate that the PSAP motif in NP, which enables binding to Tsg101, is important for the efficient actin-dependent transport of nucleocapsids to the sites of budding. Thus, the interaction between NP and Tsg101 supports several steps of MARV assembly before virus fission.Endosomal sorting complex required for transport (ESCRT) machinery supports the efficient budding of Marburg virus (MARV) and many other enveloped viruses. Interaction between components of the ESCRT machinery and viral proteins is predominantly mediated by short tetrapeptide motifs, known as late domains. MARV contains late domain motifs in the matrix protein VP40 and in the genome-encapsidating nucleoprotein (NP). The PSAP late domain motif of NP recruits the ESCRT-I protein tumor susceptibility gene 101 (Tsg101). Here, we generated a recombinant MARV encoding NP with a mutated PSAP late domain (rMARV(PSAPmut)). rMARV(PSAPmut) was attenuated by up to one log compared with recombinant wild-type MARV (rMARV(wt)), formed smaller plaques and exhibited delayed virus release. Nucleocapsids in rMARV(PSAPmut)-infected cells were more densely packed inside viral inclusions and more abundant in the cytoplasm than in rMARV(wt)-infected cells. A similar phenotype was detected when MARV-infected cells were depleted of Tsg101. Live-cell imaging analyses revealed that Tsg101 accumulated in inclusions of rMARV(wt)-infected cells and was co-transported together with nucleocapsids. In contrast, rMARV(PSAPmut) nucleocapsids did not display co-localization with Tsg101, had significantly shorter transport trajectories, and migration close to the plasma membrane was severely impaired, resulting in reduced recruitment into filopodia, the major budding sites of MARV. We further show that the Tsg101 interacting protein IQGAP1, an actin cytoskeleton regulator, was recruited into inclusions and to individual nucleocapsids together with Tsg101. Moreover, IQGAP1 was detected in a contrail-like structure at the rear end of migrating nucleocapsids. Down regulation of IQGAP1 impaired release of MARV. These results indicate that the PSAP motif in NP, which enables binding to Tsg101, is important for the efficient actin-dependent transport of nucleocapsids to the sites of budding. Thus, the interaction between NP and Tsg101 supports several steps of MARV assembly before virus fission. Endosomal sorting complex required for transport (ESCRT) machinery supports the efficient budding of Marburg virus (MARV) and many other enveloped viruses. Interaction between components of the ESCRT machinery and viral proteins is predominantly mediated by short tetrapeptide motifs, known as late domains. MARV contains late domain motifs in the matrix protein VP40 and in the genome-encapsidating nucleoprotein (NP). The PSAP late domain motif of NP recruits the ESCRT-I protein tumor susceptibility gene 101 (Tsg101). Here, we generated a recombinant MARV encoding NP with a mutated PSAP late domain (rMARV(PSAPmut)). rMARV(PSAPmut) was attenuated by up to one log compared with recombinant wild-type MARV (rMARV(wt)), formed smaller plaques and exhibited delayed virus release. Nucleocapsids in rMARV(PSAPmut)-infected cells were more densely packed inside viral inclusions and more abundant in the cytoplasm than in rMARV(wt)-infected cells. A similar phenotype was detected when MARV-infected cells were depleted of Tsg101. Live-cell imaging analyses revealed that Tsg101 accumulated in inclusions of rMARV(wt)-infected cells and was co-transported together with nucleocapsids. In contrast, rMARV(PSAPmut) nucleocapsids did not display co-localization with Tsg101, had significantly shorter transport trajectories, and migration close to the plasma membrane was severely impaired, resulting in reduced recruitment into filopodia, the major budding sites of MARV. We further show that the Tsg101 interacting protein IQGAP1, an actin cytoskeleton regulator, was recruited into inclusions and to individual nucleocapsids together with Tsg101. Moreover, IQGAP1 was detected in a contrail-like structure at the rear end of migrating nucleocapsids. Down regulation of IQGAP1 impaired release of MARV. These results indicate that the PSAP motif in NP, which enables binding to Tsg101, is important for the efficient actin-dependent transport of nucleocapsids to the sites of budding. Thus, the interaction between NP and Tsg101 supports several steps of MARV assembly before virus fission. Endosomal sorting complex required for transport (ESCRT) machinery supports the efficient budding of Marburg virus (MARV) and many other enveloped viruses. Interaction between components of the ESCRT machinery and viral proteins is predominantly mediated by short tetrapeptide motifs, known as late domains. MARV contains late domain motifs in the matrix protein VP40 and in the genome-encapsidating nucleoprotein (NP). The PSAP late domain motif of NP recruits the ESCRT-I protein tumor susceptibility gene 101 (Tsg101). Here, we generated a recombinant MARV encoding NP with a mutated PSAP late domain (rMARVPSAPmut). rMARVPSAPmut was attenuated by up to one log compared with recombinant wild-type MARV (rMARVwt), formed smaller plaques and exhibited delayed virus release. Nucleocapsids in rMARVPSAPmut-infected cells were more densely packed inside viral inclusions and more abundant in the cytoplasm than in rMARVwt-infected cells. A similar phenotype was detected when MARV-infected cells were depleted of Tsg101. Live-cell imaging analyses revealed that Tsg101 accumulated in inclusions of rMARVwt-infected cells and was co-transported together with nucleocapsids. In contrast, rMARVPSAPmut nucleocapsids did not display co-localization with Tsg101, had significantly shorter transport trajectories, and migration close to the plasma membrane was severely impaired, resulting in reduced recruitment into filopodia, the major budding sites of MARV. We further show that the Tsg101 interacting protein IQGAP1, an actin cytoskeleton regulator, was recruited into inclusions and to individual nucleocapsids together with Tsg101. Moreover, IQGAP1 was detected in a contrail-like structure at the rear end of migrating nucleocapsids. Down regulation of IQGAP1 impaired release of MARV. These results indicate that the PSAP motif in NP, which enables binding to Tsg101, is important for the efficient actin-dependent transport of nucleocapsids to the sites of budding. Thus, the interaction between NP and Tsg101 supports several steps of MARV assembly before virus fission. Endosomal sorting complex required for transport (ESCRT) machinery supports the efficient budding of Marburg virus (MARV) and many other enveloped viruses. Interaction between components of the ESCRT machinery and viral proteins is predominantly mediated by short tetrapeptide motifs, known as late domains. MARV contains late domain motifs in the matrix protein VP40 and in the genome-encapsidating nucleoprotein (NP). The PSAP late domain motif of NP recruits the ESCRT-I protein tumor susceptibility gene 101 (Tsg101). Here, we generated a recombinant MARV encoding NP with a mutated PSAP late domain (rMARVPSAPmut). rMARVPSAPmut was attenuated by up to one log compared with recombinant wild-type MARV (rMARVwt), formed smaller plaques and exhibited delayed virus release. Nucleocapsids in rMARVPSAPmut-infected cells were more densely packed inside viral inclusions and more abundant in the cytoplasm than in rMARVwt-infected cells. A similar phenotype was detected when MARV-infected cells were depleted of Tsg101. Live-cell imaging analyses revealed that Tsg101 accumulated in inclusions of rMARVwt-infected cells and was co-transported together with nucleocapsids. In contrast, rMARVPSAPmut nucleocapsids did not display co-localization with Tsg101, had significantly shorter transport trajectories, and migration close to the plasma membrane was severely impaired, resulting in reduced recruitment into filopodia, the major budding sites of MARV. We further show that the Tsg101 interacting protein IQGAP1, an actin cytoskeleton regulator, was recruited into inclusions and to individual nucleocapsids together with Tsg101. Moreover, IQGAP1 was detected in a contrail-like structure at the rear end of migrating nucleocapsids. Down regulation of IQGAP1 impaired release of MARV. These results indicate that the PSAP motif in NP, which enables binding to Tsg101, is important for the efficient actin-dependent transport of nucleocapsids to the sites of budding. Thus, the interaction between NP and Tsg101 supports several steps of MARV assembly before virus fission. Marburg virus (MARV) is endemic in central Africa and causes hemorrhagic fever in humans and non-human primates, with high lethality. Presumably, the disease severity primarily depends on the response of host-cell factors interacting with viral proteins. We generated a recombinant MARV encoding an NP with a mutated PSAP late domain motif, which has previously been shown to mediate interaction with the cellular ESCRT protein Tsg101. We found that the PSAP-mediated interaction with Tsg101 was important at several steps of MARV assembly before viral fission. First, the egress of mature rMARVPSAPmut nucleocapsids from viral inclusions was inhibited. Second, actin-driven transport of rMARVPSAPmut nucleocapsids was impaired, displaying significantly shortened trajectories and reduced movement in the cell periphery. Third, rMARVPSAPmut nucleocapsids accumulated in cell periphery, and the number of filopodia-associated nucleocapsids decreased, indicating that rMARVPSAPmut nucleocapsids were defective to enter filopodia, the major budding sites of MARV. These defects resulted in the attenuated growth of rMARVPSAPmut. Interestingly, IQGAP1, an actin cytoskeleton regulator which interacts with Tsg101, was also recruited to nucleocapsids in dependence of the PSAP late domain. Thus, the interaction of NP with Tsg101 not only impacts viral budding at the plasma membrane but also nucleocapsid transport through the cytoplasm. Endosomal sorting complex required for transport (ESCRT) machinery supports the efficient budding of Marburg virus (MARV) and many other enveloped viruses. Interaction between components of the ESCRT machinery and viral proteins is predominantly mediated by short tetrapeptide motifs, known as late domains. MARV contains late domain motifs in the matrix protein VP40 and in the genome-encapsidating nucleoprotein (NP). The PSAP late domain motif of NP recruits the ESCRT-I protein tumor susceptibility gene 101 (Tsg101). Here, we generated a recombinant MARV encoding NP with a mutated PSAP late domain ([rMARV.sub.PSAPmut]). [rMARV.sub.PSAPmut] was attenuated by up to one log compared with recombinant wild-type MARV ([rMARV.sub.wt]), formed smaller plaques and exhibited delayed virus release. Nucleocapsids in [rMARV.sub.PSAPmut]-infected cells were more densely packed inside viral inclusions and more abundant in the cytoplasm than in [rMARV.sub.wt]infected cells. A similar phenotype was detected when MARV-infected cells were depleted of Tsg101. Live-cell imaging analyses revealed that Tsg101 accumulated in inclusions of [rMARV.sub.wt]-infected cells and was co-transported together with nucleocapsids. In contrast, [rMARV.sub.PSAPmut] nucleocapsids did not display co-localization with Tsg101, had significantly shorter transport trajectories, and migration close to the plasma membrane was severely impaired, resulting in reduced recruitment into filopodia, the major budding sites of MARV. We further show that the Tsg101 interacting protein IQGAP1, an actin cytoskeleton regulator, was recruited into inclusions and to individual nucleocapsids together with Tsg101. Moreover, IQGAP1 was detected in a contrail-like structure at the rear end of migrating nucleocapsids. Down regulation of IQGAP1 impaired release of MARV. These results indicate that the PSAP motif in NP, which enables binding to Tsg101, is important for the efficient actin-dependent transport of nucleocapsids to the sites of budding. Thus, the interaction between NP and Tsg101 supports several steps of MARV assembly before virus fission.
Audience	Academic
Author	Kolesnikova, Larissa Strecker, Thomas Schudt, Gordian Welsch, Sonja Dolnik, Olga Becker, Stephan
AuthorAffiliation	Mount Sinai School of Medicine, United States of America 2 EMBL Structural and Computational Biology Unit, Heidelberg, Germany 1 Institut für Virologie, Philipps Universität Marburg, Marburg, Germany 3 DZIF, Deutsches Zentrum für Infektionsforschung, Marburg, Germany
AuthorAffiliation_xml	– name: 3 DZIF, Deutsches Zentrum für Infektionsforschung, Marburg, Germany – name: Mount Sinai School of Medicine, United States of America – name: 1 Institut für Virologie, Philipps Universität Marburg, Marburg, Germany – name: 2 EMBL Structural and Computational Biology Unit, Heidelberg, Germany
Author_xml	– sequence: 1 givenname: Olga surname: Dolnik fullname: Dolnik, Olga – sequence: 2 givenname: Larissa surname: Kolesnikova fullname: Kolesnikova, Larissa – sequence: 3 givenname: Sonja surname: Welsch fullname: Welsch, Sonja – sequence: 4 givenname: Thomas surname: Strecker fullname: Strecker, Thomas – sequence: 5 givenname: Gordian surname: Schudt fullname: Schudt, Gordian – sequence: 6 givenname: Stephan surname: Becker fullname: Becker, Stephan
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25330247$$D View this record in MEDLINE/PubMed
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ContentType	Journal Article
Copyright	COPYRIGHT 2014 Public Library of Science 2014 Dolnik et al 2014 Dolnik et al 2014 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: Dolnik O, Kolesnikova L, Welsch S, Strecker T, Schudt G, Becker S (2014) Interaction with Tsg101 Is Necessary for the Efficient Transport and Release of Nucleocapsids in Marburg Virus-Infected Cells. PLoS Pathog 10(10): e1004463. doi:10.1371/journal.ppat.1004463
Copyright_xml	– notice: COPYRIGHT 2014 Public Library of Science – notice: 2014 Dolnik et al 2014 Dolnik et al – notice: 2014 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: Dolnik O, Kolesnikova L, Welsch S, Strecker T, Schudt G, Becker S (2014) Interaction with Tsg101 Is Necessary for the Efficient Transport and Release of Nucleocapsids in Marburg Virus-Infected Cells. PLoS Pathog 10(10): e1004463. doi:10.1371/journal.ppat.1004463
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The authors have declared that no competing interests exist. Conceived and designed the experiments: OD LK SW SB. Performed the experiments: OD LK SW. Analyzed the data: OD LK SW SB. Contributed reagents/materials/analysis tools: OD LK SW SB TS GS. Wrote the paper: OD LK SW SB TS.
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PQID	1615260910
PQPubID	23479
ParticipantIDs	plos_journals_1685244948 doaj_primary_oai_doaj_org_article_d43c2906e6fb482f98c357f0a8784b15 pubmedcentral_primary_oai_pubmedcentral_nih_gov_4199773 proquest_miscellaneous_1615260910 gale_infotracmisc_A390412249 gale_infotracacademiconefile_A390412249 gale_incontextgauss_ISR_A390412249 gale_incontextgauss_ISN_A390412249 pubmed_primary_25330247 crossref_citationtrail_10_1371_journal_ppat_1004463 crossref_primary_10_1371_journal_ppat_1004463
PublicationCentury	2000
PublicationDate	2014-10-01
PublicationDateYYYYMMDD	2014-10-01
PublicationDate_xml	– month: 10 year: 2014 text: 2014-10-01 day: 01
PublicationDecade	2010
PublicationPlace	United States
PublicationPlace_xml	– name: United States – name: San Francisco, USA
PublicationTitle	PLoS pathogens
PublicationTitleAlternate	PLoS Pathog
PublicationYear	2014
Publisher	Public Library of Science Public Library of Science (PLoS)
Publisher_xml	– name: Public Library of Science – name: Public Library of Science (PLoS)
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Snippet	Endosomal sorting complex required for transport (ESCRT) machinery supports the efficient budding of Marburg virus (MARV) and many other enveloped viruses.... Endosomal sorting complex required for transport (ESCRT) machinery supports the efficient budding of Marburg virus (MARV) and many other enveloped viruses....
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StartPage	e1004463
SubjectTerms	Actin Cytoskeleton - metabolism Animals Biology and Life Sciences Cytoskeleton DNA-Binding Proteins - metabolism Endosomal Sorting Complexes Required for Transport - metabolism Fever Health aspects Host-parasite relationships Humans Marburgvirus Medicine and Health Sciences Microscopy Mortality Nucleocapsid - metabolism Plasma Plasmids Protein Transport - physiology Proteins Ribonucleoproteins - metabolism RNA viruses Transcription Factors - metabolism Viral Proteins - metabolism Virus Release - physiology Virus research Viruses
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Title	Interaction with Tsg101 Is Necessary for the Efficient Transport and Release of Nucleocapsids in Marburg Virus-Infected Cells
URI	https://www.ncbi.nlm.nih.gov/pubmed/25330247 https://www.proquest.com/docview/1615260910 https://pubmed.ncbi.nlm.nih.gov/PMC4199773 https://doaj.org/article/d43c2906e6fb482f98c357f0a8784b15 http://dx.doi.org/10.1371/journal.ppat.1004463
Volume	10
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