Vesicular Egress of Non-Enveloped Lytic Parvoviruses Depends on Gelsolin Functioning
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{"title"=>"Vesicular egress of non-enveloped lytic parvoviruses depends on gelsolin functioning", "type"=>"journal", "authors"=>[{"first_name"=>"Séverine", "last_name"=>"Bär", "scopus_author_id"=>"23484358200"}, {"first_name"=>"Laurent", "last_name"=>"Daeffler", "scopus_author_id"=>"6602221243"}, {"first_name"=>"Jean", "last_name"=>"Rommelaere", "scopus_author_id"=>"7006211516"}, {"first_name"=>"Jürg P F", "last_name"=>"Nüesch", "scopus_author_id"=>"7003266034"}], "year"=>2008, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "pui"=>"352264397", "pmid"=>"18704167", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "doi"=>"10.1371/journal.ppat.1000126", "sgr"=>"50849129909", "scopus"=>"2-s2.0-50849129909"}, "id"=>"2b1d34ff-2997-3987-825e-69f40a0f9bef", "abstract"=>"The autonomous parvovirus Minute Virus of Mice (MVM) induces specific changes in the cytoskeleton filaments of infected permissive cells, causing in particular the degradation of actin fibers and the generation of \"actin patches.\" This is attributed to a virus-induced imbalance between the polymerization factor N-WASP (Wiscott-Aldrich syndrome protein) and gelsolin, a multifunctional protein cleaving actin filaments. Here, the focus is on the involvement of gelsolin in parvovirus propagation and virus-induced actin processing. Gelsolin activity was knocked-down, and consequences thereof were determined for virus replication and egress and for actin network integrity. Though not required for virus replication or progeny particle assembly, gelsolin was found to control MVM (and related H1-PV) transport from the nucleus to the cell periphery and release into the culture medium. Gelsolin-dependent actin degradation and progeny virus release were both controlled by (NS1)/CKIIalpha, a recently identified complex between a cellular protein kinase and a MVM non-structural protein. Furthermore, the export of newly synthesized virions through the cytoplasm appeared to be mediated by (virus-modified) lysomal/late endosomal vesicles. By showing that MVM release, like entry, is guided by the cytoskeleton and mediated by vesicles, these results challenge the current view that egress of non-enveloped lytic viruses is a passive process.", "link"=>"http://www.mendeley.com/research/vesicular-egress-nonenveloped-lytic-parvoviruses-depends-gelsolin-functioning", "reader_count"=>27, "reader_count_by_academic_status"=>{"Researcher"=>5, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>2, "Student > Master"=>4, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Researcher"=>5, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>2, "Student > Master"=>4, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>16, "Medicine and Dentistry"=>2, "Chemistry"=>1, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>16}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Lithuania"=>1, "Germany"=>1}, "group_count"=>0}

Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/455700", "https://ndownloader.figshare.com/files/455712", "https://ndownloader.figshare.com/files/455725"], "description"=>"<div><p>The autonomous parvovirus Minute Virus of Mice (MVM) induces specific changes in the cytoskeleton filaments of infected permissive cells, causing in particular the degradation of actin fibers and the generation of “actin patches.” This is attributed to a virus-induced imbalance between the polymerization factor N-WASP (Wiscott-Aldrich syndrome protein) and gelsolin, a multifunctional protein cleaving actin filaments. Here, the focus is on the involvement of gelsolin in parvovirus propagation and virus-induced actin processing. Gelsolin activity was knocked-down, and consequences thereof were determined for virus replication and egress and for actin network integrity. Though not required for virus replication or progeny particle assembly, gelsolin was found to control MVM (and related H1-PV) transport from the nucleus to the cell periphery and release into the culture medium. Gelsolin-dependent actin degradation and progeny virus release were both controlled by (NS1)/CKIIα, a recently identified complex between a cellular protein kinase and a MVM non-structural protein. Furthermore, the export of newly synthesized virions through the cytoplasm appeared to be mediated by (virus-modified) lysomal/late endosomal vesicles. By showing that MVM release, like entry, is guided by the cytoskeleton and mediated by vesicles, these results challenge the current view that egress of non-enveloped lytic viruses is a passive process.</p></div>", "links"=>[], "tags"=>["vesicular", "egress", "non-enveloped", "lytic", "parvoviruses", "depends", "gelsolin", "functioning"], "article_id"=>149755, "categories"=>["Biochemistry", "Cell Biology", "Cancer"], "users"=>["Séverine Bär", "Laurent Daeffler", "Jean Rommelaere", "Jürg P. F. Nüesch"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000126.s001", "https://dx.doi.org/10.1371/journal.ppat.1000126.s002", "https://dx.doi.org/10.1371/journal.ppat.1000126.s003"], "stats"=>{"downloads"=>6, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Vesicular_Egress_of_Non_Enveloped_Lytic_Parvoviruses_Depends_on_Gelsolin_Functioning/149755", "title"=>"Vesicular Egress of Non-Enveloped Lytic Parvoviruses Depends on Gelsolin Functioning", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-08-15 02:42:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/923620"], "description"=>"<p>A9 cells and derivatives expressing dominant-negative gelsolin mutants (GlnY438A; GlnD565N) were infected with MVM (30 pfu/cell). (A) Infected cells were analyzed 48 h p.i. for the structure of their actin network by IF staining with rhodamine-phalloidin (upper panel) and by biochemical fractionation according to the solubility of actin filaments (lower panel). Cell extracts were treated with detergents in increasing amount and of increasing strength, and actin was quantified in the individual fractions by western blotting. LaminB served as a loading control. Fractions containing the most rigid filaments (i.e. insoluble components) are highlighted by dotted squares. Expression of the two gelsolin variants GlnY438A or GlnD565N, respectively, protect actin filaments from degradation through parvovirus MVM, i.e. exert a dominant-negative effect. (B) Cells and supernatants were collected separately at the indicated time p.i. Titers of cell-associated (cell) and released (medium) infectious virions were determined by standard plaque-assays on A9 cells and are expressed in plaque-forming units (PFU). Inactivation of gelsolin does not affect the production of infectious progeny particles, but inhibits egress of progeny virions into the medium supernatant.</p>", "links"=>[], "tags"=>["cells", "expressing", "dominant-negative", "gelsolin"], "article_id"=>594074, "categories"=>["Biochemistry", "Cell Biology", "Infectious Diseases", "Virology"], "users"=>["Séverine Bär", "Laurent Daeffler", "Jean Rommelaere", "Jürg P. F. Nüesch"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000126.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MVM_production_in_cells_expressing_dominant_negative_gelsolin_mutants_/594074", "title"=>"MVM production in cells expressing dominant-negative gelsolin mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-15 01:07:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/923701"], "description"=>"<p>A9 cells and A9 derivatives expressing the indicated gelsolin mutants were grown on spot slides, infected (or not) with CsCl-gradient-purified MVM (30 pfu/cell), fixed at 4, 24 or 48 h p.i., and analyzed by confocal microscopy. Capsids were detected with αB7 monoclonal antibodies and cells were visualized by Nomarski staining. Inhibition of gelsolin leads to accumulation of progeny virions in the nucleus of infected cells. (A) IF staining patterns of representative cells. Scale bar 15 µm. (B) Intracellular capsid distribution, as determined by IF microscopy on at least 300 infected cells.</p>", "links"=>[], "tags"=>["egress"], "article_id"=>594159, "categories"=>["Biochemistry", "Cell Biology", "Infectious Diseases", "Virology"], "users"=>["Séverine Bär", "Laurent Daeffler", "Jean Rommelaere", "Jürg P. F. Nüesch"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000126.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dependence_of_virus_egress_on_gelsolin_/594159", "title"=>"Dependence of virus egress on gelsolin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-15 01:09:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/923976"], "description"=>"<p>Gelsolin is subject to phosphorylation through NS1/CKIIα at least <i>in vitro</i>. (A) Bacterially expressed gelsolin (Gln) was used as a substrate for the various indicated recombinant protein kinases in the presence of [<sup>32</sup>P]-γ-ATP. CKIIαβ was tested alone or in combination with wild-type (wt) or mutant (m:S473A) GST-tagged NS1 protein. [<sup>32</sup>P]-labeled gelsolin was immunoprecipitated and analyzed by 10% SDS-PAGE and autoradiography. (B) Gelsolin (Gln) and tubulin (Tub) were subjected to <i>in vitro</i> phosphorylation by CKII/NS1wt or CKII/mNS1, purified, and processed for 2-dimensional tryptic phosphopeptide analysis.</p>", "links"=>[], "tags"=>["gelsolin", "phosphorylation", "cellular"], "article_id"=>594428, "categories"=>["Biochemistry", "Cell Biology", "Infectious Diseases", "Virology"], "users"=>["Séverine Bär", "Laurent Daeffler", "Jean Rommelaere", "Jürg P. F. Nüesch"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000126.g007", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sensitivity_of_gelsolin_to_in_vitro_phosphorylation_by_cellular_protein_kinases_/594428", "title"=>"Sensitivity of gelsolin to <i>in vitro</i> phosphorylation by cellular protein kinases.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-15 01:13:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/923865"], "description"=>"<p>CKII activity is essential to promote vesicular egress of parvovirus progeny particles. A9 cells and their P38:CKII-E81A-expressing derivatives (dnCKII) were infected with CsCl-gradient-purified MVM (30 pfu/cell), fixed at the indicated time p.i., and analyzed by confocal laser scanning microscopy. (A) Capsid staining (green) within the cell (Nomarski). (B) The intracellular distribution of newly synthesized capsids was determined on at least 200 infected cells. Gray columns: percentages of cells showing a purely (peri)nuclear capsid distribution. Hatched columns: percentages of cells showing both a (peri)nuclear and a cytoplasmic capsid distribution. (C) Actin filaments stained with rhodamine-phalloidin (red) and gelsolin (green). Colocalization areas appear yellow in the merge and were quantified using ImageJ. White arrows indicate large actin fibers. CKII-activity is involved in parvovirus-induced actin processing. Scale bars: 15 µm (A) 10 µm (C).</p>", "links"=>[], "tags"=>["ckii", "gelsolin-dependent", "actin", "parvovirus"], "article_id"=>594314, "categories"=>["Biochemistry", "Cell Biology", "Infectious Diseases", "Virology"], "users"=>["Séverine Bär", "Laurent Daeffler", "Jean Rommelaere", "Jürg P. F. Nüesch"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000126.g006", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Impact_of_CKII_on_gelsolin_dependent_actin_processing_and_parvovirus_egress_/594314", "title"=>"Impact of CKII on gelsolin-dependent actin processing and parvovirus egress.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-15 01:11:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/923558"], "description"=>"<p>Cells were transfected with control serum (αCon) or neutralizing anti-gelsolin antibodies (αGln) at 7 µg/cell. Twenty-four hours post-transfection, they were infected with the indicated parvovirus, washed extensively after 2 h to remove the inoculum, and further incubated for the indicated time (h). Cells and supernatants were collected separately at the indicated time p.i. (Inf 1). To estimate the amount of infectious virions released into the medium, naive cultures were incubated with Inf-1 supernatants and harvested 24 h later (Inf 2). Although dispensible during virus entry, DNA amplification and formation of DNA-containing capsids, gelsolin appears to play a role either in the generation of infectious progeny virions and/or the release of infectious particles into the medium. (A) The efficiencies of transfection (with antibodies) and infection (with MVM) were measured in parallel by IF staining of cultured cells treated with control antiserum (αCon) or neutralizing anti-gelsolin antibodies (αGln). (B, C) Production of replicative intermediates (dRF, mRF) and single-stranded progeny-virion DNA (ssDNA) was measured by Southern blotting in (B) MVM-infected A9 cells (10 pfu/cell) and (C) H-1-PV-infected NCH149 cells (10 pfu/cell).</p>", "links"=>[], "tags"=>["gelsolin", "parvovirus", "replication"], "article_id"=>594006, "categories"=>["Biochemistry", "Cell Biology", "Infectious Diseases", "Virology"], "users"=>["Séverine Bär", "Laurent Daeffler", "Jean Rommelaere", "Jürg P. F. Nüesch"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000126.g002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Impact_of_gelsolin_on_parvovirus_replication_and_spreading_/594006", "title"=>"Impact of gelsolin on parvovirus replication and spreading.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-15 01:06:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/923777"], "description"=>"<p>(A, B) A9 cells and derivatives expressing a mutant gelsolin were infected (or not) with CsCl-gradient-purified MVM (30 pfu/cell), treated with neuraminidase to avoid second-round infection, and fixed at 24 h p.i. Capsids (detected with αB7 [green]) were analyzed by confocal laser scanning and spinning-disk microscopy for their subcellular localization, as compared to that of Lamp2-positive vesicles. Progeny virions are associated with cellular lysosomes and/or late endosomes as apparent from colocalization with the vesicular marker Lamp2 in the cytosol. (A) a, mock-treated A9 cells; Lamp2 (main panel) and the negative control for capsid staining (insert); b, Lamp2 staining of MVM-infected A9 cells; c, MVM capsids in infected A9 cells; bc, Lamp2/capsid merge; bc′, enlarged area; d, Lamp2/capsid merge applied to MVM-infected A9 cells expressing a dominant-negative gelsolin variant. Scale bars: 8 µm. (A′) Capsid/Lamp2 colocalization determined with imageJ, expressed as the mean value of a whole stack. Capsid/mitotracker (suppl. 3) served as a negative control (Contr.). Cap in Ves, percentage of green pixels merging with red. Values in parentheses are derived from cytoplasmic areas; Ves with Cap, red pixels merging with green. (B) a, dynamin in mock-treated A9; b, dynamin in MVM-infected A9; c, MVM capsids; bc, dynamin/capsid merge. Small squares represent enlarged areas of capsid/dynamin colocalization. Scale bars 12 µm. (C) A9 cells and cells of the derivative expressing GlnY435A were infected with MVM (30 pfu/cell), harvested at 24 h p.i., and fractionated by differential (density) centrifugation to separate different organelles. The presence of progeny particles was determined by Southern blotting (revealing their single-stranded DNA). DNA-containing progeny virions co-purify with cellular vesicles during biochemical fractionations of cellular organelles. Nuc, purified nuclei; HMF, large organelles; Cyt, cytosol. Cellular vesicles were further purified from the light mitochondrial fraction (LMF) by centrifugation through an iodixanol gradient. The migration of Lamp2 is indicated by arrows. (D) A9 cells (lanes 1&2) and derivatives expressing either GST-tagged α-tubulin (lanes 3 and 4) or β-actin (lanes 5–10) were mock-treated (−) or infected with MVM for the indicated time (h). Cell extracts were prepared and run through Glutathione Sepharose columns specifically retaining the GST-tagged proteins and their associated partners. The partners were recovered (700 mM NaCl Eluate) and tested for the presence of full (virion-containing) capsids by Southern blotting (ssDNA) and Western blotting (capsid proteins), by comparison with the corresponding total extracts (Input). Black arrows indicate the migration of ssDNA, grey arrows of free replicative form viral DNAs. DNA-containing progeny particles specifically interact with actin.</p>", "links"=>[], "tags"=>["mvm", "progeny"], "article_id"=>594230, "categories"=>["Biochemistry", "Cell Biology", "Infectious Diseases", "Virology"], "users"=>["Séverine Bär", "Laurent Daeffler", "Jean Rommelaere", "Jürg P. F. Nüesch"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000126.g005", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Vesicular_transport_of_MVM_progeny_virions_/594230", "title"=>"Vesicular transport of MVM progeny virions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-15 01:10:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/923469"], "description"=>"<p>(A) A9 cells grown on spot slides were infected (or not) with MVM (30 pfu/cell), fixed with paraformaldehyde at the indicated time p.i., and analyzed by confocal laser scanning microscopy after double-labeling for actin with rhodamine-coupled phalloidin (red), and gelsolin, with Cy2-conjugated IgGs (green). Colocalization areas appear yellow in the merge. Scale bar 15 µm. Gelsolin is found associated to phalloidin-stained actin in both non-infected and MVM-infected cells. Arrows point to a slight but distinct accumulation of the actin-processing polypeptide in the perinuclear region. (B) A9 cells were infected with MVM (30 pfu/cell) and harvested at the indicated time p.i. Association of gelsolin and actin with cellular scaffold and membrane structures was determined by fractionating cell extracts by a combined sedimentation and Triton X-100 extraction procedure. The distribution of each protein among the various fractions was determined by western blotting. Upon MVM-infection, actin and gelsolin become associated with membrane structures. iS, insoluble scaffold proteins; nM, mainly nuclear (membrane) constituents; sS, soluble scaffold proteins; pM, mainly vesicular and plasma (membrane) constituents; C, soluble cytosolic proteins. (C) Binding of gelsolin to cytoskeletal proteins was determined by affinity chromatography using GST-tagged βactin or tropomyosin 5 (TM) as baits in stably transfected cells. Extracts of mock (−) and MVM-infected (+) cells (parental A9 [lanes 1 and 2] or derivatives expressing GST-tagged βactin [lanes 3 and 4] or TM [lanes 5 and 6]) were run through Glutathione Sepharose columns specifically retaining GST-tagged proteins and partners thereof. 700 mM NaCl eluates containing the partner proteins were analyzed by western blotting for the presence of gelsolin, in comparison with the cell-matched original extract (Input).</p>", "links"=>[], "tags"=>["modulation", "mvm", "a9"], "article_id"=>593919, "categories"=>["Biochemistry", "Cell Biology", "Infectious Diseases", "Virology"], "users"=>["Séverine Bär", "Laurent Daeffler", "Jean Rommelaere", "Jürg P. F. Nüesch"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000126.g001", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gelsolin_modulation_during_MVM_infection_of_A9_cells_/593919", "title"=>"Gelsolin modulation during MVM infection of A9 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-15 01:05:19"}

PMC Usage Stats | Further Information

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Relative Metric

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