The Role of the Phosphatidylinositol 4-Kinase PI4KA in Hepatitis C Virus-Induced Host Membrane Rearrangement
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{"title"=>"The role of the phosphatidylinositol 4-kinase PI4KA in hepatitis C virus-induced host membrane rearrangement", "type"=>"journal", "authors"=>[{"first_name"=>"Andrew W.", "last_name"=>"Tai", "scopus_author_id"=>"36974819100"}, {"first_name"=>"Shadi", "last_name"=>"Salloum", "scopus_author_id"=>"23986170900"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"22022594", "doi"=>"10.1371/journal.pone.0026300", "pui"=>"362735285", "issn"=>"19326203", "sgr"=>"80053962863", "scopus"=>"2-s2.0-80053962863"}, "id"=>"1d23d796-4d9a-3cff-9568-3b31978dd957", "abstract"=>"BACKGROUND: Hepatitis C virus (HCV), like other positive-sense RNA viruses, replicates on an altered host membrane compartment that has been called the \"membranous web.\" The mechanisms by which the membranous web are formed from cellular membranes are poorly understood. Several recent RNA interference screens have demonstrated a critical role for the host phosphatidylinositol 4-kinase PI4KA in HCV replication. We have sought to define the function of PI4KA in viral replication.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: Using a nonreplicative model of membranous web formation, we show that PI4KA silencing leads to aberrant web morphology. Furthermore, we find that PI4KA and its product, phosphatidylinositol 4-phosphate, are enriched on membranous webs and that PI4KA is found in association with NS5A in HCV-infected cells. While the related lipid kinase PI4KB also appears to support HCV replication, it does not interact with NS5A. Silencing of PI4KB does not overtly impair membranous web morphology or phosphatidylinositol 4-phosphate enrichment at webs, suggesting that it acts at a different point in viral replication. Finally, we demonstrate that the aberrant webs induced by PI4KA silencing require the activity of the viral NS3-4A serine protease but not integrity of the host secretory pathway.\\n\\nCONCLUSIONS/SIGNIFICANCE: PI4KA is necessary for the local enrichment of PI 4-phosphate at the HCV membranous web and for the generation of morphologically normal webs. We also show that nonreplicative systems of web formation can be used to order molecular events that drive web assembly.", "link"=>"http://www.mendeley.com/research/role-phosphatidylinositol-4kinase-pi4ka-hepatitis-c-virusinduced-host-membrane-rearrangement", "reader_count"=>37, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>13, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>1, "Student > Master"=>2, "Student > Bachelor"=>4}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>13, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>1, "Student > Master"=>2, "Student > Bachelor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>26, "Medicine and Dentistry"=>3, "Chemistry"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>26}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United States"=>3, "Germany"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/725369"], "description"=>"<p>(<b>A</b>) Schematic of the Jc1(SF) viral genome containing a tandem Strep-tag II and a FLAG tag in domain III of NS5A. (<b>B</b>) Productive infection of hepatoma cells with the Jc1(SF) virus. Huh7.5.1 cells were infected with wild-type Jc1 (upper panels) and culture-adapted Jc1(SF) viruses at an MOI of 1, fixed at six days after infection, and immunostained for NS5A (left panels) and FLAG (right panels). Nuclei were visualized by DAPI staining. (<b>C</b>) PI4KA associates with epitope-tagged NS5A in Jc1(SF)-infected cells. Lysates prepared from Huh7.5.1 cells infected six days prior with either wild-type Jc1 or culture-adapted Jc1(SF) were incubated with Strep-Tactin-conjugated beads. Unbound proteins were saved for analysis. After washing, NS5A(SF) and interacting proteins (“bound”) were eluted with biotin. Samples were separated by SDS-PAGE and immunoblotted for PI4KA, NS5A, and beta-actin.</p>", "links"=>[], "tags"=>["interacts", "ns5a", "hcv-infected"], "article_id"=>395728, "categories"=>["Microbiology", "Virology", "Biochemistry", "Chemistry", "Infectious Diseases", "Cell Biology"], "users"=>["Andrew W. Tai", "Shadi Salloum"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026300.g003", "stats"=>{"downloads"=>0, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PI4KA_interacts_with_NS5A_in_HCV_infected_cells_/395728", "title"=>"PI4KA interacts with NS5A in HCV-infected cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 13:52:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/725122"], "description"=>"<p>(<b>A</b>) Constructs used to express the subgenomic NS3-NS5B polyprotein under the control of a T7 promoter. The pTM1(NS3-5B/GFP) construct contains a GFP insertion within domain III of NS5A that has been previously shown to be compatible with viral replication <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026300#pone.0026300-Moradpour1\" target=\"_blank\">[23]</a>. (<b>B</b>) Recovery of replicative HCV RNA transcripts in Huh7/T7 cells stably expressing T7 RNA polymerase by a colony formation assay. Huh7/T7 cells were transfected with a DNA plasmid encoding the JFH-1 subgenomic replicon flanked by a 5′ T7 promoter and a 3′ hepatitis D virus antigenomic ribozyme and T7 terminator. The NS5B GNN mutation was introduced into this construct as a negative control. Transfected cells underwent G418 selection for three weeks and colonies were visualized by crystal violet staining. (<b>C</b>) Nonreplicative expression of NS3-5B polyprotein leads to punctate membrane structures similar in morphology to membranous webs in replicon cells. NS5A-GFP and NS3 were visualized in Huh7.5.1 hepatoma cells containing a stably replicating subgenomic HCV replicon (upper panels) compared to Huh7/T7 cells expressing the NS3-NS5B polyprotein by T7 RNA polymerase (lower panels). Nuclei were counterstained with DAPI. Bars, 10 µm. (<b>D</b>) Immunostaining of subgenomic replicon-expressing cells (upper panels) and Huh7/T7 cells expressing the HCV polyprotein (lower panels) for NS5A and for annexin A2, a host factor known to be recruited to membranous webs. Nuclei were counterstained with DAPI. Bar, 10 µm. (<b>E</b>) The effect of an NS3-4A protease inhibitor on membranous web formation is readily visualized using a nonreplicative HCV expression model. Huh7.5.1 hepatoma cells containing a HCV subgenomic replicon (upper row) or expressing HCV NS3-5B by T7 RNA polymerase (lower row) were incubated with 10 µM BILN-2061, a NS3-4A serine protease inhibitor (PI) for 48 hr and the distributions of NS3 and NS5A-GFP were visualized by confocal immunofluorescence microscopy. Nuclei were counterstained with DAPI. Bar, 10 µm.</p>", "links"=>[], "tags"=>["nonreplicative", "hcv", "membranous"], "article_id"=>395476, "categories"=>["Microbiology", "Virology", "Biochemistry", "Chemistry", "Infectious Diseases", "Cell Biology"], "users"=>["Andrew W. Tai", "Shadi Salloum"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026300.g001", "stats"=>{"downloads"=>1, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_nonreplicative_system_to_study_HCV_membranous_web_formation_/395476", "title"=>"A nonreplicative system to study HCV membranous web formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 13:50:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/725723"], "description"=>"<p>(<b>A</b>) Formation of membrane “clusters” in PI4KA-silenced cells expressing HCV proteins requires HCV polyprotein cleavage. Huh7/T7 cells were transduced with a nontargeting (upper panels) or a PI4KA-targeting (lower panels) shRNA vector prior to pTM1(NS3-5B) transfection. Cells were treated with 0.5% DMSO (left panels) or with 10 µM BILN-2061 (right panels) for 24 hours prior to fixation and immunostaining for NS5A. Nuclei were counterstained with DAPI. Bar, 10 µm. (<b>B</b>) Formation of membrane “clusters” in PI4KA-silenced cells expressing HCV proteins does not require integrity of the host secretory pathway. Huh7/T7 cells were transduced with a nontargeting (upper panels) or a PI4KA-targeting (lower panels) shRNA vector prior to pTM1(NS3-5B) transfection. Upon transfection, cells were treated with 0.1% ethanol or with 100 ng/mL BFA for 24 hours prior to fixation and immunostaining for NS5A and beta-COP (to demonstrate COPI coatomer dispersal by BFA). Nuclei were counterstained with DAPI. Bar, 10 µm. (<b>C</b>) Cells from the experiments shown in panels (A) and (B) were counted to determine the fraction with the membrane “cluster” phenotype. A minimum of 100 cells were counted for each condition in each of two independent experiments. Values shown are means ± SD.</p>", "links"=>[], "tags"=>["membrane", "clustering", "pi4ka-silenced", "cells", "requires", "ns3-4a", "protease", "secretory", "pathway"], "article_id"=>396070, "categories"=>["Microbiology", "Virology", "Biochemistry", "Chemistry", "Infectious Diseases", "Cell Biology"], "users"=>["Andrew W. Tai", "Shadi Salloum"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026300.g006", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HCV_induced_membrane_clustering_in_PI4KA_silenced_cells_requires_NS3_4A_protease_activity_but_does_not_require_host_secretory_pathway_integrity_/396070", "title"=>"HCV-induced membrane clustering in PI4KA-silenced cells requires NS3-4A protease activity but does not require host secretory pathway integrity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 13:54:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/725250"], "description"=>"<p>(<b>A</b>) Silencing of PI4KA leads to the disappearance of NS5A-GFP expression in HCV replicon cells. Huh7.5.1 cells expressing a subgenomic replicon were transduced with a nontargeting (left) or PI4KA-targeting (right) lentiviral shRNA vector for 5 days. HCV membranous web distribution was visualized using GFP-tagged NS5A. Bar, 20 µm. (<b>B</b>) Silencing of PI4KA leads to accumulation of membrane “clusters” in a nonreplicative model of web assembly. Huh7/T7 cells were transduced with a nontargeting (upper row) or PI4KA-targeting (lower rows) lentiviral shRNA vector and then transfected with pTM1(NS3-5B/GFP) to express the subgenomic NS3-5B polyprotein (with GFP-tagged NS5A). NS3 and NS4B were visualized by immunofluorescence staining and nuclei were counterstained with DAPI. Bars, 10 µm. (<b>C</b>) Huh7/T7 cells transduced with a nontargeting (NT) or PI4KA-targeting shRNA vector were transfected with pTM1(NS3-5B/GFP). Cells were then counted to determine the fraction with the membrane “cluster” phenotype. At least 100 cells were counted for each condition in each of three independent experiments. Values shown are means ± SD. (<b>D</b>) Colocalization of endogenous PI4KA immunofluorescence staining with NS5A in Huh7.5.1 cells expressing a subgenomic replicon (upper panels) or in Huh7/T7 cells transfected with pTM1(NS3-5B). Nuclei were counterstained with DAPI. Bars, 10 µm. (<b>E</b>) PI4KA requires kinase activity to support HCV replication. OR6 replicon cells were transduced with MMLV retroviral vectors encoding GFP, PI4KA, or a PI4KA D1899A mutant lacking kinase activity. The cells were then transduced 24 h later with lentiviral vectors encoding a nontargeting shRNA (black bars) or a shRNA targeting the PI4KA 3′UTR (white bars) to silence endogenous PI4KA. Cells were assayed 96 h after lentiviral transduction (upper panel). Values were obtained from quadruplicate wells in two independent experiments and are plotted as means ± SD. Cells in duplicate wells were lysed for immunoblotting for PI4KA, anti-FLAG, and beta-actin (lower panel) to confirm PI4KA silencing and PI4KA construct expression. PI4KA band intensities were quantitated by densitometric analysis using NIH ImageJ software and normalized to beta-actin.</p>", "links"=>[], "tags"=>["colocalizes", "hcv", "membranous", "webs", "leads", "aberrant"], "article_id"=>395607, "categories"=>["Microbiology", "Virology", "Biochemistry", "Chemistry", "Infectious Diseases", "Cell Biology"], "users"=>["Andrew W. Tai", "Shadi Salloum"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026300.g002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PI4KA_colocalizes_with_HCV_membranous_webs_and_its_silencing_leads_to_aberrant_web_morphology_/395607", "title"=>"PI4KA colocalizes with HCV membranous webs and its silencing leads to aberrant web morphology.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 13:51:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/725584"], "description"=>"<p>(<b>A</b>) PI4KB silencing inhibits HCV infection. Huh7.5.1 cells were transduced with a nontargeting lentiviral shRNA construct or shRNA constructs targeting PI4KA or PI4KB. Two independent PI4KB-targeting shRNA vectors were used at two different doses. shRNA-transduced cells were infected with a Jc1/Gluc2A reporter virus encoding a <i>Gaussia</i> luciferase reporter gene. 72 hr after infection, luciferase activity in the supernatant was assayed and normalized to cells transduced with the nontargeting shRNA. Values represent means ± SD from triplicate wells in two independent experiments. (<b>B</b>) Cell lysates prepared from cells transduced with nontargeting, PI4KA, or PI4KB shRNA vectors and infected with Jc1/Gluc2A as in (A) were separated by SDS-PAGE and immunoblotted for PI4KA, PI4KB, NS5A, and beta-actin. PI4KA and PI4KB band intensities were quantitated by densitometric analysis using NIH ImageJ software and normalized to beta-actin. (<b>C</b>) PI4KB does not interact with NS5A in HCV-infected cells. Lysates prepared from Huh7.5.1 cells infected with Jc1(SF) virus were incubated with Strep-Tactin-conjugated beads. Unbound proteins were saved for analysis. After washing, NS5A(SF) and interacting proteins (“bound” lane) were eluted with biotin. Samples were separated by SDS-PAGE and immunoblotted for PI4KA, PI4KB, and NS5A. (<b>D</b>) PI4KB does not colocalize with membranous webs. Huh7.5.1 stably expressing the SGR-JFH1(NS5A-GFP) replicon were transiently transfected with a myc-PI4KB construct and immunostained with an anti-myc antibody. Bars, 10 µm. (<b>E</b>) PI4KB silencing does not alter membranous web morphology in the T7 HCV expression system. Huh7/T7 cells were silenced with the PI4KB shRNA #1 construct used in (A) and (B) prior to transfection with pTM1(NS3-5B/GFP). Cells were immunostained with anti-NS3 and NS5A-GFP was visualized by GFP fluorescence. Nuclei were counterstained with DAPI. Bar, 10 µm. (<b>F</b>) PI4KB silencing does not lead to loss of PI(4)P immunoreactivity at membranous webs. Huh7/T7 cells were silenced for PI4KB prior to transfection with pTM1(NS3-5B/GFP). Cells were immunostained with anti-PI(4)P and nuclei were counterstained with DAPI. Bar, 10 µm.</p>", "links"=>[], "tags"=>["inhibits", "hcv", "membranous"], "article_id"=>395946, "categories"=>["Microbiology", "Virology", "Biochemistry", "Chemistry", "Infectious Diseases", "Cell Biology"], "users"=>["Andrew W. Tai", "Shadi Salloum"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026300.g005", "stats"=>{"downloads"=>1, "page_views"=>96, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PI4KB_silencing_inhibits_HCV_infection_but_does_not_affect_membranous_web_formation_/395946", "title"=>"PI4KB silencing inhibits HCV infection but does not affect membranous web formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 13:53:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/725465"], "description"=>"<p>(<b>A</b>) PI(4)P immunostaining colocalizes with NS5A(GFP) at HCV membranous webs in replicon-expressing Huh7.5.1 cells (upper panels) as well as in T7-driven nonreplicative expression of NS3-5B (lower panels). Nuclei were counterstained with DAPI. Bar, 10 µm. (<b>B</b>) The membrane clusters induced by PI4KA silencing in the T7 expression model are negative for PI(4)P immunostaining. Huh7/T7 cells were silenced for PI4KA using lentiviral shRNA expression and then transfected with pTM1(NS3-5B/GFP) 24 hr prior to fixation and immunolabeling for PI(4)P. Nuclei were counterstained with DAPI. Bar, 10 µm.</p>", "links"=>[], "tags"=>["enriched", "hcv", "membranous"], "article_id"=>395822, "categories"=>["Microbiology", "Virology", "Biochemistry", "Chemistry", "Infectious Diseases", "Cell Biology"], "users"=>["Andrew W. Tai", "Shadi Salloum"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026300.g004", "stats"=>{"downloads"=>2, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PI_4_P_is_enriched_on_HCV_membranous_webs_/395822", "title"=>"PI(4)P is enriched on HCV membranous webs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 13:52:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/725831"], "description"=>"<p>Restriction enzymes sites are bolded.</p>", "links"=>[], "tags"=>["dna"], "article_id"=>396191, "categories"=>["Microbiology", "Virology", "Biochemistry", "Chemistry", "Infectious Diseases", "Cell Biology"], "users"=>["Andrew W. Tai", "Shadi Salloum"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026300.t001", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Primers_used_for_DNA_construct_preparation_/396191", "title"=>"Primers used for DNA construct preparation.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 13:54:52"}

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