Dengue Virus Capsid Protein Binds Core Histones and Inhibits Nucleosome Formation in Human Liver Cells
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{"title"=>"Dengue virus capsid protein binds core histones and inhibits nucleosome formation in human liver cells", "type"=>"journal", "authors"=>[{"first_name"=>"Tonya M.", "last_name"=>"Colpitts", "scopus_author_id"=>"15053041100"}, {"first_name"=>"Sebastian", "last_name"=>"Barthel", "scopus_author_id"=>"51664716200"}, {"first_name"=>"Penghua", "last_name"=>"Wang", "scopus_author_id"=>"23483045700"}, {"first_name"=>"Erol", "last_name"=>"Fikrig", "scopus_author_id"=>"7102240544"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-80052361705", "sgr"=>"80052361705", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"21909430", "doi"=>"10.1371/journal.pone.0024365", "pui"=>"362482076"}, "id"=>"06fb2f54-2246-3955-b6b8-3b80403f4ae5", "abstract"=>"Dengue virus (DENV) is a member of the Flaviviridae and a globally (re)emerging pathogen that causes serious human disease. There is no specific antiviral or vaccine for dengue virus infection. Flavivirus capsid (C) is a structural protein responsible for gathering the viral RNA into a nucleocapsid that forms the core of a mature virus particle. Flaviviral replication is known to occur in the cytoplasm yet a large portion of capsid protein localizes to the nucleus during infection. The reasons for the nuclear presences of capsid are not completely understood. Here, we expressed mature DENV C in a tandem affinity purification assay to identify potential binding partners in human liver cells. DENV C targeted the four core histones, H2A, H2B, H3 and H4. DENV C bound recombinant histones in solution and colocalized with histones in the nucleus and cytoplasm of liver cells during DENV infection. We show that DENV C acts as a histone mimic, forming heterodimers with core histones, binding DNA and disrupting nucleosome formation. We also demonstrate that DENV infection increases the amounts of core histones in livers cells, which may be a cellular response to C binding away the histone proteins. Infection with DENV additionally alters levels of H2A phosphorylation in a time-dependent manner. The interactions of C and histones add an interesting new role for the presence of C in the nucleus during DENV infection.", "link"=>"http://www.mendeley.com/research/dengue-virus-capsid-protein-binds-core-histones-inhibits-nucleosome-formation-human-liver-cells-1", "reader_count"=>87, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>15, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>31, "Student > Postgraduate"=>2, "Student > Master"=>16, "Other"=>3, "Student > Bachelor"=>6, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>15, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>31, "Student > Postgraduate"=>2, "Student > Master"=>16, "Other"=>3, "Student > Bachelor"=>6, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>13, "Materials Science"=>2, "Agricultural and Biological Sciences"=>54, "Medicine and Dentistry"=>9, "Physics and Astronomy"=>1, "Chemistry"=>2, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Materials Science"=>{"Materials Science"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>9}, "Chemistry"=>{"Chemistry"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>54}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>13}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>4, "China"=>1, "Japan"=>1, "Brazil"=>1, "United Kingdom"=>1, "Mexico"=>1, "Germany"=>1, "Indonesia"=>1, "French Polynesia"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/739863"], "description"=>"<p>Huh7 cells were transfected with DEN2 C and/or infected with DEN2 24 h post-transfection. Cells were lysed 24 h post-infection (48 h post-transfection) and lysates were run on 4–12% SDS-PAGE gel. Gels were used in a Western blotting assay with antibodies against histones H2A (A), H2B (B), H3 (C) and H4 (D); monomers, dimers and octamers are indicated. Gels were stripped and reprobed with an antibody against actin as a protein loading control. The same amount of protein was loaded in each lane for each gel as a control for expression.</p>", "links"=>[], "tags"=>["disrupts", "histone"], "article_id"=>410238, "categories"=>["Microbiology", "Virology", "Infectious Diseases"], "users"=>["Tonya M. Colpitts", "Sebastian Barthel", "Penghua Wang", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024365.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_expression_disrupts_histone_oligomerization_/410238", "title"=>"DENV expression disrupts histone oligomerization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-01 00:03:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/740065"], "description"=>"<p>(A,B,C) DEN2 C and core histones were co-immunoprecipitated during DEN2 infection of Huh-7 liver cells. Cells were lysed 24 h post-infection with DEN2 at moi 0.1. DENV C was immunoprecipitated from the cell lysate using anti-capsid serum, run on a 4–12% SDS-PAGE gel and transferred to nitrocellulose. The membrane was probed with antibodies against H2A (A), H2B (B) and H3 (C). (D) The H2A, H2B and H3 proteins were separately immunoprecipitated from the lysate and the solutions were run on a 4–12% SDS-PAGE gel and transferred to nitrocellulose. The membrane was probed with mouse immune serum against DEN2 C protein. Immunoprecipitate using beta-actin antibody was used as control in A–D.</p>", "links"=>[], "tags"=>["binds", "histones", "denv"], "article_id"=>410435, "categories"=>["Microbiology", "Virology", "Infectious Diseases"], "users"=>["Tonya M. Colpitts", "Sebastian Barthel", "Penghua Wang", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024365.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_C_binds_core_histones_during_DENV_infection_/410435", "title"=>"DENV C binds core histones during DENV infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-01 00:07:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/373294", "https://ndownloader.figshare.com/files/373323", "https://ndownloader.figshare.com/files/373341", "https://ndownloader.figshare.com/files/373366"], "description"=>"<div><p>Dengue virus (DENV) is a member of the <em>Flaviviridae</em> and a globally (re)emerging pathogen that causes serious human disease. There is no specific antiviral or vaccine for dengue virus infection. Flavivirus capsid (C) is a structural protein responsible for gathering the viral RNA into a nucleocapsid that forms the core of a mature virus particle. Flaviviral replication is known to occur in the cytoplasm yet a large portion of capsid protein localizes to the nucleus during infection. The reasons for the nuclear presences of capsid are not completely understood. Here, we expressed mature DENV C in a tandem affinity purification assay to identify potential binding partners in human liver cells. DENV C targeted the four core histones, H2A, H2B, H3 and H4. DENV C bound recombinant histones in solution and colocalized with histones in the nucleus and cytoplasm of liver cells during DENV infection. We show that DENV C acts as a histone mimic, forming heterodimers with core histones, binding DNA and disrupting nucleosome formation. We also demonstrate that DENV infection increases the amounts of core histones in livers cells, which may be a cellular response to C binding away the histone proteins. Infection with DENV additionally alters levels of H2A phosphorylation in a time-dependent manner. The interactions of C and histones add an interesting new role for the presence of C in the nucleus during DENV infection.</p> </div>", "links"=>[], "tags"=>["dengue", "capsid", "binds", "histones", "inhibits", "nucleosome", "cells"], "article_id"=>133722, "categories"=>["Cancer", "Microbiology"], "users"=>["Tonya M. Colpitts", "Sebastian Barthel", "Penghua Wang", "Erol Fikrig"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0024365.s001", "https://dx.doi.org/10.1371/journal.pone.0024365.s002", "https://dx.doi.org/10.1371/journal.pone.0024365.s003", "https://dx.doi.org/10.1371/journal.pone.0024365.s004"], "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Dengue_Virus_Capsid_Protein_Binds_Core_Histones_and_Inhibits_Nucleosome_Formation_in_Human_Liver_Cells/133722", "title"=>"Dengue Virus Capsid Protein Binds Core Histones and Inhibits Nucleosome Formation in Human Liver Cells", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-01 01:02:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/739492"], "description"=>"<p>(A) Far Western blot. Purified GST-tagged DEN2 C and GST alone were run on a 4–12% SDS-PAGE gel and transferred to nitrocellulose. The membrane was incubated with each of the core histones (H2A, H2B, H3, H4) for 1 h at RT and detected using rabbit polyclonal antibodies against the histones. (B) Western blot of GST-tagged DEN2 C using an antibody against GST for detection. (C) Far Western assay done with recombinant histone proteins and probed with GST-tagged DENV C in the same manner as (A). Control proteins for specificity are BSA and GFP (far right lanes). (D) Graph of ELISA measuring levels of histones or GFP that bound GST-tagged DEN2 C, normalized to levels that bound GST alone.</p>", "links"=>[], "tags"=>["binds", "mammalian", "histone"], "article_id"=>409864, "categories"=>["Microbiology", "Virology", "Infectious Diseases"], "users"=>["Tonya M. Colpitts", "Sebastian Barthel", "Penghua Wang", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024365.g001", "stats"=>{"downloads"=>1, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_C_binds_mammalian_core_histone_proteins_/409864", "title"=>"DENV C binds mammalian core histone proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-01 02:44:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/740191"], "description"=>"<p>The 100 amino acid mature DEN2 C protein fused to streptavidin binding protein and calmodulin binding protein (CBP) tags was expressed in Huh7 liver cells and interactions identified using a tandem affinity purification assay. Proteins that bound tagged DEN2 C were isolated and identified by LC-MS/MS spectrometry.</p>", "links"=>[], "tags"=>["histones", "den2", "binding"], "article_id"=>410566, "categories"=>["Microbiology", "Virology", "Infectious Diseases"], "users"=>["Tonya M. Colpitts", "Sebastian Barthel", "Penghua Wang", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024365.t001", "stats"=>{"downloads"=>3, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mammalian_core_histones_were_identified_as_DEN2_C_binding_partners_/410566", "title"=>"Mammalian core histones were identified as DEN2 C binding partners.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-01 00:09:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/739966"], "description"=>"<p>Huh7 cells were infected with DEN1 (A and E), DEN2 (B and F), DEN3 (C and G) and DEN4 (D and H) and fixed 24 h post-infection with 4% para-formaldehyde. Cells were stained with antibodies against histone 2A (A–D) and histone 3 (E–H) with a TRITC secondary antibody as well as mouse immune serum against DENV C protein (A–H) with a FITC secondary antibody. Cells were counterstained with DAPI to visualize the nucleus. DENV C expression is green, histone staining is red and DAPI is blue.</p>", "links"=>[], "tags"=>["colocalizes", "histones", "denv"], "article_id"=>410339, "categories"=>["Microbiology", "Virology", "Infectious Diseases"], "users"=>["Tonya M. Colpitts", "Sebastian Barthel", "Penghua Wang", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024365.g006", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_C_colocalizes_with_histones_during_DENV_infection_/410339", "title"=>"DENV C colocalizes with histones during DENV infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-01 00:05:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/739559"], "description"=>"<p>DEN2 C colocalized with H2A (A), H2B (B), H3 (C) and H4 (D) in Huh7 cells. Cells were transfected with GFP-DEN2 C and fixed in 4% para-formaldehyde 48 h post-transfection. Cells were stained with antibodies against histones and a TRITC secondary antibody. Cells were counterstained with DAPI to visualize the nucleus. GFP-DEN2 C expression is green, histone staining is red and DAPI is blue.</p>", "links"=>[], "tags"=>["colocalizes", "histones", "huh7"], "article_id"=>409934, "categories"=>["Microbiology", "Virology", "Infectious Diseases"], "users"=>["Tonya M. Colpitts", "Sebastian Barthel", "Penghua Wang", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024365.g002", "stats"=>{"downloads"=>7, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_C_colocalizes_with_histones_in_Huh7_liver_cells_/409934", "title"=>"DENV C colocalizes with histones in Huh7 liver cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-01 02:45:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/740134"], "description"=>"<p>A. Huh7 cells were infected with DEN2 and lysed 24 h post-infection. Uninfected cells were also incubated as control. Cell lysates were run on 4–12% SDS-PAGE gel and gels were used in a Western blotting assay with antibodies against histones H2A, H2B, H3 and H4, as well as actin for loading control. B. Histone siRNA reduces DENV infection. Huh7 cells were transfected with siRNA targeting either H2A or H3 and infected with DEN2 48h post-transfection. Transfected and uninfected cells were also incubated as control. RNA was isolated from cells and cDNA used in a real-time qPCR reaction to measure dengue infection. Infection is indicated as copy number of envelope gene (E)/copy number GAPDH. C. DENV infection alters H2A phosphorylation in a time-dependent manner. Huh7 cells were either transfected with GFP-DEN2 and lysed 24 h post-transfection or infected with DEN2 and lysed post-infection. Cell lysates were run on 4–12% SDS-PAGE gel and gels were used in a Western blotting assay with antibodies against H2A, phosphorylated H2a (H2A*) and actin as loading control. 0–96 indicates hour post-infection, (−) indicates uninfected lysate and C indicates cells transfected with capsid for 24 hours.</p>", "links"=>[], "tags"=>["alters", "levels"], "article_id"=>410511, "categories"=>["Microbiology", "Virology", "Infectious Diseases"], "users"=>["Tonya M. Colpitts", "Sebastian Barthel", "Penghua Wang", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024365.g008", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_infection_alters_levels_of_core_histones_/410511", "title"=>"DENV infection alters levels of core histones.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-01 00:08:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/739751"], "description"=>"<p>(A) 5 µg or (B) 2 µg of BSA or histone proteins H2A, H2B, H3 and H4 were incubated with 300 ng plasmid DNA, with and without 10 µg GST-tagged DENV C, for 1 h at 37°C. (C) 1 µg of GST or H2A, H2B, H3 and H4 were incubated with 300 ng plasmid DNA, with and without 10 µg GST-tagged DENV C, for 1 h at 37°C. (D) 10 µg GST or 10 µg untagged DENV C was incubated with 300 ng plasmid DNA (left panel), 1 µg (middle panel) or 2 µg (right panel) of H2A was incubated with 300 ng plasmid DNA, both with and without 10 µg GST-tagged DENV C. Solutions were run on 1% agarose gel with ethidium bromide to visualize DNA migration. Bound/unbound DNA is indicated.</p>", "links"=>[], "tags"=>["binds", "dna", "disrupt", "histone-dna"], "article_id"=>410126, "categories"=>["Microbiology", "Virology", "Infectious Diseases"], "users"=>["Tonya M. Colpitts", "Sebastian Barthel", "Penghua Wang", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024365.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_C_binds_DNA_and_does_not_disrupt_histone_DNA_binding_/410126", "title"=>"DENV C binds DNA and does not disrupt histone-DNA binding.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-01 00:02:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/739663"], "description"=>"<p>(A) Purified GST-tagged DEN2 C and recominant histone proteins were incubated in solution for 1 h at 37°C. Proteins were separated on 4–12% SDS-PAGE gel and stained with Coomassie blue (left panel) and silver stain (GST-capsid only; right panel). Numbers at right of gel images indicate the following bands: 1-capsid monomer, 2-histone monomer, 3-GST-capsid monomer, 4-histone dimer, 5-GST-capsid/histone dimer, 6-GST-capsid dimer. (B) Histones and (C) DENV C are detected in presumed heterodimers from (A) using antibodies against histones and DEN2 capsid in Western blot assays.</p>", "links"=>[], "tags"=>["forms", "dimers", "histones"], "article_id"=>410041, "categories"=>["Microbiology", "Virology", "Infectious Diseases"], "users"=>["Tonya M. Colpitts", "Sebastian Barthel", "Penghua Wang", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024365.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_C_forms_dimers_with_core_histones_in_solution_/410041", "title"=>"DENV C forms dimers with core histones in solution.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-01 00:00:41"}

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Relative Metric

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