GP96 Interacts with HHV-6 during Viral Entry and Directs It for Cellular Degradation
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{"title"=>"GP96 interacts with HHV-6 during viral entry and directs it for cellular degradation", "type"=>"journal", "authors"=>[{"first_name"=>"Bhupesh K.", "last_name"=>"Prusty", "scopus_author_id"=>"8541380600"}, {"first_name"=>"Christine", "last_name"=>"Siegl", "scopus_author_id"=>"55391384200"}, {"first_name"=>"Nitish", "last_name"=>"Gulve", "scopus_author_id"=>"56441590300"}, {"first_name"=>"Yasuko", "last_name"=>"Mori", "scopus_author_id"=>"7404196908"}, {"first_name"=>"Thomas", "last_name"=>"Rudel", "scopus_author_id"=>"7006260007"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"600684493", "sgr"=>"84916211650", "doi"=>"10.1371/journal.pone.0113962", "scopus"=>"2-s2.0-84916211650", "pmid"=>"25470779"}, "id"=>"4b33cc53-7471-3dee-b783-695f21959a66", "abstract"=>"CD46 and CD134 mediate attachment of Human Herpesvirus 6A (HHV-6A) and HHV-6B to host cell, respectively. But many cell types interfere with viral infection through rapid degradation of viral DNA. Hence, not all cells expressing these receptors are permissive to HHV-6 DNA replication and production of infective virions suggesting the involvement of additional factors that influence HHV-6 propagation. Here, we used a proteomics approach to identify other host cell proteins necessary for HHV-6 binding and entry. We found host cell chaperone protein GP96 to interact with HHV-6A and HHV-6B and to interfere with virus propagation within the host cell. In human peripheral blood mononuclear cells (PBMCs), GP96 is transported to the cell surface upon infection with HHV-6 and interacts with HHV-6A and -6B through its C-terminal end. Suppression of GP96 expression decreased initial viral binding but increased viral DNA replication. Transient expression of human GP96 allowed HHV-6 entry into CHO-K1 cells even in the absence of CD46. Thus, our results suggest an important role for GP96 during HHV-6 infection, which possibly supports the cellular degradation of the virus.", "link"=>"http://www.mendeley.com/research/gp96-interacts-hhv6-during-viral-entry-directs-it-cellular-degradation", "reader_count"=>3, "reader_count_by_academic_status"=>{"Researcher"=>2, "Student > Postgraduate"=>1}, "reader_count_by_user_role"=>{"Researcher"=>2, "Student > Postgraduate"=>1}, "reader_count_by_subject_area"=>{"Agricultural and Biological Sciences"=>3}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>3}}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1817389"], "description"=>"<p>(<b>A</b>) Cell surface expression dynamics of GP96 in CHO-K1 cells stably expressing 55 kDa isoform of CD46. CHO-K1(5.3) cells expressing the 55 kDa isoform of CD46 were infected with HHV-6A for indicated time points. CD46 and GP96 cell surface expression were analyzed by flow cytometry (solid profiles); background fluorescence levels were measured using an isotype specific antibody (empty profiles). (<b>B</b>) Cell surface expression dynamics of GP96 in CHO-K1 cells stably expressing 65 kDa isoform of CD46. CHO-K1(5.1) cells expressing the 65 kDa isoform of CD46 were infected with HHV-6A for indicated time points. CD46 and GP96 cell surface expression were analyzed by flow cytometry (solid profiles); background fluorescence levels were measured using an isotype specific antibody (empty profiles). Mean fluorescence intensity (MFI) for each analysis is indicated below the respective figure.</p>", "links"=>[], "tags"=>["host cell proteins", "GP 96", "GP 96 Interacts", "Human Herpesvirus 6", "host cell", "pbmc", "dna", "Cellular Degradation CD 46", "host cell chaperone protein GP 96", "GP 96 expression", "HHV"], "article_id"=>1258573, "categories"=>["Biological Sciences"], "users"=>["Bhupesh K. Prusty", "Christine Siegl", "Nitish Gulve", "Yasuko Mori", "Thomas Rudel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113962.g006", "stats"=>{"downloads"=>2, "page_views"=>37, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_of_CD46_with_GP96_during_HHV_6A_infection_/1258573", "title"=>"Association of CD46 with GP96 during HHV-6A infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-03 03:03:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1817369"], "description"=>"<p>(<b>A</b>) Cell surface expression of GP96 increases in response to HHV-6 infection. HeLa and HSB-2 cells were infected with HHV-6A for one hour and analyzed by confocal laser microscopy. Draq5 staining was used to visualize nuclei. (<b>B</b>) GP96 expression is induced immediately after HHV-6A infection. HeLa cells carrying stable knock down of GP96 (HeLa.shGP96) were infected with HHV-6A for one hour. Non-infected cells served as control. Cell surface expression of GP96 was studied in non-permeabilized cells by immunofluorescence using a primary antibody against C-terminal end of GP96 and a Cy-3 conjugated secondary antibody. Total GP96 expression was studied in permeabilized cells. The scale bar represents 10 u˜ (<b>C</b>) Increase in total GP96 expression during HHV-6A infection. HeLa cells as well as HeLa.shGP96 cells were infected with HHV-6A for 48 h. Total GP96 expression was analyzed by Western blotting. Actin served as loading control. (<b>D</b>) Decrease in cell surface GP96 expression decreases HHV-6 binding and its subsequent entry. HeLa cells wildtype and GP96 knockdown cell lines (HeLa.shGP96 clone K1 and K2) were infected with HHV-6A to study viral binding and entry. Cells trypsinized to remove bound viral particles served as control. Cells were processed as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0113962#s2\" target=\"_blank\">Materials and Methods</a> and viral DNA was quantified by qPCR. Data represent the mean ± SEM of three independent experiments. *, p≤0.05 and **, p≤0.005. Statistical analysis was based on the Student t-test.</p>", "links"=>[], "tags"=>["host cell proteins", "GP 96", "GP 96 Interacts", "Human Herpesvirus 6", "host cell", "pbmc", "dna", "Cellular Degradation CD 46", "host cell chaperone protein GP 96", "GP 96 expression", "HHV"], "article_id"=>1258555, "categories"=>["Biological Sciences"], "users"=>["Bhupesh K. Prusty", "Christine Siegl", "Nitish Gulve", "Yasuko Mori", "Thomas Rudel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113962.g002", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GP96_interacts_with_HHV_6_/1258555", "title"=>"GP96 interacts with HHV-6.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-03 03:03:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1817423", "https://ndownloader.figshare.com/files/1817424", "https://ndownloader.figshare.com/files/1817426", "https://ndownloader.figshare.com/files/1817427", "https://ndownloader.figshare.com/files/1817428", "https://ndownloader.figshare.com/files/1817429"], "description"=>"<div><p>CD46 and CD134 mediate attachment of Human Herpesvirus 6A (HHV-6A) and HHV-6B to host cell, respectively. But many cell types interfere with viral infection through rapid degradation of viral DNA. Hence, not all cells expressing these receptors are permissive to HHV-6 DNA replication and production of infective virions suggesting the involvement of additional factors that influence HHV-6 propagation. Here, we used a proteomics approach to identify other host cell proteins necessary for HHV-6 binding and entry. We found host cell chaperone protein GP96 to interact with HHV-6A and HHV-6B and to interfere with virus propagation within the host cell. In human peripheral blood mononuclear cells (PBMCs), GP96 is transported to the cell surface upon infection with HHV-6 and interacts with HHV-6A and -6B through its C-terminal end. Suppression of GP96 expression decreased initial viral binding but increased viral DNA replication. Transient expression of human GP96 allowed HHV-6 entry into CHO-K1 cells even in the absence of CD46. Thus, our results suggest an important role for GP96 during HHV-6 infection, which possibly supports the cellular degradation of the virus.</p></div>", "links"=>[], "tags"=>["host cell proteins", "GP 96", "GP 96 Interacts", "Human Herpesvirus 6", "host cell", "pbmc", "dna", "Cellular Degradation CD 46", "host cell chaperone protein GP 96", "GP 96 expression", "HHV"], "article_id"=>1258604, "categories"=>["Biological Sciences"], "users"=>["Bhupesh K. Prusty", "Christine Siegl", "Nitish Gulve", "Yasuko Mori", "Thomas Rudel"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0113962.s001", "https://dx.doi.org/10.1371/journal.pone.0113962.s002", "https://dx.doi.org/10.1371/journal.pone.0113962.s003", "https://dx.doi.org/10.1371/journal.pone.0113962.s004", "https://dx.doi.org/10.1371/journal.pone.0113962.s005", "https://dx.doi.org/10.1371/journal.pone.0113962.s006"], "stats"=>{"downloads"=>1, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GP96_Interacts_with_HHV_6_during_Viral_Entry_and_Directs_It_for_Cellular_Degradation_/1258604", "title"=>"GP96 Interacts with HHV-6 during Viral Entry and Directs It for Cellular Degradation", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-12-03 03:03:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1817377"], "description"=>"<p>Cell surface expression dynamics of GP96 and CD46 in response to HHV-6A infection was determined in (<b>A</b>) HeLa and (<b>B</b>) HSB-2 cells. Cells were infected with HHV-6A for indicated time points and cell surface expression of CD46 and GP96 was performed by flow cytometry (solid profiles); background fluorescence levels were measured using an isotype specific antibody (empty profiles). Mean fluorescence intensity (MFI) for each analysis is indicated below the respective figure.</p>", "links"=>[], "tags"=>["host cell proteins", "GP 96", "GP 96 Interacts", "Human Herpesvirus 6", "host cell", "pbmc", "dna", "Cellular Degradation CD 46", "host cell chaperone protein GP 96", "GP 96 expression", "HHV"], "article_id"=>1258563, "categories"=>["Biological Sciences"], "users"=>["Bhupesh K. Prusty", "Christine Siegl", "Nitish Gulve", "Yasuko Mori", "Thomas Rudel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113962.g005", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cell_surface_expression_of_GP96_is_modulated_during_HHV_6_infection_/1258563", "title"=>"Cell surface expression of GP96 is modulated during HHV-6 infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-03 03:03:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1817370"], "description"=>"<p>(<b>A</b>) Decrease in cell surface GP96 expression decreases HHV-6 entry but increases subsequent replication of viral DNA. HeLa cells were transfected with siRNA against human GP96. In parallel, cells were transfected with siRNA against the luciferase gene (siLUC) as a control. Blank transfected as well as siGP96 and siLUC transfected cells were washed thoroughly and infected with HHV-6A for 2 hrs. After 2 hrs of viral infection, cells were washed with trypsin and extensive washing with PBS to remove any bound but non-entered HHV-6 particles. Cells were then incubated for different time intervals in the absence of viral particle in the culture media and subsequently processed for quantification of viral DNA amount by qPCR. (<b>B</b>) The experiment described under (A) was performed in HSB-2 cells. (<b>C</b>) HHV-6A entry decreases in absence of GP96. HeLa cells carrying lentivirus-mediated stable knock down of GP96 (HeLa.shGP96) and vector control (HeLa.EV) were infected with HHV-6A. In parallel, HeLa.shGP96 cells were transiently transfected with a construct expressing human GP96 (rGP96) for 24 h and were also infected with HHV-6A. Cells were processed as mentioned above and amount of viral DNA in these cells was measured by qPCR. (<b>D</b>) Increase in viral DNA replication in the absence of GP96 requires host cell translation. HeLa.shGP96 cells were infected with HHV-6A in presence or absence of cycloheximide (CHX) and subsequently analyzed by qPCR. Data represent the mean ± SEM of three independent experiments. **, p≤0.005. Statistical analysis was based on the Student t-test. (<b>E</b>) Viral gene expression is increased in the absence of GP96. HeLa and HeLa.shGP96 cells were infected with HHV-6A for different time intervals in the presence or absence of CHX. Western blotting was carried out to detect HHV-6 early antigen p41. Actin served as loading control. 41 kDa bands specific for HHV-6 p41 is marked with arrow. HHV-6A infected HSB-2 cell lysate was used as a positive control (PC).</p>", "links"=>[], "tags"=>["host cell proteins", "GP 96", "GP 96 Interacts", "Human Herpesvirus 6", "host cell", "pbmc", "dna", "Cellular Degradation CD 46", "host cell chaperone protein GP 96", "GP 96 expression", "HHV"], "article_id"=>1258557, "categories"=>["Biological Sciences"], "users"=>["Bhupesh K. Prusty", "Christine Siegl", "Nitish Gulve", "Yasuko Mori", "Thomas Rudel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113962.g003", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Absence_of_GP96_induces_viral_replication_/1258557", "title"=>"Absence of GP96 induces viral replication.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-03 03:03:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1817390"], "description"=>"<p>Host proteins differentially immunoprecipitated with both HHV-6A and HHV-6B.</p>", "links"=>[], "tags"=>["host cell proteins", "GP 96", "GP 96 Interacts", "Human Herpesvirus 6", "host cell", "pbmc", "dna", "Cellular Degradation CD 46", "host cell chaperone protein GP 96", "GP 96 expression", "HHV"], "article_id"=>1258574, "categories"=>["Biological Sciences"], "users"=>["Bhupesh K. Prusty", "Christine Siegl", "Nitish Gulve", "Yasuko Mori", "Thomas Rudel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113962.t001", "stats"=>{"downloads"=>4, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Host_proteins_differentially_immunoprecipitated_with_both_HHV_6A_and_HHV_6B_/1258574", "title"=>"Host proteins differentially immunoprecipitated with both HHV-6A and HHV-6B.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-12-03 03:03:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1817351"], "description"=>"<p>(<b>A</b>) Diagrammatic representation of immunoprecipitation (IP) experiment to detect unknown HHV-6-interacting host cell proteins. (<b>B</b>) Protein complexes directly interacting with HHV-6 viral particles were isolated by IP using anti-HHV-6 gB antibody, separated by SDS-PAGE and visualized by silver staining. Molecular weight markers are indicated on the left. Arrowheads point to some of the proteins differentially identified by mass spectrometry. Lane 1, 5 and 8 shows pre-stained protein ladders. (<b>C</b>) IP and Western blotting were carried out to validate and characterize the interaction between GP96 and HHV-6 envelope glycoproteins. As negative control no antibody (Ab), no HHV-6, no HeLa lysate were used for IP. An antibody against human Glucose-6-P dehydrogenase (G6PD) in the absence of viral particles was also used as a control. The Western blot of the IP samples was probed for human GP96 and subsequently with G6PD. Anti-HHV-6 gB and anti-HHV-6 gH antibodies were used for IP. (<b>D</b>) Lysates of HSB-2 cells infected with HHV-6A were used for IP, followed by Western blotting (WB) to detect interaction between GP96 and HHV-6 glycoprotein complexes. The blot was probed with GP96, gQ1, gM and gB antibodies. IgG heavy and light chains are marked at appropriate places.</p>", "links"=>[], "tags"=>["host cell proteins", "GP 96", "GP 96 Interacts", "Human Herpesvirus 6", "host cell", "pbmc", "dna", "Cellular Degradation CD 46", "host cell chaperone protein GP 96", "GP 96 expression", "HHV"], "article_id"=>1258547, "categories"=>["Biological Sciences"], "users"=>["Bhupesh K. Prusty", "Christine Siegl", "Nitish Gulve", "Yasuko Mori", "Thomas Rudel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113962.g001", "stats"=>{"downloads"=>0, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_HHV_6_interacting_host_cell_proteins_/1258547", "title"=>"Identification of HHV-6-interacting host cell proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-03 03:03:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1817373"], "description"=>"<p>(<b>A</b>) Antibodies raised against the C-terminal end of GP96 prevent HHV-6A binding. HeLa cells were incubated with different antibodies for 30 min (used at 50 µg/ml) and then exposed to HHV-6 at the MOI of 1. After 1 h at 37°C, the cells were washed extensively and total DNA was extracted. The amount of viral particles bound to HeLa cells was measured by qPCR. Data represent the mean ± SEM of three independent experiments. *, p≤0.05. Statistical analysis was based on the Student t-test. (<b>B</b>) Similar experiments were performed in fresh PBMCs. Fresh PBMCs were isolated and stimulated with PHA for 2 days prior to the experiments. C-GP96, antibody raised against C-terminal of GP96; N-GP96, antibody raised against N-terminal of GP96. (<b>C</b>) Knock down of GP96 abolishes HHV-6 entry into CHO-K1 cells. CHO-K1 cells were transfected with siRNA against GP96 (siGP96). In parallel, cells were transfected with scrambled siRNAs (siControl) as a control. Blank transfected (CHO.blank) as well as siGP96 and siControl transfected cells were washed thoroughly and added with HHV-6A for 2 hrs after which cells were washed with trypsin for 3–5 minutes at 37°C followed by extensive washing with PBS to remove any unbound HHV-6 particles. Cells were then incubated for another 24 hrs in the absence of viral particle in the culture media and subsequently processed for quantification of viral DNA amount by qPCR. (<b>D</b>) Transient over-expression of human GP96 in CHO-K1 cells induces HHV-6 entry. CHO-K1 cells were transfected with a construct expressing human GP96 (hGp96). Empty vectors were transfected in parallel and were used as control. 48 h after transfection, cells were washed thoroughly and were infected with HHV-6A and -6B at an MOI of 10 for 2 h. A parallel set of infected cells was trypsinized to remove unbound viral DNA just before DNA extraction. Cells were washed extensively and total DNA was extracted. Viral DNA amount was quantified by qPCR. (<b>E</b>) Transient over-expression of human GP96 in CHO-K1 cells decreases HHV-6 survival. CHO-K1 cells were transfected with a construct expressing human GP96 (hGp96). Empty vectors were transfected in parallel and were used as control. 48 h after transfection, cells were washed thoroughly and were infected with HHV-6A and -6B at an MOI of 10 for 2 hrs and were processed as mentioned above. Viral DNA amount was quantified by qPCR.</p>", "links"=>[], "tags"=>["host cell proteins", "GP 96", "GP 96 Interacts", "Human Herpesvirus 6", "host cell", "pbmc", "dna", "Cellular Degradation CD 46", "host cell chaperone protein GP 96", "GP 96 expression", "HHV"], "article_id"=>1258559, "categories"=>["Biological Sciences"], "users"=>["Bhupesh K. Prusty", "Christine Siegl", "Nitish Gulve", "Yasuko Mori", "Thomas Rudel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113962.g004", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HHV_6_interacts_with_GP96_/1258559", "title"=>"HHV-6 interacts with GP96.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-03 03:03:56"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"15", "full-text"=>"24", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"7", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"18", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}

Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Biochemistry", "average_usage"=>[282]}, {"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[286]}, {"subject_area"=>"/Biology and life sciences/Physiology", "average_usage"=>[280]}, {"subject_area"=>"/Medicine and health sciences/Immunology", "average_usage"=>[289]}]}
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