HSV-2 Specifically Down Regulates HLA-C Expression to Render HSV-2-Infected DCs Susceptible to NK Cell Killing
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{"title"=>"HSV-2 Specifically Down Regulates HLA-C Expression to Render HSV-2-Infected DCs Susceptible to NK Cell Killing", "type"=>"journal", "authors"=>[{"first_name"=>"Moran", "last_name"=>"Elboim", "scopus_author_id"=>"13005419000"}, {"first_name"=>"Inna", "last_name"=>"Grodzovski", "scopus_author_id"=>"8730209900"}, {"first_name"=>"Esther", "last_name"=>"Djian", "scopus_author_id"=>"36805629900"}, {"first_name"=>"Dana G.", "last_name"=>"Wolf", "scopus_author_id"=>"7402650512"}, {"first_name"=>"Ofer", "last_name"=>"Mandelboim", "scopus_author_id"=>"7003391581"}], "year"=>2013, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "pui"=>"368694501", "sgr"=>"84875996982", "doi"=>"10.1371/journal.ppat.1003226", "scopus"=>"2-s2.0-84875996982", "pmid"=>"23555244"}, "id"=>"b3016f5e-d92c-35d3-88dd-cb122bfa909b", "abstract"=>"Both NK cells and CTLs kill virus-infected and tumor cells. However, the ways by which these killer cells recognize the infected or the tumorigenic cells are different, in fact almost opposite. CTLs are activated through the interaction of the TCR with MHC class I proteins. In contrast, NK cells are inhibited by MHC class I molecules. The inhibitory NK receptors recognize mainly MHC class I proteins and in this regard practically all of the HLA-C proteins are recognized by inhibitory NK cell receptors, while only certain HLA-A and HLA-B proteins interact with these receptors. Sophisticated viruses developed mechanisms to avoid the attack of both NK cells and CTLs through, for example, down regulation of HLA-A and HLA-B molecules to avoid CTL recognition, leaving HLA-C proteins on the cell surface to inhibit NK cell response. Here we provide the first example of a virus that through specific down regulation of HLA-C, harness the NK cells for its own benefit. We initially demonstrated that none of the tested HSV-2 derived microRNAs affect NK cell activity. Then we show that surprisingly upon HSV-2 infection, HLA-C proteins are specifically down regulated, rendering the infected cells susceptible to NK cell attack. We identified a motif in the tail of HLA-C that is responsible for the HSV-2-meduiated HLA-C down regulation and we show that the HLA-C down regulation is mediated by the viral protein ICP47. Finally we show that HLA-C proteins are down regulated from the surface of HSV-2 infected dendritic cells (DCs) and that this leads to the killing of DC by NK cells. Thus, we propose that HSV-2 had developed this unique and surprising NK cell-mediated killing strategy of infected DC to prevent the activation of the adaptive immunity.", "link"=>"http://www.mendeley.com/research/hsv2-specifically-down-regulates-hlac-expression-render-hsv2infected-dcs-susceptible-nk-cell-killing", "reader_count"=>30, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>2, "Researcher"=>6, "Student > Ph. D. Student"=>8, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>2, "Researcher"=>6, "Student > Ph. D. Student"=>8, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>3, "Agricultural and Biological Sciences"=>17, "Medicine and Dentistry"=>3, "Veterinary Science and Veterinary Medicine"=>1, "Immunology and Microbiology"=>5}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>17}, "Unspecified"=>{"Unspecified"=>3}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Iran"=>1, "United States"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1001034"], "description"=>"<p>(A) DCs were infected with HSV-2 (MOI of 0.5), staining was performed 8 and 18 hours post infection (pi). The levels of HLA expression were determined by FACS (blue histograms, represent infected cells, red histograms represent uninfected cells). Top histograms: binding of KIR2DLI-Ig, middle histograms: binding of KIR2DL2-Ig, lower histograms; binding of the pan anti-MHC-I W6/32 antibody. Background levels (black empty histogram) are the APC-conjugated Abs. (B) Uninfected and HSV-2 infected DCs were incubated for 2 hours with primary bulk NK cells, 8 or for 18 hours post infection. NK cells were identified by staining for the expression of CD56 and the levels of NK cell degranulation was monitored by anti CD107a mAb. The percentages of NK cell degranulation are indicated. The staining was quantified by FACS. Figure show one representative experiment out of two performed.</p>", "links"=>[], "tags"=>["dcs", "hsv-2", "leads", "hla-c", "nk"], "article_id"=>662528, "categories"=>["Infectious Diseases", "Immunology"], "users"=>["Moran Elboim", "Inna Grodzovski", "Esther Djian", "Dana G. Wolf", "Ofer Mandelboim"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003226.g010", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Infection_of_DCs_by_HSV_2_leads_to_HLA_C_down_regulation_and_consequently_enhance_NK_cell_killing_/662528", "title"=>"Infection of DCs by HSV-2 leads to HLA-C down regulation and consequently enhance NK cell killing.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-29 14:04:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/1001013"], "description"=>"<p>Various human cell lines indicated in the table were transduced with lentiviruses expressing GFP together with various HSV-2 miRNAs or with control miRNA. Expression levels of MHC-I, MICA, MICB, ULBP1, ULBP2, ULBP3, PVR and ICAM1 were assessed by FACS. The figure displays the human cell lines that were transduced with each of the 21 miRNAs of HSV-2. Plus indicate that the cell line was tranduced with the indicated miRNA and tested for expression of the indicated NK ligands.</p>", "links"=>[], "tags"=>["nk", "ligands", "downregulated", "hsv-2"], "article_id"=>662507, "categories"=>["Infectious Diseases", "Immunology"], "users"=>["Moran Elboim", "Inna Grodzovski", "Esther Djian", "Dana G. Wolf", "Ofer Mandelboim"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003226.g001", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Various_NK_cell_ligands_are_not_downregulated_by_HSV_2_miRNA_/662507", "title"=>"Various NK cell ligands are not downregulated by HSV-2 miRNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-29 13:57:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1001016"], "description"=>"<p>RKO cells were transduced with lentiviruses expressing GFP together with either HSV-2 miRNAs (black empty histogram, the miRNA are indicated on the top of the histograms) or with control miRNA (dark gray shaded histogram). Expression levels of MHC-I, MICB, ULBP2, ULBP3, PVR and ICAM1 were assessed by FACS using specific antibodies. Background levels (light grey shaded histogram) are the APC-conjugated Abs. The figure show one representative experiment out of three performed.</p>", "links"=>[], "tags"=>["examples", "ligands", "nk", "receptors", "downregulated", "hsv-2"], "article_id"=>662510, "categories"=>["Infectious Diseases", "Immunology"], "users"=>["Moran Elboim", "Inna Grodzovski", "Esther Djian", "Dana G. Wolf", "Ofer Mandelboim"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003226.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Selected_examples_of_ligands_for_NK_cell_receptors_that_are_not_downregulated_by_HSV_2_miRNA_/662510", "title"=>"Selected examples of ligands for NK cell receptors that are not downregulated by HSV-2 miRNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-29 13:57:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1001019"], "description"=>"<p>HFF cells, either uninfected, infected with HSV-2 (MOI of 0.5) or infected with UV-inactivated HSV-2 (MOI of 0.5) were radioactively labeled and incubated with primary bulk NK cell cultures for 5 hours at the indicated effector to target ratios (E:T). The killing assays were performed 48 hours post infection. Shown are mean values ± SD. Statistically significant differences are indicated (<sub>*</sub> p≤0.05, <sub>**</sub> p≤0.005, by one-tailed t test). Error bars (SD) are derived from triplicates. One representative experiment is shown out of three performed.</p>", "links"=>[], "tags"=>["nk", "hsv-2", "infected", "hff"], "article_id"=>662513, "categories"=>["Infectious Diseases", "Immunology"], "users"=>["Moran Elboim", "Inna Grodzovski", "Esther Djian", "Dana G. Wolf", "Ofer Mandelboim"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003226.g003", "stats"=>{"downloads"=>1, "page_views"=>51, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_NK_cell_killing_of_HSV_2_infected_HFF_cells_/662513", "title"=>"Increased NK cell killing of HSV-2 infected HFF cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-29 13:59:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/1001020"], "description"=>"<p>Time course for the expression of various NK cell ligands following HSV-2 infection of HeLa cells (MOI of 0.1). The expression levels of NK cells ligands (indicated on top of the histograms) were determined by staining with specific antibodies. Expression following infection is indicated by the black empty histograms. The dark gray shaded histograms represent staining of the corresponding uninfected cells. Background levels (light grey shaded histogram) are the secondary FITC-conjugated Abs staining. One representative experiment is shown out of three performed.</p>", "links"=>[], "tags"=>["downregulates", "mhc-i"], "article_id"=>662514, "categories"=>["Infectious Diseases", "Immunology"], "users"=>["Moran Elboim", "Inna Grodzovski", "Esther Djian", "Dana G. Wolf", "Ofer Mandelboim"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003226.g004", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HSV_2_specifically_downregulates_MHC_I_expression_/662514", "title"=>"HSV-2 specifically downregulates MHC-I expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-29 13:59:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/1001022"], "description"=>"<p>(A) 721.221 (221) cells expressing various HLA proteins (indicated in the histograms) were infected with HSV-2 (MOI of 0.5) and the levels of the various HLA proteins expression were determined by FACS (black empty histograms represents the staining of infected cells). (B) Two clinical isolates of HSV-2 (HSV2 Iso 2 and HSV2 Iso 3) and one clinical isolate of HSV-1 were used to infect the various 721.221 transfectants indicated in the figures (MOI of 0.5 for all infections) and the levels of the HLA expression were measured FACS (black empty histograms represent the infected cell staining). (C) 221 expressing HLA-B73 or HLA-Cw6 cells were infected with HSV-2 (MOI of 1) and HLA expression was assessed right at the end of the infection, and at the indicated time points post infection (pi). In A–C the dark gray shaded histograms represent staining of the corresponding uninfected cells and the background levels (light grey shaded histogram) are the APC-conjugated Abs. For all panels, one representative experiment is shown out of at least three performed. (D) Quantification of all experiments performed in (A). The expression of each HLA allele without infection was set up to be 100%. Shown are relative average MFI ± S.D. from four to eight independent experiments.</p>", "links"=>[], "tags"=>["regulates", "hla-c"], "article_id"=>662516, "categories"=>["Infectious Diseases", "Immunology"], "users"=>["Moran Elboim", "Inna Grodzovski", "Esther Djian", "Dana G. Wolf", "Ofer Mandelboim"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003226.g005", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HSV_2_specifically_down_regulates_HLA_C_expression_/662516", "title"=>"HSV-2 specifically down regulates HLA-C expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-29 14:00:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1001025"], "description"=>"<p>(A) Top histograms: 221 cells expressing either HLA-B8 or HLA-Cw6 were infected with HSV-2 (MOI of 0.5). The levels of HLAs expression were determined by FACS (black empty histograms represent infected cells). The dark gray shaded histograms represent staining of the corresponding uninfected cells. Background levels (light grey shaded histogram) are the APC-conjugated Abs. Lower histogram: Expression of KIR2DL1 (black empty histograms) was detected with anti-KIR2DL1 antibody. Background levels (grey shaded histogram) are the APC-conjugated Abs. (B) Killing assay. 221 and 221 expressing either HLA-B8 or HLA-Cw6 were infected with HSV-2 (MOI of 0.5). Uninfected and infected (indicated in the figure as HSV2) 221 cells were radioactively labeled and incubated with primary KIR2DL1-positive NK clones for 5 hours at an E:T ratio of 10∶1. The killing assays were performed 48 hours post infection and the NK clone was incubated either with a control mAb (Ctrl, grey columns) or with an anti-KIR2DL1 blocking antibody (white columns). Shown are mean values ± SD. Statistically significant differences are indicated (<sub>*</sub> p≤0.0005, by one-tailed t test). Error bars (SD) are derived from triplicates. For all panels, one representative experiment is shown out of at least three performed.</p>", "links"=>[], "tags"=>["kir2dl1-mediated", "inhibition", "abolished", "hsv-2", "infected"], "article_id"=>662519, "categories"=>["Infectious Diseases", "Immunology"], "users"=>["Moran Elboim", "Inna Grodzovski", "Esther Djian", "Dana G. Wolf", "Ofer Mandelboim"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003226.g006", "stats"=>{"downloads"=>0, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_KIR2DL1_mediated_inhibition_is_abolished_in_HSV_2_infected_cells_/662519", "title"=>"The KIR2DL1-mediated inhibition is abolished in HSV-2 infected cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-29 14:01:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/1001028"], "description"=>"<p>221 cells expressing HLA-Cw4, HLA-Cw6, HLA-Cw4 with the cytoplasmic tail of HLA-A2 and HLA-Cw6 with the cytoplasmic tail of HLA-G (indicated above the histograms) were infected with HSV-2 (MOI of 0.5). The levels of the various HLAs were determined by FACS (black empty histograms represents the staining of the infected cells). The dark gray shaded histograms represent staining of the corresponding uninfected cells. Background levels (light grey shaded histogram) are the APC-conjugated Abs. Figure show one representative experiment out of four performed.</p>", "links"=>[], "tags"=>["targets", "cytoplasmic"], "article_id"=>662522, "categories"=>["Infectious Diseases", "Immunology"], "users"=>["Moran Elboim", "Inna Grodzovski", "Esther Djian", "Dana G. Wolf", "Ofer Mandelboim"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003226.g007", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HSV_2_targets_the_cytoplasmic_tail_of_HLA_C_/662522", "title"=>"HSV-2 targets the cytoplasmic tail of HLA-C.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-29 14:02:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/1001030"], "description"=>"<p>(A) Schematic representation of the cytoplasmic tails of various HLAs. Highlighted in red are the amino acid that are different between HLA-C and other HLA proteins. (B) The various 221 cells (expressing either wild type or mutants HLA proteins, indicated on top of the histograms) were infected with HSV-2 (MOI of 0.5). The levels of the various HLAs was determined by FACS (black empty histograms represent the infected cell staining). The dark gray shaded histograms represent staining of the corresponding uninfected cells. Background levels (light grey shaded histogram) are the APC-conjugated Abs. Figure show one representative experiment out of 3 performed.</p>", "links"=>[], "tags"=>["downregulation", "hla-cw6", "hsv-2", "glutamic", "residue"], "article_id"=>662524, "categories"=>["Infectious Diseases", "Immunology"], "users"=>["Moran Elboim", "Inna Grodzovski", "Esther Djian", "Dana G. Wolf", "Ofer Mandelboim"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003226.g008", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_downregulation_of_HLA_Cw6_by_HSV_2_is_dependent_on_the_glutamic_acid_residue_located_in_position_334_/662524", "title"=>"The downregulation of HLA-Cw6 by HSV-2 is dependent on the glutamic acid residue located in position 334.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-29 14:02:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1001032"], "description"=>"<p>Various 221 cells expressing wild type (A) and mutants (B) HLA proteins (indicated in the figure) were transduced with lenti virus vectors expressing ICP47 and GFP (indicative for the transfection efficiency). The levels of the various HLAs were determined by FACS (black empty histograms represent the ICP47 transduced cells). The dark gray shaded histograms represent staining of the corresponding cells transduced with a control lenti virus vector. Background levels (light grey shaded histogram) are the APC-conjugated Abs. Figure show one representative experiment out of 3 performed.</p>", "links"=>[], "tags"=>["icp47", "hsv-2", "hla-c"], "article_id"=>662526, "categories"=>["Infectious Diseases", "Immunology"], "users"=>["Moran Elboim", "Inna Grodzovski", "Esther Djian", "Dana G. Wolf", "Ofer Mandelboim"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003226.g009", "stats"=>{"downloads"=>1, "page_views"=>45, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_ICP47_protein_of_HSV_2_reduces_HLA_C_expression_/662526", "title"=>"The ICP47 protein of HSV-2 reduces HLA-C expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-29 14:03:10"}

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Relative Metric

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