Prostate Tumor-Derived Exosomes Down-Regulate NKG2D Expression on Natural Killer Cells and CD8+ T Cells: Mechanism of Immune Evasion
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{"title"=>"Prostate tumor-derived exosomes down-regulate NKG2D expression on natural killer cells and CD8+ T cells: Mechanism of immune evasion", "type"=>"journal", "authors"=>[{"first_name"=>"Marie", "last_name"=>"Lundholm", "scopus_author_id"=>"8297345300"}, {"first_name"=>"Mona", "last_name"=>"Schröder", "scopus_author_id"=>"56699449800"}, {"first_name"=>"Olga", "last_name"=>"Nagaeva", "scopus_author_id"=>"6506301541"}, {"first_name"=>"Vladimir", "last_name"=>"Baranov", "scopus_author_id"=>"35482968700"}, {"first_name"=>"Anders", "last_name"=>"Widmark", "scopus_author_id"=>"7003716653"}, {"first_name"=>"Lucia", "last_name"=>"Mincheva-Nilsson", "scopus_author_id"=>"6603789517"}, {"first_name"=>"Pernilla", "last_name"=>"Wikström", "scopus_author_id"=>"7005154258"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"25268476", "issn"=>"19326203", "sgr"=>"84931033158", "pui"=>"600079827", "scopus"=>"2-s2.0-84931033158", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "doi"=>"10.1371/journal.pone.0108925"}, "id"=>"0292764c-20f1-31a6-a941-5fb9e2ae7557", "abstract"=>"Tumor-derived exosomes, which are nanometer-sized extracellular vesicles of endosomal origin, have emerged as promoters of tumor immune evasion but their role in prostate cancer (PC) progression is poorly understood. In this study, we investigated the ability of prostate tumor-derived exosomes to downregulate NKG2D expression on natural killer (NK) and CD8+ T cells. NKG2D is an activating cytotoxicity receptor whose aberrant loss in cancer plays an important role in immune suppression. Using flow cytometry, we found that exosomes produced by human PC cells express ligands for NKG2D on their surface. The NKG2D ligand-expressing prostate tumor-derived exosomes selectively induced downregulation of NKG2D on NK and CD8+ T cells in a dose-dependent manner, leading to impaired cytotoxic function in vitro. Consistent with these findings, patients with castration-resistant PC (CRPC) showed a significant decrease in surface NKG2D expression on circulating NK and CD8+ T cells compared to healthy individuals. Tumor-derived exosomes are likely involved in this NKG2D downregulation, since incubation of healthy lymphocytes with exosomes isolated from serum or plasma of CRPC patients triggered downregulation of NKG2D expression in effector lymphocytes. These data suggest prostate tumor-derived exosomes as down-regulators of the NKG2D-mediated cytotoxic response in PC patients, thus promoting immune suppression and tumor escape.", "link"=>"http://www.mendeley.com/research/prostate-tumorderived-exosomes-downregulate-nkg2d-expression-natural-killer-cells-cd8-t-cells-mechan", "reader_count"=>75, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>14, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>3, "Student > Master"=>13, "Other"=>2, "Student > Bachelor"=>13, "Lecturer > Senior Lecturer"=>1, "Professor"=>2, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>14, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>3, "Student > Master"=>13, "Other"=>2, "Student > Bachelor"=>13, "Lecturer > Senior Lecturer"=>1, "Professor"=>2, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>3, "Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>18, "Agricultural and Biological Sciences"=>28, "Medicine and Dentistry"=>21, "Physics and Astronomy"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>21}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>28}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>18}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Denmark"=>1, "Mexico"=>1, "United Kingdom"=>1, "France"=>1, "Chile"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1697649"], "description"=>"<p>Human prostate tumor cell lines LNCaP, PC3, and 22Rv1 were stained with monoclonal antibodies (mAbs) specific for NKG2D ligands (ULBP-1, ULBP-2, and MICA/B) and analyzed by flow cytometry. Histograms show the mean fluorescence intensity (MFI) and the shaded histogram represents negative controls in which isotype-matched antibodies were used.</p>", "links"=>[], "tags"=>["NKG 2D", "surface NKG 2D expression", "NKG 2D cytotoxic response", "pc", "downregulate NKG 2D expression", "NKG 2D downregulation", "Natural Killer Cells", "exosome", "crpc", "NKG 2D expression", "prostate"], "article_id"=>1187759, "categories"=>["Biological Sciences"], "users"=>["Marie Lundholm", "Mona Schröder", "Olga Nagaeva", "Vladimir Baranov", "Anders Widmark", "Lucia Mincheva-Nilsson", "Pernilla Wikström"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0108925.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_NKG2D_ligands_in_prostate_cancer_cells_/1187759", "title"=>"Expression of NKG2D ligands in prostate cancer cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-30 03:28:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1697651"], "description"=>"<p>(A) Western blot analyses of CD63, TSG101, GRP78 and PSMA in whole cell lysates of the 22Rv1 cell line or isolated exosomes from supernatants from this cell line. (B) Representative electron microscopic image of 22Rv1 exosomes, showing the typical cup-shaped morphology. Scale bar represents 100 nm. (C) Flow cytometry of 22Rv1 exosomes captured by CD63-coated latex microbeads and stained with mAbs to NKG2D ligands (ULBP-1, ULBP-2, and MICA/B). The histogram shows the mean fluorescence intensity (MFI) and the shaded histogram represents negative controls in which isotype-matched antibodies were used. (D) Representative western blot analysis of CD63, GRP78, and PSMA in exosomes isolated from serum of PC patients. (E) The total amount of exosomal protein per 10 ml of human fresh plasma or serum from healthy donors (n = 6–8 in each group) and CRPC patients (n = 17–18 in each group) was determined by BCA protein assay. ** <i>P</i><0.01.</p>", "links"=>[], "tags"=>["NKG 2D", "surface NKG 2D expression", "NKG 2D cytotoxic response", "pc", "downregulate NKG 2D expression", "NKG 2D downregulation", "Natural Killer Cells", "exosome", "crpc", "NKG 2D expression", "prostate"], "article_id"=>1187761, "categories"=>["Biological Sciences"], "users"=>["Marie Lundholm", "Mona Schröder", "Olga Nagaeva", "Vladimir Baranov", "Anders Widmark", "Lucia Mincheva-Nilsson", "Pernilla Wikström"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0108925.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characterization_of_prostate_exosomes_/1187761", "title"=>"Characterization of prostate exosomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-30 03:28:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1697653"], "description"=>"<p>Purified 22Rv1 tumor exosomes or control fibroblast (WPMY1) exosomes were incubated for 24 h with healthy PMBCs, and flow cytometry was performed to determine the surface expression of NKG2D. (A) Representative dot-plots of flow cytometry gating scheme used to analyze NKG2D expression. (B) The bar graphs show the proportion of NKG2D-positive CD8<sup>+</sup> T cells and NK cells relative to untreated cells (normalized to a value of 100). (C) The line graphs show the proportion of NKG2D-positive cells relative to untreated cells (normalized to a value of 100) when 22Rv1 exosomes were added at doses of 2–20 µg. (D) The percentage inhibition of NKG2D expression on CD8<sup>+</sup> T cells and NK cells when 22Rv1 exosomes were treated with a mixture of anti-ULBP1-5 and MIC mAbs or anti-CD63 mAb. The graphs show mean ± SE (n = 8) from 2 independent experiments. * <i>P</i><0.05; ** <i>P</i><0.01.</p>", "links"=>[], "tags"=>["NKG 2D", "surface NKG 2D expression", "NKG 2D cytotoxic response", "pc", "downregulate NKG 2D expression", "NKG 2D downregulation", "Natural Killer Cells", "exosome", "crpc", "NKG 2D expression", "prostate"], "article_id"=>1187763, "categories"=>["Biological Sciences"], "users"=>["Marie Lundholm", "Mona Schröder", "Olga Nagaeva", "Vladimir Baranov", "Anders Widmark", "Lucia Mincheva-Nilsson", "Pernilla Wikström"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0108925.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_22Rv1_tumor_exosomes_downregulate_cell_surface_NKG2D_expression_on_NK_cells_and_CD8_T_cells_/1187763", "title"=>"22Rv1 tumor exosomes downregulate cell-surface NKG2D expression on NK cells and CD8<sup>+</sup> T cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-30 03:28:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1697654"], "description"=>"<p>K562 target cells were incubated with PBMCs (effector cells), that were untreated, or treated with 22Rv1 exosomes, anti-NKG2D receptor-blocking mAb, or NKG2D-ligand blocked 22Rv1 exosomes. Additionally, target cells were blocked with a mixture of anti-ULBP1–5 and anti-MIC mAbs and the effect of 22Rv1 supernatant depleted from exosomes was also tested. The data represent mean values of 3 independent experiments ± SD. *<i>P</i><0.05.</p>", "links"=>[], "tags"=>["NKG 2D", "surface NKG 2D expression", "NKG 2D cytotoxic response", "pc", "downregulate NKG 2D expression", "NKG 2D downregulation", "Natural Killer Cells", "exosome", "crpc", "NKG 2D expression", "prostate"], "article_id"=>1187764, "categories"=>["Biological Sciences"], "users"=>["Marie Lundholm", "Mona Schröder", "Olga Nagaeva", "Vladimir Baranov", "Anders Widmark", "Lucia Mincheva-Nilsson", "Pernilla Wikström"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0108925.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effector_lymphocyte_cytotoxicity_is_impaired_by_22Rv1_prostate_tumor_derived_exosomes_/1187764", "title"=>"Effector lymphocyte cytotoxicity is impaired by 22Rv1 prostate tumor-derived exosomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-30 03:28:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1697655"], "description"=>"<p>(A) and (B) NKG2D surface expression on circulating CD8<sup>+</sup> T cells from healthy controls and CRPC patients was analyzed by flow cytometry. (C) and (D) NKG2D surface expression on circulating NK cells from healthy controls and CRPC patients. The graphs show the proportion of positive cells and the mean fluorescence intensity (MFI) of NKG2D as indicated. Each dot represents one individual and horizontal bars indicate mean values. *** <i>P</i><0.001.</p>", "links"=>[], "tags"=>["NKG 2D", "surface NKG 2D expression", "NKG 2D cytotoxic response", "pc", "downregulate NKG 2D expression", "NKG 2D downregulation", "Natural Killer Cells", "exosome", "crpc", "NKG 2D expression", "prostate"], "article_id"=>1187765, "categories"=>["Biological Sciences"], "users"=>["Marie Lundholm", "Mona Schröder", "Olga Nagaeva", "Vladimir Baranov", "Anders Widmark", "Lucia Mincheva-Nilsson", "Pernilla Wikström"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0108925.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Surface_expression_of_NKG2D_is_downregulated_on_circulating_CD8_T_cells_and_NK_cells_from_patients_with_CRPC_/1187765", "title"=>"Surface expression of NKG2D is downregulated on circulating CD8<sup>+</sup> T cells and NK cells from patients with CRPC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-30 03:28:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1697656"], "description"=>"<p>Serum-derived exosomes (2 µg) from healthy individuals or CRPC patients were incubated with healthy PMBCs, and flow cytometry was performed to determine NKG2D expression. (A) and (B) NKG2D surface expression on CD8<sup>+</sup> T cells. (C) and (D) NKG2D surface expression on NK cells. The graphs show the proportion of positive cells and the mean fluorescence intensity (MFI) of NKG2D as indicated, relative to untreated PMBCs (normalized to a value of 100 and 1, respectively). Horizontal bars indicate mean values. *** <i>P</i><0.001.</p>", "links"=>[], "tags"=>["NKG 2D", "surface NKG 2D expression", "NKG 2D cytotoxic response", "pc", "downregulate NKG 2D expression", "NKG 2D downregulation", "Natural Killer Cells", "exosome", "crpc", "NKG 2D expression", "prostate"], "article_id"=>1187766, "categories"=>["Biological Sciences"], "users"=>["Marie Lundholm", "Mona Schröder", "Olga Nagaeva", "Vladimir Baranov", "Anders Widmark", "Lucia Mincheva-Nilsson", "Pernilla Wikström"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0108925.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Exosomes_isolated_from_patients_with_CRPC_downregulate_NKG2D_expression_/1187766", "title"=>"Exosomes isolated from patients with CRPC downregulate NKG2D expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-30 03:28:38"}

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