Direct TLR2 Signaling Is Critical for NK Cell Activation and Function in Response to Vaccinia Viral Infection
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{"title"=>"Direct TLR2 signaling is critical for NK cell activation and function in response to vaccinia viral infection", "type"=>"journal", "authors"=>[{"first_name"=>"Jennifer", "last_name"=>"Martinez", "scopus_author_id"=>"14010397000"}, {"first_name"=>"Xiaopei", "last_name"=>"Huang", "scopus_author_id"=>"8921373500"}, {"first_name"=>"Yiping", "last_name"=>"Yang", "scopus_author_id"=>"7409381506"}], "year"=>2010, "source"=>"PLoS Pathogens", "identifiers"=>{"arxiv"=>"NIHMS150003", "sgr"=>"77950373214", "pui"=>"358569033", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "doi"=>"10.1371/journal.ppat.1000811", "issn"=>"15537366", "scopus"=>"2-s2.0-77950373214", "pmid"=>"20300608"}, "id"=>"7ac2f0c7-7535-3dad-a853-3abbeed53d49", "abstract"=>"Natural killer (NK) cells play an essential role in innate immune control of poxviral infections in vivo. However, the mechanism(s) underlying NK cell activation and function in response to poxviruses remains poorly understood. In a mouse model of infection with vaccinia virus (VV), the most studied member of the poxvirus family, we identified that the Toll-like receptor (TLR) 2-myeloid differentiating factor 88 (MyD88) pathway was critical for the activation of NK cells and the control of VV infection in vivo. We further showed that TLR2 signaling on NK cells, but not on accessory cells such as dendritic cells (DCs), was necessary for NK cell activation and that this intrinsic TLR2-MyD88 signaling pathway was required for NK cell activation and played a critical role in the control of VV infection in vivo. In addition, we showed that the activating receptor NKG2D was also important for efficient NK activation and function, as well as recognition of VV-infected targets. We further demonstrated that VV could directly activate NK cells via TLR2 in the presence of cytokines in vitro and TLR2-MyD88-dependent activation of NK cells by VV was mediated through the phosphatidylinositol 3-kinase (PI3K)-extracellular signal-regulated kinase (ERK) pathway. Taken together, these results represent the first evidence that intrinsic TLR signaling is critical for NK cell activation and function in the control of a viral infection in vivo, indicate that multiple pathways are required for efficient NK cell activation and function in response to VV infection, and may provide important insights into the design of effective strategies to combat poxviral infections.", "link"=>"http://www.mendeley.com/research/direct-tlr2-signaling-critical-nk-cell-activation-function-response-vaccinia-viral-infection", "reader_count"=>47, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>19, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>3, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>19, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>3, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Medicine and Dentistry"=>9, "Agricultural and Biological Sciences"=>31, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Immunology and Microbiology"=>4}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>9}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>31}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Colombia"=>1, "Czech Republic"=>1, "Cyprus"=>1, "Japan"=>1, "Spain"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/859748"], "description"=>"<p>(A) DX5<sup>+</sup>CD3<sup>−</sup> NK cells were infected with VV (+VV), VV in the presence of the PI3K inhibitor, LY294002 (+LY294002) or the ERK inhibitor, PD98059 (+PD98059) in vitro. 48 h after infection, NK cells were assayed for intracellular IFN-γ and Granzyme B. The mean percentage ± SD of IFN-γ or Granzyme B positive cells among DX5<sup>+</sup>CD3<sup>−</sup> cells is shown. Data shown is representative of three independent experiments. (B–C) DX5<sup>+</sup>CD3<sup>−</sup> NK cells were stimulated in vitro with VV for the indicated time periods. After stimulation for 2, 4, and 6 h, NK cells were removed from culture and total cell lysates were collected for Western blot analysis of phosphorylated Akt (pAkt) as well as total Akt (Total Akt), which served as a loading control (B). After stimulation for 12, 18, and 24 h, NK cells were removed from culture and total cell lysates were collected for Western blot analysis of phosphorylated ERK1/2 (pERK1/2) as well as total ERK (Total ERK) (C). (D) WT, TLR2<sup>−/−</sup>, and MyD88<sup>−/−</sup> DX5<sup>+</sup>CD3<sup>−</sup> NK cells were stimulated in vitro with VV (+VV), or left unstimulated (Control) for 4 h. NK cells were removed from culture and total cell lysates were collected for Western blot analysis of phosphorylated Akt (pAkt) as well as total Akt (Total Akt). (E) WT, TLR2<sup>−/−</sup>, and MyD88<sup>−/−</sup> DX5<sup>+</sup>CD3<sup>−</sup> NK cells were stimulated in vitro with VV (+VV), VV and the PI3K inhibitor LY294002 (+LY294002), or left unstimulated (Control) for 18 h. NK cells were removed from culture and total cell lysates were collected for Western blot analysis of phosphorylated ERK1/2 (pERK1/2) as well as total ERK (Total ERK). Data shown is a representative blot of five independent experiments.</p>", "links"=>[], "tags"=>["activation", "nk", "cells", "vv", "mediated", "PI3K"], "article_id"=>530202, "categories"=>["Immunology"], "users"=>["Jennifer Martinez", "Xiaopei Huang", "Yiping Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000811.g008", "stats"=>{"downloads"=>4, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TLR2_dependent_activation_of_NK_cells_by_VV_is_mediated_by_PI3K_and_ERK_/530202", "title"=>"TLR2-dependent activation of NK cells by VV is mediated by PI3K and ERK.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-12 00:03:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/426826", "https://ndownloader.figshare.com/files/426876", "https://ndownloader.figshare.com/files/426909", "https://ndownloader.figshare.com/files/426930"], "description"=>"<div><p>Natural killer (NK) cells play an essential role in innate immune control of poxviral infections in vivo. However, the mechanism(s) underlying NK cell activation and function in response to poxviruses remains poorly understood. In a mouse model of infection with vaccinia virus (VV), the most studied member of the poxvirus family, we identified that the Toll-like receptor (TLR) 2-myeloid differentiating factor 88 (MyD88) pathway was critical for the activation of NK cells and the control of VV infection in vivo. We further showed that TLR2 signaling on NK cells, but not on accessory cells such as dendritic cells (DCs), was necessary for NK cell activation and that this intrinsic TLR2-MyD88 signaling pathway was required for NK cell activation and played a critical role in the control of VV infection in vivo. In addition, we showed that the activating receptor NKG2D was also important for efficient NK activation and function, as well as recognition of VV-infected targets. We further demonstrated that VV could directly activate NK cells via TLR2 in the presence of cytokines in vitro and TLR2-MyD88-dependent activation of NK cells by VV was mediated through the phosphatidylinositol 3-kinase (PI3K)-extracellular signal-regulated kinase (ERK) pathway. Taken together, these results represent the first evidence that intrinsic TLR signaling is critical for NK cell activation and function in the control of a viral infection in vivo, indicate that multiple pathways are required for efficient NK cell activation and function in response to VV infection, and may provide important insights into the design of effective strategies to combat poxviral infections.</p></div>", "links"=>[], "tags"=>["tlr2", "signaling", "nk", "activation", "vaccinia", "viral"], "article_id"=>144259, "categories"=>["Immunology"], "users"=>["Jennifer Martinez", "Xiaopei Huang", "Yiping Yang"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000811.s001", "https://dx.doi.org/10.1371/journal.ppat.1000811.s002", "https://dx.doi.org/10.1371/journal.ppat.1000811.s003", "https://dx.doi.org/10.1371/journal.ppat.1000811.s004"], "stats"=>{"downloads"=>4, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Direct_TLR2_Signaling_Is_Critical_for_NK_Cell_Activation_and_Function_in_Response_to_Vaccinia_Viral_Infection/144259", "title"=>"Direct TLR2 Signaling Is Critical for NK Cell Activation and Function in Response to Vaccinia Viral Infection", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-03-12 01:10:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/859079"], "description"=>"<p>(A) WT, IL1R<sup>−/−</sup>, IL12<sup>−/−</sup>, and IL6<sup>−/−</sup> mice were infected with VV (+VV) or left uninfected (Naïve), and splenocytes were assayed for intracellular IFN-γ and Granzyme B production by NK cells 48 hr later. The percentage ± SD of IFN-γ or Granzyme B positive cells among DX5<sup>+</sup>CD3<sup>−</sup> cells is indicated (n  =  6). (B) Splenocytes were harvested 48 hr after infection with VV, and NK lytic activity was assayed on YAC-1 cells for 4 hr at different effector∶target ratios. The mean percentage ± SD of specific lysis is indicated (n  =  6). Data shown is representative of three independent experiments.</p>", "links"=>[], "tags"=>["activation", "vv", "tlr2-induced", "pro-inflammatory"], "article_id"=>529538, "categories"=>["Immunology"], "users"=>["Jennifer Martinez", "Xiaopei Huang", "Yiping Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000811.g003", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NK_cell_activation_upon_VV_infection_is_independent_of_TLR2_induced_production_of_pro_inflammatory_cytokines_/529538", "title"=>"NK cell activation upon VV infection is independent of TLR2-induced production of pro-inflammatory cytokines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-12 02:38:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/859317"], "description"=>"<p>(A–D) Bone marrow chimeric mice were generated by reconstituting irradiated CD45.1<sup>+</sup> WT mice with bone marrow cells from CD45.1<sup>+</sup> WT and CD45.2<sup>+</sup> TLR2<sup>−/−</sup> (A, C) or MyD88<sup>−/−</sup> (B, D) mice at a 1∶1 ratio. 6–8 weeks after reconstitution, chimeric mice were infected with VV (+VV) or left uninfected (Naïve). 48 hr later, splenocytes were assayed for intracellular IFN-γ and Granzyme B production by NK cells. The mean percentage ± SD of IFN-γ or Granzyme B positive cells among CD45.1<sup>+</sup> or CD45.2<sup>+</sup> DX5<sup>+</sup>CD3<sup>−</sup> cells is indicated (n  =  4 per group) (A, B). Splenocytes were sorted into CD45.1<sup>+</sup> or CD45.2<sup>+</sup> DX5<sup>+</sup>CD3<sup>−</sup> populations 48 h after VV infection, and NK lytic activity was assayed on YAC-1 cells for 4 hr at different effector∶target ratios. The mean percentages of specific lysis are indicated (n  =  4 per group) (C, D). Data shown is representative of two independent experiments. (E–F) TLR2<sup>−/−</sup> mice were reconstituted with WT NK cells (+ WT NK) or TLR2<sup>−/−</sup> NK cells (+ TLR2−/− NK) followed by infection with VV. WT and TLR2<sup>−/−</sup> mice infected with VV were used as controls. 48 hr later, splenocytes were assayed for NK lytic activity on YAC-1 cells at different effector∶target ratios. The mean percentage of specific lysis is indicated (n  =  4) (E). The ovaries of female mice were harvested for measurement of viral load. Data represents the mean viral titer ± SD as pfu per ovary (n  =  4) (F). Data is representative of two independent experiments.</p>", "links"=>[], "tags"=>["tlr2-myd88", "signaling", "nk", "priming", "vv"], "article_id"=>529776, "categories"=>["Immunology"], "users"=>["Jennifer Martinez", "Xiaopei Huang", "Yiping Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000811.g005", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Direct_TLR2_MyD88_signaling_is_required_for_NK_cell_priming_in_response_to_VV_in_vivo_/529776", "title"=>"Direct TLR2-MyD88 signaling is required for NK cell priming in response to VV in vivo.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-12 02:42:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/858981"], "description"=>"<p>(A–C) Wild-type (WT), TLR2<sup>−/−</sup>, or MyD88<sup>−/−</sup> mice were infected with VV (+VV) or left uninfected (Naïve). 48 h later, splenocytes were assayed for total NK cell numbers, intracellular IFN-γ and Granzyme B production by NK cells, as well as NK cell lytic assay. (A) The mean numbers ± SD of total DX5<sup>+</sup>CD3<sup>−</sup> NK cells per spleen are indicated (n  =  6 per group). (B) FACS plots of intracellular IFN-γ and Granzyme B production by NK cells with the percentage of IFN-γ or Granzyme B positive cells among DX5<sup>+</sup>CD3<sup>−</sup> NK cells indicated. (C) The mean percentage ± SD of IFN-γ or Granzyme B positive cells among DX5<sup>+</sup>CD3<sup>−</sup> cells is indicated (n  =  6 per group). (D) 48 h after infection, splenocytes were harvested and NK cell lytic activity was assayed on YAC-1 cells or VV-infected L929 cells (L929-VV) for 4 hr at different effector∶target ratios. Naïve splenocytes (Naïve) were used as a control. The mean percentage ± SD of specific lysis is indicated (n  =  6 per group). (E) The ovaries of female mice were harvested for measurement of viral load. Data represents the mean viral titer ± SD as plaque-forming units (pfu) per ovary (n  =  6 per group). Data shown is representative of three independent experiments.</p>", "links"=>[], "tags"=>["activation", "vv", "vivo", "requires", "tlr2-myd88"], "article_id"=>529437, "categories"=>["Immunology"], "users"=>["Jennifer Martinez", "Xiaopei Huang", "Yiping Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000811.g002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NK_cell_activation_and_function_in_response_to_VV_in_vivo_requires_an_intact_TLR2_MyD88_pathway_/529437", "title"=>"NK cell activation and function in response to VV in vivo requires an intact TLR2-MyD88 pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-12 02:37:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/859463"], "description"=>"<p>(A) WT or TLR2<sup>−/−</sup> DX5<sup>+</sup>CD3<sup>−</sup> NK cells were co-cultured with WT CD11c<sup>+</sup> DCs and stimulated with VV alone (+VV), VV in the presence of anti-NKG2D (VV+anti-NKG2D) or NKp46-Fc chimera (VV+NKp46-Fc), or left uninfected (Uninfected). 24 hr later, NK cells were assayed for intracellular IFN-γ and Granzyme B. The mean percentage ± SD of IFN-γ or Granzyme B positive cells among DX5<sup>+</sup>CD3<sup>−</sup> cells is shown. (B–C) WT or TLR2<sup>−/−</sup> mice were infected with VV (+VV) or left uninfected (Naïve). Some mice were pre-treated with anti-NKG2D antibodies 24 and 6 h prior to infection with VV (VV+anti-NKG2D). 48 h after infection, splenic NK cells were analyzed for IFN-γ and Granzyme B production. The mean percentage ± SD of IFN-γ or Granzyme B positive cells among DX5<sup>+</sup>CD3<sup>−</sup> cells is indicated (n  =  4 per group) (B). The ovaries of female mice were harvested for measurement of viral load. Data represents the mean viral titer ± SD as pfu per ovary (n  =  4 per group) (C). (D) 48 h after infection, splenocytes from WT mice were assayed for NK cell lytic activity on VV-infected L929 cells in the presence of anti-NKG2D antibodies (+anti-NKG2D) or NKp46-Fc chimera (+NKp46-Fc), for 4 hr at different effector∶target ratios. The mean percentage ± SD of specific lysis is indicated (n  =  4 per group). Data shown is representative of two independent experiments.</p>", "links"=>[], "tags"=>["nkg2d", "pathway", "nk", "activation", "vv"], "article_id"=>529925, "categories"=>["Immunology"], "users"=>["Jennifer Martinez", "Xiaopei Huang", "Yiping Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000811.g006", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_NKG2D_pathway_is_required_for_efficient_NK_activation_and_function_in_response_to_VV_infection_/529925", "title"=>"The NKG2D pathway is required for efficient NK activation and function in response to VV infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-12 02:45:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/858876"], "description"=>"<p>Female C57BL/6 mice were depleted of NK cells with anti-NK1.1 antibodies (25 µg) on days −3 and 0 (+anti-NK1.1) or left untreated (Control), followed by infection with VV on day 0. (A) 48 h after infection, splenocytes were assayed for NK lytic activity on YAC-1 cells for 4 hr at different effector∶target ratios. Naïve splenocytes (Naïve) were used for comparison. The percentage of specific lysis is shown. (B) The ovaries were assayed for viral load. Data represents viral titer ± SD as pfu per ovary.</p>", "links"=>[], "tags"=>["cells", "vv"], "article_id"=>529334, "categories"=>["Immunology"], "users"=>["Jennifer Martinez", "Xiaopei Huang", "Yiping Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000811.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NK_cells_are_required_for_the_control_of_VV_infection_in_vivo_/529334", "title"=>"NK cells are required for the control of VV infection in vivo.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-12 02:35:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/859595"], "description"=>"<p>(A–B) DX5<sup>+</sup>CD3<sup>−</sup> NK cells were cultured in the medium alone (Medium) or medium supplemented with IL-2 and IFN-α (+Cytokines), or infected with live VV (+VV) or UV-inactivated VV (+UV-VV) in the presence of IL-2 and IFN-α. 48 h later, NK cells were assayed for intracellular IFN-γ and Granzyme B. The percentage of IFN-γ or Granzyme B positive cells among DX5<sup>+</sup>CD3<sup>−</sup> cells is indicated (A). The mean percentage ± SD of IFN-γ or Granzyme B positive cells among DX5<sup>+</sup>CD3<sup>−</sup> cells is shown (B). (C) DX5<sup>+</sup>CD3<sup>−</sup> NK cells from WT or TLR2<sup>−/−</sup> mice were stimulated with VV for 48 h and assayed for intracellular IFN-γ and Granzyme B. Some WT NK cells were stimulated with VV in the presence of a blocking TLR2 antibody (+anti-TLR2). The percentage ± SD of IFN-γ or Granzyme B positive cells among DX5<sup>+</sup>CD3<sup>−</sup> cells is shown. Data shown is representative of three independent experiments.</p>", "links"=>[], "tags"=>["activates", "nk", "cells", "tlr2"], "article_id"=>530052, "categories"=>["Immunology"], "users"=>["Jennifer Martinez", "Xiaopei Huang", "Yiping Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000811.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_VV_activates_NK_cells_directly_via_TLR2_in_vitro_/530052", "title"=>"VV activates NK cells directly via TLR2 in vitro.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-12 00:00:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/859212"], "description"=>"<p>WT or TLR2<sup>−/−</sup> DX5<sup>+</sup>CD3<sup>−</sup> NK cells were co-cultured with WT or TLR2<sup>−/−</sup> CD11c<sup>+</sup> DCs and stimulated with VV (+VV), LPS (+LPS) or left uninfected (Uninfected). 48 hr after infection, NK cells were assayed for intracellular IFN-γ and Granzyme B. (A) The percentage of IFN-γ or Granzyme B positive cells among DX5<sup>+</sup>CD3<sup>−</sup> cells is indicated. (B) The mean percentage ± SD of IFN-γ or Granzyme B positive cells among DX5<sup>+</sup>CD3<sup>−</sup> cells is shown. Data shown is representative of two independent experiments.</p>", "links"=>[], "tags"=>["signaling", "nk", "activation", "vv"], "article_id"=>529665, "categories"=>["Immunology"], "users"=>["Jennifer Martinez", "Xiaopei Huang", "Yiping Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000811.g004", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TLR2_signaling_on_NK_cells_but_not_on_DCs_is_required_for_NK_cell_activation_to_VV_in_vitro_/529665", "title"=>"TLR2 signaling on NK cells, but not on DCs, is required for NK cell activation to VV in vitro.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-12 02:41:05"}

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