HIV Traffics through a Specialized, Surface-Accessible Intracellular Compartment during trans-Infection of T Cells by Mature Dendritic Cells
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{"title"=>"HIV traffics through a specialized, surface-accessible intracellular compartment during trans-infection of T cells by mature dendritic cells", "type"=>"journal", "authors"=>[{"first_name"=>"Jae Yu", "last_name"=>"Hyun", "scopus_author_id"=>"24759216000"}, {"first_name"=>"Morgan A.", "last_name"=>"Reuter", "scopus_author_id"=>"24759472800"}, {"first_name"=>"David", "last_name"=>"McDonald", "scopus_author_id"=>"35577518300"}], "year"=>2008, "source"=>"PLoS Pathogens", "identifiers"=>{"pui"=>"352264393", "sgr"=>"50849114848", "issn"=>"15537366", "pmid"=>"18725936", "scopus"=>"2-s2.0-50849114848", "doi"=>"10.1371/journal.ppat.1000134", "isbn"=>"1553-7374 (Electronic)"}, "id"=>"c88da5de-9e68-3111-b3ec-6f185fedcaa4", "abstract"=>"In vitro, dendritic cells (DCs) bind and transfer intact, infectious HIV to CD4 T cells without first becoming infected, a process known as trans-infection. trans-infection is accomplished by recruitment of HIV and its receptors to the site of DC-T cell contact and transfer of virions at a structure known as the infectious synapse. In this study, we used fluorescent microscopy to track individual HIV particles trafficking in DCs during virus uptake and trans-infection. Mature DCs rapidly concentrated HIV into an apparently intracellular compartment that lacked markers characteristic of early endosomes, lysosomes, or antigen-processing vesicles. Live cell microscopy demonstrated that the HIV-containing compartment was rapidly polarized toward the infectious synapse after contact with a T cell; however, the bulk of the concentrated virus remained in the DCs after T cell engagement. Individual virions were observed emerging from the compartment and fusing with the T cell membrane at the infectious synapse. The compartmentalized HIV, although engulfed by the cytoplasm, was fully accessible to HIV envelope-specific inhibitors and other membrane-impermeable probes that were delivered to the cell surface. These results demonstrate that HIV resides in an invaginated domain within DCs that is both contiguous with the plasma membrane and distinct from endocytic vesicles. We conclude that HIV virions are routed through this specialized compartment, which allows individual particles to be delivered to T cells during trans-infection.", "link"=>"http://www.mendeley.com/research/hiv-traffics-through-specialized-surfaceaccessible-intracellular-compartment-during-transinfection-t", "reader_count"=>63, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>4, "Researcher"=>14, "Student > Ph. D. Student"=>23, "Student > Postgraduate"=>3, "Student > Master"=>7, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>4, "Researcher"=>14, "Student > Ph. D. Student"=>23, "Student > Postgraduate"=>3, "Student > Master"=>7, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>43, "Medicine and Dentistry"=>5, "Chemical Engineering"=>1, "Chemistry"=>1, "Immunology and Microbiology"=>5, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>5}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>43}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>3}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>0}

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  • {"files"=>["https://ndownloader.figshare.com/files/455863", "https://ndownloader.figshare.com/files/455899", "https://ndownloader.figshare.com/files/455931", "https://ndownloader.figshare.com/files/455958", "https://ndownloader.figshare.com/files/456007", "https://ndownloader.figshare.com/files/456068", "https://ndownloader.figshare.com/files/456119", "https://ndownloader.figshare.com/files/456178"], "description"=>"<div><p><em>In vitro</em>, dendritic cells (DCs) bind and transfer intact, infectious HIV to CD4 T cells without first becoming infected, a process known as <em>trans</em>-infection. <em>trans</em>-infection is accomplished by recruitment of HIV and its receptors to the site of DC–T cell contact and transfer of virions at a structure known as the infectious synapse. In this study, we used fluorescent microscopy to track individual HIV particles trafficking in DCs during virus uptake and <em>trans</em>-infection. Mature DCs rapidly concentrated HIV into an apparently intracellular compartment that lacked markers characteristic of early endosomes, lysosomes, or antigen-processing vesicles. Live cell microscopy demonstrated that the HIV-containing compartment was rapidly polarized toward the infectious synapse after contact with a T cell; however, the bulk of the concentrated virus remained in the DCs after T cell engagement. Individual virions were observed emerging from the compartment and fusing with the T cell membrane at the infectious synapse. The compartmentalized HIV, although engulfed by the cytoplasm, was fully accessible to HIV envelope-specific inhibitors and other membrane-impermeable probes that were delivered to the cell surface. These results demonstrate that HIV resides in an invaginated domain within DCs that is both contiguous with the plasma membrane and distinct from endocytic vesicles. We conclude that HIV virions are routed through this specialized compartment, which allows individual particles to be delivered to T cells during <em>trans</em>-infection.</p></div>", "links"=>[], "tags"=>["hiv", "traffics", "surface-accessible", "intracellular", "compartment", "cells", "mature", "dendritic"], "article_id"=>149794, "categories"=>["Cell Biology", "Cancer"], "users"=>["Hyun Jae Yu", "Morgan A. Reuter", "David McDonald"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000134.s001", "https://dx.doi.org/10.1371/journal.ppat.1000134.s002", "https://dx.doi.org/10.1371/journal.ppat.1000134.s003", "https://dx.doi.org/10.1371/journal.ppat.1000134.s004", "https://dx.doi.org/10.1371/journal.ppat.1000134.s005", "https://dx.doi.org/10.1371/journal.ppat.1000134.s006", "https://dx.doi.org/10.1371/journal.ppat.1000134.s007", "https://dx.doi.org/10.1371/journal.ppat.1000134.s008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/HIV_Traffics_through_a_Specialized_Surface_Accessible_Intracellular_Compartment_during_trans_Infection_of_T_Cells_by_Mature_Dendritic_Cells/149794", "title"=>"HIV Traffics through a Specialized, Surface-Accessible Intracellular Compartment during <em>trans</em>-Infection of T Cells by Mature Dendritic Cells", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-08-22 02:43:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/923457"], "description"=>"<p>(A,B) Mature DCs were plated onto coverslips, pulsed with HxB2 pseudotyped GFP-Vpr HIV (green) for 30 min, washed and fixed (A) or incubated an additional hour and fixed (B). Fixed cells were stained for actin cytoskeleton (red) and nuclear DNA (blue). (C–K) Mature MDDCs were pre-incubated for 15 min without (C–E) or with cytoskeletal inhibitors latrunculin B (2.5 µM) (F–H) or nocodazole (5 µM) (I–K) and then incubated with GFP-Vpr HIV (green) for 1 h with appropriate inhibitors. Cells were washed and incubated for 1 h with inhibitors, plated onto coverslips, and fixed and stained for cellular CD63 (blue) and actin (red). Note the perinuclear CD63-positive lysosomes were re-distributed in nocodazole-treated cells (I–K) and the actin cytoskeleton was disrupted in latrunculin B treated cells (F). Images are 3-D–rendered whole-cell volumes, arrows denote areas of concentrated HIV. Bars, 5 μ.</p>", "links"=>[], "tags"=>["mature", "mddcs", "requires", "actin"], "article_id"=>593905, "categories"=>["Cell Biology", "Virology"], "users"=>["Hyun Jae Yu", "Morgan A. Reuter", "David McDonald"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000134.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIV_concentration_in_mature_MDDCs_requires_an_intact_actin_cytoskeleton_/593905", "title"=>"HIV concentration in mature MDDCs requires an intact actin cytoskeleton.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-22 01:05:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/923608"], "description"=>"<p>(A–H) Mature MDDCs were pulsed with HxB2 pseudotyped GFP-Vpr HIV (green) for 1 h, washed, plated onto poly-L-Lysine coverslips, and fixed and stained for the indicated markers. (A) 3-D–rendered whole-cell volume, CD81 (red) and DNA (blue). (B) Same cell as in (A) with CD81 (red) and CD63 (blue) signals. Note that CD63 labels primarily lysosomes in the perinuclear region. (C,D) Magnified view of boxed region with HIV and (C) CD81 or (D) CD63 signals. (E) 3-D[en]rendered whole-cell volume, HIV (green), HLA Class-II (blue), and CD86 (red). (F–H) Single focal plane through the center of the cell. (G,H) Magnified view of the boxed region in (F) showing HIV and (G) CD86 or (H) HLA Class-II. I–K. Long-term sequestration of HIV. MDDCs were pulsed with GFP-Vpr HIV for 1 h, washed and incubated for 48 h, then fixed and stained as above. Images are 3-D–rendered whole-cell volumes. (I) HIV (green) , actin (red), DNA (blue). (J) HIV (green) and CD81 (red). (K) CD81 alone. Bars (A, B, E, F, I–K), 5 μ; (C, D, G, H), 2 μ.</p>", "links"=>[], "tags"=>["cell-surface", "proteins", "sequestered", "subcellular"], "article_id"=>594058, "categories"=>["Cell Biology", "Virology"], "users"=>["Hyun Jae Yu", "Morgan A. Reuter", "David McDonald"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000134.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIV_and_cell_surface_proteins_are_sequestered_into_a_distinct_subcellular_compartment_/594058", "title"=>"HIV and cell-surface proteins are sequestered into a distinct subcellular compartment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-22 01:07:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/923775"], "description"=>"<p>BDCA-1–positive myDCs were purified from PBMCs and cultured for 14 h without or with LPS to induce maturation. Cells were incubated with HxB2 pseudotyped GFP-Vpr HIV (green) for 1 h, washed and cultured for 1 h, then co-cultured with LuSIV cells, an HIV-LTR-luciferase indicator T cell line, or plated onto coverslips and prepared for microscopy. (A) LuSIV cells were assayed for luciferase activity 40 h later. HIV, cell-free input virus. Bars are the mean of triplicates±standard deviation. (B–D) Fixed, LPS-mature myDCs were stained for CD81 (red) and DNA (blue). Images are 3-D–rendered whole-cell volumes. Merged (B) and separated signals (C,D) are shown; arrows denote concentrated HIV. Scale bar, 10 μ.</p>", "links"=>[], "tags"=>["hiv", "sequestration", "mature", "myeloid"], "article_id"=>594221, "categories"=>["Cell Biology", "Virology"], "users"=>["Hyun Jae Yu", "Morgan A. Reuter", "David McDonald"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000134.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_trans_infection_and_HIV_sequestration_in_mature_blood_myeloid_DCs_/594221", "title"=>"<i>trans</i>-infection and HIV sequestration in mature blood myeloid DCs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-22 01:10:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/923870"], "description"=>"<p>(A–C) Mature MDDCs were incubated with GFP-Vpr/S15-RFP labeled HIV for 1 h at 37°C, washed, and plated onto a glass coverslip dish. GFP-Vpr (green) marks the HIV core, and S15-RFP (red) is a myristoylated fusion that marks the viral membrane prior to T cell entry. Jurkat LTR-GFP T cells were added and cells were imaged at 2-min intervals immediately after identifying DC–T cell interaction. (A) Merged fluorescent and light images of key time-points during the DC–T cell interaction. Arrows denote viral transmission events. (B,C) Magnified view of GFP/RFP (B) and RFP (C) signals at time points immediately before and during transmission of HIV particles. Arrows denote individual particles transmitted into the T cell. (D–F) Mature myeloid DCs were incubated with labeled HIV as in (A) and plated onto a glass coverslip dish. Jurkat T cells labeled with CellTrace DDAO-SE (diffuse red signal) were added and cells were imaged every 2 min as above. (E,F) Magnified view of GFP/RFP (E) and RFP (F) signals at time-points immediately before and during transmission of HIV particles. Bars, 5 μ (A, D); 2 μ (B, C, E, F). See also <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000134#ppat.1000134.s004\" target=\"_blank\">Videos S1</a> and <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000134#ppat.1000134.s005\" target=\"_blank\">S2</a>.</p>", "links"=>[], "tags"=>["hiv", "particles", "cells", "infectious"], "article_id"=>594321, "categories"=>["Cell Biology", "Virology"], "users"=>["Hyun Jae Yu", "Morgan A. Reuter", "David McDonald"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000134.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DCs_transmit_individual_HIV_particles_to_T_cells_at_the_infectious_synapse_/594321", "title"=>"DCs transmit individual HIV particles to T cells at the infectious synapse.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-22 01:12:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/923970"], "description"=>"<p>Mature MDDCs were sequentially exposed to HIV-Firefly luciferase (Luc) and HIV-Renilla luciferase (Ren) at 37°C and treated at 4°C with soluble CD4 (sCD4, 10 µg/ml) for 1 h either before, between, or after incubation with the two HIV reporters, as indicated. Cells were incubated at 4°C during sCD4 and control treatment to prevent endocytosis of the inhibitor, and sCD4 was washed away before subsequent treatment. DCs were then co-cultured with Hos/CD4 cells, and luciferase activity was measured two days later and expressed as relative light units (RLU). Open bars, Firefly luciferase activity; grey bars, Renilla luciferase activity. Bars are mean of triplicate samples±standard deviation. <i>trans</i>-infection of CD4-negative target cells resulted in background luciferase activity, confirming that the luciferase signals were not the result of DC infection (unpublished data).</p>", "links"=>[], "tags"=>["hiv", "abolishes"], "article_id"=>594427, "categories"=>["Cell Biology", "Virology"], "users"=>["Hyun Jae Yu", "Morgan A. Reuter", "David McDonald"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000134.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Inhibition_of_surface_accessible_HIV_abolishes_trans_infection_/594427", "title"=>"Inhibition of surface accessible HIV abolishes <i>trans</i>-infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-22 01:13:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/924055"], "description"=>"<p>(A–F) Mature MDDCs were pulsed with HxB2 pseudotyped GFP-Vpr HIV (green) for 1 h, washed, and cultured for 1 h at 37°C. Cells were then placed on ice and incubated for 30 min with (A–C) CD4-hIgG fusion protein or (D–F) 2G12 anti-HIV Env (gp120), a human mAb. Cells were washed at 4°C, fixed, and stained for human IgG (orange) and CD81 (red); nuclei were stained with Hoechst (blue). Images are 3-D reconstructions of whole-cell volumes. Arrows denote concentrated HIV co-localized with the surface applied probes and CD81. Bars, 5 μ.</p>", "links"=>[], "tags"=>["hiv", "applied", "hiv-specific", "inhibitory"], "article_id"=>594507, "categories"=>["Cell Biology", "Virology"], "users"=>["Hyun Jae Yu", "Morgan A. Reuter", "David McDonald"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000134.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Internalized_HIV_is_accessible_to_surface_applied_HIV_specific_inhibitory_antibodies_/594507", "title"=>"Internalized HIV is accessible to surface applied HIV-specific inhibitory antibodies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-22 01:15:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/924204"], "description"=>"<p>(A–C) Mature MDDCs were pulsed with HIV as in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000134#ppat-1000134-g006\" target=\"_blank\">Figure 6</a> and incubated with fluorescent dextran (orange) at 4°C. Cells were plated onto coverslips, fixed, and stained for Actin (Red) and DNA (Blue). (A) 3-D view of the entire cell volume. (B) Same as (A), without Actin. (C) Magnified view of compartmentalized dextran signal (boxed region). (D–F) Surface accessibility distinguishes the HIV compartment from endosomal structures. DCs were prepared as above and incubated with anti-CD63 at 4°C, washed, fixed, and immunostained with labeled anti-mouse antibody (orange). Internal CD63 (red) was then detected using the same anti-CD63 mAb and pre-labeled with a different fluorophore after detergent treatment to remove cell membranes. DNA is labeled in blue; images are 3-D views of whole-cell volumes. Solid arrows denote surface-applied anti-CD63 stained, compartmentalized HIV; open arrows denote lysosomal CD63-positive compartments that are not stained by the surface-applied antibody. Bars (A, B, D–F) 5 μ; (C) 2 μ.</p>", "links"=>[], "tags"=>["hiv", "accessed", "surface-applied"], "article_id"=>594656, "categories"=>["Cell Biology", "Virology"], "users"=>["Hyun Jae Yu", "Morgan A. Reuter", "David McDonald"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000134.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Internalized_HIV_is_accessed_by_a_surface_applied_fluid_phase_marker_/594656", "title"=>"Internalized HIV is accessed by a surface-applied fluid phase marker.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-22 01:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/924335"], "description"=>"<p>(A) Mature MDDCs were exposed to HxB2 pseudotyped GFP-HIV for 1 h, washed, and cultured at 37°C for 24 h. Cells were then incubated at 4°C with a mouse anti-CD81 mAb, washed, fixed onto coverslips, and stained with an anti-mouse antibody (red). Image is a single z-plane demonstrating concentrated HIV associated with the surface-accessible compartment. See also <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000134#ppat.1000134.s008\" target=\"_blank\">Video S5</a> for the entire z-stack compiled as a movie. (B–D) DCs prepared as in (A) were incubated at 4°C with 2G12 anti-HIV Env (gp120) mAb, washed, fixed, and immunostained for 2G12 (gp120) (orange) and CD81 (red). Images are 3-D–rendered whole-cell volumes; arrows denote compartmentalized HIV. Bars, 5 μ.</p>", "links"=>[], "tags"=>["hiv", "remains", "probes"], "article_id"=>594790, "categories"=>["Cell Biology", "Virology"], "users"=>["Hyun Jae Yu", "Morgan A. Reuter", "David McDonald"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000134.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Compartmentalized_HIV_remains_accessible_to_surface_probes_after_extended_culture_/594790", "title"=>"Compartmentalized HIV remains accessible to surface probes after extended culture.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-22 01:19:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/924477"], "description"=>"<p>(A) MVB/exosomal transfer. HIV is endocytosed and concentrated in a non-degradative late endosome/multivesicular body (MVB). The MVB is subsequently transported to the T cell interface, where it fuses to the DC plasma membrane and delivers HIV by exocytosis. (B) Surface transfer. Only surface-bound HIV is able to infect T cells. Internalized HIV is degraded following lysosomal maturation. (C) Pocket transfer. HIV is concentrated and internalized in a non-endosomal compartment that remains contiguous with the plasma membrane. HIV remains accessible to the extracellular milieu, and individual virions are delivered back to the DC surface prior to transmission.</p>", "links"=>[], "tags"=>["cell biology", "virology/immunodeficiency viruses"], "article_id"=>594929, "categories"=>["Cell Biology", "Virology"], "users"=>["Hyun Jae Yu", "Morgan A. Reuter", "David McDonald"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000134.g009"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Models_of_trans_infection_/594929", "title"=>"Models of <i>trans</i>-infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-22 01:22:09"}

PMC Usage Stats | Further Information

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Relative Metric

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