Loss of Circulating CD4 T Cells with B Cell Helper Function during Chronic HIV Infection
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{"title"=>"Loss of Circulating CD4 T Cells with B Cell Helper Function during Chronic HIV Infection", "type"=>"journal", "authors"=>[{"first_name"=>"Kristin L.", "last_name"=>"Boswell", "scopus_author_id"=>"15756908100"}, {"first_name"=>"Robert", "last_name"=>"Paris", "scopus_author_id"=>"7102470226"}, {"first_name"=>"Eli", "last_name"=>"Boritz", "scopus_author_id"=>"6506187874"}, {"first_name"=>"David", "last_name"=>"Ambrozak", "scopus_author_id"=>"6603170839"}, {"first_name"=>"Takuya", "last_name"=>"Yamamoto", "scopus_author_id"=>"36036730700"}, {"first_name"=>"Sam", "last_name"=>"Darko", "scopus_author_id"=>"24461398200"}, {"first_name"=>"Kaska", "last_name"=>"Wloka", "scopus_author_id"=>"8761754800"}, {"first_name"=>"Adam", "last_name"=>"Wheatley", "scopus_author_id"=>"35110792800"}, {"first_name"=>"Sandeep", "last_name"=>"Narpala", "scopus_author_id"=>"53868322900"}, {"first_name"=>"Adrian", "last_name"=>"McDermott", "scopus_author_id"=>"10640093300"}, {"first_name"=>"Mario", "last_name"=>"Roederer", "scopus_author_id"=>"7006822164"}, {"first_name"=>"Richard", "last_name"=>"Haubrich", "scopus_author_id"=>"7003333798"}, {"first_name"=>"Mark", "last_name"=>"Connors", "scopus_author_id"=>"56745718900"}, {"first_name"=>"Julie", "last_name"=>"Ake", "scopus_author_id"=>"9244499100"}, {"first_name"=>"Daniel C.", "last_name"=>"Douek", "scopus_author_id"=>"7003438553"}, {"first_name"=>"Jerome", "last_name"=>"Kim", "scopus_author_id"=>"7601367709"}, {"first_name"=>"Constantinos", "last_name"=>"Petrovas", "scopus_author_id"=>"35446607200"}, {"first_name"=>"Richard A.", "last_name"=>"Koup", "scopus_author_id"=>"7006766528"}], "year"=>2014, "source"=>"PLoS Pathogens", "identifiers"=>{"pui"=>"372348947", "sgr"=>"84893746319", "issn"=>"15537366", "pmid"=>"24497824", "scopus"=>"2-s2.0-84893746319", "doi"=>"10.1371/journal.ppat.1003853"}, "id"=>"2da437c0-d772-3337-8892-e29ea5affb98", "abstract"=>"The interaction between follicular T helper cells (TFH) and B cells in the lymph nodes and spleen has a major impact on the development of antigen-specific B cell responses during infection or vaccination. Recent studies described a functional equivalent of these cells among circulating CD4 T cells, referred to as peripheral TFH cells. Here, we characterize the phenotype and in vitro B cell helper activity of peripheral TFH populations, as well as the effect of HIV infection on these populations. In co-culture experiments we confirmed CXCR5+ cells from HIV-uninfected donors provide help to B cells and more specifically, we identified a CCR7(high)CXCR5(high)CCR6(high)PD-1(high) CD4 T cell population that secretes IL-21 and enhances isotype-switched immunoglobulin production. This population is significantly decreased in treatment-naïve, HIV-infected individuals and can be recovered after anti-retroviral therapy. We found impaired immunoglobulin production in co-cultures from HIV-infected individuals and found no correlation between the frequency of peripheral TFH cells and memory B cells, or with neutralization activity in untreated HIV infection in our cohort. Furthermore, we found that within the peripheral TFH population, the expression level of TFH-associated genes more closely resembles a memory, non-TFH population, as opposed to a TFH population. Overall, our data identify a heterogeneous population of circulating CD4 T cells that provides in vitro help to B cells, and challenges the origin of these cells as memory TFH cells.", "link"=>"http://www.mendeley.com/research/loss-circulating-cd4-t-cells-b-cell-helper-function-during-chronic-hiv-infection", "reader_count"=>68, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>19, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>5, "Student > Master"=>9, "Other"=>2, "Student > Bachelor"=>7, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>19, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>5, "Student > Master"=>9, "Other"=>2, "Student > Bachelor"=>7, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>38, "Medicine and Dentistry"=>11, "Physics and Astronomy"=>1, "Immunology and Microbiology"=>13}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>11}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>13}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>38}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Czech Republic"=>1, "Italy"=>1, "France"=>1, "Germany"=>1, "Spain"=>1, "Indonesia"=>1}, "group_count"=>4}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1369092"], "description"=>"<p>(<b>A</b>) Pooled data showing the frequency (%) of CXCR5<sup>high</sup>, CXCR5<sup>high</sup>CCR6<sup>high</sup> and CXCR5<sup>high</sup>CCR6<sup>high</sup>PD-1<sup>high</sup> populations in total CD4 cells from PBMC from HIV uninfected (open circles; n = 13), HIV-infected (treatment-naïve), CD4 count >200 (light gray circles; n = 44), and HIV-infected (treatment-naïve), CD4 count <200 (black circles; n = 22). Significant differences between HIV-uninfected and HIV-infected subjects were determined using the Mann-Whitney U test. ***p<0.001; **p<0.01; *p<0.05. (<b>B</b>) Longitudinal analysis showing the frequency (%) of CXCR5<sup>high</sup>, CXCR5<sup>high</sup>CCR6<sup>high</sup> and CXCR5<sup>high</sup>CCR6<sup>high</sup>PD-1<sup>high</sup> populations in total CD4 cells or indicated populations in CXCR5-expressing cells (bottom row) from HIV-infected (treatment naïve) subjects (n = 10) over 36–48 months. No significant correlations were found. (<b>C</b>) Pooled data showing the frequency (%) of CXCR5<sup>high</sup>, CXCR5<sup>high</sup>CCR6<sup>high</sup> and CXCR5<sup>high</sup>CCR6<sup>high</sup>PD-1<sup>high</sup> populations in total CD4 cells from PBMC from HIV-uninfected subjects (open circles; n = 13) and HIV-infected subjects before (n = 14, week 0; black circles) and after ART (week 24, dark gray circles; week 48, light gray circles). Significant differences between HIV-uninfected and HIV-infected subjects were determined using the Mann-Whitney U test. Significant differences between subjects before and after ART were determined using the Wilcoxon matched-pairs signed rank test. ***p<0.001; **p<0.01; *p<0.05.</p>", "links"=>[], "tags"=>["immunology", "Immune cells", "Antibody-producing cells", "b cells", "t cells", "Immune system", "cytokines", "immunoglobulins", "Infectious diseases", "Viral diseases", "hiv", "Retrovirology and HIV immunopathogenesis", "cells"], "article_id"=>920049, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Kristin L. Boswell", "Robert Paris", "Eli Boritz", "David Ambrozak", "Takuya Yamamoto", "Sam Darko", "Kaska Wloka", "Adam Wheatley", "Sandeep Narpala", "Adrian McDermott", "Mario Roederer", "Richard Haubrich", "Mark Connors", "Julie Ake", "Daniel C. Douek", "Jerome Kim", "Constantinos Petrovas", "Richard A. Koup"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003853.g002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Progressive_loss_of_pT_FH_cells_in_HIV_infection_/920049", "title"=>"Progressive loss of pT<sub>FH</sub> cells in HIV infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 04:38:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1369095"], "description"=>"<p>(<b>A</b>) CCR7<sup>high</sup>CXCR5<sup>low</sup> and CCR7<sup>high</sup>CXCR5<sup>high</sup>CCR6<sup>high</sup> CM CD4 T cells isolated from PBMCs were cultured with autologous naïve B cells (CD19<sup>high</sup>CD27<sup>low</sup>IgD<sup>−</sup>) in the presence of SEB for 12 days and Ig concentrations were measured from supernatants (HIV-uninfected, n = 8; HIV-infected (non-viremic), n = 5–7, HIV-infected (viremic), n = 1–2). Significant differences were determined using the Wilcoxon paired t-test or the Mann-Whitney test. *p<0.05; **p<0.01. (<b>B</b>) Top: HIV-uninfected PBMCs were incubated with indicated concentrations of CXCL-13 for 1 hour at 37°C (red) or 4°C (black). Bottom: Healthy PBMCs were incubated with 1 µg/mL CXCL13 for 10, 30, 60 or 120 minutes at 37°C (red) or 4°C (black). The frequency of CXCR5-positve CD4 T cells was calculated and normalized to time 0. (n = 3). (<b>C</b>) Top: Correlative analysis showing the frequency of CM CXCR5-positive CD4 T cells versus viral load (n = 27; r = −0.4036, P = 0.0368). Bottom: Correlative analysis showing the concentration of CXCL-13 in plasma or sera versus viral load (n = 27; r = 0.4414, P = 0.0165). Correlations were analyzed using the nonparametric Spearman test.</p>", "links"=>[], "tags"=>["immunology", "Immune cells", "Antibody-producing cells", "b cells", "t cells", "Immune system", "cytokines", "immunoglobulins", "Infectious diseases", "Viral diseases", "hiv", "Retrovirology and HIV immunopathogenesis", "cells"], "article_id"=>920052, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Kristin L. Boswell", "Robert Paris", "Eli Boritz", "David Ambrozak", "Takuya Yamamoto", "Sam Darko", "Kaska Wloka", "Adam Wheatley", "Sandeep Narpala", "Adrian McDermott", "Mario Roederer", "Richard Haubrich", "Mark Connors", "Julie Ake", "Daniel C. Douek", "Jerome Kim", "Constantinos Petrovas", "Richard A. Koup"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003853.g003", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Impaired_B_cell_help_by_pT_FH_cells_in_HIV_infection_/920052", "title"=>"Impaired B cell help by pT<sub>FH</sub> cells in HIV infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 04:38:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1369106", "https://ndownloader.figshare.com/files/1369107", "https://ndownloader.figshare.com/files/1369108", "https://ndownloader.figshare.com/files/1369109", "https://ndownloader.figshare.com/files/1369110"], "description"=>"<div><p>The interaction between follicular T helper cells (T<sub>FH</sub>) and B cells in the lymph nodes and spleen has a major impact on the development of antigen-specific B cell responses during infection or vaccination. Recent studies described a functional equivalent of these cells among circulating CD4 T cells, referred to as peripheral T<sub>FH</sub> cells. Here, we characterize the phenotype and in vitro B cell helper activity of peripheral T<sub>FH</sub> populations, as well as the effect of HIV infection on these populations. In co-culture experiments we confirmed CXCR5+ cells from HIV-uninfected donors provide help to B cells and more specifically, we identified a CCR7<sup>high</sup>CXCR5<sup>high</sup>CCR6<sup>high</sup>PD-1<sup>high</sup> CD4 T cell population that secretes IL-21 and enhances isotype-switched immunoglobulin production. This population is significantly decreased in treatment-naïve, HIV-infected individuals and can be recovered after anti-retroviral therapy. We found impaired immunoglobulin production in co-cultures from HIV-infected individuals and found no correlation between the frequency of peripheral T<sub>FH</sub> cells and memory B cells, or with neutralization activity in untreated HIV infection in our cohort. Furthermore, we found that within the peripheral T<sub>FH</sub> population, the expression level of T<sub>FH</sub>-associated genes more closely resembles a memory, non-T<sub>FH</sub> population, as opposed to a T<sub>FH</sub> population. Overall, our data identify a heterogeneous population of circulating CD4 T cells that provides <i>in vitro</i> help to B cells, and challenges the origin of these cells as memory T<sub>FH</sub> cells.</p></div>", "links"=>[], "tags"=>["immunology", "Immune cells", "Antibody-producing cells", "b cells", "t cells", "Immune system", "cytokines", "immunoglobulins", "Infectious diseases", "Viral diseases", "hiv", "Retrovirology and HIV immunopathogenesis", "circulating", "cd4", "cells", "helper"], "article_id"=>920063, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Kristin L. Boswell", "Robert Paris", "Eli Boritz", "David Ambrozak", "Takuya Yamamoto", "Sam Darko", "Kaska Wloka", "Adam Wheatley", "Sandeep Narpala", "Adrian McDermott", "Mario Roederer", "Richard Haubrich", "Mark Connors", "Julie Ake", "Daniel C. Douek", "Jerome Kim", "Constantinos Petrovas", "Richard A. Koup"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003853.s001", "https://dx.doi.org/10.1371/journal.ppat.1003853.s002", "https://dx.doi.org/10.1371/journal.ppat.1003853.s003", "https://dx.doi.org/10.1371/journal.ppat.1003853.s004", "https://dx.doi.org/10.1371/journal.ppat.1003853.s005"], "stats"=>{"downloads"=>12, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Loss_of_Circulating_CD4_T_Cells_with_B_Cell_Helper_Function_during_Chronic_HIV_Infection_/920063", "title"=>"Loss of Circulating CD4 T Cells with B Cell Helper Function during Chronic HIV Infection", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-01-30 04:38:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1369099"], "description"=>"<p>(<b>A</b>) Representative flow cytometry plots showing CM, CD154-positive, cytokine-positive cells after SEB stimulation. CD154-positive, cytokine-positive CD4 T cells, shown by contour plots (blue: HIV-uninfected; red: HIV-infected), are overlaid onto 2 dimensional density plots for CM CD4 T cells plotted against CCR7 and CD3, and CXCR5 and CCR6. (<b>B</b>) Bar graphs showing the frequency of SEB-stimulated CD154-positive, cytokine-positive cells that express CCR7, CXCR5 and CCR6 (Blue: uninfected; n = 5; Red: HIV-infected; n = 24). (<b>C</b>) Left: Gag-specific CD4+ T cells (CD154-positive, cytokine-positive) shown as red contour plots are overlaid onto 2 dimensional density plots for CM cells CD4 T cells plotted against CCR7 and CD3, and CXCR5 and CCR6. Right: Bar graphs showing the frequency of Gag-specific CD154-positive, cytokine-positive cells that express CCR7, CXCR5 and CCR6 (n = 14). *p<0.05.</p>", "links"=>[], "tags"=>["immunology", "Immune cells", "Antibody-producing cells", "b cells", "t cells", "Immune system", "cytokines", "immunoglobulins", "Infectious diseases", "Viral diseases", "hiv", "Retrovirology and HIV immunopathogenesis", "cells"], "article_id"=>920056, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Kristin L. Boswell", "Robert Paris", "Eli Boritz", "David Ambrozak", "Takuya Yamamoto", "Sam Darko", "Kaska Wloka", "Adam Wheatley", "Sandeep Narpala", "Adrian McDermott", "Mario Roederer", "Richard Haubrich", "Mark Connors", "Julie Ake", "Daniel C. Douek", "Jerome Kim", "Constantinos Petrovas", "Richard A. Koup"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003853.g004", "stats"=>{"downloads"=>2, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Functional_characteristics_of_pT_FH_cells_and_the_impact_of_HIV_/920056", "title"=>"Functional characteristics of pT<sub>FH</sub> cells and the impact of HIV.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 04:38:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1369101"], "description"=>"<p>(<b>A</b>) Correlative analysis showing the frequency (%) of CXCR5<sup>high</sup>, CXCR5<sup>high</sup>CCR6<sup>high</sup> and CXCR5<sup>high</sup>CCR6<sup>high</sup>PD-1<sup>high</sup> populations in total CD4 cells from HIV-infected (treatment naïve) subjects (n = 50) versus the frequency of IgG+ B cells in the total B population. Correlations were analyzed using the nonparametric Spearman test. (<b>B</b>) Pooled data showing the frequency (%) of CXCR5<sup>high</sup>, CXCR5<sup>high</sup>CCR6<sup>high</sup> and CXCR5<sup>high</sup>CCR6<sup>high</sup>PD-1<sup>high</sup> populations in total CD4 cells based on neutralization activity (median ID50>100 or <100). No significant differences were determined.</p>", "links"=>[], "tags"=>["immunology", "Immune cells", "Antibody-producing cells", "b cells", "t cells", "Immune system", "cytokines", "immunoglobulins", "Infectious diseases", "Viral diseases", "hiv", "Retrovirology and HIV immunopathogenesis", "cells", "neutralization"], "article_id"=>920058, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Kristin L. Boswell", "Robert Paris", "Eli Boritz", "David Ambrozak", "Takuya Yamamoto", "Sam Darko", "Kaska Wloka", "Adam Wheatley", "Sandeep Narpala", "Adrian McDermott", "Mario Roederer", "Richard Haubrich", "Mark Connors", "Julie Ake", "Daniel C. Douek", "Jerome Kim", "Constantinos Petrovas", "Richard A. Koup"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003853.g005", "stats"=>{"downloads"=>4, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relationship_between_pT_FH_cells_and_neutralization_activity_/920058", "title"=>"Relationship between pT<sub>FH</sub> cells and neutralization activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 04:38:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1369102"], "description"=>"<p>(<b>A</b>) Representative flow cytometry plots from HIV-uninfected, pediatric tonsils showing the gating scheme for determining the frequency of CCR6<sup>high</sup> cells in T<sub>FH</sub> (CXCR5<sup>high</sup>PD-1<sup>high</sup>) and non-T<sub>FH</sub> populations. (<b>B</b>) Bar graphs showing the frequency of CCR6<sup>high</sup> cells in T<sub>FH</sub> and non-T<sub>FH</sub> populations in human tonsils (n = 5). (<b>C</b>) Heatmap analysis of selected genes from RNA-seq data comparing pT<sub>FH</sub> cells (CXCR5<sup>high</sup>CCR6<sup>high</sup>PD-1<sup>high</sup>) from HIV-uninfected donors, pT<sub>FH</sub> cells from HIV-infected donors, non-T<sub>FH</sub> CD4 memory tonsil cells (CM CD57<sup>low</sup>PD-1<sup>dim</sup>CCR7<sup>high</sup>CCR5<sup>low</sup>CXCR4<sup>low</sup>), non-germinal center T<sub>FH</sub> tonsil cells (CM CD57<sup>low</sup>PD-1<sup>high</sup>CCR7<sup>low</sup>CXCR5<sup>high</sup>) and germinal center T<sub>FH</sub> tonsil cells (CM PD-1<sup>high</sup>CD57<sup>high</sup>) from HIV-uninfected donors. (<b>D</b>) Top: Comparison of MAF expression on CD4 T cells from blood or tonsil. Bottom: Geometric mean (MFI) of MAF expression in the indicated populations of central memory CD4 T cells normalized to MAF MFI in naïve CD4 T cells.</p>", "links"=>[], "tags"=>["immunology", "Immune cells", "Antibody-producing cells", "b cells", "t cells", "Immune system", "cytokines", "immunoglobulins", "Infectious diseases", "Viral diseases", "hiv", "Retrovirology and HIV immunopathogenesis", "cells"], "article_id"=>920059, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Kristin L. Boswell", "Robert Paris", "Eli Boritz", "David Ambrozak", "Takuya Yamamoto", "Sam Darko", "Kaska Wloka", "Adam Wheatley", "Sandeep Narpala", "Adrian McDermott", "Mario Roederer", "Richard Haubrich", "Mark Connors", "Julie Ake", "Daniel C. Douek", "Jerome Kim", "Constantinos Petrovas", "Richard A. Koup"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003853.g006", "stats"=>{"downloads"=>4, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relationship_between_pT_FH_cells_and_T_FH_cells_in_human_tonsil_/920059", "title"=>"Relationship between pT<sub>FH</sub> cells and T<sub>FH</sub> cells in human tonsil.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 04:38:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1369090"], "description"=>"<p>(<b>A</b>) Left: Representative flow cytometry plots from HIV-uninfected PBMC showing the gating scheme for isolating T cell subsets for the T cell/B cell coculture assay. Isolated populations include naïve cells (brown), CM CCR7<sup>low</sup> (pink), CM CCR7<sup>high</sup>CXCR5<sup>low</sup> (orange), CM CCR7<sup>high</sup>CXCR5<sup>high</sup>CCR6<sup>low</sup>PD-1<sup>high</sup> (green), CM CCR7<sup>high</sup>CXCR5<sup>high</sup>CCR6<sup>high</sup>PD-1<sup>low</sup> (blue) and CCR7<sup>high</sup>CXCR5<sup>high</sup>CCR6<sup>high</sup>PD-1<sup>high</sup> (red). Before gating on CCR6 and PD-1, cells were first gated on CD150<sup>high</sup>. Right: Scatter plot indicating the frequency of each population in HIV-uninfected subjects (<i>n</i> = 13). Cells were not gated on CD150 for phenotypic analysis. (<b>B</b>) Indicated CD4 T cell populations were cultured with autologous naïve B cells (CD19<sup>high</sup>CD27<sup>low</sup>IgD<sup>−</sup>) in the presence of SEB for 12 days and Ig concentrations were measured from supernatants (n = 6). (<b>C</b>) Indicated CD4 T cell populations were cultured with autologous naïve B cells in the presence of SEB for 2 days and cytokine concentrations were measured from supernatants (n = 6). Horizontal lines indicate limit of detection. Significant differences were determined using the Friedman test with Dunn's multiple comparison post-test. *p<0.05; **p<0.01.</p>", "links"=>[], "tags"=>["immunology", "Immune cells", "Antibody-producing cells", "b cells", "t cells", "Immune system", "cytokines", "immunoglobulins", "Infectious diseases", "Viral diseases", "hiv", "Retrovirology and HIV immunopathogenesis", "peripheral"], "article_id"=>920047, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Kristin L. Boswell", "Robert Paris", "Eli Boritz", "David Ambrozak", "Takuya Yamamoto", "Sam Darko", "Kaska Wloka", "Adam Wheatley", "Sandeep Narpala", "Adrian McDermott", "Mario Roederer", "Richard Haubrich", "Mark Connors", "Julie Ake", "Daniel C. Douek", "Jerome Kim", "Constantinos Petrovas", "Richard A. Koup"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003853.g001", "stats"=>{"downloads"=>5, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characterization_of_peripheral_T_FH_cells_/920047", "title"=>"Characterization of peripheral T<sub>FH</sub> cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 04:38:04"}

PMC Usage Stats | Further Information

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