The HIV-1 Gp120/CXCR4 Axis Promotes CCR7 Ligand-Dependent CD4 T Cell Migration: CCR7 Homo- and CCR7/CXCR4 Hetero-Oligomer Formation as a Possible Mechanism for Up-Regulation of Functional CCR7
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{"title"=>"The HIV-1 Gp120/CXCR4 axis promotes CCR7 ligand-dependent CD4 T cell migration: CCR7 homo- and CCR7/CXCR4 hetero-oligomer formation as a possible mechanism for up-regulation of functional CCR7", "type"=>"journal", "authors"=>[{"first_name"=>"Haruko", "last_name"=>"Hayasaka", "scopus_author_id"=>"8580540200"}, {"first_name"=>"Daichi", "last_name"=>"Kobayashi", "scopus_author_id"=>"56622336200"}, {"first_name"=>"Hiromi", "last_name"=>"Yoshimura", "scopus_author_id"=>"56622191500"}, {"first_name"=>"Emi E.", "last_name"=>"Nakayama", "scopus_author_id"=>"7102521865"}, {"first_name"=>"Tatsuo", "last_name"=>"Shioda", "scopus_author_id"=>"7005173240"}, {"first_name"=>"Masayuki", "last_name"=>"Miyasaka", "scopus_author_id"=>"8051660500"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"604166183", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0117454", "scopus"=>"2-s2.0-84928911094", "pmid"=>"25688986", "sgr"=>"84928911094"}, "id"=>"6b3ab058-3739-30ff-87a1-d09587f32f4f", "abstract"=>"During human immunodeficiency virus (HIV) infection, enhanced migration of infected cells to lymph nodes leads to efficient propagation of HIV-1. The selective chemokine receptors, including CXCR4 and CCR7, may play a role in this process, yet the viral factors regulating chemokine-dependent T cell migration remain relatively unclear. The functional cooperation between the CXCR4 ligand chemokine CXCL12 and the CCR7 ligand chemokines CCL19 and CCL21 enhances CCR7-dependent T cell motility in vitro as well as cell trafficking into the lymph nodes in vivo. In this study, we report that a recombinant form of a viral CXCR4 ligand, X4-tropic HIV-1 gp120, enhanced the CD4 T cell response to CCR7 ligands in a manner dependent on CXCR4 and CD4, and that this effect was recapitulated by HIV-1 virions. HIV-1 gp120 significantly enhanced CCR7-dependent CD4 T cell migration from the footpad of mice to the draining lymph nodes in in vivo transfer experiments. We also demonstrated that CXCR4 expression is required for stable CCR7 expression on the CD4 T cell surface, whereas CXCR4 signaling facilitated CCR7 ligand binding to the cell surface and increased the level of CCR7 homo- as well as CXCR4/CCR7 hetero-oligomers without affecting CCR7 expression levels. Our findings indicate that HIV-evoked CXCR4 signaling promotes CCR7-dependent CD4 T cell migration by up-regulating CCR7 function, which is likely to be induced by increased formation of CCR7 homo- and CXCR4/CCR7 hetero-oligomers on the surface of CD4 T cells.", "link"=>"http://www.mendeley.com/research/hiv1-gp120cxcr4-axis-promotes-ccr7-liganddependent-cd4-t-cell-migration-ccr7-homo-ccr7cxcr4-heterool", "reader_count"=>10, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>2, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>2, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>2, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>2, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>4, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>3, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>4}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Sweden"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1909110"], "description"=>"<p>(A) Human CD4 T cells were incubated for 30 min at room temperature with the culture supernatant containing the recombinant HIV-1<sub>NL4-3</sub>-derived gp120 (50 μg/ml, 420 nM) or a control solution, and chemotaxis in response to CCL21 was analyzed on a time-lapse video microscope. The number of cells in the fixed window, which was located in the assay field two-thirds away from the starting point of cell migration, was plotted against time after CCL21 injection. The result shown is a representative result of three independent experiments. (B) Quantification of the CCL21-induced CD4 T cell chemotaxis shown in panel A. The total number of migrated cells was calculated by summing the individual cell counts. The relative chemotaxis index represents the ratio of the number of migrated cells in the test treatment to that in control treatments (control solution in the presence of CCL21). Data represent means ± SEM of three independent experiments. *, p < 0.05 **, p < 0.01. (C) Human CD4 T cells (1 × 10<sup>5</sup>) were mixed with the purified gp120 or control elution buffer and added to the upper wells of the transwell plate. The number of migrated cells in response to CCL21, which was added to the lower wells of the transwell plate, was analyzed. Graphs represent means ± SD percentage of input cells from triplicate wells. *, p < 0.05 ***, p < 0.001 by the Student’s <i>t</i>-test.</p>", "links"=>[], "tags"=>["CD 4 T cells", "CD 4 T cell surface", "CXCR 4", "CCR 7 ligands", "CCR 7 ligand chemokines CCL 19", "CCR 7 Homo", "CXCR 4 ligand", "CCR 7 expression", "lymph nodes", "CXCR 4 expression", "CXCR 4 ligand chemokine CXCL 12", "CD 4 T cell response", "hiv", "Functional CCR 7", "vivo transfer experiments", "CCR 7 expression levels", "CCR 7 ligand binding"], "article_id"=>1311125, "categories"=>["Biological Sciences"], "users"=>["Haruko Hayasaka", "Daichi Kobayashi", "Hiromi Yoshimura", "Emi E. Nakayama", "Tatsuo Shioda", "Masayuki Miyasaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117454.g001", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIV_1_NL4_3_derived_gp120_promoted_CCL21_induced_CD4_T_cell_chemotaxis_/1311125", "title"=>"HIV-1<sub>NL4-3</sub>-derived gp120 promoted CCL21-induced CD4 T cell chemotaxis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-17 03:31:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1909111"], "description"=>"<p>(A) Human CD4 T cells were incubated for 30 min at room temperature with the culture supernatant containing recombinant gp120 (50 μg/ml) or a control solution, and chemotaxis in response to CCL21 was analyzed on a time-lapse video microscope. The total number of migrated cells was calculated by summing the individual cell counts. The assay was performed in the presence of a neutralizing anti-CCR7 antibody or control IgG (25 μg/ml). The relative chemotaxis index represents the ratio of the number of migrated cells in the test treatment to that in control treatments (control solution and control IgG). Data represent means ± SEM of three independent experiments. *, p < 0.05 by the Student’s <i>t</i>-test. (B) The assay described above was performed in the presence of a neutralizing anti-CXCR4 antibody or control IgG. The relative chemotaxis index represents the ratio of the number of migrated cells in the test treatment to that in control treatments (control solution and control IgG).</p>", "links"=>[], "tags"=>["CD 4 T cells", "CD 4 T cell surface", "CXCR 4", "CCR 7 ligands", "CCR 7 ligand chemokines CCL 19", "CCR 7 Homo", "CXCR 4 ligand", "CCR 7 expression", "lymph nodes", "CXCR 4 expression", "CXCR 4 ligand chemokine CXCL 12", "CD 4 T cell response", "hiv", "Functional CCR 7", "vivo transfer experiments", "CCR 7 expression levels", "CCR 7 ligand binding"], "article_id"=>1311126, "categories"=>["Biological Sciences"], "users"=>["Haruko Hayasaka", "Daichi Kobayashi", "Hiromi Yoshimura", "Emi E. Nakayama", "Tatsuo Shioda", "Masayuki Miyasaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117454.g002", "stats"=>{"downloads"=>1, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_effect_of_gp120_on_CCL21_induced_chemotaxis_was_dependent_on_CCR7_and_CXCR4_/1311126", "title"=>"The effect of gp120 on CCL21-induced chemotaxis was dependent on CCR7 and CXCR4.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-17 03:31:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1909112"], "description"=>"<p>(A) CCR7 ligand-induced H9 cell migration after treatment with 1 μg/ml recombinant gp120 (filled symbols) or control buffer (open triangles) was examined on a time-lapse video microscope. CCL19-induced cell migration in H9 cells was examined in the presence of AMD3100 (25 μg/ml, filled squares), sCD4 (3 μg/ml, filled circles), or vehicle (filled triangles). The result shown is a representative result of three independent experiments. (B) CCR7 ligand-induced cell migration in the presence of a neutralizing anti-CXCR4 antibody, sCD4, or control IgG in H9 cells after treatment with 1 μg/ml recombinant gp120 (black bars) or control buffer (open bars). CCL21-induced cell migration was examined by a time-lapse video microscope, and the total number of migrated cells was calculated. The relative chemotaxis index represents the ratio of the number of migrated cells in the test treatment to that in control treatments (control solution in the presence of IgG). Data represent means ± SEM of three independent experiments. *, p < 0.05 by the Student’s <i>t</i>-test.</p>", "links"=>[], "tags"=>["CD 4 T cells", "CD 4 T cell surface", "CXCR 4", "CCR 7 ligands", "CCR 7 ligand chemokines CCL 19", "CCR 7 Homo", "CXCR 4 ligand", "CCR 7 expression", "lymph nodes", "CXCR 4 expression", "CXCR 4 ligand chemokine CXCL 12", "CD 4 T cell response", "hiv", "Functional CCR 7", "vivo transfer experiments", "CCR 7 expression levels", "CCR 7 ligand binding"], "article_id"=>1311127, "categories"=>["Biological Sciences"], "users"=>["Haruko Hayasaka", "Daichi Kobayashi", "Hiromi Yoshimura", "Emi E. Nakayama", "Tatsuo Shioda", "Masayuki Miyasaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117454.g003", "stats"=>{"downloads"=>5, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIV_1_gp120_acted_on_CXCR4_and_CD4_to_promote_CCR7_dependent_human_CD4_T_cell_migration_/1311127", "title"=>"HIV-1 gp120 acted on CXCR4 and CD4 to promote CCR7-dependent human CD4 T cell migration.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-17 03:31:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1909113"], "description"=>"<p>(A) A CCR7 ligand-induced cell migration assay was performed using H9 cells (5 × 10<sup>4</sup>) pre-treated with or without AT-2-inactivated HIV-1 virions (final concentration corresponding to 10 μg/ml p24) or control supernatant for 15 min. The number of migrated cells in response to CCL21 added to the lower wells of the transwell plate was analyzed. Graphs represent means ± SD percentage of input cells from triplicate wells. *, p < 0.05 by the Student’s <i>t</i>-test. The result shown is a representative result of three independent experiments. (B) The time-lapse cell migration assay was performed in the presence of a neutralizing anti-CXCR4 antibody or control IgG. The relative chemotaxis index represents the ratio of the number of migrated cells in the test treatment to that in control treatments (control AT-2-treated mock supernatant in the presence of IgG). Data represent means ± SEM of three independent experiments. *, p < 0.05 by the Student’s <i>t</i>-test. (C) CCR7 ligand-induced H9 cell migration after treatment with AT-2-inactivated wild-type (WT) HIV-1 (filled triangles), gp120-deficient HIV-1 virions (filled squares) or control mock supernatant (open triangles). CCL19-induced cell migration was examined on a time-lapse video microscope. The result shown is a representative result of three independent experiments. (D) CCR7 ligand-induced H9 cell migration after treatment with AT-2-inactivated HIV-1 virions (filled symbols) or control supernatant (open triangles) in the presence of a neutralizing anti-gp120 antibody (50 μg/ml, filled squares) or control IgG (filled triangles). CCL21-induced cell migration was analyzed on a time-lapse video microscope. The result shown is a representative result of three independent experiments.</p>", "links"=>[], "tags"=>["CD 4 T cells", "CD 4 T cell surface", "CXCR 4", "CCR 7 ligands", "CCR 7 ligand chemokines CCL 19", "CCR 7 Homo", "CXCR 4 ligand", "CCR 7 expression", "lymph nodes", "CXCR 4 expression", "CXCR 4 ligand chemokine CXCL 12", "CD 4 T cell response", "hiv", "Functional CCR 7", "vivo transfer experiments", "CCR 7 expression levels", "CCR 7 ligand binding"], "article_id"=>1311128, "categories"=>["Biological Sciences"], "users"=>["Haruko Hayasaka", "Daichi Kobayashi", "Hiromi Yoshimura", "Emi E. Nakayama", "Tatsuo Shioda", "Masayuki Miyasaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117454.g004", "stats"=>{"downloads"=>3, "page_views"=>98, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIV_1_virions_enhanced_CCL21_induced_CD4_T_cell_chemotaxis_/1311128", "title"=>"HIV-1 virions enhanced CCL21-induced CD4 T cell chemotaxis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-17 03:31:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1909123"], "description"=>"<p>(A) CFSE-labeled human CD4 T cells (5 × 10<sup>6</sup>) were injected into the footpads of C57BL/6 WT mice. A sham operation (PBS injection) was performed on the contralateral side. Popliteal lymph nodes (pLNs) were harvested from the recipient mice at 2 h, 5 h, and 15 h after the transfer. (B) CFSE-labeled human CD4 T cells (5 × 10<sup>6</sup>) were injected into the footpads of C57BL/6 WT mice or <i>plt/plt</i> mice. pLNs were harvested from the recipient mice at 15 h after cell transfer. The images of pLNs were analyzed by fluorescence confocal microscopy (original magnification ×100). Scale bar, 250 μm. (C) CFSE-labeled human CD4 T cells (5 × 10<sup>6</sup>) were pretreated with purified gp120 (40 μg/ml) or control elution buffer, and injected into each side of C57BL/6 mouse footpad. pLNs were harvested from recipient mice at 5, 15, and 24 h after the transfer and analyzed by confocal microscopy (TCS SP5; Leica). Representative images of pLNs obtained from 11 recipient mice subjected to CD4 T cell injection are shown. (D) The images obtained from individual mice (n = 11) at 5 h after the transfer were analyzed and the total numbers of migrated cells per 5 × 10<sup>6</sup> cells in a recipient mouse tissue was quantified using ImageJ software (NIH). *, p < 0.05 by the Wilcoxon signed-rank test.</p>", "links"=>[], "tags"=>["CD 4 T cells", "CD 4 T cell surface", "CXCR 4", "CCR 7 ligands", "CCR 7 ligand chemokines CCL 19", "CCR 7 Homo", "CXCR 4 ligand", "CCR 7 expression", "lymph nodes", "CXCR 4 expression", "CXCR 4 ligand chemokine CXCL 12", "CD 4 T cell response", "hiv", "Functional CCR 7", "vivo transfer experiments", "CCR 7 expression levels", "CCR 7 ligand binding"], "article_id"=>1311130, "categories"=>["Biological Sciences"], "users"=>["Haruko Hayasaka", "Daichi Kobayashi", "Hiromi Yoshimura", "Emi E. Nakayama", "Tatsuo Shioda", "Masayuki Miyasaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117454.g005", "stats"=>{"downloads"=>4, "page_views"=>33, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIV_1_gp120_promoted_CCR7_dependent_CD4_T_cell_trafficking_to_the_popliteal_lymph_nodes_/1311130", "title"=>"HIV-1 gp120 promoted CCR7-dependent CD4 T cell trafficking to the popliteal lymph nodes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-17 03:31:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1909126"], "description"=>"<p>(A) The cell surface expression levels of CXCR4 and CCR1 were evaluated by flow cytometry using anti-CXCR4 (left) or anti-CCR1 (right) antibodies in control or CXCR4 siRNA-treated H9 cells. Mean fluorescence intensity is indicated on the histograms. (B) The cell surface CCR7 expression was evaluated by flow cytometry using anti-CCR7 antibody. H9 cells treated with control, CXCR4, or CCR7 siRNAs were analyzed (left). The total cellular CCR7 and CCR1 expression levels in control, CXCR4, or CCR7 siRNA-treated H9 cells were analyzed by Western blotting. Anti-β actin mAb was used to confirm equal loading (right). (C) The <i>CCR7</i> mRNA expression levels were analyzed in control, CXCR4, or CCR7 siRNA-treated H9 cells by quantitative RT-PCR. (D) The cell surface CCR7 expression levels were analyzed in gp120-treated human CD4 T cells (upper panel), and CXCL12-treated H9 cells (lower panel) by flow cytometry. (E) The CCR7 ligand-binding abilities in H9 cells pretreated with a native (N) or control, heat-denatured gp120 (D), or with (+) or without (−) 100 ng/ml CXCL12 were examined by CCL19-Ig binding. A minimum of three images per section was observed by confocal microscopy, and the relative fluorescence signal or the percentage of CCL19-Ig bound cells was quantified using Duolink Image Tool software. The images of CCL19-bound cells with or without CXCL12 pretreatment are shown in the right panel (indicated by white triangles). *, p < 0.05, Student’s <i>t</i>-test.</p>", "links"=>[], "tags"=>["CD 4 T cells", "CD 4 T cell surface", "CXCR 4", "CCR 7 ligands", "CCR 7 ligand chemokines CCL 19", "CCR 7 Homo", "CXCR 4 ligand", "CCR 7 expression", "lymph nodes", "CXCR 4 expression", "CXCR 4 ligand chemokine CXCL 12", "CD 4 T cell response", "hiv", "Functional CCR 7", "vivo transfer experiments", "CCR 7 expression levels", "CCR 7 ligand binding"], "article_id"=>1311131, "categories"=>["Biological Sciences"], "users"=>["Haruko Hayasaka", "Daichi Kobayashi", "Hiromi Yoshimura", "Emi E. Nakayama", "Tatsuo Shioda", "Masayuki Miyasaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117454.g006", "stats"=>{"downloads"=>3, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CXCR4_is_required_for_stable_CCR7_expression_CCR7_ligand_binding_and_CCR7_homo_oligomer_formation_/1311131", "title"=>"CXCR4 is required for stable CCR7 expression, CCR7 ligand binding, and CCR7 homo-oligomer formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-17 03:31:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1909127"], "description"=>"<p>(A) CCR7 homo-oligomer formation in H9 cells after treatment with or without 1 μg/ml recombinant gp120 was examined by <i>in situ</i> PLA. The number of <i>in situ</i> PLA signals per cell was counted by using the Duolink Image Tool software. The result shown is a representative result from three independent experiments showing the mean number of the signals plotted on the vertical axis. *, p < 0.05 by Mann-Whitney’s U test. (B) CCR7 homo-oligomer formation in H9 cells after treatment with 100 ng/ml CXCL12 was examined, as described in (A). Quantification of CCR7 homo-oligomers after CXCL12 pretreatment in the presence or absence of 1 or 5 μg/ml AMD3100. The result shown is a representative result from five independent experiments. *, p < 0.05 by Mann-Whitney’s U test. (C) CXCR4/CCR7 or CXCR4/CCR1 hetero-oligomer formation in H9 cells by <i>in situ</i> PLA using the indicated combinations of antibodies. The z-stack images derived from sections covering 10 μm with a 0.5-μm step are shown. Scale bar represents 50 μm. (D) Quantification of the detected <i>in situ</i> PLA signals per cell was performed. The result shown is a representative result from three independent experiments. *, p < 0.05 by Mann-Whitney’s U test. (E) CXCR4/CCR7 hetero-oligomer formation in H9 cells after treatment with 1 μg/ml gp120 in a native form (N) or control heat-denatured form (D) was examined by the PLA using the indicated combinations of antibodies. (F) CXCR4/CCR7 hetero-oligomer formation was examined with 100 ng/ml CXCL12 as described in (E).</p>", "links"=>[], "tags"=>["CD 4 T cells", "CD 4 T cell surface", "CXCR 4", "CCR 7 ligands", "CCR 7 ligand chemokines CCL 19", "CCR 7 Homo", "CXCR 4 ligand", "CCR 7 expression", "lymph nodes", "CXCR 4 expression", "CXCR 4 ligand chemokine CXCL 12", "CD 4 T cell response", "hiv", "Functional CCR 7", "vivo transfer experiments", "CCR 7 expression levels", "CCR 7 ligand binding"], "article_id"=>1311132, "categories"=>["Biological Sciences"], "users"=>["Haruko Hayasaka", "Daichi Kobayashi", "Hiromi Yoshimura", "Emi E. Nakayama", "Tatsuo Shioda", "Masayuki Miyasaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117454.g007", "stats"=>{"downloads"=>4, "page_views"=>34, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CXCR4_ligand_binding_facilitates_CXCR4_CCR7_hetero_oligomer_formation_/1311132", "title"=>"CXCR4 ligand binding facilitates CXCR4/CCR7 hetero-oligomer formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-17 03:31:46"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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