Intraperitoneal Administration of a Tumor-Associated Antigen SART3, CD40L, and GM-CSF Gene-Loaded Polyplex Micelle Elicits a Vaccine Effect in Mouse Tumor Models
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{"title"=>"Intraperitoneal administration of a tumor-associated antigen SART3, CD40L, and GM-CSF gene-loaded polyplex micelle elicits a vaccine effect in mouse tumor models", "type"=>"journal", "authors"=>[{"first_name"=>"Kouichi", "last_name"=>"Furugaki", "scopus_author_id"=>"6602441604"}, {"first_name"=>"Lin", "last_name"=>"Cui", "scopus_author_id"=>"26649381000"}, {"first_name"=>"Yumi", "last_name"=>"Kunisawa", "scopus_author_id"=>"36839345700"}, {"first_name"=>"Kensuke", "last_name"=>"Osada", "scopus_author_id"=>"7101855885"}, {"first_name"=>"Kentaro", "last_name"=>"Shinkai", "scopus_author_id"=>"55550655300"}, {"first_name"=>"Masao", "last_name"=>"Tanaka", "scopus_author_id"=>"55628572213"}, {"first_name"=>"Kazunori", "last_name"=>"Kataoka", "scopus_author_id"=>"35448581000"}, {"first_name"=>"Kenji", "last_name"=>"Nakano", "scopus_author_id"=>"7402011326"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84904154803", "sgr"=>"84904154803", "pui"=>"373518459", "pmid"=>"25013909", "doi"=>"10.1371/journal.pone.0101854"}, "id"=>"6d431668-eff2-3877-acd3-13413595564f", "abstract"=>"Polyplex micelles have demonstrated biocompatibility and achieve efficient gene transfection in vivo. Here, we investigated a polyplex micelle encapsulating genes encoding the tumor-associated antigen squamous cell carcinoma antigen recognized by T cells-3 (SART3), adjuvant CD40L, and granulocyte macrophage colony-stimulating factor (GM-CSF) as a DNA vaccine platform in mouse tumor models with different types of major histocompatibility antigen complex (MHC). Intraperitoneally administrated polyplex micelles were predominantly found in the lymph nodes, spleen, and liver. Compared with mock controls, the triple gene vaccine significantly prolonged the survival of mice harboring peritoneal dissemination of CT26 colorectal cancer cells, of which long-term surviving mice showed complete rejection when re-challenged with CT26 tumors. Moreover, the DNA vaccine inhibited the growth and metastasis of subcutaneous CT26 and Lewis lung tumors in BALB/c and C57BL/6 mice, respectively, which represent different MHC haplotypes. The DNA vaccine highly stimulated both cytotoxic T lymphocyte and natural killer cell activities, and increased the infiltration of CD11c+ DCs and CD4+/CD8a+ T cells into tumors. Depletion of CD4+ or CD8a+ T cells by neutralizing antibodies deteriorated the anti-tumor efficacy of the DNA vaccine. In conclusion, a SART3/CD40L+GM-CSF gene-loaded polyplex micelle can be applied as a novel vaccine platform to elicit tumor rejection immunity regardless of the recipient MHC haplotype.", "link"=>"http://www.mendeley.com/research/intraperitoneal-administration-tumorassociated-antigen-sart3-cd40l-gmcsf-geneloaded-polyplex-micelle", "reader_count"=>20, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>4, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>4, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>5, "Materials Science"=>1, "Medicine and Dentistry"=>5, "Agricultural and Biological Sciences"=>3, "Chemical Engineering"=>1, "Chemistry"=>4}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Chemistry"=>{"Chemistry"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1589391"], "description"=>"<p>(A) Tissue sections of subcutaneous CT26 tumors after administration of polyplex micelles were immunostained with anti-CD4 or CD8a antibodies. CD4<sup>+</sup> and CD8a<sup>+</sup> T cells were highly infiltrated into tumors of the SART3/CD40L+GM-CSF vaccine group compared with that in the mock control. *<i>P<</i>0.05 (n = 4). (B) Depletion of CD4<sup>+</sup> and/or CD8a<sup>+</sup> T cells by i.p. administration of their neutralizing antibodies was confirmed by flow cytometric analysis of blood samples. (C) Kaplan-Meier analysis showed that depletion of CD4<sup>+</sup> or CD8a<sup>+</sup> T cells decreased the survival of the SART3/CD40L+GM-CSF vaccine group compared with that that of the isotype IgG2 control (<i>P</i> = 0.084 and 0.003, respectively, n = 7−8) in mice with peritoneal dissemination of CT26 cells.</p>", "links"=>[], "tags"=>["immunology", "Clinical immunology", "immunotherapy", "molecular biology", "Molecular biology techniques", "Gene therapy", "oncology", "Basic cancer research", "Cancer treatment", "Surgical and invasive medical procedures", "Model organisms", "Animal models", "Mouse models", "numbers", "tumors", "vaccination", "depletion", "deteriorates", "anti-tumor"], "article_id"=>1100737, "categories"=>["Biological Sciences"], "users"=>["Kouichi Furugaki", "Lin Cui", "Yumi Kunisawa", "Kensuke Osada", "Kentaro Shinkai", "Masao Tanaka", "Kazunori Kataoka", "Kenji Nakano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0101854.g006", "stats"=>{"downloads"=>4, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CD4_CD8a_cell_numbers_increase_in_tumors_by_SART3_CD40L_GM_CSF_vaccination_and_depletion_deteriorates_the_anti_tumor_efficacy_/1100737", "title"=>"CD4<sup>+</sup>/CD8a<sup>+</sup> cell numbers increase in tumors by SART3/CD40L+GM-CSF vaccination and depletion deteriorates the anti-tumor efficacy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-11 02:57:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1589397"], "description"=>"<p>SART3: squamous cell carcinoma antigen recognized by T cells 3; GM-CSF: granulocyte macrophage colony-stimulating factor. *<i>P</i><0.05, **<i>P</i><0.01, and <sup>†</sup><i>P</i><0.0001 vs. Mock control.</p>", "links"=>[], "tags"=>["immunology", "Clinical immunology", "immunotherapy", "molecular biology", "Molecular biology techniques", "Gene therapy", "oncology", "Basic cancer research", "Cancer treatment", "Surgical and invasive medical procedures", "Model organisms", "Animal models", "Mouse models", "genes", "encapsulated", "polyplex", "micelles", "periods", "mice", "peritoneal", "dissemination", "ct26"], "article_id"=>1100738, "categories"=>["Biological Sciences"], "users"=>["Kouichi Furugaki", "Lin Cui", "Yumi Kunisawa", "Kensuke Osada", "Kentaro Shinkai", "Masao Tanaka", "Kazunori Kataoka", "Kenji Nakano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0101854.t001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Therapeutic_genes_encapsulated_by_polyplex_micelles_and_the_survival_periods_of_mice_with_peritoneal_dissemination_of_CT26_tumors_/1100738", "title"=>"Therapeutic genes encapsulated by polyplex micelles and the survival periods of mice with peritoneal dissemination of CT26 tumors.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-07-11 02:57:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1589401", "https://ndownloader.figshare.com/files/1589402", "https://ndownloader.figshare.com/files/1589403", "https://ndownloader.figshare.com/files/1589404"], "description"=>"<div><p>Polyplex micelles have demonstrated biocompatibility and achieve efficient gene transfection <i>in vivo</i>. Here, we investigated a polyplex micelle encapsulating genes encoding the tumor-associated antigen squamous cell carcinoma antigen recognized by T cells-3 (SART3), adjuvant CD40L, and granulocyte macrophage colony-stimulating factor (GM-CSF) as a DNA vaccine platform in mouse tumor models with different types of major histocompatibility antigen complex (MHC). Intraperitoneally administrated polyplex micelles were predominantly found in the lymph nodes, spleen, and liver. Compared with mock controls, the triple gene vaccine significantly prolonged the survival of mice harboring peritoneal dissemination of CT26 colorectal cancer cells, of which long-term surviving mice showed complete rejection when re-challenged with CT26 tumors. Moreover, the DNA vaccine inhibited the growth and metastasis of subcutaneous CT26 and Lewis lung tumors in BALB/c and C57BL/6 mice, respectively, which represent different MHC haplotypes. The DNA vaccine highly stimulated both cytotoxic T lymphocyte and natural killer cell activities, and increased the infiltration of CD11c<sup>+</sup> DCs and CD4<sup>+</sup>/CD8a<sup>+</sup> T cells into tumors. Depletion of CD4<sup>+</sup> or CD8a<sup>+</sup> T cells by neutralizing antibodies deteriorated the anti-tumor efficacy of the DNA vaccine. In conclusion, a SART3/CD40L+GM-CSF gene-loaded polyplex micelle can be applied as a novel vaccine platform to elicit tumor rejection immunity regardless of the recipient MHC haplotype.</p></div>", "links"=>[], "tags"=>["immunology", "Clinical immunology", "immunotherapy", "molecular biology", "Molecular biology techniques", "Gene therapy", "oncology", "Basic cancer research", "Cancer treatment", "Surgical and invasive medical procedures", "Model organisms", "Animal models", "Mouse models", "tumor-associated", "antigen", "gm-csf", "gene-loaded", "polyplex", "micelle", "elicits"], "article_id"=>1100741, "categories"=>["Biological Sciences"], "users"=>["Kouichi Furugaki", "Lin Cui", "Yumi Kunisawa", "Kensuke Osada", "Kentaro Shinkai", "Masao Tanaka", "Kazunori Kataoka", "Kenji Nakano"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0101854.s001", "https://dx.doi.org/10.1371/journal.pone.0101854.s002", "https://dx.doi.org/10.1371/journal.pone.0101854.s003", "https://dx.doi.org/10.1371/journal.pone.0101854.s004"], "stats"=>{"downloads"=>3, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Intraperitoneal_Administration_of_a_Tumor_Associated_Antigen_SART3_CD40L_and_GM_CSF_Gene_Loaded_Polyplex_Micelle_Elicits_a_Vaccine_Effect_in_Mouse_Tumor_Models_/1100741", "title"=>"Intraperitoneal Administration of a Tumor-Associated Antigen SART3, CD40L, and GM-CSF Gene-Loaded Polyplex Micelle Elicits a Vaccine Effect in Mouse Tumor Models", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-07-11 02:57:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1589362"], "description"=>"<p>Fluolid orange-labeled polyplex micelles with the GM-CSF gene (50 µg; N/P ratio  = 10) were administered to the peritoneal cavity of mice. (A) Polyplex micelles were mainly localized in the spleen, lymph nodes, and liver. The merged image (yellow) shows co-localization of polyplex micelles (orange) and CD11c<sup>+</sup> DCs (green). DAPI nuclear staining (blue). RP: red pulp of spleen; WP: white pulp of spleen. (B) Total RNA was extracted from frozen tissues after i.p. administration, followed by real-time RT-PCR analysis of GM-CSF gene expression. The gene expression of GM-CSF was up-regulated by several-hundred fold compared with that in the mock control (relative expression  = 1) in lymph nodes, spleen, and liver, and minimally in the lungs and kidney (n = 4 each). *<i>P</i><0.05; †<i>P</i><0.001. Scale Bar  = 200 µm.</p>", "links"=>[], "tags"=>["immunology", "Clinical immunology", "immunotherapy", "molecular biology", "Molecular biology techniques", "Gene therapy", "oncology", "Basic cancer research", "Cancer treatment", "Surgical and invasive medical procedures", "Model organisms", "Animal models", "Mouse models", "micelle", "transgene"], "article_id"=>1100721, "categories"=>["Biological Sciences"], "users"=>["Kouichi Furugaki", "Lin Cui", "Yumi Kunisawa", "Kensuke Osada", "Kentaro Shinkai", "Masao Tanaka", "Kazunori Kataoka", "Kenji Nakano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0101854.g001", "stats"=>{"downloads"=>2, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Polyplex_micelle_distribution_and_transgene_expression_in_vivo_/1100721", "title"=>"Polyplex micelle distribution and transgene expression <i>in vivo</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-11 02:57:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1589363"], "description"=>"<p>(A) Vaccination schedule of polyplex micelles encapsulating therapeutic genes (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0101854#pone-0101854-t001\" target=\"_blank\">Table 1</a>) in the peritoneal dissemination model of CT26 tumors. (B) There were significant increases in the survival rates of SART3/CD40L+GM-CSF, GM-CSF, and SART3+GM-CSF groups (<i>P</i><0.0001, n = 18; <i>P</i><0.01, n = 10; <i>P</i><0.01, n = 7 vs. mock control, n = 19, respectively; left panel). Long-term surviving mice were only obtained by vaccination of polyplex micelles with SART3, CD40L, and GM-CSF genes. No significant improvement in survival was detected by transfection of SART3 or CD40L genes alone (n = 6 and 10; right panel). (C) Vaccination schedule of polyplex micelles with therapeutic genes in subcutaneous CT26 and LLC tumor models. (D) Polyplex micelles with SART3, CD40L, and GM-CSF genes (n = 7 and 9), but not other transgenes (n = 5−6), significantly decreased the weights of CT26 (left panel) and LLC subcutaneous tumors (right panel) compared with those in the mock control (n = 6 and 7). *<i>P</i><0.01.</p>", "links"=>[], "tags"=>["immunology", "Clinical immunology", "immunotherapy", "molecular biology", "Molecular biology techniques", "Gene therapy", "oncology", "Basic cancer research", "Cancer treatment", "Surgical and invasive medical procedures", "Model organisms", "Animal models", "Mouse models", "efficacy", "polyplex", "micelle-based", "dna", "mice", "harboring", "peritoneal", "subcutaneous"], "article_id"=>1100722, "categories"=>["Biological Sciences"], "users"=>["Kouichi Furugaki", "Lin Cui", "Yumi Kunisawa", "Kensuke Osada", "Kentaro Shinkai", "Masao Tanaka", "Kazunori Kataoka", "Kenji Nakano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0101854.g002", "stats"=>{"downloads"=>1, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Anti_tumor_efficacy_of_the_polyplex_micelle_based_DNA_vaccine_in_mice_harboring_peritoneal_and_subcutaneous_tumors_/1100722", "title"=>"Anti-tumor efficacy of the polyplex micelle-based DNA vaccine in mice harboring peritoneal and subcutaneous tumors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-11 02:57:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1589368"], "description"=>"<p>(A) Hematoxylin and eosin staining of lung tissues showed that lung metastatic nodules were highly developed by day 28 after subcutaneous injection of LLC cancer cells in the mock control (4/4 cases), but not present in the SART3/CD40L+GM-CSF vaccine group (0/4 cases). (B) Lung tissues were immunostained with anti-CD4 or CD8a antibodies. Increased infiltration of CD4<sup>+</sup> and CD8a<sup>+</sup> T cells into the lung beds was observed in the SART3/CD40L+GM-CSF group. *<i>P</i><0.05, n = 4.</p>", "links"=>[], "tags"=>["immunology", "Clinical immunology", "immunotherapy", "molecular biology", "Molecular biology techniques", "Gene therapy", "oncology", "Basic cancer research", "Cancer treatment", "Surgical and invasive medical procedures", "Model organisms", "Animal models", "Mouse models", "polyplex", "micelle-based", "dna", "metastasis", "llc"], "article_id"=>1100727, "categories"=>["Biological Sciences"], "users"=>["Kouichi Furugaki", "Lin Cui", "Yumi Kunisawa", "Kensuke Osada", "Kentaro Shinkai", "Masao Tanaka", "Kazunori Kataoka", "Kenji Nakano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0101854.g003", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Protective_effect_of_the_polyplex_micelle_based_DNA_vaccine_on_lung_metastasis_of_LLC_tumors_/1100727", "title"=>"Protective effect of the polyplex micelle-based DNA vaccine on lung metastasis of LLC tumors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-11 02:57:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1589375"], "description"=>"<p>(A) Splenocytes (effector cells) were isolated from mice bearing CT26 and LLC subcutaneous tumors, and then co-cultured with irradiated CSFE-labeled CT26 or YAC-1 target cells at the indicated E/T cell ratios. NK cell activity (upper panel) was increased in all treatment groups with the GM-CSF transgene. In contrast, CTL activity (lower panel) was remarkably elevated by the polyplex micelle encapsulating SART3/CD40L+GM-CSF genes (DNA vaccine group) in an E/T cell ratio-dependent manner. (B) CT26 cells were re-challenged in the flank region of mice that survived for more than 80 days. The formation of subcutaneous tumors was monitored for a further 60 days. Complete rejection of re-challenged tumor cells was detected in the SART3/CD40L+GM-CSF vaccine group, but not in the control. (C) Splenocytes isolated from mice with re-challenge of CT26 cells were subjected to the CTL assay. CTL activity was increased in long-term surviving mice that received the SART3/CD40L+GM-CSF vaccine, but not in the control. (D) CTL activity against CT26 target cells with anti-MHC class 1 (H-2L and -2D) antibodies in mice that were administered the SART3/CD40L+GM-CSF vaccine was reduced to the almost same level as that in the no vaccination control (left panel; n = 2). The CTL activity against SART3-knockdown CT26 cells in mice that were administered the SART3/CD40L+GM-CSF vaccine was reduced compared with that against control CT26 cells, but the knockdown efficiency of SART3 siRNA at the protein level was only 50% (right panel; n = 2).</p>", "links"=>[], "tags"=>["immunology", "Clinical immunology", "immunotherapy", "molecular biology", "Molecular biology techniques", "Gene therapy", "oncology", "Basic cancer research", "Cancer treatment", "Surgical and invasive medical procedures", "Model organisms", "Animal models", "Mouse models", "micelle-based", "dna", "ctl", "activation"], "article_id"=>1100732, "categories"=>["Biological Sciences"], "users"=>["Kouichi Furugaki", "Lin Cui", "Yumi Kunisawa", "Kensuke Osada", "Kentaro Shinkai", "Masao Tanaka", "Kazunori Kataoka", "Kenji Nakano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0101854.g004", "stats"=>{"downloads"=>4, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Polyplex_micelle_based_DNA_vaccine_induces_CTL_activation_and_memory_immunity_/1100732", "title"=>"Polyplex micelle-based DNA vaccine induces CTL activation and memory immunity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-11 02:57:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1589377"], "description"=>"<p>(A) Tissue sections of the lymph nodes, spleen, and tumors from mice that received polyplex micelles with the indicated transgenes were immunostained with an anti-CD11c antibody. Scale Bar  = 200 µm. (B) The number of CD11c<sup>+</sup> DCs was significantly increased in the lymphatic organs of GM-CSF and SART3/CD40L+GM-CSF transfection groups. In tumor tissues, a significant increase of CD11c<sup>+</sup> DC numbers was detected in SART3/CD40L+GM-CSF vaccine group. <i>*P<</i>0.05, <i>**P<</i>0.01 vs. mock control (n = 5).</p>", "links"=>[], "tags"=>["immunology", "Clinical immunology", "immunotherapy", "molecular biology", "Molecular biology techniques", "Gene therapy", "oncology", "Basic cancer research", "Cancer treatment", "Surgical and invasive medical procedures", "Model organisms", "Animal models", "Mouse models", "dcs", "lymph"], "article_id"=>1100735, "categories"=>["Biological Sciences"], "users"=>["Kouichi Furugaki", "Lin Cui", "Yumi Kunisawa", "Kensuke Osada", "Kentaro Shinkai", "Masao Tanaka", "Kazunori Kataoka", "Kenji Nakano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0101854.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Immunohistochemical_analysis_of_CD11c_DCs_in_lymph_node_spleen_and_tumor_tissues_/1100735", "title"=>"Immunohistochemical analysis of CD11c<sup>+</sup> DCs in lymph node, spleen, and tumor tissues.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-11 02:57:25"}

PMC Usage Stats | Further Information

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