Active Immunization with Extracellular Vesicles Derived from Staphylococcus aureus Effectively Protects against Staphylococcal Lung Infections, Mainly via Th1 Cell-Mediated Immunity
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{"title"=>"Active immunization with extracellular vesicles derived from Staphylococcus aureus effectively protects against staphylococcal lung infections, mainly via Th1 cell-mediated immunity", "type"=>"journal", "authors"=>[{"first_name"=>"Seng Jin", "last_name"=>"Choi", "scopus_author_id"=>"36697615400"}, {"first_name"=>"Min Hye", "last_name"=>"Kim", "scopus_author_id"=>"55572220900"}, {"first_name"=>"Jinseong", "last_name"=>"Jeon", "scopus_author_id"=>"56941315200"}, {"first_name"=>"Oh Youn", "last_name"=>"Kim", "scopus_author_id"=>"57191491030"}, {"first_name"=>"Youngwoo", "last_name"=>"Choi", "scopus_author_id"=>"55927859000"}, {"first_name"=>"Jihye", "last_name"=>"Seo", "scopus_author_id"=>"56562249300"}, {"first_name"=>"Sung Wook", "last_name"=>"Hong", "scopus_author_id"=>"42761376300"}, {"first_name"=>"Won Hee", "last_name"=>"Lee", "scopus_author_id"=>"55635124200"}, {"first_name"=>"Seong Gyu", "last_name"=>"Jeon", "scopus_author_id"=>"26635198500"}, {"first_name"=>"Yong Song", "last_name"=>"Gho", "scopus_author_id"=>"55890576200"}, {"first_name"=>"Young Koo", "last_name"=>"Jee", "scopus_author_id"=>"7005104108"}, {"first_name"=>"Yoon Keun", "last_name"=>"Kim", "scopus_author_id"=>"7410211755"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"606946068", "sgr"=>"84947461405", "issn"=>"19326203", "pmid"=>"26333035", "scopus"=>"2-s2.0-84947461405", "doi"=>"10.1371/journal.pone.0136021", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"e59d3786-9cdd-3dee-9853-5d6e2e3213db", "abstract"=>"Staphylococcus aureus is an important pathogenic bacterium that causes various infectious diseases. Extracellular vesicles (EVs) released from S. aureus contain bacterial proteins, nucleic acids, and lipids. These EVs can induce immune responses leading to similar symptoms as during staphylococcal infection condition and have the potential as vaccination agent. Here, we show that active immunization (vaccination) with S. aureus-derived EVs induce adaptive immunity of antibody and T cell responses. In addition, these EVs have the vaccine adjuvant ability to induce protective immunity such as the up-regulation of co-stimulatory molecules and the expression of T cell polarizing cytokines in antigen-presenting cells. Moreover, vaccination with S. aureus EVs conferred protection against lethality induced by airway challenge with lethal dose of S. aureus and also pneumonia induced by the administration of sub-lethal dose of S. aureus. These protective effects were also found in mice that were adoptively transferred with splenic T cells isolated from S. aureus EV-immunized mice, but not in serum transferred mice. Furthermore, this protective effect of S. aureus EVs was significantly reduced by the absence of interferon-gamma, but not by the absence of interleukin-17. Together, the study herein suggests that S. aureus EVs are a novel vaccine candidate against S. aureus infections, mainly via Th1 cellular response.", "link"=>"http://www.mendeley.com/research/active-immunization-extracellular-vesicles-derived-staphylococcus-aureus-effectively-protects-agains", "reader_count"=>26, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Librarian"=>1, "Student > Doctoral Student"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Librarian"=>1, "Student > Doctoral Student"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>5, "Medicine and Dentistry"=>3, "Agricultural and Biological Sciences"=>13, "Computer Science"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>13}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2250974"], "description"=>"<p>For all figures, SEVs (5 μg) and sham (PBS) were injected intramuscularly to mice at weekly intervals for 3 weeks, and then the lethal dose (4.0 × 10<sup>8</sup> CFU<i>)</i> of <i>S</i>. <i>aureus</i> were challenged oropharyngeally to the immunized mice one week after the last immunization. The survival was monitored every 12 h after the bacterial challenge for 3 days (n = 10 each group). (A) The survival rates of wild type (WT), MyD88-deficient, TLR2-deficient, TLR4-deficient, and TLR9-deficient (all C57BL/6 background) mice after <i>S</i>. <i>aureus</i> challenge. (B) The survival rates of WT, IFN-γ-deficient, and IL-17-deficient (all BABL/c background) mice after <i>S</i>. <i>aureus</i> challenge.</p>", "links"=>[], "tags"=>["novel vaccine candidate", "Extracellular Vesicles Derived", "vaccine adjuvant ability", "T cell responses", "aureus EVs", "Staphylococcal Lung Infections", "Splenic T cells"], "article_id"=>1533863, "categories"=>["Biological Sciences"], "users"=>["Seng Jin Choi", "Min-Hye Kim", "Jinseong Jeon", "Oh Youn Kim", "Youngwoo Choi", "Jihye Seo", "Sung-Wook Hong", "Won-Hee Lee", "Seong Gyu Jeon", "Yong Song Gho", "Young-Koo Jee", "Yoon-Keun Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0136021.g006", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Role_of_Toll_like_receptor_signaling_and_T_cell_derived_cytokines_on_the_protective_effect_of_SEV_vaccination_/1533863", "title"=>"Role of Toll-like receptor signaling and T cell-derived cytokines on the protective effect of SEV vaccination.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-02 03:27:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/2250979"], "description"=>"<p>(A) Study protocol for SEV vaccination and bacterial challenge. SEVs (5 μg) and sham (PBS) were injected intramuscularly at weekly intervals for 3 weeks, and then <i>S</i>. <i>aureus</i> (4 × 10<sup>8</sup> CFU) was challenged by oropharyngeal application 40 days after the last immunization. (B) Survival rates of SEV- and sham-immunized mice challenged with <i>S</i>. <i>aureus</i> (n = 10, each group). Survival was monitored every 12 h for 40 days.</p>", "links"=>[], "tags"=>["novel vaccine candidate", "Extracellular Vesicles Derived", "vaccine adjuvant ability", "T cell responses", "aureus EVs", "Staphylococcal Lung Infections", "Splenic T cells"], "article_id"=>1533864, "categories"=>["Biological Sciences"], "users"=>["Seng Jin Choi", "Min-Hye Kim", "Jinseong Jeon", "Oh Youn Kim", "Youngwoo Choi", "Jihye Seo", "Sung-Wook Hong", "Won-Hee Lee", "Seong Gyu Jeon", "Yong Song Gho", "Young-Koo Jee", "Yoon-Keun Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0136021.g007", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Long_term_effect_of_SEV_vaccination_on_the_protection_against_lethality_induced_by_S_aureus_infection_/1533864", "title"=>"Long-term effect of SEV vaccination on the protection against lethality induced by <i>S</i>. <i>aureus</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-02 03:27:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/2250960"], "description"=>"<p>For all figures, SEVs (5 μg) and sham (PBS) were injected intramuscularly to mice at weekly intervals for 3 weeks, and then sub-lethal dose (1 × 10<sup>8</sup> CFU<i>)</i> of <i>S</i>. <i>aureus</i> was applied via the oropharyngeal route one week after the last immunization. Normal: PBS-immunized and PBS-challenged mice; PBS: PBS-immunized and <i>S</i>. <i>aureus</i>-challenged mice; SEV: SEV-immunized and <i>S</i>. <i>aureus</i>-challenged mice. (A) Colony forming unit (CFU) counts from lung of SEV- and sham (PBS)-immunized mice 24 h after the <i>S</i>. <i>aureus</i> challenge (n = 10, each group). (B) Histology (left panel) and gross image (right panel) of lung from SEV- and sham (PBS)-immunized mice after the sub-lethal dose of <i>S</i>. <i>aureus</i> challenge. (C) Distribution of <i>S</i>. <i>aureus</i> before and after SEV-immunization. Cy7-labeled <i>S</i>. <i>aureus</i> was applied via the oropharyngeal route to SEV- and sham (PBS)-immunized mice. Cy7 fluorescence of whole mouse (upper panel) or lung (lower panel) was acquired by IVIS spectrum 24 h after the <i>S</i>. <i>aureus</i> challenge. (D) Bioluminescence signal in the lung tissue after Cy7-labeled <i>S</i>. <i>aureus</i> administration. The amount of the bioluminescence signal (photons/s) in the lung tissue was measured by IVIS spectrum 24h after <i>S</i>. <i>aureus</i> challenge (n = 5, each group). (E) The levels of IL-β and IL-6 in serum of SEV- and sham (PBS)-immunized mice 24 h after the <i>S</i>. <i>aureus</i> challenge (n = 10, each group). * indicates p< 0.05 vs. PBS.</p>", "links"=>[], "tags"=>["novel vaccine candidate", "Extracellular Vesicles Derived", "vaccine adjuvant ability", "T cell responses", "aureus EVs", "Staphylococcal Lung Infections", "Splenic T cells"], "article_id"=>1533859, "categories"=>["Biological Sciences"], "users"=>["Seng Jin Choi", "Min-Hye Kim", "Jinseong Jeon", "Oh Youn Kim", "Youngwoo Choi", "Jihye Seo", "Sung-Wook Hong", "Won-Hee Lee", "Seong Gyu Jeon", "Yong Song Gho", "Young-Koo Jee", "Yoon-Keun Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0136021.g003", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Efficacy_of_SEV_vaccination_on_protection_against_pneumonia_induced_by_sub_lethal_dose_of_S_aureus_/1533859", "title"=>"Efficacy of SEV vaccination on protection against pneumonia induced by sub-lethal dose of <i>S</i>. <i>aureus</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-02 03:27:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/2250959"], "description"=>"<p>(A) Determination of lethal and sub-lethal doses of <i>S</i>. <i>aureus</i> in mouse pneumonia model. Survival rates in mice were evaluated after oropharyngeal application with different doses (1 × 10<sup>8</sup>, 2 × 10<sup>8</sup>, 3 × 10<sup>8</sup> and 4 × 10<sup>8</sup> CFU) of <i>S</i>. <i>aureus</i>. Survival was monitored every 12 h for 3 days (n = 10, each group). (B) Histologic image of mouse lung after oropharyngeal application of <i>S</i>. <i>aureus</i> (1 × 10<sup>8</sup> CFU) 24 h post-infection. (C) Study protocol for SEV-immunization and challenge of the lethal dose (4 × 10<sup>8</sup> CFU<i>)</i> of <i>S</i>. <i>aureus</i>. SEVs and sham (PBS) were injected intramuscularly at weekly intervals for 3 weeks, and then <i>S</i>. <i>aureus</i> was applied via oropharyngeal route one week after the last immunization. (D) Efficacy of different doses (1, 5, and 10 μg) of SEV vaccination. Survival was monitored every 12 h for 3 days (n = 10, each group). (E) Efficacy of SEV vaccination according to immunization frequency. Survival rates were monitored every 12 h for 3 days in mice immunized with SEVs (5 μg) once, twice, or three times (n = 10, each group).</p>", "links"=>[], "tags"=>["novel vaccine candidate", "Extracellular Vesicles Derived", "vaccine adjuvant ability", "T cell responses", "aureus EVs", "Staphylococcal Lung Infections", "Splenic T cells"], "article_id"=>1533858, "categories"=>["Biological Sciences"], "users"=>["Seng Jin Choi", "Min-Hye Kim", "Jinseong Jeon", "Oh Youn Kim", "Youngwoo Choi", "Jihye Seo", "Sung-Wook Hong", "Won-Hee Lee", "Seong Gyu Jeon", "Yong Song Gho", "Young-Koo Jee", "Yoon-Keun Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0136021.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Efficacy_of_S_aureus_EVs_SEVs_vaccination_on_protection_against_lethality_induced_by_S_aureus_lung_infection_/1533858", "title"=>"Efficacy of <i>S</i>. <i>aureus</i> EVs (SEVs) vaccination on protection against lethality induced by <i>S</i>. <i>aureus</i> lung infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-02 03:27:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/2250982"], "description"=>"<p>Mice were intramuscularly administered with 5 μg or 50 μg of SEV and monitored for 14 days. (n = 10) (A) The survival rate, body temperature, and body weight of mice measured at indicated times. (B) The levels of IL-1β, IL-6 and TNF-α in serum of SEV- and sham (PBS)-immunized mice 24 h after the SEV administration. n.s. indicates not significant.</p>", "links"=>[], "tags"=>["novel vaccine candidate", "Extracellular Vesicles Derived", "vaccine adjuvant ability", "T cell responses", "aureus EVs", "Staphylococcal Lung Infections", "Splenic T cells"], "article_id"=>1533867, "categories"=>["Biological Sciences"], "users"=>["Seng Jin Choi", "Min-Hye Kim", "Jinseong Jeon", "Oh Youn Kim", "Youngwoo Choi", "Jihye Seo", "Sung-Wook Hong", "Won-Hee Lee", "Seong Gyu Jeon", "Yong Song Gho", "Young-Koo Jee", "Yoon-Keun Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0136021.g008", "stats"=>{"downloads"=>2, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Toxicity_of_SEV_vaccine_/1533867", "title"=>"Toxicity of SEV vaccine.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-02 03:27:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/2250962"], "description"=>"<p>CD4+ T cells and blood sera were isolated from SEV-and sham (PBS)-immunized mice 6 days after three immunizations. Either CD4+ T cells (A) or sera (B) were applied intraperitoneally to naïve mice. After 24 h of the injection, lethal dose (4.0 × 10<sup>8</sup> CFU<i>)</i> of <i>S</i>. <i>aureus</i> was applied via the oropharyngeal route to the adoptive transferred mice. The survival rates were monitored every 12 h after the bacterial challenge for 3 days (n = 10, each group).</p>", "links"=>[], "tags"=>["novel vaccine candidate", "Extracellular Vesicles Derived", "vaccine adjuvant ability", "T cell responses", "aureus EVs", "Staphylococcal Lung Infections", "Splenic T cells"], "article_id"=>1533861, "categories"=>["Biological Sciences"], "users"=>["Seng Jin Choi", "Min-Hye Kim", "Jinseong Jeon", "Oh Youn Kim", "Youngwoo Choi", "Jihye Seo", "Sung-Wook Hong", "Won-Hee Lee", "Seong Gyu Jeon", "Yong Song Gho", "Young-Koo Jee", "Yoon-Keun Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0136021.g005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Role_of_antibody_and_T_helper_cells_on_the_protective_effect_of_SEV_vaccination_/1533861", "title"=>"Role of antibody and T helper cells on the protective effect of SEV vaccination.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-02 03:27:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/2250961"], "description"=>"<p>For (A) and (B), SEVs (5 μg) and sham (PBS) were injected intramuscularly to mice at weekly intervals for 3 weeks (n = 10, each group). (A) The levels of SEV-reactive IgG in serum. Sera were obtained from SEV- and sham-immunized mice 7 days after each immunization and serum levels of SEV-reactive IgG were measured by ELISA. (B) SEV-specific production of IFN-γ, IL-17, and IL-4 from splenic T cells. Splenic T cells were isolated from spleens of SEV- and sham-immunized mice, and then stimulated with anti- CD3/CD28 for 72 h. The levels of IFN-γ, IL-17, and IL-4 in the cell supernatants were measured by ELISA. For (C) and (D) SEVs (5 μg) and sham (PBS) were applied intraperitoneally (IP), subcutaneously (SC), or intramuscularly (IM) at weekly intervals for 3 weeks (n = 10, each group). (C) The levels of SEV-reactive IgG in serum. Sera were obtained from SEV- and sham (PBS)-immunized mice 7 days after the last immunization. (D) SEV-specific production of IFN-γ, IL-17, and IL-4 from splenic T cells. Splenic T cells were isolated from spleen of SEV- and sham (PBS)-immunized mice, and then stimulated with anti-CD3/CD28 for 72 h. The levels of IFN-γ, IL-17 and IL-4 in the cell supernatants were measured by ELISA. * indicates p< 0.05 vs. PBS and ** indicates p< 0.01 vs. the other groups.</p>", "links"=>[], "tags"=>["novel vaccine candidate", "Extracellular Vesicles Derived", "vaccine adjuvant ability", "T cell responses", "aureus EVs", "Staphylococcal Lung Infections", "Splenic T cells"], "article_id"=>1533860, "categories"=>["Biological Sciences"], "users"=>["Seng Jin Choi", "Min-Hye Kim", "Jinseong Jeon", "Oh Youn Kim", "Youngwoo Choi", "Jihye Seo", "Sung-Wook Hong", "Won-Hee Lee", "Seong Gyu Jeon", "Yong Song Gho", "Young-Koo Jee", "Yoon-Keun Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0136021.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Antibody_and_T_cell_responses_after_SEV_vaccination_/1533860", "title"=>"Antibody and T cell responses after SEV vaccination.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-02 03:27:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/2250958"], "description"=>"<p>(A) Uptake of SEVs by bone marrow-derived dendritic cells (BMDCs). BMDCs were treated with SEVs (10 μg/ml) for 24 h. BMDCs cytoplasm were stained with CellTracker Green CMFDA (5-chloromethylfluorescein diacetate, green), nuclei with Hoechst (blue), and SEVs with DiI (red). The quantification of SEV-florescence in no-treatment and SEV-treatment group (n = 20, each group). (B) The expression of co-stimulatory molecules in BMDCs. The expression of CD80 and CD86 in BMDCs were measured 24 h after treatment with SEVs (10 μg/ml) or PBS. (C) Production of pro-inflammatory cytokines from BMDCs 24 h after SEVs treatment. BMDCs were treated with various concentrations of SEVs, and the levels of TNF-ɑ, IL-6, and IL-12 in the cell supernatants were measured by ELISA. *** indicates p< 0.001.</p>", "links"=>[], "tags"=>["novel vaccine candidate", "Extracellular Vesicles Derived", "vaccine adjuvant ability", "T cell responses", "aureus EVs", "Staphylococcal Lung Infections", "Splenic T cells"], "article_id"=>1533857, "categories"=>["Biological Sciences"], "users"=>["Seng Jin Choi", "Min-Hye Kim", "Jinseong Jeon", "Oh Youn Kim", "Youngwoo Choi", "Jihye Seo", "Sung-Wook Hong", "Won-Hee Lee", "Seong Gyu Jeon", "Yong Song Gho", "Young-Koo Jee", "Yoon-Keun Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0136021.g001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_vitro_immunogenicity_of_S_aureus_derived_EVs_SEVs_/1533857", "title"=>"<i>In vitro</i> immunogenicity of <i>S</i>. <i>aureus</i>-derived EVs (SEVs).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-02 03:27:59"}

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"=>[]}

F1000Prime | Further Information

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