Neutrophils Are Resistant to Yersinia YopJ/P-Induced Apoptosis and Are Protected from ROS-Mediated Cell Death by the Type III Secretion System
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{"title"=>"Neutrophils are resistant to Yersinia YopJ/P-induced apoptosis and are protected from ROS-mediated cell death by the type III secretion system", "type"=>"journal", "authors"=>[{"first_name"=>"Justin L.", "last_name"=>"Spinner", "scopus_author_id"=>"24503368400"}, {"first_name"=>"Keun Seok", "last_name"=>"Seo", "scopus_author_id"=>"8287486700"}, {"first_name"=>"Jason L.", "last_name"=>"O'Loughlin", "scopus_author_id"=>"35488467000"}, {"first_name"=>"Jennifer A.", "last_name"=>"Cundiff", "scopus_author_id"=>"57197169307"}, {"first_name"=>"Scott A.", "last_name"=>"Minnich", "scopus_author_id"=>"7004075071"}, {"first_name"=>"Gregory A.", "last_name"=>"Bohach", "scopus_author_id"=>"7003380076"}, {"first_name"=>"Scott D.", "last_name"=>"Kobayashi", "scopus_author_id"=>"7405379680"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"77949528563", "doi"=>"10.1371/journal.pone.0009279", "pui"=>"358466875", "pmid"=>"20174624", "scopus"=>"2-s2.0-77949528563", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"0d82b450-d69e-3f16-9eb9-6c8dd96ac16a", "abstract"=>"BACKGROUND: The human innate immune system relies on the coordinated activity of macrophages and polymorphonuclear leukocytes (neutrophils or PMNs) for defense against bacterial pathogens. Yersinia spp. subvert the innate immune response to cause disease in humans. In particular, the Yersinia outer protein YopJ (Y. pestis and Y. pseudotuberculosis) and YopP (Y. enterocolitica) rapidly induce apoptosis in murine macrophages and dendritic cells. However, the effects of Yersinia Yop J/P on neutrophil fate are not clearly defined.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: In this study, we utilized wild-type and mutant strains of Yersinia to test the contribution of YopJ and YopP on induction of apoptosis in human monocyte-derived macrophages (HMDM) and neutrophils. Whereas YopJ and YopP similarly induced apoptosis in HMDMs, interaction of human neutrophils with virulence plasmid-containing Yersinia did not result in PMN caspase activation, release of LDH, or loss of membrane integrity greater than PMN controls. In contrast, interaction of human PMNs with the virulence plasmid-deficient Y. pestis strain KIM6 resulted in increased surface exposure of phosphatidylserine (PS) and cell death. PMN reactive oxygen species (ROS) production was inhibited in a virulence plasmid-dependent but YopJ/YopP-independent manner. Following phagocytic interaction with Y. pestis strain KIM6, inhibition of PMN ROS production with diphenyleneiodonium chloride resulted in a reduction of PMN cell death similar to that induced by the virulence plasmid-containing strain Y. pestis KIM5.\\n\\nCONCLUSIONS: Our findings showed that Yersinia YopJ and/or YopP did not induce pronounced apoptosis in human neutrophils. Furthermore, robust PMN ROS production in response to virulence plasmid-deficient Yersinia was associated with increased PMN cell death, suggesting that Yersinia inhibition of PMN ROS production plays a role in evasion of the human innate immune response in part by limiting PMN apoptosis.", "link"=>"http://www.mendeley.com/research/neutrophils-resistant-yersinia-yopjpinduced-apoptosis-protected-rosmediated-cell-death-type-iii-secr", "reader_count"=>34, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>3, "Researcher"=>7, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>2, "Student > Master"=>3, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>3, "Researcher"=>7, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>2, "Student > Master"=>3, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Engineering"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>24, "Medicine and Dentistry"=>3, "Veterinary Science and Veterinary Medicine"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>24}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>2}, "Environmental Science"=>{"Environmental Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>2, "China"=>1, "United Kingdom"=>1, "Madagascar"=>1}, "group_count"=>1}

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  • {"files"=>["https://ndownloader.figshare.com/files/863112"], "description"=>"<p>PMNs were incubated alone or with <i>Y. pestis</i> KIM5, KIM5 YopJ-YopP, KIM5Δ<i>yopJ</i>, KIM6 or <i>Y. enterocolitica</i> 8081v grown at 37°C. (<b>A</b>) PMN ROS production following incubation with the indicated <i>Yersinia</i> strains. (<b>B</b>) PMN ROS production with or without 10 µM DPI. PMN cell death following phagocytic interaction with <i>Yersinia</i> was assessed by (<b>C</b>) PMN release of LDH into the supernatant and (<b>D</b>) PMN uptake of EthD-1. Results are expressed as the mean ± SEM of three experiments. *, represents difference from PMN controls (<i>P</i><0.05).</p>", "links"=>[], "tags"=>["neutrophil", "ros"], "article_id"=>533562, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Justin L. Spinner", "Keun Seok Seo", "Jason L. O'Loughlin", "Jennifer A. Cundiff", "Scott A. Minnich", "Gregory A. Bohach", "Scott D. Kobayashi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009279.g006", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_Yersinia_on_neutrophil_ROS_production_and_cell_death_/533562", "title"=>"Effects of <i>Yersinia</i> on neutrophil ROS production and cell death.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:40:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/862501"], "description"=>"<p><i>Y. pestis</i> strains with the virulence plasmid expressing YopJ (KIM5), YopP (KIM5 YopJ-YopP), or lacking YopJ (KIM5Δ<i>yopJ</i>), along with <i>Y. enterocolitica</i> 8081v and the virulence plasmid–deficient strain (KIM6) were grown at 37°C to induce expression of the TTSS and Yops. <i>Yersinia</i> strains were combined with J774A.1 and HMDM cells and compared to detergent lysed controls as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009279#s2\" target=\"_blank\">Materials and Methods</a>. The percentage of J774A.1 cell death following incubation alone or with <i>Yersinia</i> strains at the indicated time was determined by (<b>A</b>) LDH release into the supernatant and by (<b>B</b>) EthD-1 staining of J774A.1 cells. HMDM cell death was determined by measuring (<b>C</b>) LDH release and (<b>D</b>) EthD-1 uptake into HMDMs. The results are expressed as the mean ± SEM of at least three experiments. *, represents difference from J774A.1 or HMDM controls (<i>P</i><0.05).</p>", "links"=>[], "tags"=>["yopj", "yopp", "mdm"], "article_id"=>532945, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Justin L. Spinner", "Keun Seok Seo", "Jason L. O'Loughlin", "Jennifer A. Cundiff", "Scott A. Minnich", "Gregory A. Bohach", "Scott D. Kobayashi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009279.g001", "stats"=>{"downloads"=>1, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Role_of_YopJ_and_YopP_in_J774A_1_macrophage_like_and_human_MDM_cell_death_/532945", "title"=>"Role of YopJ and YopP in J774A.1 macrophage<i>-</i>like and human MDM cell death.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:36:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/863297"], "description"=>"<p>Oligonucleotides used in this study.</p>", "links"=>[], "tags"=>["microbiology/cellular microbiology and pathogenesis", "microbiology/innate immunity", "infectious diseases/bacterial infections"], "article_id"=>533743, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Justin L. Spinner", "Keun Seok Seo", "Jason L. O'Loughlin", "Jennifer A. Cundiff", "Scott A. Minnich", "Gregory A. Bohach", "Scott D. Kobayashi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009279.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Oligonucleotides_used_in_this_study_/533743", "title"=>"Oligonucleotides used in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 02:41:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/862656"], "description"=>"<p>HMDMs and J774A.1 cells were incubated alone or with <i>Y. pestis</i> KIM5, KIM5 YopJ-YopP, KIM5Δ<i>yopJ</i>, KIM6 and <i>Y. enterocolitica</i> 8081v grown at 37°C. Caspase-3, -8, -9, and -2 activity was measured after 6 h of incubation as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009279#s2\" target=\"_blank\"><i>Materials and Methods</i></a> and is expressed in relative fluorescence units (RFLU). Results are expressed as the mean ± SEM of three experiments. *, represents difference from HMDM and J774A.1 controls (<i>P</i><0.05).</p>", "links"=>[], "tags"=>["caspase", "delayed", "mdms", "compared"], "article_id"=>533102, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Justin L. Spinner", "Keun Seok Seo", "Jason L. O'Loughlin", "Jennifer A. Cundiff", "Scott A. Minnich", "Gregory A. Bohach", "Scott D. Kobayashi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009279.g002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Induction_of_caspase_activity_is_YopJ_YopP_dependent_but_delayed_in_human_MDMs_compared_to_J774A_1_cells_/533102", "title"=>"Induction of caspase activity is YopJ/YopP dependent but delayed in human MDMs compared to J774A.1 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:37:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/862966"], "description"=>"<p>PMNs were incubated alone or with <i>Y. pestis</i> KIM5, KIM5 YopJ-YopP, KIM5Δ<i>yopJ</i>, KIM6 and <i>Y. enterocolitica</i> 8081v grown at 37°C. Caspase-3, -8, -9, and -2 activity was measured after 3 h and 6 h of incubation as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009279#s2\" target=\"_blank\"><i>Materials and Methods</i></a> and is expressed in relative fluorescence units. Results are expressed as the mean ± SEM of three experiments. *, represents difference from PMN controls (<i>P</i><0.05).</p>", "links"=>[], "tags"=>["-2", "pmns", "incubation"], "article_id"=>533413, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Justin L. Spinner", "Keun Seok Seo", "Jason L. O'Loughlin", "Jennifer A. Cundiff", "Scott A. Minnich", "Gregory A. Bohach", "Scott D. Kobayashi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009279.g005", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Caspase_3_8_9_and_2_activity_in_PMNs_following_incubation_with_Yersinia_/533413", "title"=>"Caspase-3, -8, -9, and -2 activity in PMNs following incubation with <i>Yersinia</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:39:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/862894"], "description"=>"<p><i>Y. pestis</i> KIM5, KIM5 YopJ-YopP, KIM5Δ<i>yopJ</i>, KIM6 and <i>Y. enterocolitica</i> were grown at 37°C, combined with PMNs, and incubated for the times indicated. PS externalization was determined by annexin V-FITC and flow cytometry following interaction with <i>Yersinia</i> Results are expressed as the mean ± SEM of at least three experiments. *, represents difference from PMN controls (<i>P</i><0.05).</p>", "links"=>[], "tags"=>["pmn", "phosphatidylserine"], "article_id"=>533345, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Justin L. Spinner", "Keun Seok Seo", "Jason L. O'Loughlin", "Jennifer A. Cundiff", "Scott A. Minnich", "Gregory A. Bohach", "Scott D. Kobayashi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009279.g004", "stats"=>{"downloads"=>2, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_PMN_phosphatidylserine_PS_externalization_/533345", "title"=>"Analysis of PMN phosphatidylserine (PS) externalization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:38:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/862802"], "description"=>"<p>PMNs were incubated alone or with <i>Y. pestis</i> KIM5, KIM5 YopJ-YopP, KIM5Δ<i>yopJ</i>, KIM6 and <i>Y. enterocolitica</i> 8081v grown at 37°C. The percentage of PMN cell death following incubation with each strain for the indicated time was determined by comparison to detergent lysed controls. Indicators of cell death measured were release of (<b>A</b>) LDH into the supernatant and (<b>B</b>) EthD-1 uptake into PMN cells as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009279#s2\" target=\"_blank\"><i>Materials and Methods</i></a>. Results are expressed as the mean ± SEM of three experiments. *, represents difference from PMN controls (<i>P</i><0.05).</p>", "links"=>[], "tags"=>["yopj", "yopp", "pmn"], "article_id"=>533247, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Justin L. Spinner", "Keun Seok Seo", "Jason L. O'Loughlin", "Jennifer A. Cundiff", "Scott A. Minnich", "Gregory A. Bohach", "Scott D. Kobayashi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009279.g003", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Role_of_YopJ_and_YopP_in_human_PMN_cell_death_/533247", "title"=>"Role of YopJ and YopP in human PMN cell death.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:38:24"}

PMC Usage Stats | Further Information

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Relative Metric

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