Transgenic Expression of the Helicobacter pylori Virulence Factor CagA Promotes Apoptosis or Tumorigenesis through JNK Activation in Drosophila
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{"title"=>"Transgenic Expression of the Helicobacter pylori Virulence Factor CagA Promotes Apoptosis or Tumorigenesis through JNK Activation in Drosophila", "type"=>"journal", "authors"=>[{"first_name"=>"Anica M.", "last_name"=>"Wandler", "scopus_author_id"=>"23391041900"}, {"first_name"=>"Karen", "last_name"=>"Guillemin", "scopus_author_id"=>"6602609258"}], "year"=>2012, "source"=>"PLoS Pathogens", "identifiers"=>{"pmid"=>"23093933", "sgr"=>"84868141695", "doi"=>"10.1371/journal.ppat.1002939", "scopus"=>"2-s2.0-84868141695", "pui"=>"365953677", "issn"=>"15537366"}, "id"=>"81c0a0ce-1bd1-381f-9df3-4f01f316ff30", "abstract"=>"Gastric cancer development is strongly correlated with infection by Helicobacter pylori possessing the effector protein CagA. Using a transgenic Drosophila melanogaster model, we show that CagA expression in the simple model epithelium of the larval wing imaginal disc causes dramatic tissue perturbations and apoptosis when CagA-expressing and non-expressing cells are juxtaposed. This cell death phenotype occurs through activation of JNK signaling and is enhanced by loss of the neoplastic tumor suppressors in CagA-expressing cells or loss of the TNF homolog Eiger in wild type neighboring cells. We further explored the effects of CagA-mediated JNK pathway activation on an epithelium in the context of oncogenic Ras activation, using a Drosophila model of metastasis. In this model, CagA expression in epithelial cells enhances the growth and invasion of tumors in a JNK-dependent manner. These data suggest a potential role for CagA-mediated JNK pathway activation in promoting gastric cancer progression.", "link"=>"http://www.mendeley.com/research/transgenic-expression-helicobacter-pylori-virulence-factor-caga-promotes-apoptosis-tumorigenesis-thr", "reader_count"=>27, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Student > Doctoral Student"=>3, "Researcher"=>9, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>2, "Student > Master"=>1, "Student > Bachelor"=>4, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Student > Doctoral Student"=>3, "Researcher"=>9, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>2, "Student > Master"=>1, "Student > Bachelor"=>4, "Professor"=>2}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>18, "Medicine and Dentistry"=>3, "Pharmacology, Toxicology and Pharmaceutical 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"=>18}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/556094"], "description"=>"<p>(A) Schematic illustrating the fate of different domains within the wing imaginal disc. Each color-coded region of the larval structure on the left corresponds to the specified region of the adult wing on the right (modified from <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002939#ppat.1002939-Bate1\" target=\"_blank\">[24]</a>). (B–G) Confocal cross sections of male third instar larval wing imaginal discs showing mGFP expression and stained with an antibody against active caspase-3 to mark apoptotic cells. A control wing disc epithelium expressing only mGFP with the bx-GAL4 dorsal wing driver (B) lacks apoptotic cells. Ubiquitous expression of CagA in the wing disc with the 765-GAL4 driver (C) does not cause apoptosis, while expressing CagA with bx-GAL4 (D) triggers formation of apoptotic clusters within the expression domain. Expressing two copies of CagA with bx-GAL4 (E) causes a dose-dependent enhancement of the apoptosis phenotype. Expressing CagA<sup>EPISA</sup> with bx-GAL4 (F) does not cause a phenotype, while expressing two copies of CagA<sup>EPISA</sup> (G) produces small apoptotic clusters. Scale bars, 50 µm. (H) XZ confocal plane of a male wing imaginal disc epithelium expressing mGFP and CagA with bx-GAL4 stained with antibodies against active caspase-3 to show basal extrusion of apoptotic cells and matrix metalloproteinase 1 (Mmp1) to show evidence of basement membrane breakdown. Scale bar, 20 µm. (I–N) Adult wing images from male flies of each indicated genotype. Neither expression of mGFP alone with bx-GAL4 (I) nor expression of CagA with 765-GAL4 (J) causes a phenotype in the adult wing. Dorsal wing expression of CagA with bx-GAL4 (K) disrupts epithelial integrity in a dose-dependent manner (L). Expressing CagA<sup>EPISA</sup> with bx-GAL4 (M) does not cause an adult wing phenotype, while expressing two copies of CagA<sup>EPISA</sup> (N) causes epithelial disruption. Scale bar, 500 µm.</p>", "links"=>[], "tags"=>["causes", "apoptosis", "epithelial"], "article_id"=>226592, "categories"=>["Cell Biology", "Genetics", "Microbiology"], "users"=>["Anica M. Wandler", "Karen Guillemin"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002939.g001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CagA_expression_causes_apoptosis_and_epithelial_disruption_/226592", "title"=>"CagA expression causes apoptosis and epithelial disruption.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-18 01:49:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/296893", "https://ndownloader.figshare.com/files/297030", "https://ndownloader.figshare.com/files/297071", "https://ndownloader.figshare.com/files/297120", "https://ndownloader.figshare.com/files/297143", "https://ndownloader.figshare.com/files/297183"], "description"=>"<div><p>Gastric cancer development is strongly correlated with infection by <em>Helicobacter pylori</em> possessing the effector protein CagA. Using a transgenic <em>Drosophila melanogaster</em> model, we show that CagA expression in the simple model epithelium of the larval wing imaginal disc causes dramatic tissue perturbations and apoptosis when CagA-expressing and non-expressing cells are juxtaposed. This cell death phenotype occurs through activation of JNK signaling and is enhanced by loss of the neoplastic tumor suppressors in CagA-expressing cells or loss of the TNF homolog Eiger in wild type neighboring cells. We further explored the effects of CagA-mediated JNK pathway activation on an epithelium in the context of oncogenic Ras activation, using a <em>Drosophila</em> model of metastasis. In this model, CagA expression in epithelial cells enhances the growth and invasion of tumors in a JNK-dependent manner. These data suggest a potential role for CagA-mediated JNK pathway activation in promoting gastric cancer progression.</p> </div>", "links"=>[], "tags"=>["transgenic", "virulence", "caga", "promotes", "apoptosis", "tumorigenesis", "jnk", "activation"], "article_id"=>118503, "categories"=>["Cell Biology", "Genetics", "Microbiology"], "users"=>["Anica M. Wandler", "Karen Guillemin"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002939.s001", "https://dx.doi.org/10.1371/journal.ppat.1002939.s002", "https://dx.doi.org/10.1371/journal.ppat.1002939.s003", "https://dx.doi.org/10.1371/journal.ppat.1002939.s004", "https://dx.doi.org/10.1371/journal.ppat.1002939.s005", "https://dx.doi.org/10.1371/journal.ppat.1002939.s006"], "stats"=>{"downloads"=>5, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Transgenic_Expression_of_the_Helicobacter_pylori_Virulence_Factor_CagA_Promotes_Apoptosis_or_Tumorigenesis_through_JNK_Activation_in_Drosophila_/118503", "title"=>"Transgenic Expression of the <em>Helicobacter pylori</em> Virulence Factor CagA Promotes Apoptosis or Tumorigenesis through JNK Activation in <em>Drosophila</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-10-18 02:21:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/556212"], "description"=>"<p>(A–E) Confocal cross sections of male third instar larval wing imaginal discs showing mGFP expression with bx-GAL4 and stained with an anti-active caspase-3 antibody to mark apoptotic cells. Ectopic overexpression of wild type Bsk in the dorsal wing disc (A) causes a mild apoptosis phenotype that is strongly enhanced by coexpression with CagA (B). Coexpression of Bsk with CagA<sup>EPISA</sup> (C) also enhances the apoptosis phenotype. Expression of Bsk<sup>DN</sup> alone (D) does not cause apoptosis, and coexpression with CagA (E) strongly suppresses apoptosis induced by CagA expression. Scale bars, 50 µm. (F–J) Adult wing images from male flies expressing different forms of Bsk alone or in combination with CagA. Ectopic overexpression of Bsk with bx-GAL4 (F) causes only subtle vein defects in the adult wing, while coexpression with CagA (G) enhances epithelial disruption. Coexpression of Bsk with CagA<sup>EPISA</sup> (H) does not significantly affect formation of the adult wing structure. Expression of Bsk<sup>DN</sup> with bx-GAL4 (I) also causes only subtle vein defects in the adult wing, while coexpression with CagA (J) enhances epithelial disruption. Arrowheads highlight ectopic veins in adult wings expressing different forms of Bsk alone. Scale bar, 500 µm. (K) Quantitation of apoptosis as a percentage of the expression domain showing active caspase-3 staining, n = 15 wing discs per genotype; bar indicates average value for each group. * indicates values that differ significantly from the control with expression of a single transgene; † indicates values that show significant enhancement or suppression compared to CagA; ‡ indicates values that show significant enhancement compared to CagA<sup>EPISA</sup>; p<0.0001. (L) Confocal cross section of a male wing imaginal disc epithelium carrying the <i>puc-lacZ</i> reporter allele and expressing mGFP and CagA with bx-GAL4. Staining with antibodies against active caspase-3 and β-galactosidase (β-gal) shows that apoptotic cells lie adjacent to those in which JNK signaling has been activated. Scale bar, 50 µm. (M) A model of the JNK pathway depicting the multiple upstream activators known to induce JNK-dependent apoptosis in <i>Drosophila</i>, and indicating human homologs for each pathway component.</p>", "links"=>[], "tags"=>["apoptosis", "occurs", "jnk", "pathway"], "article_id"=>226711, "categories"=>["Cell Biology", "Genetics", "Microbiology"], "users"=>["Anica M. Wandler", "Karen Guillemin"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002939.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CagA_induced_apoptosis_occurs_through_JNK_pathway_activation_/226711", "title"=>"CagA-induced apoptosis occurs through JNK pathway activation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-18 01:51:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/556444"], "description"=>"<p>(A–B) Schematics depicting GFP-marked whole eye clones in third instar larvae (A) and a dissected cephalic complex (B), which includes the eye discs (ed), brain lobes (bl) and ventral nerve cord (vnc). (C–G) Images of female third instar larvae and dissected cephalic complexes with GFP-marked tumors. Expression of Ras<sup>V12</sup> in whole eye clones (C) causes overgrowth which results in tumor formation. Coexpression of CagA with Ras<sup>V12</sup> (D) markedly enhances the size of tumors, while coexpression of CagA<sup>EPISA</sup> with Ras<sup>V12</sup> (E) causes only a minor enhancement of tumor growth. Whole eye clone expression of Bsk<sup>DN</sup> with Ras<sup>V12</sup> (F) does not significantly alter tumor size, while coexpression of Bsk<sup>DN</sup> with Ras<sup>V12</sup> and CagA (G) suppresses the growth advantage conferred by CagA expression. Scale bar for whole larvae images, 1 mm; scale bar for dissected cephalic complex images, 250 µm. (H) Quantitation of cephalic complex size as a measure of area in µm<sup>2</sup>, n = at least 30 cephalic complexes per genotype; bar indicates average value for each group. * indicates significant enhancement compared to Ras<sup>V12</sup>; † indicates significant suppression compared to Ras<sup>V12</sup>, CagA; p<0.05.</p>", "links"=>[], "tags"=>["enhances", "jnk"], "article_id"=>226946, "categories"=>["Cell Biology", "Genetics", "Microbiology"], "users"=>["Anica M. Wandler", "Karen Guillemin"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002939.g004", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CagA_enhances_tumor_growth_through_JNK_activation_/226946", "title"=>"CagA enhances tumor growth through JNK activation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-18 01:55:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/556532"], "description"=>"<p>(A–E) Confocal cross sections of cephalic complexes from third instar larvae with GFP-marked tumors stained with an antibody against ElaV to mark terminally differentiated cells and phalloidin to reveal f-actin structure. VNCs are outlined in panels showing GFP expression, and arrows highlight invading tumor tissue. Expressing Ras<sup>V12</sup> alone in whole eye clones (A) causes a mild invasive phenotype characterized by either no invasion or migration of tumor cells from one optic lobe. Coexpression of CagA with Ras<sup>V12</sup> (B) dramatically enhances the extent of VNC invasion from both optic lobes, while coexpression of CagA<sup>EPISA</sup> with Ras<sup>V12</sup> (C) shows a milder enhancement of invasion. Coexpression of Bsk<sup>DN</sup> with Ras<sup>V12</sup> (D) does not significantly affect the invasive capacity of tumor cells, while coexpression of Bsk<sup>DN</sup> with Ras<sup>V12</sup> and CagA (E) suppresses the VNC invasion phenotype. Scale bar, 50 µm. (F) Projections of several confocal cross sections from third instar larval cephalic complexes with GFP-marked tumors showing different classes of invasiveness: (0) noninvasive, (1) invasion from one optic lobe, (2) invasion from both optic lobes, (3) significant invasion of the VNC. Brain lobes and ventral nerve cords are outlined. Scale bar, 50 µm. (G) Quantitation of the percentage of cephalic complexes classified into each category. The number of samples analyzed is shown above each column. * indicates a distribution that differs significantly compared to Ras<sup>V12</sup>; † indicates a distribution that differs significantly compared to Ras<sup>V12</sup>, CagA; p<0.0001.</p>", "links"=>[], "tags"=>["enhances", "jnk"], "article_id"=>227036, "categories"=>["Cell Biology", "Genetics", "Microbiology"], "users"=>["Anica M. Wandler", "Karen Guillemin"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002939.g005", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CagA_enhances_tumor_invasion_through_JNK_activation_/227036", "title"=>"CagA enhances tumor invasion through JNK activation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-18 01:57:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/556344"], "description"=>"<p>(A–E) Confocal cross sections of male third instar larval wing imaginal discs showing mGFP expression with bx-GAL4 and stained with anti-active caspase-3 antibody to mark apoptotic cells. Dorsal wing expression of CagA with bx-GAL4 (A) causes formation of apoptotic clusters. RNAi-mediated knockdown of the nTSG Dlg alone (B) does not cause significant apoptosis, but enhances apoptosis induced by CagA expression (C). The apoptosis phenotype is enhanced when CagA is expressed in an <i>egr</i> mutant background (D). Coexpression of Rho1 with CagA (E) also enhances apoptosis. Scale bars, 50 µm. (F) Quantitation of apoptosis as a percentage of the expression domain showing active caspase-3 staining, n = 10 or 15 wing discs per genotype; bar indicates average value for each group. * indicates values that show significant enhancement compared to CagA, whose quantitation (from <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002939#ppat-1002939-g002\" target=\"_blank\">Figure 2</a>) is provided for comparison; p<0.0001. (G) A model showing the localization of polarity protein complexes in an epithelial cell, their known interactions with other upstream activators of JNK signaling in <i>Drosophila</i>, and the downstream effects of these interactions.</p>", "links"=>[], "tags"=>["genetically", "interacts", "eiger"], "article_id"=>226839, "categories"=>["Cell Biology", "Genetics", "Microbiology"], "users"=>["Anica M. Wandler", "Karen Guillemin"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002939.g003", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CagA_genetically_interacts_with_nTSGs_Eiger_and_Rho1_/226839", "title"=>"CagA genetically interacts with nTSGs, Eiger and Rho1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-18 01:53:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/556635"], "description"=>"<p>(A) Once inside the host epithelial cell, CagA effector protein downregulates the neoplastic tumor suppressors (nTSGs) which induces endocytic activation of the TNF homolog Eiger (Egr) leading to activation of JNK (Bsk). CagA also triggers Egr-dependent JNK pathway activation in neighboring wild type cells. In the absence of this pathway, CagA activates JNK signaling through other upstream pathway components including the small GTPase Rho1. In a wild type host genetic background, CagA-mediated JNK pathway activation causes apoptosis and subsequent extrusion from the epithelium, or engulfment by neighboring cells. (B) Introduction of CagA into host cells causes upregulation of JNK signaling which triggers apoptosis and compensatory proliferation within the epithelium as part of the cell editing process. When the host genetic background is perturbed by expression of an oncogenic mutation which blocks apoptosis, CagA-mediated JNK pathway activation drives tumor progression.</p>", "links"=>[], "tags"=>["illustrating", "caga", "epithelium", "resulting"], "article_id"=>227135, "categories"=>["Cell Biology", "Genetics", "Microbiology"], "users"=>["Anica M. Wandler", "Karen Guillemin"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002939.g006", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Models_illustrating_short_term_effects_of_CagA_on_an_epithelium_and_long_term_effects_resulting_from_a_change_in_host_genetic_background_/227135", "title"=>"Models illustrating short-term effects of CagA on an epithelium and long-term effects resulting from a change in host genetic background.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-18 01:58:55"}

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Relative Metric

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