The Legionella pneumophila Effector VipA Is an Actin Nucleator That Alters Host Cell Organelle Trafficking
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{"title"=>"The Legionella pneumophila effector VipA is an actin nucleator that alters host cell organelle trafficking", "type"=>"journal", "authors"=>[{"first_name"=>"Irina Saraiva", "last_name"=>"Franco", "scopus_author_id"=>"35182883200"}, {"first_name"=>"Nadim", "last_name"=>"Shohdy", "scopus_author_id"=>"6508005896"}, {"first_name"=>"Howard A.", "last_name"=>"Shuman", "scopus_author_id"=>"35459274900"}], "year"=>2012, "source"=>"PLoS Pathogens", "identifiers"=>{"sgr"=>"84860895147", "scopus"=>"2-s2.0-84860895147", "doi"=>"10.1371/journal.ppat.1002546", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "pui"=>"364799326", "issn"=>"15537366", "pmid"=>"22383880"}, "id"=>"586a91ad-3561-3d31-8c0c-b98d22fcca76", "abstract"=>"Legionella pneumophila, the causative agent of Legionnaires' disease, invades and replicates within macrophages and protozoan cells inside a vacuole. The type IVB Icm/Dot secretion system is necessary for the translocation of effector proteins that modulate vesicle trafficking pathways in the host cell, thus avoiding phagosome-lysosome fusion. The Legionella VipA effector was previously identified by its ability to interfere with organelle trafficking in the Multivesicular Body (MVB) pathway when ectopically expressed in yeast. In this study, we show that VipA binds actin in vitro and directly polymerizes microfilaments without the requirement of additional proteins, displaying properties distinct from other bacterial actin nucleators. Microscopy studies revealed that fluorescently tagged VipA variants localize to puncta in eukaryotic cells. In yeast these puncta are associated with actin-rich regions and components of the Multivesicular Body pathway such as endosomes and the MVB-associated protein Bro1. During macrophage infection, native translocated VipA associated with actin patches and early endosomes. When ectopically expressed in mammalian cells, VipA-GFP displayed a similar distribution ruling out the requirement of additional effectors for binding to its eukaryotic targets. Interestingly, a mutant form of VipA, VipA-1, that does not interfere with organelle trafficking is also defective in actin binding as well as association with early endosomes and shows a homogeneous cytosolic localization. These results show that the ability of VipA to bind actin is related to its association with a specific subcellular location as well as its role in modulating organelle trafficking pathways. VipA constitutes a novel type of actin nucleator that may contribute to the intracellular lifestyle of Legionella by altering cytoskeleton dynamics to target host cell pathways.", "link"=>"http://www.mendeley.com/research/legionella-pneumophila-effector-vipa-actin-nucleator-alters-host-cell-organelle-trafficking", "reader_count"=>42, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>4, "Student > Doctoral Student"=>3, "Researcher"=>15, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Other"=>1, "Student > Master"=>2, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>4, "Student > Doctoral Student"=>3, "Researcher"=>15, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Other"=>1, "Student > Master"=>2, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>24, "Medicine and Dentistry"=>3, "Chemical Engineering"=>1, "Chemistry"=>2, "Social Sciences"=>1, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Chemistry"=>{"Chemistry"=>2}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>24}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>1}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"Iran"=>1, "United States"=>1, "United Kingdom"=>1, "France"=>1, "Portugal"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/676469"], "description"=>"<p><b>A.</b> Primary sequence of VipA and localization of in-frame insertions in mutant proteins encoded by the 5 obtained Vps<sup>+</sup> alleles (<i>vipA-1</i> to <i>vipA-5</i>). The inserted residues in each allele are shown below the sequence. The predicted secondary structure is depicted, with alpha-helices as rectangles, beta-strands as block arrows (PSIPRED v2.6 software <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#ppat.1002546-Jones1\" target=\"_blank\">[54]</a> and the central coiled-coil motif as dashed line (SMART software <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#ppat.1002546-Letunic1\" target=\"_blank\">[55]</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#ppat.1002546-Schultz1\" target=\"_blank\">[56] </a><b>B.</b> Pull-down assays with G-actin and wild-type VipA or mutant VipA-1 proteins. U937 Post-nuclear supernatants were incubated with Ni-NTA agarose beads preloaded with His<sub>6</sub>-VipA or His<sub>6</sub>-VipA-1, washed and eluted with 500 mM Imidazole. Eluates were resolved by SDS-PAGE, transferred to nitrocellulose and analyzed by Western-blot with monoclonal antibodies against polyHistidine (α-polyHis) or against actin (α-Actin).</p>", "links"=>[], "tags"=>["phenotype", "vipa", "mutants", "linked", "actin"], "article_id"=>346971, "categories"=>["Cell Biology"], "users"=>["Irina Saraiva Franco", "Nadim Shohdy", "Howard A. Shuman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002546.g002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Vps_phenotype_of_VipA_mutants_is_linked_to_actin_binding_/346971", "title"=>"Vps <sup>+</sup> phenotype of VipA mutants is linked to actin binding.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-23 01:56:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/345767", "https://ndownloader.figshare.com/files/345836", "https://ndownloader.figshare.com/files/345946", "https://ndownloader.figshare.com/files/346014", "https://ndownloader.figshare.com/files/346080"], "description"=>"<div><p><em>Legionella pneumophila</em>, the causative agent of Legionnaires' disease, invades and replicates within macrophages and protozoan cells inside a vacuole. The type IVB Icm/Dot secretion system is necessary for the translocation of effector proteins that modulate vesicle trafficking pathways in the host cell, thus avoiding phagosome-lysosome fusion. The Legionella VipA effector was previously identified by its ability to interfere with organelle trafficking in the Multivesicular Body (MVB) pathway when ectopically expressed in yeast. In this study, we show that VipA binds actin <em>in vitro</em> and directly polymerizes microfilaments without the requirement of additional proteins, displaying properties distinct from other bacterial actin nucleators. Microscopy studies revealed that fluorescently tagged VipA variants localize to puncta in eukaryotic cells. In yeast these puncta are associated with actin-rich regions and components of the Multivesicular Body pathway such as endosomes and the MVB-associated protein Bro1. During macrophage infection, native translocated VipA associated with actin patches and early endosomes. When ectopically expressed in mammalian cells, VipA-GFP displayed a similar distribution ruling out the requirement of additional effectors for binding to its eukaryotic targets. Interestingly, a mutant form of VipA, VipA-1, that does not interfere with organelle trafficking is also defective in actin binding as well as association with early endosomes and shows a homogeneous cytosolic localization. These results show that the ability of VipA to bind actin is related to its association with a specific subcellular location as well as its role in modulating organelle trafficking pathways. VipA constitutes a novel type of actin nucleator that may contribute to the intracellular lifestyle of Legionella by altering cytoskeleton dynamics to target host cell pathways.</p> </div>", "links"=>[], "tags"=>["effector", "vipa", "actin", "nucleator", "alters", "organelle", "trafficking"], "article_id"=>128346, "categories"=>["Cell Biology"], "users"=>["Irina Saraiva Franco", "Nadim Shohdy", "Howard A. Shuman"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002546.s001", "https://dx.doi.org/10.1371/journal.ppat.1002546.s002", "https://dx.doi.org/10.1371/journal.ppat.1002546.s003", "https://dx.doi.org/10.1371/journal.ppat.1002546.s004", "https://dx.doi.org/10.1371/journal.ppat.1002546.s005"], "stats"=>{"downloads"=>41, "page_views"=>37, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Legionella_pneumophila_Effector_VipA_Is_an_Actin_Nucleator_That_Alters_Host_Cell_Organelle_Trafficking/128346", "title"=>"The <em>Legionella pneumophila</em> Effector VipA Is an Actin Nucleator That Alters Host Cell Organelle Trafficking", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-02-23 02:19:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/676699"], "description"=>"<p><b>A.</b> Yeast strains producing GFP, VipA-GFP or VipA-1-GFP (respectively strains SCIF00, SCIF01 and SCIF02) were grown in medium with fructose or galactose to an OD<sub>600</sub>∼0.5. Equivalent amounts of cell lysates were run on SDS-PAGE and analysed by Western-blot using an anti-GFP polyclonal antibody <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#ppat.1002546-Murata1\" target=\"_blank\">[57]</a>. The arrow points to the bands corresponding to VipA-GFP or VipA-1-GFP fusion proteins. <b>B.</b> The same strains grown in galactose were viewed using Laser Scanning Confocal microscopy and representative images are shown (left). <b>C.</b> Colocalization of VipA-mCherry and actin structures in yeast. Yeast strains producing mCherry, VipA-mCherry or VipA-1-mCherry and Abp1-GFP (left) or Abp140-GFP (right; see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#ppat.1002546.s004\" target=\"_blank\">Table S1</a>) were grown and visualized as above.</p>", "links"=>[], "tags"=>["vipa-gfp"], "article_id"=>347194, "categories"=>["Cell Biology"], "users"=>["Irina Saraiva Franco", "Nadim Shohdy", "Howard A. Shuman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002546.g004", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Localization_of_VipA_GFP_in_S_cerevisiae_/347194", "title"=>"Localization of VipA-GFP in <i>S. cerevisiae</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-23 01:59:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/676808"], "description"=>"<p><b>A.</b> For vacuole staining, <i>S. cerevisiae</i> strains were grown as above (see legend of <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#ppat-1002546-g004\" target=\"_blank\">Figure 4</a>), harvested and additionally pulse-chased with N-(3-triethylammoniumpropyl)-4-(p-diethylaminophenylhexatrienyl)-pyridinium dibromide (FM4-64). <b>B.</b> Strains carrying the fusions Bro1-GFP (left) and mCherry, VipA-mCherry or VipA-1-mCherry were grown and visualized as above.</p>", "links"=>[], "tags"=>["associates", "components", "yeast", "mvb"], "article_id"=>347304, "categories"=>["Cell Biology"], "users"=>["Irina Saraiva Franco", "Nadim Shohdy", "Howard A. Shuman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002546.g005", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_VipA_associates_with_components_of_the_yeast_MVB_pathway_/347304", "title"=>"VipA associates with components of the yeast MVB pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-23 02:01:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/677065"], "description"=>"<p><b>A.</b> THP-1 macrophages were infected as above (see Legend of <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#ppat-1002546-g006\" target=\"_blank\">Figure 6</a> and <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#s2\" target=\"_blank\">Materials and Methods</a>). F-Actin was stained with Rhodamine-phalloidin and Early Endosomes using an αEEA-1 antibody. <b>B.</b> Quantification of colocalization between VipA and F-Actin or EEA-1 was performed by calculating the Manders coefficient using ImageJ and the Plugin JACoP (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#s2\" target=\"_blank\">Materials and Methods</a> for details). The Manders coefficient corresponds to the fraction of VipA-GFP or VipA-1-GFP (blue signal) overlapping with each marker (green or red signal) divided by the total green signal in an image. Filled symbols represent cells expressing VipA-GFP (n>15), open symbols cells expressing VipA-1-GFP, and bars indicate mean and standard deviation. Statistical analysis was performed with unpaired t test, and p values obtained are indicated (**, p<0.01; ***, p<0.001).</p>", "links"=>[], "tags"=>["vipa", "endosomes", "actin", "macrophage"], "article_id"=>347554, "categories"=>["Cell Biology"], "users"=>["Irina Saraiva Franco", "Nadim Shohdy", "Howard A. Shuman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002546.g007", "stats"=>{"downloads"=>1, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Colocalization_of_VipA_with_host_cell_early_endosomes_and_actin_in_macrophage_infection_/347554", "title"=>"Colocalization of VipA with host cell early endosomes and actin in macrophage infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-23 02:05:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/676400"], "description"=>"<p><b>A.</b> U937 cell Post-Nuclear Supernatants (U937 PNS) were incubated with Ni-NTA agarose beads preloaded with His<sub>6</sub>-VipA or His<sub>6</sub>-FabI (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#s2\" target=\"_blank\">Materials and Methods</a> for details). After washing, bound proteins were eluted with 500 mM Imidazole. Samples containing preloaded beads or eluates were resolved by SDS-PAGE and bands visualized by Coomassie staining. The differential band appearing in the VipA eluate (arrow) was excised and identified by LC/MS as β-actin. <b>B.</b> Similarly prepared samples were resolved by SDS-PAGE, transferred to nitrocellulose and immunoblotted with an anti-actin monoclonal antibody (α-actin). <b>C.</b> Ni-NTA agarose beads preloaded with His<sub>6</sub>-FabI or His<sub>6</sub>-VipA were incubated with increasing concentrations of purified G-actin, washed and eluted. Eluates were resolved by SDS-PAGE, transferred to nitrocellulose and Western-blotted with an anti-histidine antibody (α-polyHis, panel above) or an anti-actin monoclonal antibody (α-actin, panel below).</p>", "links"=>[], "tags"=>["actin", "pull-down"], "article_id"=>346894, "categories"=>["Cell Biology"], "users"=>["Irina Saraiva Franco", "Nadim Shohdy", "Howard A. Shuman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002546.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_vitro_interaction_analysis_between_His_6_VipA_and_actin_by_pull_down_assays_/346894", "title"=>"<i>In vitro</i> interaction analysis between His<sub>6</sub>-VipA and actin by pull-down assays.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-23 01:54:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/676583"], "description"=>"<p>Samples contained 2 µM monomeric actin (10% Pyrene-actin) and fluorescence (expressed in Arbitrary Units, AU) was measured over time after initiation of polymerization. <b>A.</b> The displayed concentrations of His<sub>6</sub>-VipA were added to the samples and polymerization initiated. The graph on the right is a plot of the average and standard deviation for the rates of actin polymerization for each His<sub>6</sub>-VipA concentration. Velocities were determined for the interval 600–1200 s using the results of two independent experiments. <b>B</b> and <b>C.</b> Actin samples contained 10 nM Arp2/3 complex, 400 nM WASP-VCA (Cytoskeleton), 400 nM His<sub>6</sub>-VipA, 560 nM His<sub>6</sub>-VipA-1 and 10 nM of mDia2 where indicated. <b>D.</b> Elongation of filaments was carried out using phalloidin-stabilized actin seeds and 1 µM of G-actin (10% Py-labeled), in the presence of His<sub>6</sub>-VipA-1 (100 nM) or Cytochalasin D (100 nM). Determination of F-actin concentration and rates of polymerization are described in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#s2\" target=\"_blank\">Materials and Methods</a>.</p>", "links"=>[], "tags"=>["actin", "polymerization"], "article_id"=>347076, "categories"=>["Cell Biology"], "users"=>["Irina Saraiva Franco", "Nadim Shohdy", "Howard A. Shuman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002546.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_vitro_actin_polymerization_assays_/347076", "title"=>"<i>In vitro</i> actin polymerization assays.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-23 01:57:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/676928"], "description"=>"<p>THP-1 macrophages were infected with <i>L. pneumophila</i> strains (JR32, <i>ΔvipA</i>, <i>ΔvipA pMMB207c-Ptac-vipA</i> or <i>ΔvipA pMMB207c-Ptac-vipA-1</i>) with an MOI = 50 for 8 hours. Immunofluorescence was carried out as described (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002546#s2\" target=\"_blank\">Materials and Methods</a>). DNA was stained with DAPI and VipA with a purified polyclonal anti-VipA antibody. <b>A.</b> and F-actin was stained with Rhodamine-phalloidin. <b>B.</b> Representative confocal microscopy images are shown. <b>C.</b> Immunoblot of samples containing lysates of THP-1 macrophages infected for 3 hr with the indicated <i>L. pneumophila</i> strains at an MOI = 50 (see Material and Methods). P, lysate pellet; SN, lysate supernatant.</p>", "links"=>[], "tags"=>["translocated", "vipa", "vipa-1", "thp-1"], "article_id"=>347423, "categories"=>["Cell Biology"], "users"=>["Irina Saraiva Franco", "Nadim Shohdy", "Howard A. Shuman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002546.g006", "stats"=>{"downloads"=>2, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Localization_of_translocated_VipA_and_VipA_1_during_infection_of_THP_1_macrophages_/347423", "title"=>"Localization of translocated VipA and VipA-1 during infection of THP-1 macrophages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-23 02:03:43"}

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Relative Metric

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