Cellular Levels and Binding of c-di-GMP Control Subcellular Localization and Activity of the Vibrio cholerae Transcriptional Regulator VpsT
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{"title"=>"Cellular levels and binding of c-di-GMP control subcellular localization and activity of the Vibrio cholerae transcriptional regulator VpsT", "type"=>"journal", "authors"=>[{"first_name"=>"Nicholas J.", "last_name"=>"Shikuma", "scopus_author_id"=>"26658756100"}, {"first_name"=>"Jiunn C N", "last_name"=>"Fong", "scopus_author_id"=>"34568641400"}, {"first_name"=>"Fitnat H.", "last_name"=>"Yildiz", "scopus_author_id"=>"7006760654"}], "year"=>2012, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "pui"=>"365220903", "doi"=>"10.1371/journal.ppat.1002719", "sgr"=>"84863692958", "scopus"=>"2-s2.0-84863692958", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "pmid"=>"22654664"}, "id"=>"9d98617e-7256-341d-9ffd-8bfdec8e4442", "abstract"=>"The second messenger, cyclic diguanylate (c-di-GMP), regulates diverse cellular processes in bacteria. C-di-GMP is produced by diguanylate cyclases (DGCs), degraded by phosphodiesterases (PDEs), and receptors couple c-di-GMP production to cellular responses. In many bacteria, including Vibrio cholerae, multiple DGCs and PDEs contribute to c-di-GMP signaling, and it is currently unclear whether the compartmentalization of c-di-GMP signaling components is required to mediate c-di-GMP signal transduction. In this study we show that the transcriptional regulator, VpsT, requires c-di-GMP binding for subcellular localization and activity. Only the additive deletion of five DGCs markedly decreases the localization of VpsT, while single deletions of each DGC do not impact VpsT localization. Moreover, mutations in residues required for c-di-GMP binding, c-di-GMP-stabilized dimerization and DNA binding of VpsT abrogate wild type localization and activity. VpsT does not co-localize or interact with DGCs suggesting that c-di-GMP from these DGCs diffuses to VpsT, supporting a model in which c-di-GMP acts at a distance. Furthermore, VpsT localization in a heterologous host, Escherichia coli, requires a catalytically active DGC and is enhanced by the presence of VpsT-target sequences. Our data show that c-di-GMP signaling can be executed through an additive cellular c-di-GMP level from multiple DGCs affecting the localization and activity of a c-di-GMP receptor and furthers our understanding of the mechanisms of second messenger signaling.", "link"=>"http://www.mendeley.com/research/cellular-levels-binding-cdigmp-control-subcellular-localization-activity-vibrio-cholerae-transcripti", "reader_count"=>37, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>13, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>6, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>13, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>6, "Professor"=>2}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>27, "Physics and Astronomy"=>1, "Chemistry"=>2, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>27}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}}, "reader_count_by_country"=>{"Belgium"=>1, "United States"=>1, "Estonia"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/633882"], "description"=>"<p>(A) Representative epifluorescence micrographs of <i>E. coli</i> strains expressing GFP or GFP-VpsT and containing a pKNT25 compatible plasmid or pKNT25 harboring <i>cdgA</i>, <i>cdgA</i><sup>G287A</sup>, <i>vpsL</i> promoter (<i>vpsLp</i>), <i>cdgA</i> and <i>vpsLp</i> or <i>adrA</i> from <i>S. typhimurium</i>. Marker is 2 µm. (B) Single-cell quantification of subcellular fluorescence localization. The number of spots per cell is shown as a histogram for <i>E. coli</i> strains containing the indicated plasmids. Data are acquired from at least 3 independent experiments and quantification was performed on at least 150 cells per treatment. (C) Representative motility phenotypes of <i>E. coli</i> expressing the indicated plasmids grown on soft agar plates containing kanamycin and 10 µM IPTG at 37°C for 12 h.</p>", "links"=>[], "tags"=>["localization", "heterologous", "depends"], "article_id"=>304379, "categories"=>["Genetics"], "users"=>["Nicholas J. Shikuma", "Jiunn C. N. Fong", "Fitnat H. Yildiz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002719.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_VpsT_Localization_in_a_Heterologous_Host_Depends_on_c_di_GMP_/304379", "title"=>"VpsT Localization in a Heterologous Host Depends on c-di-GMP.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-24 01:12:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/634006"], "description"=>"<p>Expression of the <i>vpsL</i> promoter fused to a <i>lux</i> reporter operon in <i>E. coli</i> expressing GFP or GFP-VpsT and harboring pKNT vector alone or pKNT containing <i>cdgA</i>. Expression is reported in luminescence counts min<sup>−1</sup> ml<sup>−1</sup>/OD<sub>600 nm</sub>. One representative experiment of three biological replicates is shown. Error bars indicate standard deviations of four technical replicates.</p>", "links"=>[], "tags"=>["vpst", "cdga", "activates"], "article_id"=>304506, "categories"=>["Genetics"], "users"=>["Nicholas J. Shikuma", "Jiunn C. N. Fong", "Fitnat H. Yildiz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002719.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Co_expression_of_VpsT_and_CdgA_Activates_vpsL_Expression_in_E_coli_/304506", "title"=>"Co-expression of VpsT and CdgA Activates <i>vpsL</i> Expression in <i>E. coli.</i>", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-24 01:15:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/633770"], "description"=>"<p>(A) The expression of a chromosomal <i>vpsL</i> promoter-<i>lacZ</i> fusion was measured in wild type (Wt) or Δ<i>vpsT</i> strains containing pBAD vector alone, or pBAD containing <i>gfp</i> fused to wild type and mutated versions of <i>vpsT</i> using β-galactosidase assays. A R134A mutation disrupts c-di-GMP binding and an I141E mutation abolishes c-di-GMP-dependent dimerization. H193A lies in the DNA binding domain of VpsT. (B) Subcellular localization of GFP, GFP-VpsT or GFP-VpsT containing the indicated point mutations, expressed in <i>V. cholerae</i> Δ<i>vpsT</i>. Representative epifluorescence micrographs are shown. Marker is 2 µm. (C) Single-cell quantification of subcellular fluorescence localization. The number of spots per cell is shown as a histogram for Δ<i>vpsT</i> strains expressing GFP, GFP-VpsT or GFP-VpsT containing the indicated point mutations. Data are acquired from at least 3 independent experiments and quantification was performed on at least 150 cells per treatment.</p>", "links"=>[], "tags"=>["subcellular", "localization", "vpst", "c-di-gmp", "binding", "dna"], "article_id"=>304259, "categories"=>["Genetics"], "users"=>["Nicholas J. Shikuma", "Jiunn C. N. Fong", "Fitnat H. Yildiz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002719.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Subcellular_Localization_of_VpsT_is_Dependent_on_c_di_GMP_Binding_and_DNA_Binding_Residues_/304259", "title"=>"The Subcellular Localization of VpsT is Dependent on c-di-GMP Binding and DNA Binding Residues.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-24 01:10:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/633656"], "description"=>"<p>(A) Representative epifluorescence micrographs of wild-type <i>V. cholerae</i> expressing GFP-VpsT, CdgA-GFP or CdgH-GFP fusion proteins. Marker is 2 µm. (B) Subcellular fractionation of <i>V. cholerae</i> strains containing <i>vpsT</i>, <i>cdgA</i> or <i>cdgH</i> tagged with an HA epitope in their native chromosomal loci. Western immunoblot was performed on cellular fractions representing whole cell (WC), cytoplasmic (C) and total membrane (M) fractions. HA-tagged proteins were detected using a polyclonal anti-HA antibody. <i>gfp</i> was constitutively expressed from a chromosomal locus. GFP was detected using monoclonal anti-GFP antibody and is used as a cytoplasmic fraction control. OmpU was detected using a polyclonal anti-OmpU antibody and is used as a total membrane fraction control. One representative experiment of three biological replicates is shown. (C) Bacterial two-hybrid analysis of VpsT, CdgA and CdgH. Reconstitution of CyaA, indicative of protein-protein interaction, was detected by β-galactosidase activity on LB plates containing ampicillin (100 µg/ml), kanamycin (50 µg/ml), IPTG (500 µM) and X-gal (40 µg/ml). Plates were incubated at 30°C for 48 h.</p>", "links"=>[], "tags"=>["cdga", "cdgh"], "article_id"=>304144, "categories"=>["Genetics"], "users"=>["Nicholas J. Shikuma", "Jiunn C. N. Fong", "Fitnat H. Yildiz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002719.g002", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_VpsT_Does_Not_Interact_with_CdgA_or_CdgH_Directly_/304144", "title"=>"VpsT Does Not Interact with CdgA or CdgH Directly.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-24 01:09:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/633530"], "description"=>"<p>(A) The expression of a chromosomal <i>vpsL</i> promoter-<i>lacZ</i> fusion was measured in wild type (Wt) or Δ<i>vpsT</i> strains containing pBAD vector alone, or pBAD containing <i>vpsT</i> or <i>gfp</i>-<i>vpsT</i> using β-galactosidase assays. One representative experiment of three biological replicates is shown. Error bars indicate standard deviations of eight technical replicates. (B) Representative epifluorescence micrographs are shown of the subcellular localization of GFP or GFP-VpsT fusion protein in wild-type or Δ5DGC <i>V. cholerae</i> strains. Marker is 2 µm. (C) Single-cell quantification of subcellular fluorescence localization. The number of spots per cell is shown as a histogram for wild type or Δ5DGC strains expressing GFP or GFP-VpsT. Data are acquired from at least 3 independent experiments and quantification was performed on at least 150 cells per treatment. (D) Expression of the <i>vpsL</i> promoter fused to a <i>lux</i> reporter operon in wild-type <i>V. cholerae</i> (Wt) or strains containing single in-frame deletions of the genes encoding DGCs <i>cdgA</i>, <i>cdgH</i>, <i>cdgK</i>, <i>cdgL</i>, <i>cdgM</i> or a strain containing in-frame deletions all 5 DGCs (Δ5DGC). Expression is reported in luminescence counts min<sup>−1</sup> ml<sup>−1</sup>/OD<sub>600 nm</sub>. One representative experiment of three biological replicates is shown. Error bars indicate standard deviations of four technical replicates. (E) Percent c-di-GMP levels of single in-frame deletion DGC mutants or the Δ5DGC strain compared to wild type <i>V. cholerae</i> using high-performance liquid chromatography-tandem mass spectrometry. Error bars indicate standard deviations of three biological replicates.</p>", "links"=>[], "tags"=>["localization", "diguanylate"], "article_id"=>304024, "categories"=>["Genetics"], "users"=>["Nicholas J. Shikuma", "Jiunn C. N. Fong", "Fitnat H. Yildiz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002719.g001", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_VpsT_Localization_is_Dependent_on_Multiple_Diguanylate_Cyclases_/304024", "title"=>"VpsT Localization is Dependent on Multiple Diguanylate Cyclases.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-24 01:07:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/634066"], "description"=>"<p>Cellular c-di-GMP levels modulate VpsT oligomerization and subcellular localization. The additive effect of 5 membrane-bound DGCs regulates cellular c-di-GMP levels modulating VpsT oligomerization state, localization and DNA binding. Cytoplasmic membrane (CM).</p>", "links"=>[], "tags"=>["c-di-gmp", "transduction"], "article_id"=>304567, "categories"=>["Genetics"], "users"=>["Nicholas J. Shikuma", "Jiunn C. N. Fong", "Fitnat H. Yildiz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002719.g006", "stats"=>{"downloads"=>1, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_of_c_di_GMP_Signal_Transduction_in_V_cholerae_/304567", "title"=>"Model of c-di-GMP Signal Transduction in <i>V. cholerae</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-24 01:16:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/327682", "https://ndownloader.figshare.com/files/327783", "https://ndownloader.figshare.com/files/327846", "https://ndownloader.figshare.com/files/327882", "https://ndownloader.figshare.com/files/327930", "https://ndownloader.figshare.com/files/327990", "https://ndownloader.figshare.com/files/328025", "https://ndownloader.figshare.com/files/328099", "https://ndownloader.figshare.com/files/328156"], "description"=>"<div><p>The second messenger, cyclic diguanylate (c-di-GMP), regulates diverse cellular processes in bacteria. C-di-GMP is produced by diguanylate cyclases (DGCs), degraded by phosphodiesterases (PDEs), and receptors couple c-di-GMP production to cellular responses. In many bacteria, including <em>Vibrio cholerae</em>, multiple DGCs and PDEs contribute to c-di-GMP signaling, and it is currently unclear whether the compartmentalization of c-di-GMP signaling components is required to mediate c-di-GMP signal transduction. In this study we show that the transcriptional regulator, VpsT, requires c-di-GMP binding for subcellular localization and activity. Only the additive deletion of five DGCs markedly decreases the localization of VpsT, while single deletions of each DGC do not impact VpsT localization. Moreover, mutations in residues required for c-di-GMP binding, c-di-GMP-stabilized dimerization and DNA binding of VpsT abrogate wild type localization and activity. VpsT does not co-localize or interact with DGCs suggesting that c-di-GMP from these DGCs diffuses to VpsT, supporting a model in which c-di-GMP acts at a distance. Furthermore, VpsT localization in a heterologous host, <em>Escherichia coli</em>, requires a catalytically active DGC and is enhanced by the presence of VpsT-target sequences. Our data show that c-di-GMP signaling can be executed through an additive cellular c-di-GMP level from multiple DGCs affecting the localization and activity of a c-di-GMP receptor and furthers our understanding of the mechanisms of second messenger signaling.</p> </div>", "links"=>[], "tags"=>["cellular", "levels", "binding", "c-di-gmp", "subcellular", "localization", "transcriptional", "vpst"], "article_id"=>124696, "categories"=>["Genetics"], "users"=>["Nicholas J. Shikuma", "Jiunn C. N. Fong", "Fitnat H. Yildiz"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002719.s001", "https://dx.doi.org/10.1371/journal.ppat.1002719.s002", "https://dx.doi.org/10.1371/journal.ppat.1002719.s003", "https://dx.doi.org/10.1371/journal.ppat.1002719.s004", "https://dx.doi.org/10.1371/journal.ppat.1002719.s005", "https://dx.doi.org/10.1371/journal.ppat.1002719.s006", "https://dx.doi.org/10.1371/journal.ppat.1002719.s007", "https://dx.doi.org/10.1371/journal.ppat.1002719.s008", "https://dx.doi.org/10.1371/journal.ppat.1002719.s009"], "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Cellular_Levels_and_Binding_of_c_di_GMP_Control_Subcellular_Localization_and_Activity_of_the_Vibrio_cholerae_Transcriptional_Regulator_VpsT/124696", "title"=>"Cellular Levels and Binding of c-di-GMP Control Subcellular Localization and Activity of the <em>Vibrio cholerae</em> Transcriptional Regulator VpsT", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-05-24 01:18:16"}

PMC Usage Stats | Further Information

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Relative Metric

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