The Common Structural Architecture of Shigella flexneri and Salmonella typhimurium Type Three Secretion Needles
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{"title"=>"The Common Structural Architecture of Shigella flexneri and Salmonella typhimurium Type Three Secretion Needles", "type"=>"journal", "authors"=>[{"first_name"=>"Jean Philippe", "last_name"=>"Demers", "scopus_author_id"=>"35195439500"}, {"first_name"=>"Nikolaos G.", "last_name"=>"Sgourakis", "scopus_author_id"=>"8855979100"}, {"first_name"=>"Rashmi", "last_name"=>"Gupta", "scopus_author_id"=>"57198324877"}, {"first_name"=>"Antoine", "last_name"=>"Loquet", "scopus_author_id"=>"23767233300"}, {"first_name"=>"Karin", "last_name"=>"Giller", "scopus_author_id"=>"8545546100"}, {"first_name"=>"Dietmar", "last_name"=>"Riedel", "scopus_author_id"=>"7006348787"}, {"first_name"=>"Britta", "last_name"=>"Laube", "scopus_author_id"=>"35748802700"}, {"first_name"=>"Michael", "last_name"=>"Kolbe", "scopus_author_id"=>"35491060900"}, {"first_name"=>"David", "last_name"=>"Baker", "scopus_author_id"=>"55463548900"}, {"first_name"=>"Stefan", "last_name"=>"Becker", "scopus_author_id"=>"7402398883"}, {"first_name"=>"Adam", "last_name"=>"Lange", "scopus_author_id"=>"12785303300"}], "year"=>2013, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "sgr"=>"84875971148", "scopus"=>"2-s2.0-84875971148", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "pui"=>"368694529", "doi"=>"10.1371/journal.ppat.1003245", "pmid"=>"23555258"}, "id"=>"bebdb4df-5ce9-3f92-aa0a-2874376b686a", "abstract"=>"... Abstract. The Type Three Secretion System (T3SS), or injectisome , is a macromolecular infection machinery present in many pathogenic Gram-negative bacteria. It consists of a basal body, anchored in both bacterial membranes ... \\n", "link"=>"http://www.mendeley.com/research/common-structural-architecture-shigella-flexneri-salmonella-typhimurium-type-three-secretion-needles", "reader_count"=>54, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>4, "Researcher"=>13, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>6, "Lecturer"=>5, "Professor"=>1, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>4, "Researcher"=>13, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>6, "Lecturer"=>5, "Professor"=>1, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>12, "Mathematics"=>1, "Agricultural and Biological Sciences"=>32, "Medicine and Dentistry"=>2, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>3, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>32}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>12}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"United States"=>1, "United Kingdom"=>2}, "group_count"=>3}

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Figshare

  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/994662/Figure_1.tif"], "description"=>"<p><i>A</i>, Model of <i>Shigella flexneri</i> T3SS needle based on a 7.7-Å cryoEM map, according to Ref. <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003245#ppat.1003245-Fujii1\" target=\"_blank\">[19]</a>, PDB ID: 3J0R. The structure of the MxiH subunit protein contains an α-helix (S2-A38), a loop (K39-P44), an α-helix (Q45-Y50), a 14-residue-long β-hairpin (Q51–Q64) and an α-helix (S65-R83) with a kink at D73. The N-terminus faces inward to the lumen of the needle. <i>B</i>, Solid-state NMR atomic model of the <i>Salmonella typhimurium</i> T3SS needle according to Ref. <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003245#ppat.1003245-Loquet1\" target=\"_blank\">[20]</a>, PDB ID: 2LPZ. The structure of the PrgI subunit protein comprises a rigid-extended conformation (T3-Y8), an α-helix (L9-A35) with a kink at N22, a loop (A36-P41), and an α-helix (A42-R80). The N-terminus is located at the surface of the needle. Top views of the needle assemblies are shown in the top corners. The structures in the bottom corners present the location of highly conserved residues that were identified from multiple sequence alignment (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003245#ppat-1003245-g002\" target=\"_blank\">Fig. 2</a>). The atoms of conserved amino acids are represented as spheres and are colored respectively blue or red depending if their amino acid belongs to the N- or the C-terminal region. Conserved residues are lining the lumen of the needle in the <i>Salmonella</i> model but are exposed to the extracellular milieu in the <i>Shigella</i> model.</p>", "links"=>[], "tags"=>["topologies", "t3ss", "proteins"], "article_id"=>657724, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Jean-Philippe Demers", "Nikolaos G. Sgourakis", "Rashmi Gupta", "Antoine Loquet", "Karin Giller", "Dietmar Riedel", "Britta Laube", "Michael Kolbe", "David Baker", "Stefan Becker", "Adam Lange"], "doi"=>["http://dx.doi.org/10.1371/journal.ppat.1003245.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Proposed_topologies_for_T3SS_needle_proteins_in_the_needle_assembly_/657724", "title"=>"Proposed topologies for T3SS needle proteins in the needle assembly.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-22 08:19:49"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/994663/Figure_2.tif"], "description"=>"<p>Conserved residues are colored according to amino acid type following the Clustal X color scheme <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003245#ppat.1003245-Thompson1\" target=\"_blank\">[75]</a>. Highly conserved residues (≥12 identical amino acids in both clusters) are highlighted with a star (N-terminal region: blue; C-terminal region: red). The numbering of residues corresponds to the sequence of MxiH. Database accession identifiers for the primary sequences are given in supplementary Table S3 in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003245#ppat.1003245.s001\" target=\"_blank\">Text S1</a>.</p>", "links"=>[], "tags"=>["alignment", "t3ss"], "article_id"=>657725, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Jean-Philippe Demers", "Nikolaos G. Sgourakis", "Rashmi Gupta", "Antoine Loquet", "Karin Giller", "Dietmar Riedel", "Britta Laube", "Michael Kolbe", "David Baker", "Stefan Becker", "Adam Lange"], "doi"=>["http://dx.doi.org/10.1371/journal.ppat.1003245.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Multiple_sequence_alignment_of_T3SS_needle_proteins_/657725", "title"=>"Multiple sequence alignment of T3SS needle proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-22 08:20:11"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/994664/Figure_3.tif"], "description"=>"<p><i>A</i>, Transmission electron microscopy images of WT <i>Shigella flexneri</i> needles used for solid-state NMR measurements. <i>B</i>, 1D <sup>13</sup>C cross-polarization spectra of [uniform-<sup>13</sup>C<sub>6</sub>]glucose (Glc)-labeled (black), [1-<sup>13</sup>C]Glc-labeled (green) and [2-<sup>13</sup>C]Glc-labeled (magenta) needles. Representative line-widths are indicated for two resonances (T23Cβ and N81Cα) for the sparsely-labeled samples. The free-induction decay of the signal was recorded for a total of 8192 scans, with signal remaining after an acquisition time of 60 ms. No apodization function was employed in the processing. <i>C</i>, N-Cα spectrum of [2-<sup>13</sup>C]Glc-labeled needles. The 2D spectrum correlates backbone amide nitrogen frequencies (δ<sub>1</sub><sup>15</sup>N) to backbone Cα frequencies (δ<sub>2</sub><sup>13</sup>C). N-Cα cross-peaks are numbered according to the MxiH amino acid sequence and N-Cδ cross-peaks of prolines are indicated. Unmarked cross-peaks correspond to sequential correlations. Spectra were recorded at a magnetic field of 21.1 T (850 MHz <sup>1</sup>H resonance frequency) at 5.5°C.</p>", "links"=>[], "tags"=>["nmr", "spectroscopy", "mxih"], "article_id"=>657726, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Jean-Philippe Demers", "Nikolaos G. Sgourakis", "Rashmi Gupta", "Antoine Loquet", "Karin Giller", "Dietmar Riedel", "Britta Laube", "Michael Kolbe", "David Baker", "Stefan Becker", "Adam Lange"], "doi"=>["http://dx.doi.org/10.1371/journal.ppat.1003245.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Solid_state_NMR_spectroscopy_of_Shigella_flexneri_MxiH_needles_/657726", "title"=>"Solid-state NMR spectroscopy of <i>Shigella flexneri</i> MxiH needles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-22 08:20:26"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/994665/Figure_4.tif"], "description"=>"<p><i>A</i>, Secondary structure elements identified in the cryoEM model of Fujii <i>et al.</i>; adapted from <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003245#ppat-1003245-g001\" target=\"_blank\">Fig. 1e</a> in Ref. <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003245#ppat.1003245-Fujii1\" target=\"_blank\">[19]</a> where H1, H2, and H3 indicate the position of α-helices and “prot” that of the β-hairpin between H2 and H3. <i>B</i>, Secondary structure elements of MxiH needles determined by solid-state NMR (this study). <i>C</i>, Secondary chemical shifts (ΔδCα – ΔδCβ) of the <i>Shigella flexneri</i> MxiH protein in the assembled needle. Regions which do not present α-helical propensity are highlighted. <i>D,</i> Secondary chemical shifts of the <i>Salmonella tympimurium</i> PrgI protein in the assembled needle taken from Ref. <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003245#ppat.1003245-Loquet2\" target=\"_blank\">[37]</a>.</p>", "links"=>[], "tags"=>["microbiology", "Biochemistry"], "article_id"=>657727, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Jean-Philippe Demers", "Nikolaos G. Sgourakis", "Rashmi Gupta", "Antoine Loquet", "Karin Giller", "Dietmar Riedel", "Britta Laube", "Michael Kolbe", "David Baker", "Stefan Becker", "Adam Lange"], "doi"=>["http://dx.doi.org/10.1371/journal.ppat.1003245.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Identification_of_secondary_structure_elements_/657727", "title"=>"Identification of secondary structure elements.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-22 08:20:37"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/994667/Figure_5.tif"], "description"=>"<p><i>A</i>, Top and <i>B</i>, side views of the T3SS needle assembly of <i>Shigella flexneri</i>. The homology model of the 29-subunit MxiH needle assembly generated by Rosetta modeling (cartoon representation) shows a correlation of 0.66 with the 7.7-Å cryoEM density map (grey surface). Using the nomenclature of Fujii <i>et al.</i>, the EM density regions H1, H2 and H3 are indicated for the central subunit (i), as well as the kink in region H3. The first 11 N-terminal residues are not depicted due to the poor sequence homology of the rigid-extended segment (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003245#ppat-1003245-g002\" target=\"_blank\">Fig. 2</a>); however the protrusion in the EM map at subunit (i), labeled prot. and highlighted by a purple dashed contour trace, may be well explained by the N-terminus of subunit (i+5). The central subunit (i), colored as in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003245#ppat-1003245-g001\" target=\"_blank\">Fig. 1<i>B</i></a>, forms a lateral interface with subunits (i±5), in red, and subunits (i±6), in dark blue. The axial interface is formed with subunits (i±11) shown in pink.</p>", "links"=>[], "tags"=>["t3ss"], "article_id"=>657729, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Jean-Philippe Demers", "Nikolaos G. Sgourakis", "Rashmi Gupta", "Antoine Loquet", "Karin Giller", "Dietmar Riedel", "Britta Laube", "Michael Kolbe", "David Baker", "Stefan Becker", "Adam Lange"], "doi"=>["http://dx.doi.org/10.1371/journal.ppat.1003245.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Structural_model_of_the_T3SS_Shigella_needle_/657729", "title"=>"Structural model of the T3SS <i>Shigella</i> needle.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-22 08:21:04"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/994669/Figure_6.tif"], "description"=>"<p><i>A</i>–<i>C</i>, Immunogold labeling of recombinant <i>Shigella flexneri</i> MxiH needles using a monoclonal Anti-His tag antibody. <i>A</i>, WT MxiH needles <i>B</i>, needles polymerized from N-terminal His tag fusion construct, <i>mxiH</i>-N(His), <i>C</i>, <i>mxiH</i>-N(His) needles labeled without primary Anti-His tag antibody. In <i>B</i>, some gold particles are indicated by arrows. Proteins expressed from a C-terminal His tag fusion construct did not polymerize. <i>D</i>, Effector protein secretion assay of <i>Shigella</i> strains used in Fig. <i>E</i>–<i>G</i> by addition of Congo Red (CR) followed by western blot analysis against IpaB, IpaC and DnaK. <i>E</i>–<i>G</i>, Non-polar <i>Shigella</i> mxiH-knockout cells (<i>ΔmxiH</i>) expressing <i>E</i>, wild-type <i>mxiH</i>, <i>F</i>, mxiH with N-terminal Strep-tag, <i>mxiH</i>-N(Strep) or <i>G</i>, MxiH with C-terminal Strep-tag, <i>mxiH</i>-C(Strep). In <i>E</i> and <i>F</i>, needles are indicated by arrows and two needles complexes are highlighted.</p>", "links"=>[], "tags"=>["mxih", "subunit", "n-terminus"], "article_id"=>657730, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Jean-Philippe Demers", "Nikolaos G. Sgourakis", "Rashmi Gupta", "Antoine Loquet", "Karin Giller", "Dietmar Riedel", "Britta Laube", "Michael Kolbe", "David Baker", "Stefan Becker", "Adam Lange"], "doi"=>["http://dx.doi.org/10.1371/journal.ppat.1003245.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Localization_of_the_MxiH_subunit_N_terminus_in_vitro_and_in_vivo_/657730", "title"=>"Localization of the MxiH subunit N-terminus <i>in vitro</i> and <i>in vivo</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-22 08:21:33"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/994672/Text_S1.doc"], "description"=>"<div><p>The Type Three Secretion System (T3SS), or injectisome, is a macromolecular infection machinery present in many pathogenic Gram-negative bacteria. It consists of a basal body, anchored in both bacterial membranes, and a hollow needle through which effector proteins are delivered into the target host cell. Two different architectures of the T3SS needle have been previously proposed. First, an atomic model of the <i>Salmonella typhimurium</i> needle was generated from solid-state NMR data. The needle subunit protein, PrgI, comprises a rigid-extended N-terminal segment and a helix-loop-helix motif with the N-terminus located on the outside face of the needle. Second, a model of the <i>Shigella flexneri</i> needle was generated from a high-resolution 7.7-Å cryo-electron microscopy density map. The subunit protein, MxiH, contains an N-terminal α-helix, a loop, another α-helix, a 14-residue-long β-hairpin (Q51–Q64) and a C-terminal α-helix, with the N-terminus facing inward to the lumen of the needle. In the current study, we carried out solid-state NMR measurements of wild-type <i>Shigella flexneri</i> needles polymerized <i>in vitro</i> and identified the following secondary structure elements for MxiH: a rigid-extended N-terminal segment (S2-T11), an α-helix (L12-A38), a loop (E39-P44) and a C-terminal α-helix (Q45-R83). Using immunogold labeling <i>in vitro</i> and <i>in vivo</i> on functional needles, we located the N-terminus of MxiH subunits on the exterior of the assembly, consistent with evolutionary sequence conservation patterns and mutagenesis data. We generated a homology model of <i>Shigella flexneri</i> needles compatible with both experimental data: the MxiH solid-state NMR chemical shifts and the state-of-the-art cryoEM density map. These results corroborate the solid-state NMR structure previously solved for <i>Salmonella typhimurium</i> PrgI needles and establish that <i>Shigella flexneri</i> and <i>Salmonella typhimurium</i> subunit proteins adopt a conserved structure and orientation in their assembled state. Our study reveals a common structural architecture of T3SS needles, essential to understand T3SS-mediated infection and develop treatments.</p> </div>", "links"=>[], "tags"=>["secretion", "needles"], "article_id"=>657731, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Jean-Philippe Demers", "Nikolaos G. Sgourakis", "Rashmi Gupta", "Antoine Loquet", "Karin Giller", "Dietmar Riedel", "Britta Laube", "Michael Kolbe", "David Baker", "Stefan Becker", "Adam Lange"], "doi"=>["http://dx.doi.org/10.1371/journal.ppat.1003245"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/The_Common_Structural_Architecture_of_Shigella_flexneri_and_Salmonella_typhimurium_Type_Three_Secretion_Needles__/657731", "title"=>"The Common Structural Architecture of <em>Shigella flexneri</em> and <em>Salmonella typhimurium</em> Type Three Secretion Needles", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-03-22 08:22:16"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/1007906/Table_1.xls"], "description"=>"*<p>Full-atom interface energy in Rosetta energy units, median value of the 10 lowest-energy models.</p>**<p>After refinement of the PDB coordinates.</p>", "links"=>[], "tags"=>["microbiology", "Biochemistry"], "article_id"=>668527, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Jean-Philippe Demers", "Nikolaos G. Sgourakis", "Rashmi Gupta", "Antoine Loquet", "Karin Giller", "Dietmar Riedel", "Britta Laube", "Michael Kolbe", "David Baker", "Stefan Becker", "Adam Lange"], "doi"=>["http://dx.doi.org/10.1371/journal.ppat.1003245.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Structural_statistics_of_different_needle_models_/668527", "title"=>"Structural statistics of different needle models.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-03-21 02:22:07"}

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Relative Metric

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