Structural and Functional Studies on the Interaction of GspC and GspD in the Type II Secretion System
Publication Date
September 08, 2011
Journal
PLOS Pathogens
Authors
Konstantin V. Korotkov, Tanya L. Johnson, Michael G. Jobling, Jonathan Pruneda, et al
Volume
7
Issue
9
Pages
e1002228
DOI
https://dx.plos.org/10.1371/journal.ppat.1002228
Publisher URL
http://journals.plos.org/plospathogens/article?id=10.1371%2Fjournal.ppat.1002228
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21931548
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3169554
Europe PMC
http://europepmc.org/abstract/MED/21931548
Web of Science
000295409000031
Scopus
80053453930
Mendeley
http://www.mendeley.com/research/structural-functional-studies-interaction-gspc-gspd-type-ii-secretion-system-7
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Mendeley | Further Information

{"title"=>"Structural and functional studies on the interaction of gspc and gspd in the type ii secretion system", "type"=>"journal", "authors"=>[{"first_name"=>"Konstantin V.", "last_name"=>"Korotkov", "scopus_author_id"=>"35552072500"}, {"first_name"=>"Tanya L.", "last_name"=>"Johnson", "scopus_author_id"=>"8083663700"}, {"first_name"=>"Michael G.", "last_name"=>"Jobling", "scopus_author_id"=>"57195311527"}, {"first_name"=>"Jonathan", "last_name"=>"Pruneda", "scopus_author_id"=>"42361572000"}, {"first_name"=>"Els", "last_name"=>"Pardon", "scopus_author_id"=>"6506655031"}, {"first_name"=>"Annie", "last_name"=>"Héroux", "scopus_author_id"=>"6701529134"}, {"first_name"=>"Stewart", "last_name"=>"Turley", "scopus_author_id"=>"7004549579"}, {"first_name"=>"Jan", "last_name"=>"Steyaert", "scopus_author_id"=>"7005263030"}, {"first_name"=>"Randall K.", "last_name"=>"Holmes", "scopus_author_id"=>"7402012636"}, {"first_name"=>"Maria", "last_name"=>"Sandkvist", "scopus_author_id"=>"6603909168"}, {"first_name"=>"Wim G.J.", "last_name"=>"Hol", "scopus_author_id"=>"7103324489"}], "year"=>2011, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "scopus"=>"2-s2.0-80053453930", "pui"=>"362681243", "doi"=>"10.1371/journal.ppat.1002228", "isbn"=>"1553-7366", "sgr"=>"80053453930", "pmid"=>"21931548"}, "id"=>"5a17a5c9-5dda-33cc-acfb-1eef843313f9", "abstract"=>"Type II secretion systems (T2SSs) are critical for secretion of many proteins from Gram-negative bacteria. In the T2SS, the outer membrane secretin GspD forms a multimeric pore for translocation of secreted proteins. GspD and the inner membrane protein GspC interact with each other via periplasmic domains. Three different crystal structures of the homology region domain of GspC (GspC(HR)) in complex with either two or three domains of the N-terminal region of GspD from enterotoxigenic Escherichia coli show that GspC(HR) adopts an all-β topology. N-terminal β-strands of GspC and the N0 domain of GspD are major components of the interface between these inner and outer membrane proteins from the T2SS. The biological relevance of the observed GspC-GspD interface is shown by analysis of variant proteins in two-hybrid studies and by the effect of mutations in homologous genes on extracellular secretion and subcellular distribution of GspC in Vibrio cholerae. Substitutions of interface residues of GspD have a dramatic effect on the focal distribution of GspC in V. cholerae. These studies indicate that the GspC(HR)-GspD(N0) interactions observed in the crystal structure are essential for T2SS function. Possible implications of our structures for the stoichiometry of the T2SS and exoprotein secretion are discussed.", "link"=>"http://www.mendeley.com/research/structural-functional-studies-interaction-gspc-gspd-type-ii-secretion-system-7", "reader_count"=>23, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>7, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>3, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>7, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>3, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>11, "Business, Management and Accounting"=>1, "Chemistry"=>2, "Social Sciences"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>2}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>11}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>0}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/373052", "https://ndownloader.figshare.com/files/373113", "https://ndownloader.figshare.com/files/373159", "https://ndownloader.figshare.com/files/373230", "https://ndownloader.figshare.com/files/373300", "https://ndownloader.figshare.com/files/373348"], "description"=>"<div><p>Type II secretion systems (T2SSs) are critical for secretion of many proteins from Gram-negative bacteria. In the T2SS, the outer membrane secretin GspD forms a multimeric pore for translocation of secreted proteins. GspD and the inner membrane protein GspC interact with each other via periplasmic domains. Three different crystal structures of the homology region domain of GspC (GspC<sup>HR</sup>) in complex with either two or three domains of the N-terminal region of GspD from enterotoxigenic <em>Escherichia coli</em> show that GspC<sup>HR</sup> adopts an all-β topology. N-terminal β-strands of GspC and the N0 domain of GspD are major components of the interface between these inner and outer membrane proteins from the T2SS. The biological relevance of the observed GspC–GspD interface is shown by analysis of variant proteins in two-hybrid studies and by the effect of mutations in homologous genes on extracellular secretion and subcellular distribution of GspC in <em>Vibrio cholerae.</em> Substitutions of interface residues of GspD have a dramatic effect on the focal distribution of GspC in <em>V. cholerae</em>. These studies indicate that the GspC<sup>HR</sup>–GspD<sup>N0</sup> interactions observed in the crystal structure are essential for T2SS function. Possible implications of our structures for the stoichiometry of the T2SS and exoprotein secretion are discussed.</p> </div>", "links"=>[], "tags"=>["studies", "gspc", "gspd", "ii", "secretion"], "article_id"=>133676, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Konstantin V. Korotkov", "Tanya L. Johnson", "Michael G. Jobling", "Jonathan Pruneda", "Els Pardon", "Annie Héroux", "Stewart Turley", "Jan Steyaert", "Randall K. Holmes", "Maria Sandkvist", "Wim G. J. Hol"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002228.s001", "https://dx.doi.org/10.1371/journal.ppat.1002228.s002", "https://dx.doi.org/10.1371/journal.ppat.1002228.s003", "https://dx.doi.org/10.1371/journal.ppat.1002228.s004", "https://dx.doi.org/10.1371/journal.ppat.1002228.s005", "https://dx.doi.org/10.1371/journal.ppat.1002228.s006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Structural_and_Functional_Studies_on_the_Interaction_of_GspC_and_GspD_in_the_Type_II_Secretion_System/133676", "title"=>"Structural and Functional Studies on the Interaction of GspC and GspD in the Type II Secretion System", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-08 01:01:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/737874"], "description"=>"<p>(<b>A</b>) Schematic diagrams of the domain structures of GspC and GspD. TMS – transmembrane segment; SP – signal peptide. (<b>B</b>) Structure of the GspC<sup>HR</sup>–GspD<sup>N0-N1</sup> binary complex. GspC, GspD and the LBT loop are colored green, cyan and blue, respectively. A Ca<sup>2+</sup> ion that occupies the LBT metal binding site is shown as an orange sphere. Secondary structure elements are labeled. (<b>C</b>) Structure of the GspC<sup>HR</sup>–GspD<sup>N0-N1-N2</sup>–Nb3 ternary complex. The structure is shown in the same orientation as in (<b>B</b>) for the GspD domains. The orientation of the GspC<sup>HR</sup> domain with respect to the GspD<sup>N0</sup> domain is very similar in (<b>B</b>) and (<b>C</b>). Nanobody Nb3 is colored in orange. The N2 subdomain of GspD is statistically disordered in the crystal lattice (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002228#ppat.1002228.s002\" target=\"_blank\">Figure S2</a>). The structure of the GspC<sup>HR</sup>–GspD<sup>N0-N1</sup>–Nb3 ternary complex is essentially the same, despite the differences in GspD constructs, crystallization conditions and crystal forms (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002228#ppat.1002228.s003\" target=\"_blank\">Figure S3</a>).</p>", "links"=>[], "tags"=>["complexes", "etec", "gspd"], "article_id"=>408233, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Konstantin V. Korotkov", "Tanya L. Johnson", "Michael G. Jobling", "Jonathan Pruneda", "Els Pardon", "Annie Héroux", "Stewart Turley", "Jan Steyaert", "Randall K. Holmes", "Maria Sandkvist", "Wim G. J. Hol"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002228.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structures_of_complexes_of_ETEC_GspC_HR_and_GspD_domains_/408233", "title"=>"Structures of complexes of ETEC GspC<sup>HR</sup> and GspD domains.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:17:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/738053"], "description"=>"<p>A stereo representation of surface charge distribution of GspC<sup>HR</sup>. The HR domain structure is from the binary complex with GspD<sup>N0-N1</sup>; the LBT is omitted for clarity. Note the deep pocket in the front surface of GspC<sup>HR</sup> in the upper panel.</p>", "links"=>[], "tags"=>["characteristics", "etec"], "article_id"=>408421, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Konstantin V. Korotkov", "Tanya L. Johnson", "Michael G. Jobling", "Jonathan Pruneda", "Els Pardon", "Annie Héroux", "Stewart Turley", "Jan Steyaert", "Randall K. Holmes", "Maria Sandkvist", "Wim G. J. Hol"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002228.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Surface_characteristics_of_ETEC_GspC_HR_/408421", "title"=>"Surface characteristics of ETEC GspC<sup>HR</sup>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:20:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/738198"], "description"=>"<p>(<b>A</b>) Structural superposition of the ETEC GspC<sup>HR</sup> domain with the <i>N. meningitidis</i> PilP structure (PDB 2IVW) <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002228#ppat.1002228-Golovanov1\" target=\"_blank\">[42]</a>. GspC and <i>Nm</i>PilP are colored in green and yellow, respectively. Flexible N- and C-terminal residues of <i>Nm</i>PilP are not shown for clarity. The conserved hydrophobic residues are shown as sticks. (<b>B</b>) Surface representation of GspC and PilP in the same orientation as in (<b>A</b>). The crevice on the surface of PilP is absent in GspC. (<b>C</b>) Sequence alignment of GspC and <i>Nm</i>PilP based on the structural superposition in (<b>A</b>). Secondary structure elements of GspC and <i>Nm</i>PilP are displayed above and below the sequences, respectively; the colored dots represent the conserved hydrophobic residues of GspC and <i>Nm</i>PilP.</p>", "links"=>[], "tags"=>["gspc", "t2ss", "pilp"], "article_id"=>408563, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Konstantin V. Korotkov", "Tanya L. Johnson", "Michael G. Jobling", "Jonathan Pruneda", "Els Pardon", "Annie Héroux", "Stewart Turley", "Jan Steyaert", "Randall K. Holmes", "Maria Sandkvist", "Wim G. J. Hol"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002228.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_GspC_from_the_T2SS_and_PilP_from_the_T4PS_/408563", "title"=>"Comparison of GspC from the T2SS and PilP from the T4PS.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:22:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/738403"], "description"=>"<p>(<b>A</b>) An ‘open book’ view of the GspC<sup>HR</sup>–GspD<sup>N0-N1</sup> binary complex in surface representation. Residues in the interface are colored according to the degree of burial upon complex formation: yellow, up to 40% reduction in accessible surface area (ASA); orange, 40–70% reduction in ASA; and brown, more than 70% reduction in ASA. Atoms participating in intermolecular hydrogen bond formation are colored in cyan. (<b>B</b>) Same view as in (<b>A</b>) with the interaction surfaces colored according to the solvent accessible electrostatic potential. The interaction surface is contoured by black lines. (<b>C</b>) Anti-parallel β1<sup>HR</sup>–β1<sup>N0</sup> interactions in the GspC<sup>HR</sup>–GspD<sup>N0-N1</sup> complex. The upper strand is β1<sup>N0</sup>. Interacting residues are shown as sticks and labeled. Hydrogen bonds are shown as dashed lines. A σA-weighted 2<i>F</i><sub>O</sub>–<i>F</i><sub>C</sub> electron density map contoured at 1.2 σ is shown as a dark blue mesh. (<b>D</b>) Interface surface of a homology model of the <i>V. cholerae</i> GspC–GspD complex <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002228#ppat.1002228-Arnold1\" target=\"_blank\">[79]</a>. Residues in the interface are colored according to the color of the interacting partner: GspD in cyan and GspC in green. The residues that were subjected to mutational analysis are colored in magenta and labeled. (<b>E</b>) Amino acid sequence alignments of the HR domains of GspC and the N0 domains of GspD from ETEC and <i>V. cholerae.</i> The corresponding secondary structure elements are shown above the sequences. Residues that make intermolecular Van der Waals contacts and H-bonds in the ETEC GspC<sup>HR</sup>–GspD<sup>N0-N1</sup> complex are labeled by triangles and stars, respectively. The residues that were subjected to mutational analysis in <i>V. cholerae</i> GspC and GspD are indicated by magenta triangles underneath the alignments.</p>", "links"=>[], "tags"=>["interface"], "article_id"=>408773, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Konstantin V. Korotkov", "Tanya L. Johnson", "Michael G. Jobling", "Jonathan Pruneda", "Els Pardon", "Annie Héroux", "Stewart Turley", "Jan Steyaert", "Randall K. Holmes", "Maria Sandkvist", "Wim G. J. Hol"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002228.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_interface_of_the_GspC_8211_GspD_complex_/408773", "title"=>"The interface of the GspC–GspD complex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:26:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/738546"], "description"=>"<p>(<b>A</b>) <i>V. cholerae</i> wild-type or <i>gspD</i> mutant strain (<i>Δ</i>gspD) containing either pMMB or pGspD variants were grown overnight in LB. Culture supernatants were separated from cells by centrifugation and tested for the presence of extracellular protease. The rate of hydrolysis was obtained from three independent experiments, and the results are presented with standard error. Both the pMMB vector control and pGspD<sub>I18R/N22Y</sub> were below the limits of detection. (<b>B</b>) <i>V. cholerae gspD<sup>–</sup></i> cells containing either pMMB or pGspD variants were disrupted and subjected to SDS-PAGE and immunoblotting with anti-GspD antibodies to determine the relative level of expression. The positions of molecular mass markers are shown. Arrow indicates monomeric GspD and arrowhead indicates multimeric GspD.</p>", "links"=>[], "tags"=>["substitution", "ile18", "asn22", "gspd", "inactivation", "protease", "secretion"], "article_id"=>408902, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Konstantin V. Korotkov", "Tanya L. Johnson", "Michael G. Jobling", "Jonathan Pruneda", "Els Pardon", "Annie Héroux", "Stewart Turley", "Jan Steyaert", "Randall K. Holmes", "Maria Sandkvist", "Wim G. J. Hol"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002228.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Simultaneous_substitution_of_Ile18_and_Asn22_in_V_cholerae_GspD_results_in_inactivation_of_protease_secretion_by_V_cholerae_/408902", "title"=>"Simultaneous substitution of Ile18 and Asn22 in <i>V. cholerae</i> GspD results in inactivation of protease secretion by <i>V. cholerae.</i>", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:28:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/738623"], "description"=>"<p>Localization of chromosomally expressed GFP-GspC was examined in wild-type and <i>gspD</i> mutant backgrounds by fluorescence microscopy. GFP-GspC displayed a continuous membrane localization in the <i>gfp-gspC gspD<sup>–</sup></i> strain (second panel) compared to the wild-type background (first panel). Punctate fluorescence was restored when the <i>gfp-gspC gspD<sup>-</sup></i> strain was complemented with GspD on a plasmid (third panel). Expression of GspD<sub>I18R/N22Y</sub> in the <i>gfp-gspC gspD<sup>–</sup></i> strain resulted in membrane localization similar the pMMB vector control (fourth panel).</p>", "links"=>[], "tags"=>["localization", "gfp-gspc"], "article_id"=>408989, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Konstantin V. Korotkov", "Tanya L. Johnson", "Michael G. Jobling", "Jonathan Pruneda", "Els Pardon", "Annie Héroux", "Stewart Turley", "Jan Steyaert", "Randall K. Holmes", "Maria Sandkvist", "Wim G. J. Hol"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002228.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differential_localization_in_V_cholerae_of_GFP_GspC_in_the_presence_of_GspD_I18R_N22Y_/408989", "title"=>"Differential localization in <i>V. cholerae</i> of GFP-GspC in the presence of GspD<sub>I18R/N22Y</sub>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:29:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/738740"], "description"=>"<p>(<b>A</b>) Two perpendicular views of the dodecameric ring of GspD<sup>N0-N1</sup> (blue) obtained from crystallographic and electron microscopy studies <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002228#ppat.1002228-Reichow1\" target=\"_blank\">[20]</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002228#ppat.1002228-Korotkov2\" target=\"_blank\">[24]</a> with a dodecameric ring of GspC<sup>HR</sup> (green) assembled as described in the text. (<b>B</b>) Two perpendicular views of the same dodecameric ring of GspD<sup>N0-N1</sup> (blue) shown in (<b>A</b>) with six GspC<sup>HR</sup> subunits (green) binding to alternating GspD subunits as described in the text. (<b>C</b>) Two perpendicular views of the exoprotein cholera toxin (B pentamer in gold, A subunit in yellow) positioned inside the dodecameric GspC<sup>HR</sup>–GspD<sup>N0-N1</sup> ring depicted in (<b>A</b>). The five-fold axis of the B-pentamer is aligned by hand with the twelve-fold axis of the ring. The orientation of the AB<sub>5</sub> hexamer with respect to the dodecamer is otherwise arbitrary. The cross-section of the double dodecamer of GspD<sup>N0-N1</sup> and GspC<sup>HR</sup> is just sufficient to permit binding of the toxin heterohexamer. Obviously, the alternative assembly shown in (<b>B</b>) would also provide sufficient space for the toxin to bind at this location.</p>", "links"=>[], "tags"=>["gspd", "gspc", "exoprotein", "cholera"], "article_id"=>409100, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Konstantin V. Korotkov", "Tanya L. Johnson", "Michael G. Jobling", "Jonathan Pruneda", "Els Pardon", "Annie Héroux", "Stewart Turley", "Jan Steyaert", "Randall K. Holmes", "Maria Sandkvist", "Wim G. J. Hol"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002228.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Combining_structural_data_of_GspD_and_GspC_and_the_exoprotein_cholera_toxin_/409100", "title"=>"Combining structural data of GspD and GspC and the exoprotein cholera toxin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:31:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/738834"], "description"=>"a<p>Values in parenthesis are for the highest resolution shell.</p>b<p>Molprobity <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002228#ppat.1002228-Chen1\" target=\"_blank\">[73]</a>, <a href=\"http://molprobity.biochem.duke.edu/\" target=\"_blank\">http://molprobity.biochem.duke.edu/</a>.</p>", "links"=>[], "tags"=>["refinement"], "article_id"=>409201, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Konstantin V. Korotkov", "Tanya L. Johnson", "Michael G. Jobling", "Jonathan Pruneda", "Els Pardon", "Annie Héroux", "Stewart Turley", "Jan Steyaert", "Randall K. Holmes", "Maria Sandkvist", "Wim G. J. Hol"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002228.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Data_collection_and_refinement_statistics_/409201", "title"=>"Data collection and refinement statistics.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-08 02:33:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/738873"], "description"=>"a<p>wt – wild type.</p>", "links"=>[], "tags"=>["bacterial", "two-hybrid"], "article_id"=>409236, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Konstantin V. Korotkov", "Tanya L. Johnson", "Michael G. Jobling", "Jonathan Pruneda", "Els Pardon", "Annie Héroux", "Stewart Turley", "Jan Steyaert", "Randall K. Holmes", "Maria Sandkvist", "Wim G. J. Hol"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002228.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characterization_of_GspC_8211_GspD_interaction_in_the_bacterial_two_hybrid_system_/409236", "title"=>"Characterization of GspC–GspD interaction in the bacterial two-hybrid system.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-08 02:33:56"}

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  • {"unique-ip"=>"10", "full-text"=>"6", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"20", "full-text"=>"14", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
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  • {"unique-ip"=>"8", "full-text"=>"17", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"17", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"15", "full-text"=>"13", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"10", "year"=>"2016", "month"=>"9"}
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  • {"unique-ip"=>"10", "full-text"=>"13", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
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  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
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  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
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  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
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  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"12", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"18", "full-text"=>"13", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"19", "full-text"=>"19", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"18", "full-text"=>"15", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
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Relative Metric

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