Structure and Kinetic Investigation of Streptococcus pyogenes Family GH38 α-Mannosidase
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{"title"=>"Structure and kinetic investigation of Streptococcus pyogenes family GH38 α-mannosidase", "type"=>"journal", "authors"=>[{"first_name"=>"Michael D.L.", "last_name"=>"Suits", "scopus_author_id"=>"15728521600"}, {"first_name"=>"Yanping", "last_name"=>"Zhu", "scopus_author_id"=>"55723774600"}, {"first_name"=>"Edward J.", "last_name"=>"Taylor", "scopus_author_id"=>"35547974900"}, {"first_name"=>"Julia", "last_name"=>"Walton", "scopus_author_id"=>"15740178000"}, {"first_name"=>"David L.", "last_name"=>"Zechel", "scopus_author_id"=>"6602699097"}, {"first_name"=>"Harry J.", "last_name"=>"Gilbert", "scopus_author_id"=>"7202943610"}, {"first_name"=>"Gideon J.", "last_name"=>"Davies", "scopus_author_id"=>"35517179900"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-77949380654", "isbn"=>"1932-6203", "doi"=>"10.1371/journal.pone.0009006", "pui"=>"358448400", "sgr"=>"77949380654", "issn"=>"19326203", "pmid"=>"20140249"}, "id"=>"a3e0b328-b9ae-3480-ba19-bac004d465d8", "abstract"=>"BACKGROUND: The enzymatic hydrolysis of alpha-mannosides is catalyzed by glycoside hydrolases (GH), termed alpha-mannosidases. These enzymes are found in different GH sequence-based families. Considerable research has probed the role of higher eukaryotic \"GH38\" alpha-mannosides that play a key role in the modification and diversification of hybrid N-glycans; processes with strong cellular links to cancer and autoimmune disease. The most extensively studied of these enzymes is the Drosophila GH38 alpha-mannosidase II, which has been shown to be a retaining alpha-mannosidase that targets both alpha-1,3 and alpha-1,6 mannosyl linkages, an activity that enables the enzyme to process GlcNAc(Man)(5)(GlcNAc)(2) hybrid N-glycans to GlcNAc(Man)(3)(GlcNAc)(2). Far less well understood is the observation that many bacterial species, predominantly but not exclusively pathogens and symbionts, also possess putative GH38 alpha-mannosidases whose activity and specificity is unknown.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: Here we show that the Streptococcus pyogenes (M1 GAS SF370) GH38 enzyme (Spy1604; hereafter SpGH38) is an alpha-mannosidase with specificity for alpha-1,3 mannosidic linkages. The 3D X-ray structure of SpGH38, obtained in native form at 1.9 A resolution and in complex with the inhibitor swainsonine (K(i) 18 microM) at 2.6 A, reveals a canonical GH38 five-domain structure in which the catalytic \"-1\" subsite shows high similarity with the Drosophila enzyme, including the catalytic Zn(2+) ion. In contrast, the \"leaving group\" subsites of SpGH38 display considerable differences to the higher eukaryotic GH38s; features that contribute to their apparent specificity.\\n\\nCONCLUSIONS/SIGNIFICANCE: Although the in vivo function of this streptococcal GH38 alpha-mannosidase remains unknown, it is shown to be an alpha-mannosidase active on N-glycans. SpGH38 lies on an operon that also contains the GH84 hexosaminidase (Spy1600) and an additional putative glycosidase. The activity of SpGH38, together with its genomic context, strongly hints at a function in the degradation of host N- or possibly O-glycans. The absence of any classical signal peptide further suggests that SpGH38 may be intracellular, perhaps functioning in the subsequent degradation of extracellular host glycans following their initial digestion by secreted glycosidases.", "link"=>"http://www.mendeley.com/research/structure-kinetic-investigation-streptococcus-pyogenes-family-gh38-%CE%B1mannosidase", "reader_count"=>54, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>20, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Other"=>4, "Student > Master"=>2, "Student > Bachelor"=>5, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>20, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Other"=>4, "Student > Master"=>2, "Student > Bachelor"=>5, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>35, "Medicine and Dentistry"=>2, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Business, Management and Accounting"=>1, "Chemistry"=>6}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>6}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>35}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>2, "Italy"=>2}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/864479"], "description"=>"<p>An overlap of the <i>Drosophila</i> GH38 α−mannosidase II complexes <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009006#pone.0009006-Zhong1\" target=\"_blank\">[15]</a> with α−1,3 (green bonds) and α−1,6 linked ligands (blue bonds) with the SpGH38 structure (grey surface) focussing on the +1 subsite (the -1 subsites are essentially identical, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009006#pone-0009006-g005\" target=\"_blank\">Fig. 5A</a>). Features which may contribute to 1,3 specificity include the position of W764, the interactions afforded by D763 and the tightness of the “sphincter” formed by D763 and the catalytic acid/base D232. The figure is shown in divergent (“wall-eyed”) stereo.</p>", "links"=>[], "tags"=>["specificity"], "article_id"=>534937, "categories"=>["Biophysics", "Biochemistry", "Chemistry"], "users"=>["Michael D. L. Suits", "Yanping Zhu", "Edward J. Taylor", "Julia Walton", "David L. Zechel", "Harry J. Gilbert", "Gideon J. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009006.g006", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Substrate_specificity_in_SpGH38_/534937", "title"=>"Substrate specificity in SpGH38.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:47:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/864391"], "description"=>"<p>(<b>A</b>) Conserved active-centre constellation (here -1 subsite only) between the SpGH38 (grey), bovine bLAM (cyan) and the <i>Drosophila</i> GH38 α−mannosidase (blue). (<b>B</b>). GH38 α−mannosidases are known to act with net retention of anomeric configuration; a mechanism in which a glycosyl-enzyme intermediate is flanked by oxocarbenium-ion like transition-states. The intermediate has been trapped by the Withers and Rose groups <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009006#pone.0009006-Numao1\" target=\"_blank\">[17]</a> and shown to bind in a <sup>1</sup>S<sub>5</sub> skew-boat conformation which in the absence of evidence to the contrary might imply a transition-state close to a B<sub>2,5</sub>. Pseudo-Michaelis complexes published on the <i>Drosophila</i> α−mannosidase II show the −1 sugar in a <sup>4</sup>C<sub>1</sub> chair conformation but these have been obtained on a nucleophile-alanine variant so their conformational relevance to catalysis is unclear <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009006#pone.0009006-Zhong1\" target=\"_blank\">[15]</a>.</p>", "links"=>[], "tags"=>["gh38"], "article_id"=>534849, "categories"=>["Biophysics", "Biochemistry", "Chemistry"], "users"=>["Michael D. L. Suits", "Yanping Zhu", "Edward J. Taylor", "Julia Walton", "David L. Zechel", "Harry J. Gilbert", "Gideon J. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009006.g005", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conservation_of_GH38_reaction_mechanism_/534849", "title"=>"Conservation of GH38 reaction mechanism.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:47:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/864287"], "description"=>"<p>(<b>A</b>) 3-D topology cartoon (divergent stereo) colored according to domains with swainsonine in ball-and-stick. N-term (red: 1–294) 3-α (green: 295–392), β-1 (blue: 393–514,806–825), β−2 (yellow: 522–805) and β−3 (cyan: 825–901) (<b>B</b>) Surface representation of SpGH38 colored as for part (A). (<b>C</b>) Active centre and electron density for the Swainsonine/Zn<sup>2+</sup> complex of SpGH38 (divergent stereo). The map shown is the unbiased F<sub>obs</sub>-F<sub>calc</sub> synthesis, contoured at 2.5 σ, calculated with model phases prior to the incorporation of Swainsonine/Zn<sup>2+</sup> in any refinement. (<b>D</b>) schematic diagram of the interactions of swainsonine (shown in panel C) with H-bonds >3.0 Å shown as dashed lines and residue numbers for the SpGH38 indicated. Arg149 makes a close contact to a swainsonine carbon (indicated with an arrow) of 2.9 Å (spatially equivalent to an H-bond to mannose O6 of the true substrate).</p>", "links"=>[], "tags"=>["spgh38", "swainsonine"], "article_id"=>534741, "categories"=>["Biophysics", "Biochemistry", "Chemistry"], "users"=>["Michael D. L. Suits", "Yanping Zhu", "Edward J. Taylor", "Julia Walton", "David L. Zechel", "Harry J. Gilbert", "Gideon J. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009006.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_3_D_structure_of_SpGH38_and_its_swainsonine_complex_/534741", "title"=>"3-D structure of SpGH38 and its swainsonine complex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:46:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/864555"], "description"=>"<p>Data collection and refinement statistics for the <i>Streptococcus pyogenes</i> GH38 α−mannosidase.</p>", "links"=>[], "tags"=>["refinement", "gh38"], "article_id"=>535015, "categories"=>["Biophysics", "Biochemistry", "Chemistry"], "users"=>["Michael D. L. Suits", "Yanping Zhu", "Edward J. Taylor", "Julia Walton", "David L. Zechel", "Harry J. Gilbert", "Gideon J. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009006.t001", "stats"=>{"downloads"=>4, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Data_collection_and_refinement_statistics_for_the_Streptococcus_pyogenes_GH38_mannosidase_/535015", "title"=>"Data collection and refinement statistics for the <i>Streptococcus pyogenes</i> GH38 α−mannosidase.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 02:48:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/863994"], "description"=>"<p>(<b>A</b>) Golgi α−mannosidase II is responsible for the hydrolysis of both α−1,3 and α−1–6 mannosides during the diversification of hybrid N glycans (GlcNAcMan<sub>5</sub>GlcNAc<sub>2</sub> becoming GlcNAcMan<sub>3</sub>GlcNAc<sub>2</sub>). (B) The catalytic action of a retaining α−mannosidase, here exemplified for the α−1,3 mannosidase activity of GH38 enzymes; catalysis occurs with net retention of anomeric configuration.</p>", "links"=>[], "tags"=>["gh38"], "article_id"=>534440, "categories"=>["Biophysics", "Biochemistry", "Chemistry"], "users"=>["Michael D. L. Suits", "Yanping Zhu", "Edward J. Taylor", "Julia Walton", "David L. Zechel", "Harry J. Gilbert", "Gideon J. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009006.g001", "stats"=>{"downloads"=>2, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Catalytic_activity_of_GH38_945_8722_mannosidases_/534440", "title"=>"Catalytic activity of GH38 α−mannosidases.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:45:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/864087"], "description"=>"<p>(<b>A</b>) Activity on 4-methylumbelliferyl α−D mannoside (4-MeUMB) and (<b>B</b>) α−1,3 mannobiose (see text for details) Substrate insolubility under the conditions used precluded higher [S] values. (<b>C</b>) The <i>K</i><sub>i</sub> for swainsonine was determined using α−1,3 mannobiose as substrate with [S] < < K<sub>m</sub> and [I] straddling the <i>K</i><sub>i</sub>. V<sub>0</sub> and V<sub>i</sub> are the rates of the reaction in the absence and presence of inhibitor, respectively. The <i>K</i><sub>i</sub> for a competitive inhibitor is derived from the gradient of 1/<i>K</i><sub>i</sub> (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009006#s3\" target=\"_blank\">Methods</a> ); here 18±0.5 µM.</p>", "links"=>[], "tags"=>["spgh38", "inhibition"], "article_id"=>534540, "categories"=>["Biophysics", "Biochemistry", "Chemistry"], "users"=>["Michael D. L. Suits", "Yanping Zhu", "Edward J. Taylor", "Julia Walton", "David L. Zechel", "Harry J. Gilbert", "Gideon J. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009006.g002", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Catalytic_activity_of_SpGH38_945_8722_mannosidase_and_inhibition_by_swainsonine_/534540", "title"=>"Catalytic activity of SpGH38 α−mannosidase and inhibition by swainsonine.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:45:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/864186"], "description"=>"<p>(<b>A</b>) Action of SpGH38, alone, on Man<sub>9</sub>(GlcNAc)<sub>2</sub>. The glycan remains unmodified. (<b>B</b>) Action of SpGH38 in combination with a specific α−1,2 mannosidase the <i>Bacteroides thetaiotaomicron</i> Bt3990. Following α−1,2 mannoside removal (which has previously been shown to be specific, see Supplemental <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009006#pone-0009006-g001\" target=\"_blank\">Figure 1</a> in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009006#pone.0009006-Zhu1\" target=\"_blank\">[10]</a>, SpGH38 is able to further degrade the unmasked glycans, with the action pattern most indicative of α−1,3 mannosidase activity. An α−1,3 mannosidase activity for SpGH38 is further supported by the specificity of the enzyme for the disaccharide α−1,3 mannobiose (see text).</p>", "links"=>[], "tags"=>["hydrolysis"], "article_id"=>534636, "categories"=>["Biophysics", "Biochemistry", "Chemistry"], "users"=>["Michael D. L. Suits", "Yanping Zhu", "Edward J. Taylor", "Julia Walton", "David L. Zechel", "Harry J. Gilbert", "Gideon J. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009006.g003", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SpGH38_catalysed_hydrolysis_of_Man_9_GlcNAc_2_glycans_/534636", "title"=>"SpGH38-catalysed hydrolysis of Man<sub>9</sub>(GlcNAc)<sub>2</sub> glycans.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:46:10"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"4"}
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  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"6"}
  • {"unique-ip"=>"7", "full-text"=>"13", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"7"}
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