The Murine Coronavirus Hemagglutinin-esterase Receptor-binding Site: A Major Shift in Ligand Specificity through Modest Changes in Architecture
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{"title"=>"The murine coronavirus hemagglutinin-esterase receptor-binding site: A major shift in ligand specificity through modest changes in architecture", "type"=>"journal", "authors"=>[{"first_name"=>"Martijn A.", "last_name"=>"Langereis", "scopus_author_id"=>"10639551100"}, {"first_name"=>"Qinghong", "last_name"=>"Zeng", "scopus_author_id"=>"55425596300"}, {"first_name"=>"Balthasar", "last_name"=>"Heesters", "scopus_author_id"=>"37053973500"}, {"first_name"=>"Eric G.", "last_name"=>"Huizinga", "scopus_author_id"=>"7004310068"}, {"first_name"=>"Raoul J.", "last_name"=>"de Groot", "scopus_author_id"=>"7103077066"}], "year"=>2012, "source"=>"PLoS Pathogens", "identifiers"=>{"pui"=>"364330007", "sgr"=>"84857493514", "scopus"=>"2-s2.0-84857493514", "isbn"=>"1553-7374", "issn"=>"15537366", "pmid"=>"22291594", "doi"=>"10.1371/journal.ppat.1002492"}, "id"=>"e57edeec-6638-308c-8dee-4caa1716c790", "abstract"=>"The hemagglutinin-esterases (HEs), envelope glycoproteins of corona-, toro- and orthomyxoviruses, mediate reversible virion attachment to O-acetylated sialic acids (O-Ac-Sias). They do so through concerted action of distinct receptor-binding (\"lectin\") and receptor-destroying sialate O-acetylesterase (\"esterase\") domains. Most HEs target 9-O-acetylated Sias. In one lineage of murine coronaviruses, however, HE esterase substrate and lectin ligand specificity changed dramatically as these viruses evolved to use 4-O-acetylated Sias instead. Here we present the crystal structure of the lectin domain of mouse hepatitis virus (MHV) strain S HE, resolved both in its native state and in complex with a receptor analogue. The data show that the shift from 9-O- to 4-O-Ac-Sia receptor usage primarily entailed a change in ligand binding topology and, surprisingly, only modest changes in receptor-binding site architecture. Our findings illustrate the ease with which viruses can change receptor-binding specificity with potential consequences for host-, organ and/or cell tropism, and for pathogenesis.", "link"=>"http://www.mendeley.com/research/murine-coronavirus-hemagglutininesterase-receptorbinding-site-major-shift-ligand-specificity-through", "reader_count"=>28, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Student > Doctoral Student"=>4, "Researcher"=>2, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>3, "Student > Master"=>2, "Student > Bachelor"=>5, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Student > Doctoral Student"=>4, "Researcher"=>2, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>3, "Student > Master"=>2, "Student > Bachelor"=>5, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>18, "Medicine and Dentistry"=>3, "Chemistry"=>3, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Chemistry"=>{"Chemistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>18}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}}, "reader_count_by_country"=>{"China"=>1, "United Kingdom"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/688256"], "description"=>"<p>*Values between brackets refer to the highest resolution shell of data.</p>†<p>Rfree is calculated from 5% of data randomly chosen not to be included in refinement.</p>‡<p>Two HE molecules are present in the asymmetric unit of the crystal; during refinement no NCS restraints were applied.</p>", "links"=>[], "tags"=>["refinement"], "article_id"=>358747, "categories"=>["Virology", "Biochemistry", "Chemistry"], "users"=>["Martijn A. Langereis", "Qinghong Zeng", "Balthasar Heesters", "Eric G. Huizinga", "Raoul J. de Groot"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002492.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Data_collection_and_refinement_statistics_/358747", "title"=>"Data collection and refinement statistics.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-01-26 02:25:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/350610", "https://ndownloader.figshare.com/files/350635", "https://ndownloader.figshare.com/files/350659", "https://ndownloader.figshare.com/files/350682", "https://ndownloader.figshare.com/files/350721"], "description"=>"<div><p>The hemagglutinin-esterases (HEs), envelope glycoproteins of corona-, toro- and orthomyxoviruses, mediate reversible virion attachment to <em>O</em>-acetylated sialic acids (<em>O</em>-Ac-Sias). They do so through concerted action of distinct receptor-binding (“lectin”) and receptor-destroying sialate <em>O</em>-acetylesterase (”esterase”) domains. Most HEs target 9-<em>O</em>-acetylated Sias. In one lineage of murine coronaviruses, however, HE esterase substrate and lectin ligand specificity changed dramatically as these viruses evolved to use 4-<em>O</em>-acetylated Sias instead. Here we present the crystal structure of the lectin domain of mouse hepatitis virus (MHV) strain <em>S</em> HE, resolved both in its native state and in complex with a receptor analogue. The data show that the shift from 9-<em>O</em>- to 4-<em>O</em>-Ac-Sia receptor usage primarily entailed a change in ligand binding topology and, surprisingly, only modest changes in receptor-binding site architecture. Our findings illustrate the ease with which viruses can change receptor-binding specificity with potential consequences for host-, organ and/or cell tropism, and for pathogenesis.</p> </div>", "links"=>[], "tags"=>["murine", "coronavirus", "hemagglutinin-esterase", "receptor-binding", "ligand", "specificity", "changes"], "article_id"=>129306, "categories"=>["Biochemistry", "Cancer", "Chemistry"], "users"=>["Martijn A. Langereis", "Qinghong Zeng", "Balthasar Heesters", "Eric G. Huizinga", "Raoul J. de Groot"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002492.s001", "https://dx.doi.org/10.1371/journal.ppat.1002492.s002", "https://dx.doi.org/10.1371/journal.ppat.1002492.s003", "https://dx.doi.org/10.1371/journal.ppat.1002492.s004", "https://dx.doi.org/10.1371/journal.ppat.1002492.s005"], "stats"=>{"downloads"=>5, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Murine_Coronavirus_Hemagglutinin_esterase_Receptor_binding_Site_A_Major_Shift_in_Ligand_Specificity_through_Modest_Changes_in_Architecture/129306", "title"=>"The Murine Coronavirus Hemagglutinin-esterase Receptor-binding Site: A Major Shift in Ligand Specificity through Modest Changes in Architecture", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-01-26 02:35:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/688142"], "description"=>"<p>(A) Surface and (B) stick representation of the MHV<i>-S</i> HE receptor-binding site in complex with a receptor analogue. The ligand bound to the HE receptor-binding site is shown in stick representation and the potassium ion as a magenta sphere, indicated by a black arrow in panel A. Hydrogen bonds between HE and the receptor are shown as black dashed lines. Surface representation of the MHV<i>-S</i> HE receptor-binding site reveals two pockets accommodating the 4-<i>O</i>- and 5-<i>N</i>-acetyl groups of the receptor, respectively. Note that crystals were soaked with αNeu4,5,9Ac<sub>3</sub>2Me, but most likely as a result of the low pH crystallization conditions, the 9-<i>O</i>-Ac group was lost <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002492#ppat.1002492-Kamerling2\" target=\"_blank\">[42]</a>. (C) Surface and (D) stick representation of the BCoV-Mebus HE receptor-binding site. Note that the topology of the two hydrophobic pockets is conserved, except they bind different substituents of the receptor analogue. (E) The effect of Ala substitutions on receptor binding. Relative binding affinity of wild-type HE<sup>0</sup> (wt) and its derivatives was assessed by hemagglutination assay with rat erythrocytes and twofold serial dilutions of each of the HE<sup>0</sup>-Fc chimeras (5,000 to 10 ng per well, arrow). (F) Binding of twofold serial dilutions of wild-type (wt) HE<sup>0</sup>-Fc chimera and its derivatives in a solid-phase lectin-binding assay towards horse serum glycoproteins (HSG) as described in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002492#ppat-1002492-g002\" target=\"_blank\">Figure 2A</a>.</p>", "links"=>[], "tags"=>["receptor-binding", "binds", "sialic"], "article_id"=>358631, "categories"=>["Virology", "Biochemistry", "Chemistry"], "users"=>["Martijn A. Langereis", "Qinghong Zeng", "Balthasar Heesters", "Eric G. Huizinga", "Raoul J. de Groot"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002492.g005", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MHV_S_HE_has_a_unique_receptor_binding_site_that_binds_specifically_4_O_acetylated_sialic_acid_/358631", "title"=>"MHV<i>-S</i> HE has a unique receptor-binding site that binds specifically 4-<i>O</i>-acetylated sialic acid.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-26 02:23:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/687704"], "description"=>"<p>Stick representation of (<i>left</i>) αNeu5,9Ac<sub>2</sub>2Me and (right) αNeu4,5Ac<sub>2</sub>2Me. Backbone αNeu5Ac2Me is colored in gray (carbon), red (oxygen) and blue (nitrogen). The 9-<i>O</i>-Ac group of αNeu5,9Ac<sub>2</sub>2Me and 4-<i>O</i>-Ac group of αNeu4,5Ac<sub>2</sub>2Me are highlighted in cyan (carbon).</p>", "links"=>[], "tags"=>["differences", "sialic"], "article_id"=>358191, "categories"=>["Virology", "Biochemistry", "Chemistry"], "users"=>["Martijn A. Langereis", "Qinghong Zeng", "Balthasar Heesters", "Eric G. Huizinga", "Raoul J. de Groot"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002492.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Stereochemical_differences_between_9_O_and_4_O_acetylated_sialic_acid_/358191", "title"=>"Stereochemical differences between 9-<i>O</i>- and 4-<i>O</i>-acetylated sialic acid.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-26 02:16:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/687897"], "description"=>"<p>(A) Ribbon representation of the dimeric MHV<i>-S</i> (residues 25–395) and BCoV-Mebus HE (residues 19–376) structures. One monomer is colored grey, the other by domain: lectin domain (R, blue) with bound αNeu4,5Ac<sub>2</sub>2Me (MHV<i>-S</i> HE) or αNeu4,5,9Ac<sub>3</sub>2Me (BCoV-Mebus HE; cyan sticks) and potassium ion (magenta sphere); esterase domain (E, green); membrane-proximal domain (MP, red). (B) Linear representation of MHV HE with domains color-coded as in panel A. Grey segments indicate the signal-peptide (SP) and transmembrane (TM) domain. The bracket indicates the part of the protein for which the structure has been solved. (C) Structure- (MHV<i>-S</i> and BCoV-Mebus) and sequence-based (MHV-DVIM) alignment of HE sequences. Colored boxes above the sequences indicate domain organization as in panel A and B and black lines indicate loops involved in receptor binding. Note that in MHV-<i>S</i> HE two insertions increase the length of loops R3 and R4. Asterisks indicate the highly conserved residues of the potassium binding site and boxes indicate the critical serine, histidine and aspartic acid residues of the catalytic site. Residues that interact with the ligand are indicated in bold; those conserved among all three HEs are highlighted by grey shading. Other residues also conserved in all three HEs are highlighted in yellow. The residues in disordered loops of the esterase domain are indicated in light gray lettering.</p>", "links"=>[], "tags"=>["bcov-mebus"], "article_id"=>358392, "categories"=>["Virology", "Biochemistry", "Chemistry"], "users"=>["Martijn A. Langereis", "Qinghong Zeng", "Balthasar Heesters", "Eric G. Huizinga", "Raoul J. de Groot"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002492.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overall_structure_and_comparison_to_BCoV_Mebus_HE_/358392", "title"=>"Overall structure and comparison to BCoV-Mebus HE.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-26 02:19:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/687775"], "description"=>"<p>(A) Binding of two-fold serial dilutions (starting at 100 µg/ml) of esterase-deficient Fc-fusion proteins (HE<sup>0</sup>-Fc) of BCoV-Mebus and MHV<i>-S</i> in a solid-phase lectin-binding assay towards horse serum glycoproteins (HSG) and bovine submaxillary mucins (BSM). Relative binding in percentages is calculated with the binding of the highest concentration lectin set at a 100%. Wells incubated without lectin (“mock”) were included as negative control. (B) Receptor destroying enzyme activity towards HSG. Coated HSG was treated with two-fold serial dilutions (starting at 100 ng/ml) of enzymatically-active BCoV-Mebus and MHV-<i>S</i> HE Fc-fusion proteins and 4-<i>O</i>-Ac-Sia content was detected by solid phase lectin binding assay with MHV-<i>S</i> HE<sup>0</sup>-Fc. Decrease in signal as compared to untreated HSG is plotted in percentages. (C) MHV-<i>S</i> HE ectodomain displays sialate-4-<i>O</i>-acetylesterase activity towards the synthetic di-<i>O</i>-acetylated sialic acid analogue αNeu4,5,9Ac<sub>3</sub>2Me. Graphs show total ion current gas-chromatograms and Sia subtypes were identified by mass spectrometry: Sia (αNeu5Ac2Me [peak 1]), 4-<i>O</i>-Ac-Sia (αNeu4,5Ac<sub>2</sub>2Me [peak 2]), 9-<i>O</i>-Ac-Sia (αNeu5,9Ac<sub>2</sub>2Me [peak 4], 4,9-di-<i>O</i>-Ac-Sia (αNeu4,5,9Ac<sub>3</sub>2Me [peak 5]). Peak 3 represents a non-sialic acid compound. (D) Receptor binding activity of MHV-<i>S</i> HE ectodomain was assessed by hemagglutination assay with rat erythrocytes and twofold serial dilutions of the HE proteins (10,000 to 5 ng per well, arrow).</p>", "links"=>[], "tags"=>["fusion", "displays", "receptor-binding", "enzymatic"], "article_id"=>358262, "categories"=>["Virology", "Biochemistry", "Chemistry"], "users"=>["Martijn A. Langereis", "Qinghong Zeng", "Balthasar Heesters", "Eric G. Huizinga", "Raoul J. de Groot"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002492.g002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HE_Fc_fusion_protein_displays_proper_receptor_binding_and_enzymatic_activities_/358262", "title"=>"HE-Fc fusion protein displays proper receptor-binding and enzymatic activities.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-26 02:17:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/688045"], "description"=>"<p>(A) Ribbon superposition of the MHV-<i>S</i> and BCoV-Mebus HE receptor binding sites. BCoV-Mebus HE is colored gray, coloring of MHV-<i>S</i> HE as in panel A. Bound receptor analogues are shown as cyan sticks and potassium ions as magenta spheres. The five surface exposed loops and the RBS-hairpin that interact with the receptor are indicated. Note that only the R3- and R4-loops differ in conformation. (B) Close-up of the HE-potassium binding-site of MHV<i>-S</i> HE and BCoV-Mebus HE. Shown in ribbon representation are the R3-loop (salmon) and RBS-hairpin (purple) that interacts with the potassium ion (magenta sphere).</p>", "links"=>[], "tags"=>["mhv-s", "bcov-mebus", "receptor", "binding"], "article_id"=>358529, "categories"=>["Virology", "Biochemistry", "Chemistry"], "users"=>["Martijn A. Langereis", "Qinghong Zeng", "Balthasar Heesters", "Eric G. Huizinga", "Raoul J. de Groot"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002492.g004", "stats"=>{"downloads"=>4, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_the_MHV_S_and_BCoV_Mebus_HE_receptor_binding_sites_/358529", "title"=>"Comparison of the MHV-S and BCoV-Mebus HE receptor binding sites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-26 02:22:09"}

PMC Usage Stats | Further Information

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Relative Metric

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