A Structure-Guided Mutation in the Major Capsid Protein Retargets BK Polyomavirus
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{"title"=>"A Structure-Guided Mutation in the Major Capsid Protein Retargets BK Polyomavirus", "type"=>"journal", "authors"=>[{"first_name"=>"Ursula", "last_name"=>"Neu", "scopus_author_id"=>"24076969800"}, {"first_name"=>"Stacy ann A.", "last_name"=>"Allen", "scopus_author_id"=>"55922289400"}, {"first_name"=>"Bärbel S.", "last_name"=>"Blaum", "scopus_author_id"=>"17343432600"}, {"first_name"=>"Yan", "last_name"=>"Liu", "scopus_author_id"=>"35741087900"}, {"first_name"=>"Martin", "last_name"=>"Frank", "scopus_author_id"=>"35573408800"}, {"first_name"=>"Angelina S.", "last_name"=>"Palma", "scopus_author_id"=>"55729139000"}, {"first_name"=>"Luisa J.", "last_name"=>"Ströh", "scopus_author_id"=>"37038574600"}, {"first_name"=>"Ten", "last_name"=>"Feizi", "scopus_author_id"=>"7103224576"}, {"first_name"=>"Thomas", "last_name"=>"Peters", "scopus_author_id"=>"7402959309"}, {"first_name"=>"Walter J.", "last_name"=>"Atwood", "scopus_author_id"=>"7005032811"}, {"first_name"=>"Thilo", "last_name"=>"Stehle", "scopus_author_id"=>"7003736109"}], "year"=>2013, "source"=>"PLoS Pathogens", "identifiers"=>{"pmid"=>"24130487", "sgr"=>"84887302514", "doi"=>"10.1371/journal.ppat.1003688", "scopus"=>"2-s2.0-84887302514", "pui"=>"370218078", "isbn"=>"1553-7374 (Electronic) 1553-7366 (Linking)", "issn"=>"15537366"}, "id"=>"3ebe4683-2bca-338d-94dd-f569d000229c", "abstract"=>"Viruses within a family often vary in their cellular tropism and pathogenicity. In many cases, these variations are due to viruses switching their specificity from one cell surface receptor to another. The structural requirements that underlie such receptor switching are not well understood especially for carbohydrate-binding viruses, as methods capable of structure-specificity studies are only relatively recently being developed for carbohydrates. We have characterized the receptor specificity, structure and infectivity of the human polyomavirus BKPyV, the causative agent of polyomavirus-associated nephropathy, and uncover a molecular switch for binding different carbohydrate receptors. We show that the b-series gangliosides GD3, GD2, GD1b and GT1b all can serve as receptors for BKPyV. The crystal structure of the BKPyV capsid protein VP1 in complex with GD3 reveals contacts with two sialic acid moieties in the receptor, providing a basis for the observed specificity. Comparison with the structure of simian virus 40 (SV40) VP1 bound to ganglioside GM1 identifies the amino acid at position 68 as a determinant of specificity. Mutation of this residue from lysine in BKPyV to serine in SV40 switches the receptor specificity of BKPyV from GD3 to GM1 both in vitro and in cell culture. Our findings highlight the plasticity of viral receptor binding sites and form a template to retarget viruses to different receptors and cell types.", "link"=>"http://www.mendeley.com/research/structureguided-mutation-major-capsid-protein-retargets-bk-polyomavirus", "reader_count"=>40, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>14, "Student > Master"=>4, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>14, "Student > Master"=>4, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>21, "Medicine and Dentistry"=>5, "Chemistry"=>1, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>21}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"United States"=>2, "France"=>1, "Germany"=>2}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1231459"], "description"=>"<p>r.m.s.d. = root-mean-square deviation.</p>*<p>R<sub>free</sub> was calculated with 3.5% of the data.</p>", "links"=>[], "tags"=>["refinement"], "article_id"=>819003, "categories"=>["Biological Sciences"], "users"=>["Ursula Neu", "Stacy-ann A. Allen", "Bärbel S. Blaum", "Yan Liu", "Martin Frank", "Angelina S. Palma", "Luisa J. Ströh", "Ten Feizi", "Thomas Peters", "Walter J. Atwood", "Thilo Stehle"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003688.t001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Crystallographic_data_collection_and_refinement_statistics_/819003", "title"=>"Crystallographic data collection and refinement statistics.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-10-10 06:11:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231458"], "description"=>"<p>(A) Binding of BKPyV K68S to Vero cells. Cells were treated as in 3C fixed and pentamer binding to cells untreated (left) or treated with NeuNAc-GM1 (right) assessed by flow cytometry. Histograms show the fluorescence intensity of the Alexa 488 antibody alone (gray-filled), WT pentamer (black) and K68S pentamer (green) for 1×10<sup>4</sup> events. (B) Growth assay for BKPyV K68S in Vero cells. Cells were transfected as previously described, treated with NeuNAc-GM1, fixed and stained over 23 days. Viral spread was quantified by scoring for cells expressing T-Ag. The anti-V antigen monoclonal antibody 597 used in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003688#ppat-1003688-g001\" target=\"_blank\">Figures 1</a> and <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003688#ppat-1003688-g003\" target=\"_blank\">3</a> recognizes an epitope that is disrupted by the K68S mutation, requiring the use of an mAb against T-Ag. The average number of T-Ag positive cells is plotted from 3 independent experiments. (C) Binding of BKPyV K68S to HEK cells. Cells were treated as previously described, fixed and pentamer binding to cells untreated (left), or treated with NeuNAc-GM1 and CTX (right) assessed by flow cytometry. Histograms show the fluorescence intensity of the Alexa 488 antibody alone (gray-filled), K68S pentamer (green) WT pentamer (black), WT pentamer with CTX (orange) and K68S pentamer with CTX (blue) for 1×10<sup>4</sup> events. (D) Growth assay for BKPyV K68S in HEK cells. Cells were transfected as previously described, treated with NeuNAc-GM1, fixed and stained over 13 days. Viral spread was quantified as above. Gangliosides were added every 3 days.</p>", "links"=>[], "tags"=>["bkpyv", "uses", "neuac-gm1", "receptor", "attachment"], "article_id"=>819002, "categories"=>["Biological Sciences"], "users"=>["Ursula Neu", "Stacy-ann A. Allen", "Bärbel S. Blaum", "Yan Liu", "Martin Frank", "Angelina S. Palma", "Luisa J. Ströh", "Ten Feizi", "Thomas Peters", "Walter J. Atwood", "Thilo Stehle"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003688.g006", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_K68S_BKPyV_uses_NeuAc_GM1_as_a_receptor_for_attachment_and_infection_/819002", "title"=>"K68S BKPyV uses NeuAc-GM1 as a receptor for attachment and infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:11:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231452"], "description"=>"<p>(A) Structure of BKPyV VP1 pentamer in complex with GD3 oligosaccharide. One VP1 monomer is highlighted in green. Monosaccharides unbiased by crystal contacts are colored orange, while the ones binding to crystal contacts are colored white. (B) Composite annealed difference electron density for the terminal disialic acid motif of GD3 oligosaccharide bound to BKPyV VP1 at a σ level of 2.5. cw/ccw = belonging to the clockwise/counterclockwise neighboring VP1 monomer within the pentamer. (C) Interactions of GD3 oligosaccharide with BKPyV VP1. The oligosaccharide is shown in orange. Side chains contacting the sugar are colored as follows: those making hydrogen bonds are colored dark green, those making van der Waals interactions are light green, and those making water-mediated hydrogen bonds are colored yellow. Atoms of the protein backbone are shown in gray, and water molecules are in cyan. Direct hydrogen bonds are indicated as black dashed lines, water-mediated ones are grey. (D+E) Model of the interaction of BKPyV VP1 with GD1b oligosaccharide. The left arm and the stem of GD1b are colored orange. Residues interacting with the left arm of GD1b are colored as in (C). The disialic acid motif of GD1b and the protein residues contacting it are colored white.</p>", "links"=>[], "tags"=>["bkpyv", "vp1-gd3", "oligosaccharide"], "article_id"=>818997, "categories"=>["Biological Sciences"], "users"=>["Ursula Neu", "Stacy-ann A. Allen", "Bärbel S. Blaum", "Yan Liu", "Martin Frank", "Angelina S. Palma", "Luisa J. Ströh", "Ten Feizi", "Thomas Peters", "Walter J. Atwood", "Thilo Stehle"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003688.g002", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structure_of_a_BKPyV_VP1_GD3_oligosaccharide_complex_/818997", "title"=>"Structure of a BKPyV VP1-GD3 oligosaccharide complex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:11:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231448"], "description"=>"<p>(A) Schematic representation of structures of disialic acid-containing b-series gangliosides GD3, GD2, GD1b, GT1b and of the monosialylated a-series ganglioside GM1 indicating the abbreviated designations used here for individual residues in the gangliosides. (B) Ganglioside supplementation assays. Vero cells were incubated with gangliosides, challenged with BKPyV and scored for infection. The average number of VP1 positive cells is plotted compared to controls. Error bars represent the standard deviation for 3 independent experiments. Asterisks indicate p-value (*p<0.05). (C) STD off-resonance (top) and difference (bottom) spectra of WT BKPyV VP1 in the presence of 50-fold excess GD3 oligosaccharide. The off-resonance spectrum was scaled to 3%. GD3 resonances labeled in the difference spectrum receive considerable saturation transfer from the protein. Regions with strong signal overlap are not labeled because saturation effects in this region cannot be unambiguously assigned. Signals that were truncated are denoted by diagonal bars. (D) STD off-resonance (top) and difference spectrum (bottom) of wild type BKPyV in the presence of 50-fold excess GD1b oligosaccharide. The spectrum is labeled as in C.</p>", "links"=>[], "tags"=>["gangliosides", "receptors"], "article_id"=>818993, "categories"=>["Biological Sciences"], "users"=>["Ursula Neu", "Stacy-ann A. Allen", "Bärbel S. Blaum", "Yan Liu", "Martin Frank", "Angelina S. Palma", "Luisa J. Ströh", "Ten Feizi", "Thomas Peters", "Walter J. Atwood", "Thilo Stehle"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003688.g001", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_B_series_gangliosides_are_receptors_for_BKPyV_/818993", "title"=>"B-series gangliosides are receptors for BKPyV.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:11:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231461", "https://ndownloader.figshare.com/files/1231462", "https://ndownloader.figshare.com/files/1231463"], "description"=>"<div><p>Viruses within a family often vary in their cellular tropism and pathogenicity. In many cases, these variations are due to viruses switching their specificity from one cell surface receptor to another. The structural requirements that underlie such receptor switching are not well understood especially for carbohydrate-binding viruses, as methods capable of structure-specificity studies are only relatively recently being developed for carbohydrates. We have characterized the receptor specificity, structure and infectivity of the human polyomavirus BKPyV, the causative agent of polyomavirus-associated nephropathy, and uncover a molecular switch for binding different carbohydrate receptors. We show that the b-series gangliosides GD3, GD2, GD1b and GT1b all can serve as receptors for BKPyV. The crystal structure of the BKPyV capsid protein VP1 in complex with GD3 reveals contacts with two sialic acid moieties in the receptor, providing a basis for the observed specificity. Comparison with the structure of simian virus 40 (SV40) VP1 bound to ganglioside GM1 identifies the amino acid at position 68 as a determinant of specificity. Mutation of this residue from lysine in BKPyV to serine in SV40 switches the receptor specificity of BKPyV from GD3 to GM1 both <i>in vitro</i> and in cell culture. Our findings highlight the plasticity of viral receptor binding sites and form a template to retarget viruses to different receptors and cell types.</p></div>", "links"=>[], "tags"=>["structure-guided", "mutation", "capsid", "retargets", "bk"], "article_id"=>819005, "categories"=>["Biological Sciences"], "users"=>["Ursula Neu", "Stacy-ann A. Allen", "Bärbel S. Blaum", "Yan Liu", "Martin Frank", "Angelina S. Palma", "Luisa J. Ströh", "Ten Feizi", "Thomas Peters", "Walter J. Atwood", "Thilo Stehle"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003688.s001", "https://dx.doi.org/10.1371/journal.ppat.1003688.s002", "https://dx.doi.org/10.1371/journal.ppat.1003688.s003"], "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_Structure_Guided_Mutation_in_the_Major_Capsid_Protein_Retargets_BK_Polyomavirus_/819005", "title"=>"A Structure-Guided Mutation in the Major Capsid Protein Retargets BK Polyomavirus", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-10-10 06:11:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231457"], "description"=>"<p>STD difference spectra of (A) BKPyV K68S with GD3, (B and C, respectively) BKPyV K68S and SV40 with GM1. (D) SV40-GM1 off-resonance spectrum. A 50-fold excess of oligosaccharide was used for each spectrum. The off-resonance spectrum was scaled to 3%. Resonances labeled in the difference spectra with GM1 (B and C) receive considerable saturation transfer from BKPyV K68S and SV40. Regions with strong signal overlap are not labeled because they cannot be unambiguously assigned. Binding of BKPyV K68S to GD3, previously seen for WT BKPyV (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003688#ppat-1003688-g001\" target=\"_blank\">Fig. 1C</a>), is abolished by the mutation (A). Carbohydrate microarray analyses of recombinant VP1 of (E) BKPyV, (F) BKPyV K68S and (G) SV40 using 21 ganglioside-related saccharide probes, which included the b-series gangliosides as well as GM1 variants NeuNAc-GM1 and NeuNGc-GM1. The doses of probes arrayed per spot are indicated. Numerical scores of the binding signals are means of duplicate spots (with error bars). The complete list of probes and their sequences are in Supplemental <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003688#ppat.1003688.s003\" target=\"_blank\">Table S1</a>.</p>", "links"=>[], "tags"=>["k68s", "mutation", "targets", "bkpyv", "sv40", "receptor"], "article_id"=>819001, "categories"=>["Biological Sciences"], "users"=>["Ursula Neu", "Stacy-ann A. Allen", "Bärbel S. Blaum", "Yan Liu", "Martin Frank", "Angelina S. Palma", "Luisa J. Ströh", "Ten Feizi", "Thomas Peters", "Walter J. Atwood", "Thilo Stehle"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003688.g005", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_K68S_mutation_targets_BKPyV_to_the_SV40_receptor_GM1_/819001", "title"=>"The K68S mutation targets BKPyV to the SV40 receptor GM1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:11:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231454"], "description"=>"<p>Recognition of carbohydrate receptors by BKPyV (A), SV40 (B), and JCPyV (C). Only residues making direct hydrogen bonds or van der Waals interactions are shown. Residues that make conserved interactions are colored in yellow, side chains whose positions are not conserved are shown in green (BKPyV), blue (SV40) and pink (JCPyV). (D) Comparison of carbohydrate ligands of BKPyV, SV40 and JCPyV. The oligosaccharides are colored green, blue and pink for the BKPyV, SV40 and JCPyV ligands, respectively. The structures were aligned using the protein main chain.</p>", "links"=>[], "tags"=>["binding", "sites", "jcpyv"], "article_id"=>818999, "categories"=>["Biological Sciences"], "users"=>["Ursula Neu", "Stacy-ann A. Allen", "Bärbel S. Blaum", "Yan Liu", "Martin Frank", "Angelina S. Palma", "Luisa J. Ströh", "Ten Feizi", "Thomas Peters", "Walter J. Atwood", "Thilo Stehle"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003688.g004", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Carbohydrate_binding_sites_of_BKPyV_JCPyV_and_SV40_/818999", "title"=>"Carbohydrate binding sites of BKPyV, JCPyV and SV40.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:11:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231453"], "description"=>"<p>(A) Structural model of the BKPyV-GD1b complex. Residues targeted for mutation are colored dark green for the disialic acid motif and light green for the left arm binding sites, respectively. (B) Growth assay for the sialic acid binding site mutants. Vero cells were transfected with linearized WT or mutant BKPyV DNA. Cells were fixed permeabilized and stained for VP1 at 3 day intervals for 22 days and analyzed by indirect immunofluorescence. Viral spread was quantified by scoring for cells expressing VP1. The average number of VP1 positive cells is plotted from 3 independent experiments with each time point representing the average number of infected cells per visual field for 8 fields. (C) Binding of the sialic acid binding site mutants to Vero cells. Cells were incubated with purified His-tagged WT or mutant BKPyV pentamers and an Alexa Fluor 488 conjugated penta-His secondary antibody. Cells were fixed and pentamer binding to cells assessed by flow cytometry. Histograms show the fluorescence intensity of the Alexa 488 antibody alone (gray-filled), WT pentamer (black) and mutants (color) for 1×10<sup>4</sup> events. (D) Growth assay for the left arm binding site mutants assessed as in B.</p>", "links"=>[], "tags"=>["residues", "branches", "gd1b", "abolish"], "article_id"=>818998, "categories"=>["Biological Sciences"], "users"=>["Ursula Neu", "Stacy-ann A. Allen", "Bärbel S. Blaum", "Yan Liu", "Martin Frank", "Angelina S. Palma", "Luisa J. Ströh", "Ten Feizi", "Thomas Peters", "Walter J. Atwood", "Thilo Stehle"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003688.g003", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mutation_of_residues_that_interact_with_the_left_and_right_branches_of_GD1b_abolish_or_reduce_growth_/818998", "title"=>"Mutation of residues that interact with the left and right branches of GD1b abolish or reduce growth.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:11:16"}

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Relative Metric

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