Adaptive Mutations in the JC Virus Protein Capsid Are Associated with Progressive Multifocal Leukoencephalopathy (PML)
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{"title"=>"Adaptive mutations in the JC virus protein capsid are associated with progressive multifocal leukoencephalopathy (PML)", "type"=>"journal", "authors"=>[{"first_name"=>"Shamil R.", "last_name"=>"Sunyaev", "scopus_author_id"=>"35351656700"}, {"first_name"=>"Alexey", "last_name"=>"Lugovskoy", "scopus_author_id"=>"57190670004"}, {"first_name"=>"Kenneth", "last_name"=>"Simon", "scopus_author_id"=>"7202694026"}, {"first_name"=>"Leonid", "last_name"=>"Gorelik", "scopus_author_id"=>"7005836764"}], "year"=>2009, "source"=>"PLoS Genetics", "identifiers"=>{"scopus"=>"2-s2.0-61449209921", "pmid"=>"19197354", "sgr"=>"61449209921", "doi"=>"10.1371/journal.pgen.1000368", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "issn"=>"15537390", "pui"=>"354253492"}, "id"=>"356c04a0-a9be-3de3-baf7-1afdaa0eff7e", "abstract"=>"PML is a progressive and mostly fatal demyelinating disease caused by JC virus infection and destruction of infected oligodendrocytes in multiple brain foci of susceptible individuals. While JC virus is highly prevalent in the human population, PML is a rare disease that exclusively afflicts only a small percentage of immunocompromised individuals including those affected by HIV (AIDS) or immunosuppressive drugs. Viral- and/or host-specific factors, and not simply immune status, must be at play to account for the very large discrepancy between viral prevalence and low disease incidence. Here, we show that several amino acids on the surface of the JC virus capsid protein VP1 display accelerated evolution in viral sequences isolated from PML patients but not in sequences isolated from healthy subjects. We provide strong evidence that at least some of these mutations are involved in binding of sialic acid, a known receptor for the JC virus. Using statistical methods of molecular evolution, we performed a comprehensive analysis of JC virus VP1 sequences isolated from 55 PML patients and 253 sequences isolated from the urine of healthy individuals and found that a subset of amino acids found exclusively among PML VP1 sequences is acquired via adaptive evolution. By modeling of the 3-D structure of the JC virus capsid, we showed that these residues are located within the sialic acid binding site, a JC virus receptor for cell infection. Finally, we go on to demonstrate the involvement of some of these sites in receptor binding by demonstrating a profound reduction in hemagglutination properties of viral-like particles made of the VP1 protein carrying these mutations. Collectively, these results suggest that a more virulent PML causing phenotype of JC virus is acquired via adaptive evolution that changes viral specificity for its cellular receptor(s).", "link"=>"http://www.mendeley.com/research/adaptive-mutations-jc-virus-protein-capsid-associated-progressive-multifocal-leukoencephalopathy-pml", "reader_count"=>57, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>25, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>2, "Other"=>5, "Student > Master"=>3, "Student > Bachelor"=>5, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>25, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>2, "Other"=>5, "Student > Master"=>3, "Student > Bachelor"=>5, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>31, "Medicine and Dentistry"=>16, "Neuroscience"=>3, "Sports and Recreations"=>1, "Chemistry"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>16}, "Neuroscience"=>{"Neuroscience"=>3}, "Chemistry"=>{"Chemistry"=>1}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>31}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United States"=>4, "Japan"=>1, "Brazil"=>2, "South Africa"=>1, "Germany"=>1}, "group_count"=>1}

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  • {"files"=>["https://ndownloader.figshare.com/files/908997"], "description"=>"<p>(A) A model of JCV VP1 basic pentamer in complex with NeuNAc–(α2,3)–Gal–(β1,3)–[(α2,6)-NeuNAc]–Glc-NAc tetrasaccharide. Surfaces of five chains of JCV VP1 are shown in different colors. The RG motif essential for binding of core sialic acid is shown in blue. PML-associated mutated residues confirmed by PAML (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000368#pgen-1000368-t001\" target=\"_blank\">Table 1</a>) are shown in red (L55, K60, S265, S267, S269). Additional mutations unique to PML-isolated samples (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000368#pgen.1000368.s003\" target=\"_blank\">Table S2</a>) are shown in green (S61, D66, S123, H129, V223 and Q271). (B) A close-up view of NeuNAc–(α2,3)–Gal–(β1,3)–[(α2,6)-NeuNAc]–Glc-NAc tetrasaccharide/JCV VP1 complex. The color scheme is as described in panel (A). Location of V296 of MPyV VP1 which is predicted to be equivalent to S269 of JCV VP1 is shown in yellow mesh.</p>", "links"=>[], "tags"=>["jcv", "tetrasaccharide"], "article_id"=>579459, "categories"=>["Medicine", "Evolutionary Biology", "Plant Biology", "Infectious Diseases", "Neuroscience"], "users"=>["Shamil R. Sunyaev", "Alexey Lugovskoy", "Kenneth Simon", "Leonid Gorelik"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000368.g002", "stats"=>{"downloads"=>6, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structural_model_of_JCV_VP1_NeuNAc_8211_945_2_3_8211_Gal_8211_946_1_3_8211_945_2_6_NeuNAc_8211_Glc_NAc_tetrasaccharide_complex_/579459", "title"=>"Structural model of JCV VP1/NeuNAc–(α2,3)–Gal–(β1,3)–[(α2,6)-NeuNAc]–Glc-NAc tetrasaccharide complex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-02-06 02:37:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/909090"], "description"=>"<p>Hemagglutination was conducted as described in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000368#s3\" target=\"_blank\">Materials and Methods</a> using serial dilutions of VLPs starting from 200 µg/ml. VLPs were added to type O RBC and incubated at 4°C for 3 hours. Agglutination is visualized by the lack of a round pellet formed by the settling of RBCs out of suspension. F55 is a VP1 variant with phenylalanine at the position 55 (AAT09831), F269 is a VP1 variant with phenylalanine at the position 269 (BAE0011). WT (AAQ88264) and Mad-1 (P03089) are VP1 variants with leucine and serine at positions 55 and 269 respectively.</p>", "links"=>[], "tags"=>["55", "269", "vp1", "hemagglutination", "rbcs", "viral", "particles"], "article_id"=>579540, "categories"=>["Medicine", "Evolutionary Biology", "Plant Biology", "Infectious Diseases", "Neuroscience"], "users"=>["Shamil R. Sunyaev", "Alexey Lugovskoy", "Kenneth Simon", "Leonid Gorelik"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000368.t002", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Residues_55_and_269_in_VP1_protein_play_very_important_role_in_hemagglutination_of_RBCs_by_Viral_Like_Particles_VLPs_/579540", "title"=>"Residues 55 and 269 in VP1 protein play very important role in hemagglutination of RBCs by Viral Like Particles (VLPs).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-02-06 02:39:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/909119"], "description"=>"<p><i>VP1</i> sequences isolated from PML patients and random subsets of sequences isolated from healthy subjects were further analyzed using PAML <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000368#pgen.1000368-Yang1\" target=\"_blank\">[23]</a>. We examined multiple models of sequence evolution incorporated in PAML including purely neutral model (M0), nearly neutral model (M1), model with positive selection (M2) and additional more complex models (M3–M8). We used likelihood ratio test (LRT) to compare the difference between models M1 and M2 to test for positive selection. P-values for positive selection in three datasets are shown together with Bayesian posterior probabilities for each codon position. Residues with Bayes Empirical Bayes posterior probabilities exceeding 0.5 are shown.</p>", "links"=>[], "tags"=>["pml"], "article_id"=>579582, "categories"=>["Medicine", "Evolutionary Biology", "Plant Biology", "Infectious Diseases", "Neuroscience"], "users"=>["Shamil R. Sunyaev", "Alexey Lugovskoy", "Kenneth Simon", "Leonid Gorelik"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000368.t001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Codons_under_positive_selection_in_the_PML_sample_/579582", "title"=>"Codons under positive selection in the PML sample.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-02-06 02:39:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/449286", "https://ndownloader.figshare.com/files/449322", "https://ndownloader.figshare.com/files/449372", "https://ndownloader.figshare.com/files/449419"], "description"=>"<div><p>PML is a progressive and mostly fatal demyelinating disease caused by JC virus infection and destruction of infected oligodendrocytes in multiple brain foci of susceptible individuals. While JC virus is highly prevalent in the human population, PML is a rare disease that exclusively afflicts only a small percentage of immunocompromised individuals including those affected by HIV (AIDS) or immunosuppressive drugs. Viral- and/or host-specific factors, and not simply immune status, must be at play to account for the very large discrepancy between viral prevalence and low disease incidence. Here, we show that several amino acids on the surface of the JC virus capsid protein VP1 display accelerated evolution in viral sequences isolated from PML patients but not in sequences isolated from healthy subjects. We provide strong evidence that at least some of these mutations are involved in binding of sialic acid, a known receptor for the JC virus. Using statistical methods of molecular evolution, we performed a comprehensive analysis of JC virus VP1 sequences isolated from 55 PML patients and 253 sequences isolated from the urine of healthy individuals and found that a subset of amino acids found exclusively among PML VP1 sequences is acquired via adaptive evolution. By modeling of the 3-D structure of the JC virus capsid, we showed that these residues are located within the sialic acid binding site, a JC virus receptor for cell infection. Finally, we go on to demonstrate the involvement of some of these sites in receptor binding by demonstrating a profound reduction in hemagglutination properties of viral-like particles made of the VP1 protein carrying these mutations. Collectively, these results suggest that a more virulent PML causing phenotype of JC virus is acquired via adaptive evolution that changes viral specificity for its cellular receptor(s).</p></div>", "links"=>[], "tags"=>["adaptive", "mutations", "jc", "capsid", "are", "multifocal", "leukoencephalopathy"], "article_id"=>148558, "categories"=>["Medicine", "Evolutionary Biology", "Cell Biology", "Cancer", "Neuroscience"], "users"=>["Shamil R. Sunyaev", "Alexey Lugovskoy", "Kenneth Simon", "Leonid Gorelik"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000368.s001", "https://dx.doi.org/10.1371/journal.pgen.1000368.s002", "https://dx.doi.org/10.1371/journal.pgen.1000368.s003", "https://dx.doi.org/10.1371/journal.pgen.1000368.s004"], "stats"=>{"downloads"=>10, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Adaptive_Mutations_in_the_JC_Virus_Protein_Capsid_Are_Associated_with_Progressive_Multifocal_Leukoencephalopathy_PML_/148558", "title"=>"Adaptive Mutations in the JC Virus Protein Capsid Are Associated with Progressive Multifocal Leukoencephalopathy (PML)", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-02-06 02:22:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/908915"], "description"=>"<p>(A) Broad phylogenetic distribution of PML causing JC viruses. Tree branches (labeled by GI numbers) corresponding to PML causing viruses are marked by red stars, viruses isolated from healthy subjects are marked by green stars. The tree is constructed based on DNA sequences of <i>VP1</i> gene using maximum likelihood method. Only one sequence per patient was included. (B) Phylogenetic distribution of mutations in the codon 269. The tree represents <i>VP1</i> genes (labeled by GI numbers) of viruses isolated from PML patients. Mutations in Ser269 codons are indicated by text inserts. Circles on branches reflect aLRT support. Position 269 was masked prior to constructing the tree to avoid attraction of branches with mutations of this codon.</p>", "links"=>[], "tags"=>["pml"], "article_id"=>579375, "categories"=>["Medicine", "Evolutionary Biology", "Plant Biology", "Infectious Diseases", "Neuroscience"], "users"=>["Shamil R. Sunyaev", "Alexey Lugovskoy", "Kenneth Simon", "Leonid Gorelik"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000368.g001", "stats"=>{"downloads"=>4, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_distribution_of_PML_associated_viruses_/579375", "title"=>"Phylogenetic distribution of PML associated viruses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-02-06 02:36:15"}

PMC Usage Stats | Further Information

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