Inferring Stabilizing Mutations from Protein Phylogenies: Application to Influenza Hemagglutinin
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{"title"=>"Inferring Stabilizing Mutations from Protein Phylogenies: Application to Influenza Hemagglutinin", "type"=>"journal", "authors"=>[{"first_name"=>"Jesse D.", "last_name"=>"Bloom", "scopus_author_id"=>"7201379306"}, {"first_name"=>"Matthew J.", "last_name"=>"Glassman", "scopus_author_id"=>"26639240000"}], "year"=>2009, "source"=>"PLoS Computational Biology", "identifiers"=>{"issn"=>"1553734X", "pui"=>"354658168", "sgr"=>"66249122803", "doi"=>"10.1371/journal.pcbi.1000349", "scopus"=>"2-s2.0-66249122803", "isbn"=>"1553-7358 (Electronic)\\r1553-734X (Linking)", "pmid"=>"19381264"}, "id"=>"568dc101-7646-32a0-8ea7-68e72a6a3620", "abstract"=>"One selection pressure shaping sequence evolution is the requirement that a protein fold with sufficient stability to perform its biological functions. We present a conceptual framework that explains how this requirement causes the probability that a particular amino acid mutation is fixed during evolution to depend on its effect on protein stability. We mathematically formalize this framework to develop a Bayesian approach for inferring the stability effects of individual mutations from homologous protein sequences of known phylogeny. This approach is able to predict published experimentally measured mutational stability effects (DeltaDeltaG values) with an accuracy that exceeds both a state-of-the-art physicochemical modeling program and the sequence-based consensus approach. As a further test, we use our phylogenetic inference approach to predict stabilizing mutations to influenza hemagglutinin. We introduce these mutations into a temperature-sensitive influenza virus with a defect in its hemagglutinin gene and experimentally demonstrate that some of the mutations allow the virus to grow at higher temperatures. Our work therefore describes a powerful new approach for predicting stabilizing mutations that can be successfully applied even to large, complex proteins such as hemagglutinin. This approach also makes a mathematical link between phylogenetics and experimentally measurable protein properties, potentially paving the way for more accurate analyses of molecular evolution.", "link"=>"http://www.mendeley.com/research/inferring-stabilizing-mutations-protein-phylogenies-application-influenza-hemagglutinin", "reader_count"=>92, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>5, "Researcher"=>32, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>2, "Student > Bachelor"=>3, "Professor"=>11}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>5, "Researcher"=>32, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>2, "Student > Bachelor"=>3, "Professor"=>11}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Biochemistry, Genetics and Molecular Biology"=>15, "Mathematics"=>1, "Agricultural and Biological Sciences"=>58, "Medicine and Dentistry"=>1, "Physics and Astronomy"=>4, "Chemical Engineering"=>1, "Chemistry"=>4, "Computer Science"=>2, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>4}, "Physics and Astronomy"=>{"Physics and Astronomy"=>4}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>58}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>15}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>4}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"Canada"=>2, "Czech Republic"=>1, "Netherlands"=>1, "United States"=>3, "Finland"=>1, "Denmark"=>1, "United Kingdom"=>2, "Kenya"=>1, "Germany"=>2}, "group_count"=>4}

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  • {"files"=>["https://ndownloader.figshare.com/files/901901"], "description"=>"<p>Results are for wildtype (WT), temperature-sensitive (ts), and ts\n virus with predicted stabilizing mutations. The plaques are scored\n as ++ for clear plaques, + for smaller or\n opaque plaques, +/− for barely distinguishable\n plaques, − for no plaques, and ND for not determined. The\n first mutation numbers are for sequential numbering of the A/WSN/33\n hemagglutinin sequence beginning with zero at the N-terminal\n methionine, while the numbers in parentheses correspond to those\n used in the crystal structure with PDB code 1RVZ.</p>", "links"=>[], "tags"=>["influenza", "viruses", "carrying", "mutations"], "article_id"=>572363, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.t001", "stats"=>{"downloads"=>4, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Plaque_growth_of_influenza_A_WSN_33_H1N1_viruses_carrying_mutations____in_hemagglutinin_/572363", "title"=>"Plaque growth of influenza A/WSN/33 (H1N1) viruses carrying mutations\n in hemagglutinin.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 06:18:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/901695"], "description"=>"<p>The full hemagglutinin trimer is shown in green, with the HA1 chains in\n dark green and the HA2 chains in light green. The temperature-sensitive\n mutation (ts-134 <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000349#pcbi.1000349-Ueda1\" target=\"_blank\">[104]</a>–<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000349#pcbi.1000349-Tong1\" target=\"_blank\">[106]</a>) is shown\n with red spheres. The yellow spheres show the mutations that were\n predicted to be stabilizing by the PIPS program. The blue spheres show\n the four predicted mutations that were experimentally confirmed to\n actually increase the temperature stability. The structure is PDB code\n 1RVZ <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000349#pcbi.1000349-Gamblin1\" target=\"_blank\">[107]</a>.</p>", "links"=>[], "tags"=>["confirmed", "stabilizing", "mutations", "h1"], "article_id"=>572154, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.g010", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Locations_of_the_predicted_and_confirmed_stabilizing_mutations_to_H1____hemagglutinin_/572154", "title"=>"Locations of the predicted and confirmed stabilizing mutations to H1\n hemagglutinin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:17:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/901537"], "description"=>"<p>The PIPS predictions using informative priors were run using subsets of\n all of the available protein sequences. The resulting predictions were then correlated with the experimental values (top) or the PIPS predictions obtained using all available sequences\n (bottom). The values are the squared Pearson correlation\n coefficients. For each number of sequences used, the PIPS predictions\n were made using 10 different random sequence subsets, and the displayed values are the average correlations over these 10\n subsets. For cold shock protein, the subsets were made at intervals of\n 20 sequences, while for ribonuclease HI and thioredoxin they were made\n at intervals of 10 sequences.</p>", "links"=>[], "tags"=>["phylogenetic", "inference", "of", "sequences"], "article_id"=>571994, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.g008", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Performance_of_the_phylogenetic_inference_approach_as_a_function_of____the_number_of_sequences_used_/571994", "title"=>"Performance of the phylogenetic inference approach as a function of\n the number of sequences used.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:16:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/901144"], "description"=>"<p>The “regularizing priors” are peaked at the\n moderately destabilizing value of to capture the general knowledge that most mutations\n are destabilizing. The “hydrophobic priors” capture\n the knowledge that mutations that cause large changes in hydrophobicity\n are often more destabilizing. These priors are peaked at a value equal\n the the absolute value of the difference in amino acid hydrophobicity\n (as defined by the widely used Kyte-Doolittle scale <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000349#pcbi.1000349-Kyte1\" target=\"_blank\">[81]</a>). For example, the prior for a mutation\n from hydrophobic valine (V) to similarly hydrophobic leucine (L) is\n peaked near zero, while that for mutation from valine to charged lysine\n (K) is peaked at a much more destabilizing value. The\n “informative priors” are peaked at the values predicted by the state-of-the-art\n physicochemically based program CUPSAT <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000349#pcbi.1000349-Parthiban1\" target=\"_blank\">[8]</a>, and so\n are designed to leverage extensive pre-existing knowledge about values. All the priors are fairly loose to make the values responsive to their effect on the likelihood.\n The priors also help regularize <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000349#pcbi.1000349-Chen1\" target=\"_blank\">[80]</a> the predictions by biasing them towards a reasonable\n range.</p>", "links"=>[], "tags"=>["biochemistry/molecular evolution", "biochemistry/protein folding", "biotechnology/bioengineering", "computational biology/comparative sequence analysis", "computational biology/evolutionary modeling", "computational biology/population genetics", "evolutionary biology/evolutionary and comparative genetics", "evolutionary biology/microbial evolution and genomics", "infectious diseases/viral infections", "molecular biology/molecular evolution", "virology/virion structure, assembly, and egress", "virology/virus evolution and symbiosis"], "article_id"=>571592, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.g004", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Prior_distributions_over_the_values_/571592", "title"=>"Prior distributions, , over the values.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:13:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/901074"], "description"=>"<p>This tree shows the sequence data for five sequences at a single site . The amino acid codes at the tips of the branches () show the residue identities for the five sequences at\n this site. The variables at the internal nodes () are the amino acid identities at the site for the\n ancestral sequences, and must be inferred. The branch lengths () are proportional to the time since the divergence of\n the sequences.</p>", "links"=>[], "tags"=>["phylogenetic"], "article_id"=>571536, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_An_example_phylogenetic_tree_/571536", "title"=>"An example phylogenetic tree .", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:13:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/901024"], "description"=>"<p>The panel at left show the probability that a protein in an evolving population will have\n extra stability , as given by Equation 3. The panel at right shows the\n probability that a mutation that causes a stability change of will be neutral, as given by Equation 4. The units for are arbitrary; for concreteness here we give them\n units of kcal/mol.</p>", "links"=>[], "tags"=>["distributions", "fixation"], "article_id"=>571485, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Stability_distributions_and_fixation_probabilities_/571485", "title"=>"Stability distributions and fixation probabilities.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:13:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/901820"], "description"=>"<p>All four of the single mutations allow the virus to plaque at higher\n temperatures than the ts parent. The multiple mutants plaque more\n effectively at higher temperatures than the single mutants. Mutations\n are named according to the numbering scheme described in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000349#pcbi-1000349-t001\" target=\"_blank\">Table 1</a>.</p>", "links"=>[], "tags"=>["assays", "temperature-sensitive", "ts", "influenza", "stabilizing", "hemagglutinin"], "article_id"=>572267, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.g011", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Plaque_assays_of_wildtype_temperature_sensitive_ts_and_ts____influenza_with_predicted_stabilizing_hemagglutinin_mutations_/572267", "title"=>"Plaque assays of wildtype, temperature-sensitive (ts), and ts\n influenza with predicted stabilizing hemagglutinin mutations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:17:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/901321"], "description"=>"<p>The plots at left show the predictions made by the CUPSAT physicochemical\n modeling program, the consensus approach, and the PIPS phylogenetic\n inference program using the informative, regularizing, and\n hydrophobicity priors. To the right is the phylogenetic tree of 239\n sequences that was utilized by the PIPS program. The values are the squared Pearson correlation\n coefficients.</p>", "links"=>[], "tags"=>["156-residue", "ribonuclease"], "article_id"=>571781, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.g006", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Experimentally_measured_and_predicted_values_for_the_156_residue_ribonuclease_HI_protein_/571781", "title"=>"Experimentally measured and predicted values for the 156-residue ribonuclease HI protein.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:14:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/901212"], "description"=>"<p>The plots at left show the predictions made by the CUPSAT physicochemical\n modeling program, the consensus approach, and the PIPS phylogenetic\n inference program using the informative, regularizing, and\n hydrophobicity priors. To the right is the phylogenetic tree of 763\n sequences that was utilized by the PIPS program. The values are the squared Pearson correlation\n coefficients.</p>", "links"=>[], "tags"=>["68-residue"], "article_id"=>571670, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.g005", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Experimentally_measured_and_predicted_values_for_the_68_residue_cold_shock_protein_/571670", "title"=>"Experimentally measured and predicted values for the 68-residue cold shock protein.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:14:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/901430"], "description"=>"<p>The plots at left show the predictions made by the CUPSAT physicochemical\n modeling program, the consensus approach, and the PIPS phylogenetic\n inference program using the informative, regularizing, and\n hydrophobicity. To the right is the phylogenetic tree of 213 sequences\n that was utilized by the PIPS program. The values are the squared Pearson correlation\n coefficients.</p>", "links"=>[], "tags"=>["109-residue", "thioredoxin"], "article_id"=>571891, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.g007", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Experimentally_measured_and_predicted_values_for_the_109_residue_thioredoxin_protein_/571891", "title"=>"Experimentally measured and predicted values for the 109-residue thioredoxin protein.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:15:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/900970"], "description"=>"<p>Proteins are assumed to be functional if and only if they are more stable\n than some minimal threshold (in the figure, , which is a typical value for natural proteins <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000349#pcbi.1000349-Fersht2\" target=\"_blank\">[53]</a>; note that more stable proteins have more\n negative values). When a particular destabilizing mutation () occurs, the evolutionary result will depend on the\n stability of the proteins in the parent population. When the parent\n proteins are sufficiently stable (top panel), the mutant protein still\n satisfies the threshold, and so the mutation has the opportunity to\n spread by neutral genetic drift. But when the parent proteins are not\n sufficiently stable (bottom panel), the mutant protein fails to stably\n fold, and is eliminated by natural selection. Therefore, the probability\n that a mutation that induces a stability change of will have an opportunity to spread by neutral genetic\n drift is simply the probability that the parent protein has a stability .</p>", "links"=>[], "tags"=>["biochemistry/molecular evolution", "biochemistry/protein folding", "biotechnology/bioengineering", "computational biology/comparative sequence analysis", "computational biology/evolutionary modeling", "computational biology/population genetics", "evolutionary biology/evolutionary and comparative genetics", "evolutionary biology/microbial evolution and genomics", "infectious diseases/viral infections", "molecular biology/molecular evolution", "virology/virion structure, assembly, and egress", "virology/virus evolution and symbiosis"], "article_id"=>571410, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_stability_threshold_model_of_protein_evolution_/571410", "title"=>"A stability threshold model of protein evolution.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:12:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/901610"], "description"=>"<p>In the plots at left, bars indicate the distribution of predicted values for all single mutations, while symbols show\n predicted values for the temperature-sensitive and revertant mutations.\n At right is the phylogenetic tree utilized by the PIPS program. The tree\n labels give the hemagglutinin subtypes and corresponding numbers of\n sequences. The PIPS predictions are made using the informative\n priors.</p>", "links"=>[], "tags"=>["temperature-sensitive", "and", "revertant", "mutations", "h1"], "article_id"=>572063, "categories"=>["Medicine", "Evolutionary Biology", "Biotechnology", "Infectious Diseases", "Molecular Biology", "Biochemistry", "Virology"], "users"=>["Jesse D. Bloom", "Matthew J. Glassman"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000349.g009", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Predicted_stability_effects_of_known_temperature_sensitive_and____revertant_mutations_to_H1_hemagglutinin_/572063", "title"=>"Predicted stability effects of known temperature-sensitive and\n revertant mutations to H1 hemagglutinin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:16:33"}

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Relative Metric

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