Directed Evolution Reveals the Binding Motif Preference of the LC8/DYNLL Hub Protein and Predicts Large Numbers of Novel Binders in the Human Proteome
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{"title"=>"Directed evolution reveals the binding motif preference of the LC8/DYNLL hub protein and predicts large numbers of novel binders in the human proteome", "type"=>"journal", "authors"=>[{"first_name"=>"Péter", "last_name"=>"Rapali", "scopus_author_id"=>"37026877100"}, {"first_name"=>"László", "last_name"=>"Radnai", "scopus_author_id"=>"15021466700"}, {"first_name"=>"Dániel", "last_name"=>"Süveges", "scopus_author_id"=>"23098638800"}, {"first_name"=>"Veronika", "last_name"=>"Harmat", "scopus_author_id"=>"6603495570"}, {"first_name"=>"Ferenc", "last_name"=>"Tölgyesi", "scopus_author_id"=>"6602792450"}, {"first_name"=>"Weixiao Y.", "last_name"=>"Wahlgren", "scopus_author_id"=>"24437420600"}, {"first_name"=>"Gergely", "last_name"=>"Katona", "scopus_author_id"=>"7006021091"}, {"first_name"=>"László", "last_name"=>"Nyitray", "scopus_author_id"=>"6701819243"}, {"first_name"=>"Gábor", "last_name"=>"Pál", "scopus_author_id"=>"7005651724"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"79955142468", "scopus"=>"2-s2.0-79955142468", "doi"=>"10.1371/journal.pone.0018818", "pui"=>"361656153", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"21533121"}, "id"=>"1ac25492-54de-3da5-b3f6-53b916982370", "abstract"=>"LC8 dynein light chain (DYNLL) is a eukaryotic hub protein that is thought to function as a dimerization engine. Its interacting partners are involved in a wide range of cellular functions. In its dozens of hitherto identified binding partners DYNLL binds to a linear peptide segment. The known segments define a loosely characterized binding motif: [D/S](-4)K(-3)X(-2)[T/V/I](-1)Q(0)[T/V](1)[D/E](2). The motifs are localized in disordered segments of the DYNLL-binding proteins and are often flanked by coiled coil or other potential dimerization domains. Based on a directed evolution approach, here we provide the first quantitative characterization of the binding preference of the DYNLL binding site. We displayed on M13 phage a naïve peptide library with seven fully randomized positions around a fixed, naturally conserved glutamine. The peptides were presented in a bivalent manner fused to a leucine zipper mimicking the natural dimer to dimer binding stoichiometry of DYNLL-partner complexes. The phage-selected consensus sequence V(-5)S(-4)R(-3)G(-2)T(-1)Q(0)T(1)E(2) resembles the natural one, but is extended by an additional N-terminal valine, which increases the affinity of the monomeric peptide twentyfold. Leu-zipper dimerization increases the affinity into the subnanomolar range. By comparing crystal structures of an SRGTQTE-DYNLL and a dimeric VSRGTQTE-DYNLL complex we find that the affinity enhancing valine is accommodated in a binding pocket on DYNLL. Based on the in vitro evolved sequence pattern we predict a large number of novel DYNLL binding partners in the human proteome. Among these EML3, a microtubule-binding protein involved in mitosis contains an exact match of the phage-evolved consensus and binds to DYNLL with nanomolar affinity. These results significantly widen the scope of the human interactome around DYNLL and will certainly shed more light on the biological functions and organizing role of DYNLL in the human and other eukaryotic interactomes.", "link"=>"http://www.mendeley.com/research/directed-evolution-reveals-binding-motif-preference-lc8dynll-hub-protein-predicts-large-numbers-nove", "reader_count"=>50, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>10, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>22, "Student > Postgraduate"=>1, "Student > Master"=>4, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>10, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>22, "Student > Postgraduate"=>1, "Student > Master"=>4, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Engineering"=>2, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>34, "Medicine and Dentistry"=>1, "Neuroscience"=>1, "Chemistry"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>34}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"United States"=>1, "Poland"=>1, "Denmark"=>1, "Spain"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/392312", "https://ndownloader.figshare.com/files/392326", "https://ndownloader.figshare.com/files/392334", "https://ndownloader.figshare.com/files/392344", "https://ndownloader.figshare.com/files/392351", "https://ndownloader.figshare.com/files/392361", "https://ndownloader.figshare.com/files/392368"], "description"=>"<div><p>LC8 dynein light chain (DYNLL) is a eukaryotic hub protein that is thought to function as a dimerization engine. Its interacting partners are involved in a wide range of cellular functions. In its dozens of hitherto identified binding partners DYNLL binds to a linear peptide segment. The known segments define a loosely characterized binding motif: [D/S]<sub>-4</sub>K<sub>-3</sub>X<sub>-2</sub>[T/V/I]<sub>-1</sub>Q<sub>0</sub>[T/V]<sub>1</sub>[D/E]<sub>2</sub>. The motifs are localized in disordered segments of the DYNLL-binding proteins and are often flanked by coiled coil or other potential dimerization domains. Based on a directed evolution approach, here we provide the first quantitative characterization of the binding preference of the DYNLL binding site. We displayed on M13 phage a naïve peptide library with seven fully randomized positions around a fixed, naturally conserved glutamine. The peptides were presented in a bivalent manner fused to a leucine zipper mimicking the natural dimer to dimer binding stoichiometry of DYNLL-partner complexes. The phage<em>-</em>selected consensus sequence V<sub>-5</sub>S<sub>-4</sub>R<sub>-3</sub>G<sub>-2</sub>T<sub>-1</sub>Q<sub>0</sub>T<sub>1</sub>E<sub>2</sub> resembles the natural one, but is extended by an additional N-terminal valine, which increases the affinity of the monomeric peptide twentyfold. Leu-zipper dimerization increases the affinity into the subnanomolar range. By comparing crystal structures of an SRGTQTE-DYNLL and a dimeric VSRGTQTE-DYNLL complex we find that the affinity enhancing valine is accommodated in a binding pocket on DYNLL. Based on the <em>in vitro</em> evolved sequence pattern we predict a large number of novel DYNLL binding partners in the human proteome. Among these EML3, a microtubule-binding protein involved in mitosis contains an exact match of the phage-evolved consensus and binds to DYNLL with nanomolar affinity. These results significantly widen the scope of the human interactome around DYNLL and will certainly shed more light on the biological functions and organizing role of DYNLL in the human and other eukaryotic interactomes.</p> </div>", "links"=>[], "tags"=>["directed", "reveals", "binding", "motif", "hub", "numbers", "binders", "proteome"], "article_id"=>137483, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Péter Rapali", "László Radnai", "Dániel Süveges", "Veronika Harmat", "Ferenc Tölgyesi", "Weixiao Y. Wahlgren", "Gergely Katona", "László Nyitray", "Gábor Pál"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0018818.s001", "https://dx.doi.org/10.1371/journal.pone.0018818.s002", "https://dx.doi.org/10.1371/journal.pone.0018818.s003", "https://dx.doi.org/10.1371/journal.pone.0018818.s004", "https://dx.doi.org/10.1371/journal.pone.0018818.s005", "https://dx.doi.org/10.1371/journal.pone.0018818.s006", "https://dx.doi.org/10.1371/journal.pone.0018818.s007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Directed_Evolution_Reveals_the_Binding_Motif_Preference_of_the_LC8_DYNLL_Hub_Protein_and_Predicts_Large_Numbers_of_Novel_Binders_in_the_Human_Proteome/137483", "title"=>"Directed Evolution Reveals the Binding Motif Preference of the LC8/DYNLL Hub Protein and Predicts Large Numbers of Novel Binders in the Human Proteome", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-04-18 02:04:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/782970"], "description"=>"<p>Bivalent phage display.</p>", "links"=>[], "tags"=>["phage"], "article_id"=>453335, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Péter Rapali", "László Radnai", "Dániel Süveges", "Veronika Harmat", "Ferenc Tölgyesi", "Weixiao Y. Wahlgren", "Gergely Katona", "László Nyitray", "Gábor Pál"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0018818.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bivalent_phage_display_/453335", "title"=>"Bivalent phage display.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-18 00:55:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/783102"], "description"=>"<p>Position heights represent the degree of conservation. Letter heights indicate normalized amino acid proportions. (A) Sequence logo calculated from 41 known natural binding motifs listed in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0018818#pone.0018818.s003\" target=\"_blank\">Table S1</a> and (B) from phage selected DYNLL-binding clones listed in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0018818#pone.0018818.s004\" target=\"_blank\">Table S2</a>. Similar colors indicate similar chemical properties <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0018818#pone.0018818-Crooks1\" target=\"_blank\">[44]</a>.</p>", "links"=>[], "tags"=>["logos", "evolved", "binding"], "article_id"=>453466, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Péter Rapali", "László Radnai", "Dániel Süveges", "Veronika Harmat", "Ferenc Tölgyesi", "Weixiao Y. Wahlgren", "Gergely Katona", "László Nyitray", "Gábor Pál"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0018818.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sequence_logos_of_naturally_evolved_and_in_vitro_evolved_binding_motifs_/453466", "title"=>"Sequence logos of naturally evolved and <i>in vitro</i> evolved binding motifs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-18 00:57:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/783290"], "description"=>"<p>Data for natural consensus (Ac-DKSTQTD) and its two control peptides and data for phage selected consensus (Ac-VSRGTQTE) and its two control peptides are shown in A and B, respectively.</p>", "links"=>[], "tags"=>["binding", "properties", "evolved", "motifs", "isothermal", "titration"], "article_id"=>453649, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Péter Rapali", "László Radnai", "Dániel Süveges", "Veronika Harmat", "Ferenc Tölgyesi", "Weixiao Y. Wahlgren", "Gergely Katona", "László Nyitray", "Gábor Pál"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0018818.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Thermodynamic_binding_properties_of_natural_and_in_vitro_evolved_motifs_determined_by_isothermal_titration_calorimetry_/453649", "title"=>"Thermodynamic binding properties of natural and <i>in vitro</i> evolved motifs determined by isothermal titration calorimetry.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-18 01:00:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/783444"], "description"=>"<p>Peptides bound to DYNLL adopt similar conformation, see alignment in C. As shown in B the Leu-zipper dimerized VSRGTQTE peptides lay into two parallel binding grooves on DYNLL2 forming a dimer-dimer complex. Colors from red to blue correspond to high and low B-factors, respectively (from 131 to 48). The GGSG linker between the binding motif and the Leu-zipper appears to be flexible. Side chain interactions between the peptides and the binding grove of DYNLL2 are shown in D and E. Side chains of DYNLL2 having at least one atom within 4 Å distance from the peptide are shown as sticks. F and G are rotated versions (by approximately 90° along the axes of the binding motifs) of D and E, respectively, and show that the peptides bind to DYNLL2 in a β-strand conformation. Interestingly, the interaction is partially mediated by H-bridges of several buried structural waters represented as red spheres in D and E. Comparing F and G shows that the backbone of Val<sub>-5</sub> forms one additional hydrogen bond, while E and G illustrate that its side chain interacts with DYNLL2 His68. Details of this interaction are highlighted by orange areas.</p>", "links"=>[], "tags"=>["ac-srgtqte", "dynll2", "leu-zipper", "dimerized", "vsrgtqte"], "article_id"=>453795, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Péter Rapali", "László Radnai", "Dániel Süveges", "Veronika Harmat", "Ferenc Tölgyesi", "Weixiao Y. Wahlgren", "Gergely Katona", "László Nyitray", "Gábor Pál"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0018818.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Crystal_structure_of_Ac_SRGTQTE_8211_DYNLL2_A_C_D_and_F_and_Leu_zipper_dimerized_VSRGTQTE_8211_DYNLL2_complex_B_C_E_and_G_/453795", "title"=>"Crystal structure of Ac-SRGTQTE – DYNLL2 (A, C, D and F) and Leu-zipper dimerized VSRGTQTE – DYNLL2 complex (B, C, E and G).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-18 01:03:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/783559"], "description"=>"<p>Step A: all non intracellular segments were excluded from the search. Step B: sequences were split into overlapping eight residue segments; only disordered segments with Gln at position 0 were scored. Step C: a score was assigned (see Methods). Motifs with scores above threshold are considered potential DYNLL binders. Step D: based on amino acid composition, motifs were sorted into three classes with different binding probabilities.</p>", "links"=>[], "tags"=>["binding"], "article_id"=>453923, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Péter Rapali", "László Radnai", "Dániel Süveges", "Veronika Harmat", "Ferenc Tölgyesi", "Weixiao Y. Wahlgren", "Gergely Katona", "László Nyitray", "Gábor Pál"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0018818.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Flowchart_of_the_binding_partner_prediction_/453923", "title"=>"Flowchart of the binding partner prediction.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-18 01:05:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/783675"], "description"=>"<p>(A) Density distributions of scores. Dashed baseline is derived from average values from 1000 randomized score sets (see Methods) while continuous line represents the <i>in vitro</i> selected scores. In the high score region (inset), the phage-selected set yields higher frequencies than the randomized baseline set. (Error bars show standard deviation of frequencies in the randomized sets). (B) The ratio of the density distribution functions of the scores. Above a threshold score value of 220 predicted DYNLL-binding motif frequencies exceed stochastic frequencies obtained from the randomized set, therefore their ratio exceeds one.</p>", "links"=>[], "tags"=>["biophysics", "Biochemistry"], "article_id"=>454043, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Péter Rapali", "László Radnai", "Dániel Süveges", "Veronika Harmat", "Ferenc Tölgyesi", "Weixiao Y. Wahlgren", "Gergely Katona", "László Nyitray", "Gábor Pál"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0018818.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Statistical_analysis_for_threshold_score_determination_/454043", "title"=>"Statistical analysis for threshold score determination.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-18 01:07:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/783812"], "description"=>"<p>Data were collected from the functional and Gene Ontology annotations of UniProt entry for each protein.</p>", "links"=>[], "tags"=>["41", "110", "binding", "partners"], "article_id"=>454177, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Péter Rapali", "László Radnai", "Dániel Süveges", "Veronika Harmat", "Ferenc Tölgyesi", "Weixiao Y. Wahlgren", "Gergely Katona", "László Nyitray", "Gábor Pál"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0018818.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Functional_distribution_of_41_known_A_and_110_predicted_B_binding_partners_of_DYNLL_/454177", "title"=>"Functional distribution of 41 known (A) and 110 predicted (B) binding partners of DYNLL.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-18 01:09:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/783900"], "description"=>"<p>*Data reach the dynamic range limit of the ITC method.</p>", "links"=>[], "tags"=>["dynll-binding"], "article_id"=>454261, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Péter Rapali", "László Radnai", "Dániel Süveges", "Veronika Harmat", "Ferenc Tölgyesi", "Weixiao Y. Wahlgren", "Gergely Katona", "László Nyitray", "Gábor Pál"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0018818.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Thermodynamic_analysis_of_DYNLL_binding_interactions_/454261", "title"=>"Thermodynamic analysis of DYNLL-binding interactions.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-04-18 01:11:01"}

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Relative Metric

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