Molecular Dynamics Studies of the Nucleoprotein of Influenza A Virus: Role of the Protein Flexibility in RNA Binding
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Mendeley | Further Information

{"title"=>"Molecular Dynamics Studies of the Nucleoprotein of Influenza A Virus: Role of the Protein Flexibility in RNA Binding", "type"=>"journal", "authors"=>[{"first_name"=>"Bogdan", "last_name"=>"Tarus"}, {"first_name"=>"Christophe", "last_name"=>"Chevalier"}, {"first_name"=>"Charles-Adrien", "last_name"=>"Richard"}, {"first_name"=>"Bernard", "last_name"=>"Delmas"}, {"first_name"=>"Carmelo", "last_name"=>"Di Primo"}, {"first_name"=>"Anny", "last_name"=>"Slama-Schwok"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"1932-6203", "pmid"=>"22272272", "doi"=>"10.1371/journal.pone.0030038"}, "id"=>"6d2ff5c4-acdc-3020-9117-cc746a0f0d39", "abstract"=>"The influenza viruses contain a segmented, negative stranded RNA genome. Each RNA segment is covered by multiple copies of the nucleoprotein (NP). X-ray structures have shown that NP contains well-structured domains juxtaposed with regions of missing electron densities corresponding to loops. In this study, we tested if these flexible loops gated or promoted RNA binding and RNA-induced oligomerization of NP. We first performed molecular dynamics simulations of wt NP monomer and trimer in comparison with the R361A protein mutated in the RNA binding groove, using the H1N1 NP as the initial structure. Calculation of the root-mean-square fluctuations highlighted the presence of two flexible loops in NP trimer: loop 1 (73-90), loop 2 (200-214). In NP, loops 1 and 2 formed a 10-15 Å-wide pinch giving access to the RNA binding groove. Loop 1 was stabilized by interactions with K113 of the adjacent β-sheet 1 (91-112) that interacted with the RNA grove (linker 360-373) via multiple hydrophobic contacts. In R361A, a salt bridge formed between E80 of loop 1 and R208 of loop 2 driven by hydrophobic contacts between L79 and W207, due to a decreased flexibility of loop 2 and loop 1 unfolding. Thus, RNA could not access its binding groove in R361A; accordingly, R361A had a much lower affinity for RNA than NP. Disruption of the E80-R208 interaction in the triple mutant R361A-E80A-E81A increased its RNA binding affinity and restored its oligomerization back to wt levels in contrast with impaired levels of R361A. Our data suggest that the flexibility of loops 1 and 2 is required for RNA sampling and binding which likely involve conformational change(s) of the nucleoprotein.", "link"=>"http://www.mendeley.com/research/molecular-dynamics-studies-nucleoprotein-influenza-virus-role-protein-flexibility-rna-binding-2", "reader_count"=>23, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Student > Doctoral Student"=>2, "Researcher"=>4, "Student > Ph. D. Student"=>9, "Student > Master"=>4, "Student > Bachelor"=>2, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Student > Doctoral Student"=>2, "Researcher"=>4, "Student > Ph. D. Student"=>9, "Student > Master"=>4, "Student > Bachelor"=>2, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>11, "Medicine and Dentistry"=>2, "Physics and Astronomy"=>2, "Chemistry"=>3, "Unspecified"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>3}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>11}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Belgium"=>1, "Spain"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/691127"], "description"=>"<p>It characterized the differences in loops interactions between wt NP and R361A.</p>", "links"=>[], "tags"=>["loops", "np", "r361a"], "article_id"=>361600, "categories"=>["Virology", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Biological Sciences", "Chemistry"], "users"=>["Bogdan Tarus", "Christophe Chevalier", "Charles-Adrien Richard", "Bernard Delmas", "Carmelo Di Primo", "Anny Slama-Schwok"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030038.g003", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_the_minimal_distance_between_loops_1_and_2_in_NP_and_the_R361A_mutant_/361600", "title"=>"Distribution of the minimal distance between loops 1 and 2 in NP and the R361A mutant.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 09:47:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/691376"], "description"=>"<p><b>A:</b> Comparison of the association to and dissociation from RNA of R361A-R204A-R208A (full triangles) and wt-R204A-R208A (open triangles); <b>B:</b> Comparison of the oligomerization kinetics of 10 µM proteins after addition of RNA (3 µM): wt NP (full squares), R361A (open squares), wt-R204A-R208A (open circles) and R361A-R204A-R208A (full triangles) (10 µM). The lines represent single exponential fits.</p>", "links"=>[], "tags"=>["mutations", "np", "rna", "binding", "rna-induced"], "article_id"=>361837, "categories"=>["Virology", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Biological Sciences", "Chemistry"], "users"=>["Bogdan Tarus", "Christophe Chevalier", "Charles-Adrien Richard", "Bernard Delmas", "Carmelo Di Primo", "Anny Slama-Schwok"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030038.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Influence_of_mutations_in_loop_2_of_NP_on_RNA_binding_and_RNA_induced_oligomerization_/361837", "title"=>"Influence of mutations in loop 2 of NP on RNA binding and RNA-induced oligomerization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 09:49:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/691072"], "description"=>"<p>The position of the mutated residue R361 is highlighted in CPK representation; the salt bridge between residues E80 and R208 and hydrophobic interactions between L79 and W207 stabilized the relative positions of the two loops at shorter distance in R361A than in NP (insert).</p>", "links"=>[], "tags"=>["structures", "np", "r361a", "mutant"], "article_id"=>361544, "categories"=>["Virology", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Biological Sciences", "Chemistry"], "users"=>["Bogdan Tarus", "Christophe Chevalier", "Charles-Adrien Richard", "Bernard Delmas", "Carmelo Di Primo", "Anny Slama-Schwok"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030038.g002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_representative_structures_of_NP_red_and_the_R361A_mutant_green_proteins_/361544", "title"=>"Comparison of representative structures of NP (red) and the R361A mutant (green) proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 09:47:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/691432"], "description"=>"<p>Loop 1 (residues 73–90), loop2 (residues 200–211), β-sheet 1 (residues 91–112), and the linker (residues 360–373).</p><p>These interactions define a path between loop 1 and the residue R361 of the linker, located in the RNA binding groove (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0030038#pone-0030038-g002\" target=\"_blank\">Figures 2</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0030038#pone-0030038-g004\" target=\"_blank\">4</a>).</p>1<p>HB stands for hydrogen bond.</p>2<p>HPh stands for hydrophobic interaction.</p><p>See the Experimental section for definitions of the contact domains and the two contact types.</p>a)<p><u>Loop 1-loop 2 contact</u>: In R361A, hydrophobic interactions between L79 and loop 2 drove loop 1 to contact loop2; transient salt-bridges between R204 or R208, on the one hand, and E80 or E81, on the other hand, stabilized the interaction between loop 1 and loop 2 at short distances. Such loop-loop interactions were not found in wt NP.</p>b)<p><u>Loop 1 stability (base</u>): The side-chain of K113 was engaged in a strong hydrogen bond with the C-terminus of the loop 1; the guanidinium moiety of K113 formed a salt bridge with E73 at the N-terminus of loop 1, contributing to the stability of loop 1 in wt NP. The R361A mutation drastically reduced the interactions of the K113 with the loop 1, increasing loop 1 flexibility.</p>c)<p><u>Linker-β sheet 1 contacts</u>: The linker was connected to the β sheet 1 through conserved hydrophobic interaction between M371 and the ring of Y97, stable hydrogen bonds between R106 and the linker backbone oxygen atoms. The R361A mutation decreased the population of the solvated K103-E372 salt-bridge.</p>d)<p><u>Inter-linker contacts</u>: In NP, E369 interacted with both R361 and R317. In R361A, the R317-E369 contact population increased to 93% as compared to 73% in wt NP and the R361-E369 interaction was canceled by the mutation.</p>", "links"=>[], "tags"=>["interactions", "observed", "domains", "wt", "np", "r361a"], "article_id"=>361890, "categories"=>["Virology", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Biological Sciences", "Chemistry"], "users"=>["Bogdan Tarus", "Christophe Chevalier", "Charles-Adrien Richard", "Bernard Delmas", "Carmelo Di Primo", "Anny Slama-Schwok"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030038.t001", "stats"=>{"downloads"=>4, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_the_interactions_observed_in_four_domains_of_the_wt_NP_and_R361A_mutant_/361890", "title"=>"Analysis of the interactions observed in four domains of the wt NP and R361A mutant.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 09:49:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/690980"], "description"=>"<p><b>A:</b> Comparison the flexibility of loops 1 and 2 in the trimer (black) and monomer (red) forms of NP quantified by their backbone root-mean-square fluctuations during 4 ns and 50 ns simulation time, respectively. Loop 1 (73–90) and loop 2 (200–214) remained flexible in both NP forms; in contrast, a large difference is seen in the oligomerization loop 3 (402–428) of NP monomer and trimer. <b>B:</b> Root-mean-square fluctuations of the NP (red) and R361A (green) monomers during the simulated trajectories: one can see a reduced flexibility in loop 2 and a small increase of the flexibility of loop 1 of the R361A mutant.</p>", "links"=>[], "tags"=>["np", "r361a", "proteins", "molecular"], "article_id"=>361451, "categories"=>["Virology", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Biological Sciences", "Chemistry"], "users"=>["Bogdan Tarus", "Christophe Chevalier", "Charles-Adrien Richard", "Bernard Delmas", "Carmelo Di Primo", "Anny Slama-Schwok"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030038.g001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_the_NP_and_R361A_proteins_by_molecular_modelling_/361451", "title"=>"Comparison of the NP and R361A proteins by molecular modelling.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 09:46:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/691188"], "description"=>"<p>K113 located at the edge of β-sheet 1 strongly interacts with loop 1, in particular E73. The other extremity of the β-sheet had multiple contacts with residues of the RNA grove, in particular hydrophobic interactions between Y97 and M371, interactions between R106 and the linker backbone (residues 360–373 shown in magenta) and electrostatic interactions between K103 and E372. The linker itself was stabilized by salt bridges between E369 and R361 and E369 and R317 (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0030038#pone-0030038-t001\" target=\"_blank\">Table 1</a>).</p>", "links"=>[], "tags"=>["rna"], "article_id"=>361657, "categories"=>["Virology", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Biological Sciences", "Chemistry"], "users"=>["Bogdan Tarus", "Christophe Chevalier", "Charles-Adrien Richard", "Bernard Delmas", "Carmelo Di Primo", "Anny Slama-Schwok"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030038.g004", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proposed_communication_path_between_loop_1_and_the_RNA_groove_/361657", "title"=>"Proposed communication path between loop 1 and the RNA groove.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 09:48:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/691311"], "description"=>"<p><b>A</b> - Size distribution of monomeric wt NP (5 µM) alone (black, 6.8 nm, 93%, 5.0 µ, 7%) and 1 hour (dotted blue, 13.8 nm 91%, 760 nm 9%) or 3 hours after addition of 1.8 µM RNA (16.3 nm, 100%); <b>B</b>- Size distribution of monomeric R361A (5 µM) alone (black, 7.8 nm, 100%) and 4 hours after addition of 1.8 µM RNA (dashed green, 9.85 nm, 75%, 279 nm, 25%) <b>C</b>: Comparison of the oligomerization kinetics of R361A (violet squares) and R361A-E80A-E81A (green stars) (10 µM) after addition of RNA (3 µM). Note the large difference in the final size of the protein-RNA oligomers being 10±1 nm and 16±1 nm for R361A and R361A-E80A-E81A, the latter resembling the size of oligomeric NP-RNA complexes.</p>", "links"=>[], "tags"=>["np", "oligomers", "rna", "monitored"], "article_id"=>361778, "categories"=>["Virology", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Biological Sciences", "Chemistry"], "users"=>["Bogdan Tarus", "Christophe Chevalier", "Charles-Adrien Richard", "Bernard Delmas", "Carmelo Di Primo", "Anny Slama-Schwok"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030038.g006", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Size_of_NP_oligomers_in_the_presence_of_RNA_monitored_by_Dynamic_Light_Scattering_/361778", "title"=>"Size of NP oligomers in the presence of RNA monitored by Dynamic Light Scattering.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 09:48:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/691256"], "description"=>"<p><b>A:</b> Effect of the mutations R361A (green circles) and R361A-E80A-E81A (blue squares) compared to wt NP (black triangles) binding to RNA; Inset: comparison of the SPR signals obtained in the presence of Flu1-RNA with 300 nM C-terminal His-tagged NP, R361A or R361A-E80A-E81A. Due to its low affinity for RNA, the signal of the R361A-RNA complex (green) is ca four times smaller than NP-RNA (black), while the signal of the triple mutant (blue) is intermediate between them. The binding of NP or mutants to the surface-bound Flu1-RNA oligonucleotide followed a saturation curve with maximal RU at large protein concentration; the signal deduced from the plateau of the association kinetics as a function of NP concentration was used to obtain the Kd, taken as the concentration at which the RU is 50% of the maximal RU. <b>B:</b> Binding to Flu1-RNA of the double and triple mutants, wt-E80A-E81A (blue squares), R361A-E80A-E81A (red circles) respectively.</p>", "links"=>[], "tags"=>["mutations", "np", "rna"], "article_id"=>361727, "categories"=>["Virology", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Biological Sciences", "Chemistry"], "users"=>["Bogdan Tarus", "Christophe Chevalier", "Charles-Adrien Richard", "Bernard Delmas", "Carmelo Di Primo", "Anny Slama-Schwok"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030038.g005", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Influence_of_mutations_in_loop_1_of_NP_on_RNA_binding_/361727", "title"=>"Influence of mutations in loop 1 of NP on RNA binding.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 09:48:25"}

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Relative Metric

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