Anchored Design of Protein-Protein Interfaces
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Mendeley | Further Information

{"title"=>"Anchored design of protein-protein interfaces", "type"=>"journal", "authors"=>[{"first_name"=>"Steven M.", "last_name"=>"Lewis", "scopus_author_id"=>"56965750300"}, {"first_name"=>"Brian A.", "last_name"=>"Kuhlman", "scopus_author_id"=>"6701347944"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-79959188043", "sgr"=>"79959188043", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "pmid"=>"21698112", "doi"=>"10.1371/journal.pone.0020872", "pui"=>"361966484"}, "id"=>"057d748c-b847-3307-a29b-1e1c6280ae1b", "abstract"=>"BACKGROUND: Few existing protein-protein interface design methods allow for extensive backbone rearrangements during the design process. There is also a dichotomy between redesign methods, which take advantage of the native interface, and de novo methods, which produce novel binders.\\n\\nMETHODOLOGY: Here, we propose a new method for designing novel protein reagents that combines advantages of redesign and de novo methods and allows for extensive backbone motion. This method requires a bound structure of a target and one of its natural binding partners. A key interaction in this interface, the anchor, is computationally grafted out of the partner and into a surface loop on the design scaffold. The design scaffold's surface is then redesigned with backbone flexibility to create a new binding partner for the target. Careful choice of a scaffold will bring experimentally desirable characteristics into the new complex. The use of an anchor both expedites the design process and ensures that binding proceeds against a known location on the target. The use of surface loops on the scaffold allows for flexible-backbone redesign to properly search conformational space.\\n\\nCONCLUSIONS AND SIGNIFICANCE: This protocol was implemented within the Rosetta3 software suite. To demonstrate and evaluate this protocol, we have developed a benchmarking set of structures from the PDB with loop-mediated interfaces. This protocol can recover the correct loop-mediated interface in 15 out of 16 tested structures, using only a single residue as an anchor.", "link"=>"http://www.mendeley.com/research/anchored-design-proteinprotein-interfaces", "reader_count"=>76, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>9, "Researcher"=>26, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>26, "Student > Postgraduate"=>1, "Student > Master"=>5, "Other"=>2, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>9, "Researcher"=>26, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>26, "Student > Postgraduate"=>1, "Student > Master"=>5, "Other"=>2, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>3, "Biochemistry, Genetics and Molecular Biology"=>16, "Materials Science"=>1, "Agricultural and Biological Sciences"=>43, "Medicine and Dentistry"=>1, "Physics and Astronomy"=>1, "Chemistry"=>9, "Psychology"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>9}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>43}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>16}}, "reader_count_by_country"=>{"Canada"=>2, "Korea (South)"=>1, "United States"=>1, "China"=>3, "Serbia and Montenegro"=>1, "Brazil"=>1, "United Kingdom"=>1, "Chile"=>1, "Germany"=>3}, "group_count"=>3}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/765085"], "description"=>"<p>This table collects structural parameters for the complexes used in this work, along with chosen parameters like anchor placement. The PDB column identifies the structure. The chains column identifies which complex within the PDB file was used (several have many complexes in the asymmetric unit). *: 2obg was not crystallized as a heterodimer; it was expressed as a fusion protein and crystallized as an infinitely domain-swapped polymer.<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020872#pone.0020872-Koide3\" target=\"_blank\">[24]</a> The resolution column contains the reported crystal structure resolution; all are reasonable. The dimer type column identifies the type of dimer. **: 1dle represents a crystal dimer rather than a biological one, making it a good test of weak interactions. The SASA column notes the area buried by the interface. The anchor and chain columns together identify the residue used as an anchor. The loop column identifies which residues (on the same chain as the anchor) were flexible. The loop length column collects the lengths of these loops. ***: 1dle has residues with insertion codes in the loops, leading to a longer loop than is obvious. The name column identifies the name and function of the protein as listed in the PDB.</p>", "links"=>[], "tags"=>["structures", "accessory"], "article_id"=>435456, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020872.t002", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Input_structures_and_accessory_data_/435456", "title"=>"Input structures and accessory data.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-06-17 01:30:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/764024"], "description"=>"<p>Panel A demonstrates the AnchoredDesign process with a simple cartoon. At left, we start with a known interaction between a target (cyan) and a natural partner (orange) with a characteristic interaction (the anchor, yellow). In the middle, we graft the anchor into the scaffold (magenta) to create a rough starting structure. At right, we fill out the scaffold-target interface with the AnchoredDesign protocol. Panel B demonstrates the process using protein structures for greater clarity (using the same color scheme).</p>", "links"=>[], "tags"=>["chemistry", "Computational biology", "biophysics", "Biochemistry"], "article_id"=>434398, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020872.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Anchor_insertion_/434398", "title"=>"Anchor insertion.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-17 01:13:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/764886"], "description"=>"<p>This figure shows the insufficiency of AnchoredDesign's loop predictions for 1qni and 2hp2. In gray is the nonmoving side of the interface and in black is the correct structure. Each of the ten colors represents the loops of one of the top ten predictions by lowest energy. The predictions' protein cores are green. Notice that the loops themselves do not converge, but that the rigid-body placement and interface as a whole is correct (the green and black portions are overlaid towards the top of each panel).</p>", "links"=>[], "tags"=>["1qni", "2hp2"], "article_id"=>435259, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020872.g007", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Poorly_predicted_1qni_and_2hp2_loops_/435259", "title"=>"Poorly predicted 1qni and 2hp2 loops.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-17 01:27:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/764512"], "description"=>"<p>This figure demonstrates the relaxed crystal structure input and AnchoredDesign's lowest-score prediction for 8 of the 16 structures. The first and third rows show whole structures, and the second and fourth zoom in on the predicted loops. The nonmoving side of the interface is in green, the actual partner in cyan and the prediction in yellow. The predicted loop is red and the anchor is white. Structures are labeled with their PDB code in the lower right of each cell. For most structures, the predicted rigid-body placement and loop is indistinguishable from the relaxed crystal structure; 3cgc (lower left) is the exception. The other 8 structures are shown similarly in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020872#pone.0020872.s002\" target=\"_blank\">Figure S2</a>.</p>", "links"=>[], "tags"=>["scoring"], "article_id"=>434889, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020872.g005", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Best_scoring_prediction_for_8_complexes_/434889", "title"=>"Best scoring prediction for 8 complexes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-17 01:21:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/765144"], "description"=>"<p>This table demonstrates the rough equality of results from KIC, CCD, and combined loop sampling. The default protocol columns are the same as in Table RMSD; the CCD and KIC columns were generated using either loop modeling type alone. Each column represents one of the RMSD metrics described in the Results. Each of the loop modeling choices is broadly equivalent. Notice that structure 3cgc has in lower RMSDs under the combined protocol than either loop sampling type alone; this is a falsely optimistic interpretation because AnchoredDesign is never correctly predicting 3cgc under any of these protocols. The structures produced for 3cgc are isoenergetic and it is coincidental that the combined protocol happens to have lower RMSDs.</p>", "links"=>[], "tags"=>["closure"], "article_id"=>435526, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020872.t004", "stats"=>{"downloads"=>4, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_loop_closure_methods_/435526", "title"=>"Comparison of loop closure methods.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-06-17 01:32:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/764367"], "description"=>"<p>This figure, modeled after the fold tree diagrams in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020872#pone-0020872-g001\" target=\"_blank\">Figure 1</a> of Wang et al. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020872#pone.0020872-Wang1\" target=\"_blank\">[26]</a>, demonstrates the kinematic connectivity that makes AnchoredDesign work. The arrows trace the direction of folding as Rosetta recalculates 3D coordinates from internal coordinates, starting at the green root residue. The upper and lower sections represent the target and scaffold respectively. Shaded regions represent rigid torsions (including the entire target and the core of the scaffold, in this case). Unshaded regions represent mobile torsions: the loops. All jumps between noncontiguous residues (dotted lines) are held rigid. AnchoredDesign embeds rigid torsions (the anchor, red) inside a loop, and affixes the anchor to the target by having the anchor's coordinates depend on the target instead of the scaffold in which the anchor is embedded. The scaffold is then dependent on the anchor via the mobile loop containing the anchor. Also allowed are arbitrarily placed other loops, handled with the standard loop fold tree.</p>", "links"=>[], "tags"=>["chemistry", "Computational biology", "biophysics", "Biochemistry"], "article_id"=>434740, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020872.g004", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fold_tree_diagram_/434740", "title"=>"Fold tree diagram.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-17 01:19:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/384379", "https://ndownloader.figshare.com/files/384416", "https://ndownloader.figshare.com/files/384476", "https://ndownloader.figshare.com/files/384548", "https://ndownloader.figshare.com/files/384640", "https://ndownloader.figshare.com/files/384699", "https://ndownloader.figshare.com/files/384754"], "description"=>"<div><h3>Background</h3><p>Few existing protein-protein interface design methods allow for extensive backbone rearrangements during the design process. There is also a dichotomy between redesign methods, which take advantage of the native interface, and <em>de novo</em> methods, which produce novel binders.</p> <h3>Methodology</h3><p>Here, we propose a new method for designing novel protein reagents that combines advantages of redesign and <em>de novo</em> methods and allows for extensive backbone motion. This method requires a bound structure of a target and one of its natural binding partners. A key interaction in this interface, the anchor, is computationally grafted out of the partner and into a surface loop on the design scaffold. The design scaffold's surface is then redesigned with backbone flexibility to create a new binding partner for the target. Careful choice of a scaffold will bring experimentally desirable characteristics into the new complex. The use of an anchor both expedites the design process and ensures that binding proceeds against a known location on the target. The use of surface loops on the scaffold allows for flexible-backbone redesign to properly search conformational space.</p> <h3>Conclusions and Significance</h3><p>This protocol was implemented within the Rosetta3 software suite. To demonstrate and evaluate this protocol, we have developed a benchmarking set of structures from the PDB with loop-mediated interfaces. This protocol can recover the correct loop-mediated interface in 15 out of 16 tested structures, using only a single residue as an anchor.</p> </div>", "links"=>[], "tags"=>["anchored", "protein-protein", "interfaces"], "article_id"=>135906, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0020872.s001", "https://dx.doi.org/10.1371/journal.pone.0020872.s002", "https://dx.doi.org/10.1371/journal.pone.0020872.s003", "https://dx.doi.org/10.1371/journal.pone.0020872.s004", "https://dx.doi.org/10.1371/journal.pone.0020872.s005", "https://dx.doi.org/10.1371/journal.pone.0020872.s006", "https://dx.doi.org/10.1371/journal.pone.0020872.s007"], "stats"=>{"downloads"=>20, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Anchored_Design_of_Protein_Protein_Interfaces/135906", "title"=>"Anchored Design of Protein-Protein Interfaces", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-06-17 01:38:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/764664"], "description"=>"<p>This figure shows score versus IRMSD plots for each of the 16 structures. RMSD was calculated between the relaxed crystal structure (input) and AnchoredDesign's output. Plots are labeled with their PDB ID in the lower right of each cell. Black points are predictions, red points are relaxed native trajectories, and blue points are conservative relaxed native trajectories which skipped the centroid phase (see main text). Blue points may lie under red points, and red points may lie under black points. Some high-score points are out of view on all plots; all low-score points are present. On the RMSD (X) axis, the first, second, and third tic marks represent 1, 2.5, and 5 Ångstroms. Some plots are zoomed in beyond 5 or 2.5 Ångstroms and fewer tics appear.</p>", "links"=>[], "tags"=>["chemistry", "Computational biology", "biophysics", "Biochemistry"], "article_id"=>435037, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020872.g006", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IRMSD_versus_score_plots_/435037", "title"=>"IRMSD versus score plots.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-17 01:23:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/765055"], "description"=>"<p>This table summarizes predictions of the AnchoredDesign benchmark. Each value represents the RMSD of the lowest-scoring model produced by AnchoredDesign for that structure using its standard protocol. The PDB column identifies the structure. The loop RMSD, IRMSD, and LRMSD columns describe the RMSD of the lowest-scoring prediction against the relaxed input structure. The input columns compare AnchoredDesign's output to the scorefunction-minimized crystal structures used as input. The crystal columns compare the same output to the unrelaxed crystal structures. The low values throughout indicate that AnchoredDesign does a good job recovering native interfaces starting from extended loops. The similarity of the input and crystal columns indicates that the relaxed starting structures are not far from the crystal structures.</p>", "links"=>[], "tags"=>["lowest-scoring"], "article_id"=>435435, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020872.t003", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RMSD_of_lowest_scoring_models_/435435", "title"=>"RMSD of lowest-scoring models.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-06-17 01:30:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/764156"], "description"=>"<p>These complexes demonstrate how the AnchoredDesign protocol samples the rigid-body degree of freedom via loop sampling. These complexes are colored as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020872#pone-0020872-g001\" target=\"_blank\">Figure 1</a>: cyan for the target, yellow for the anchor, and magenta for the scaffold. The flexible residues of the loop containing the anchor are colored red. The two complexes are related only by the alteration of the backbone torsion angles of the red positions; the overall viewpoint has not been rotated (notice the targets are identical). Remodeling of this loop (and no other changes) produces a large rigid-body like change between the two partners, while leaving the anchor/target interface and both protein cores intact. This allows sampling of the target/scaffold interface without losing the anchor information.</p>", "links"=>[], "tags"=>["rigid-body", "degrees"], "article_id"=>434538, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020872.g002", "stats"=>{"downloads"=>3, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_AnchoredDesign_treatment_of_rigid_body_and_loop_degrees_of_freedom_/434538", "title"=>"AnchoredDesign treatment of rigid-body and loop degrees of freedom.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-17 01:15:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/764251"], "description"=>"<p>This flowchart summarizes the AnchoredDesign protocol and process. In the top part, preliminary steps are marked in green. These steps are primarily manual but can be assisted with AnchorFinder and AnchoredPDBCreator. Initial steps vary depending on whether the benchmarking case for this paper, or the more general design case, is being addressed. The steps of the AnchoredDesign protocol are shown in blue and pink. The perturbation steps, performed in centroid mode, are in blue. The refinement steps, performed with a fully atomic representation, are in pink. In both portions of the protocol, many Monte Carlo cycles are performed; the results here used 500 perturb and 1000 refine cycles, but optimal cycle counts are best determined on a per-experiment basis.</p>", "links"=>[], "tags"=>["chemistry", "Computational biology", "biophysics", "Biochemistry"], "article_id"=>434625, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020872.g003", "stats"=>{"downloads"=>3, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Protocol_flowchart_/434625", "title"=>"Protocol flowchart.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-17 01:17:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/765110"], "description"=>"<p>This table annotates the regions of the scorefile produced by AnchoredDesign. The first column lists metrics useful for analyzing benchmark or designed structures, and the second lists the meanings of those metrics. Of particular interest are total_score, loop_CA_sup_RMSD (loop RMSD), I_sup_bb_RMSD (IRMSD), and ch2_CA_RMSD (LRMSD), which provide the metrics used for the other plots and tables in this paper. Scorefile columns not listed here are either scorefunction terms <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020872#pone.0020872-Rohl1\" target=\"_blank\">[31]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020872#pone.0020872-Kuhlman1\" target=\"_blank\">[36]</a> or InterfaceAnalyzerMover metrics not useful for AnchoredDesign.</p>", "links"=>[], "tags"=>["scorefile"], "article_id"=>435487, "categories"=>["Biological Sciences", "Biochemistry", "Chemistry", "Biophysics"], "users"=>["Steven M. Lewis", "Brian A. Kuhlman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020872.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Annotated_scorefile_headers_/435487", "title"=>"Annotated scorefile headers.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-06-17 01:31:27"}

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  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"11"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2021", "month"=>"1"}

Relative Metric

{"start_date"=>"2011-01-01T00:00:00Z", "end_date"=>"2011-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Molecular biology", "average_usage"=>[295, 553, 688, 802, 914, 1017, 1108, 1194, 1278, 1351, 1419, 1500, 1570, 1633, 1712, 1774, 1839, 1903, 1970, 2033, 2101, 2162, 2228, 2291, 2352, 2418, 2486, 2547, 2610, 2680, 2737, 2799, 2859, 2919, 2974, 3029, 3082]}, {"subject_area"=>"/Computer and information sciences/Software engineering", "average_usage"=>[286, 559, 684, 828, 913, 981, 1076, 1159, 1229, 1285, 1346, 1394, 1458, 1529, 1580, 1644, 1699, 1779, 1845, 1898, 1973, 2055, 2108, 2155, 2220, 2280, 2347, 2403, 2459, 2509, 2622, 2709, 2818, 2951, 3071, 3168, 3242]}, {"subject_area"=>"/Engineering and technology", "average_usage"=>[312, 536, 658, 770, 877, 959, 1047, 1128, 1203, 1267, 1324, 1404, 1481, 1548, 1609, 1671, 1739, 1802, 1854, 1915, 1974, 2027, 2101, 2161, 2218, 2280, 2340, 2406, 2457, 2507, 2565, 2631, 2682, 2749, 2796, 2844, 2892]}, {"subject_area"=>"/Physical sciences", "average_usage"=>[303, 547, 667, 770, 875, 974, 1062, 1140, 1210, 1276, 1344, 1408, 1473, 1534, 1602, 1665, 1732, 1800, 1863, 1920, 1984, 2048, 2099, 2161, 2222, 2285, 2341, 2404, 2473, 2528, 2595, 2650, 2713, 2772, 2835, 2886, 2938]}, {"subject_area"=>"/Physical sciences/Chemistry", "average_usage"=>[272, 506, 626, 733, 837, 944, 1031, 1116, 1192, 1253, 1324, 1388, 1459, 1528, 1593, 1653, 1718, 1787, 1854, 1916, 1974, 2045, 2111, 2167, 2232, 2297, 2355, 2425, 2489, 2549, 2615, 2675, 2734, 2793, 2851, 2904, 2961]}]}
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