MHC Class I Bound to an Immunodominant Theileria parva Epitope Demonstrates Unconventional Presentation to T Cell Receptors
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{"title"=>"MHC class I bound to an immunodominant Theileria parva epitope demonstrates unconventional presentation to T cell receptors", "type"=>"journal", "authors"=>[{"first_name"=>"Isabel K.", "last_name"=>"MacDonald", "scopus_author_id"=>"14060647000"}, {"first_name"=>"Maria", "last_name"=>"Harkiolaki", "scopus_author_id"=>"6506874194"}, {"first_name"=>"Lawrence", "last_name"=>"Hunt", "scopus_author_id"=>"7202131454"}, {"first_name"=>"Timothy", "last_name"=>"Connelley", "scopus_author_id"=>"23977446000"}, {"first_name"=>"A. Victoria", "last_name"=>"Carroll", "scopus_author_id"=>"36796653200"}, {"first_name"=>"Niall D.", "last_name"=>"MacHugh", "scopus_author_id"=>"7003629243"}, {"first_name"=>"Simon P.", "last_name"=>"Graham", "scopus_author_id"=>"55596678000"}, {"first_name"=>"E. Yvonne", "last_name"=>"Jones", "scopus_author_id"=>"7404236867"}, {"first_name"=>"W. Ivan", "last_name"=>"Morrison", "scopus_author_id"=>"7202131346"}, {"first_name"=>"Darren R.", "last_name"=>"Flower", "scopus_author_id"=>"35479658200"}, {"first_name"=>"Shirley A.", "last_name"=>"Ellis", "scopus_author_id"=>"7402788031"}], "year"=>2010, "source"=>"PLoS Pathogens", "identifiers"=>{"pmid"=>"20976198", "sgr"=>"78449239015", "doi"=>"10.1371/journal.ppat.1001149", "scopus"=>"2-s2.0-78449239015", "pui"=>"359979617", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "issn"=>"15537366"}, "id"=>"f4fdd7cc-b6a8-391b-95af-dee45f1dc927", "abstract"=>"T cell receptor (TCR) recognition of peptide-MHC class I (pMHC) complexes is a crucial event in the adaptive immune response to pathogens. Peptide epitopes often display a strong dominance hierarchy, resulting in focusing of the response on a limited number of the most dominant epitopes. Such T cell responses may be additionally restricted by particular MHC alleles in preference to others. We have studied this poorly understood phenomenon using Theileria parva, a protozoan parasite that causes an often fatal lymphoproliferative disease in cattle. Despite its antigenic complexity, CD8+ T cell responses induced by infection with the parasite show profound immunodominance, as exemplified by the Tp1(214-224) epitope presented by the common and functionally important MHC class I allele N*01301. We present a high-resolution crystal structure of this pMHC complex, demonstrating that the peptide is presented in a distinctive raised conformation. Functional studies using CD8+ T cell clones show that this impacts significantly on TCR recognition. The unconventional structure is generated by a hydrophobic ridge within the MHC peptide binding groove, found in a set of cattle MHC alleles. Extremely rare in all other species, this feature is seen in a small group of mouse MHC class I molecules. The data generated in this analysis contribute to our understanding of the structural basis for T cell-dependent immune responses, providing insight into what determines a highly immunogenic p-MHC complex, and hence can be of value in prediction of antigenic epitopes and vaccine design.", "link"=>"http://www.mendeley.com/research/mhc-class-i-bound-immunodominant-theileria-parva-epitope-demonstrates-unconventional-presentation-t", "reader_count"=>23, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>1, "Researcher"=>6, "Student > Ph. D. Student"=>6, "Student > Master"=>2, "Other"=>2, "Lecturer > Senior Lecturer"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>1, "Researcher"=>6, "Student > Ph. D. Student"=>6, "Student > Master"=>2, "Other"=>2, "Lecturer > Senior Lecturer"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>13, "Business, Management and Accounting"=>1, "Chemistry"=>1, "Psychology"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>1}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>13}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"France"=>1}, "group_count"=>1}

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  • {"files"=>["https://ndownloader.figshare.com/files/824424"], "description"=>"<p>T cell recognition was examined using a 4-hour <sup>111</sup>Indium release cytotoxicity assay employing target cells incubated with 1 ug/ml of peptide. The maximum level of cytotoxicity obtained with the native Tp1<sub>214–224</sub> peptide is shown for each clone. Killing of unpulsed target cells was <2% for all clones. The degree of reduction in killing obtained with each of the single Ala substituted peptides (A1–A11) compared to that obtained with the native Tp1<sub>214–224</sub> peptide is represented as follows: 0–20% reduction (white); 21–40% reduction (pale grey); 41–60% reduction (medium grey); 61–80% reduction (dark grey); 81–100% reduction (black). The expressed TCR Vβ genes were identified using Vβ subfamily-specific PCR assays. NT = not tested.</p>", "links"=>[], "tags"=>["alanine", "substitutions", "epitope"], "article_id"=>494784, "categories"=>["Biochemistry", "Immunology", "Physics"], "users"=>["Isabel K. Macdonald", "Maria Harkiolaki", "Lawrence Hunt", "Timothy Connelley", "A. Victoria Carroll", "Niall D. MacHugh", "Simon P. Graham", "E. Yvonne Jones", "W. Ivan Morrison", "Darren R. Flower", "Shirley A. Ellis"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001149.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_single_alanine_substitutions_in_the_Tp1_214_8211_224_epitope_on_recognition_by_specific_CD8_T_cell_clones_/494784", "title"=>"Effects of single alanine substitutions in the Tp1<sub>214–224</sub> epitope on recognition by specific CD8<sup>+</sup> T cell clones.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-10-14 01:19:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/823993"], "description"=>"<p>pBL<sub>50</sub> values obtained with N*01301 using an RMA-S stabilization assay, (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1001149#s4\" target=\"_blank\">Materials and Methods</a> for explanation), (A) for the reference peptide (TIMPKDIQL) and Ala-substituted peptides and (B) forTp1<sub>214–224</sub> (VGYPKVKEEML) and Ala- substituted peptides.</p>", "links"=>[], "tags"=>["binding"], "article_id"=>494352, "categories"=>["Biochemistry", "Immunology", "Physics"], "users"=>["Isabel K. Macdonald", "Maria Harkiolaki", "Lawrence Hunt", "Timothy Connelley", "A. Victoria Carroll", "Niall D. MacHugh", "Simon P. Graham", "E. Yvonne Jones", "W. Ivan Morrison", "Darren R. Flower", "Shirley A. Ellis"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001149.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Peptide_binding_to_N_01301_/494352", "title"=>"Peptide binding to N*01301.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-10-14 01:12:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/824516"], "description"=>"1<p>BoLA N*01402, which has Lys in place of Trp at position 73, has only been recorded once (<a href=\"http://www.ebi.ac.uk/ipd/mhc/bola\" target=\"_blank\">www.ebi.ac.uk/ipd/mhc/bola</a>); Lys at position 73 has not been observed in any other cattle class I allele.</p>", "links"=>[], "tags"=>["residues", "positions", "73", "147", "mhc"], "article_id"=>494874, "categories"=>["Biochemistry", "Immunology", "Physics"], "users"=>["Isabel K. Macdonald", "Maria Harkiolaki", "Lawrence Hunt", "Timothy Connelley", "A. Victoria Carroll", "Niall D. MacHugh", "Simon P. Graham", "E. Yvonne Jones", "W. Ivan Morrison", "Darren R. Flower", "Shirley A. Ellis"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001149.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Amino_acid_residues_at_positions_73_and_147_in_7_cattle_MHC_class_I_alleles_/494874", "title"=>"Amino acid residues at positions 73 and 147 in 7 cattle MHC class I alleles.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-10-14 01:21:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/824351"], "description"=>"<p>Peptide Tp1<sub>214–224</sub> bound to N*01301 (cyan), compared to peptides in other mammalian pMHC structures. View shows the Cα-traces of the bound peptide from the α2 helix side of the binding groove, unless stated otherwise. (A) Long peptide comparison: 11mer peptide (green, PDB accession code 3BEV) bound to chicken B21; 11mer (gold, PBD code 2FZ3), 12mer (red, PBD code 3BW9) and 13mer (orange, PBD code 1ZHL) peptides bound to HLA-B*3508; 11mer peptides (purple, PBD code 2BVQ; grey, PBD code 2BVO) bound to HLA-B*5703. (B) Long peptide comparison: view onto the binding groove of <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1001149#ppat-1001149-g004\" target=\"_blank\">Fig. 4A</a>. (C) Long peptide comparison: 11mer peptide bound to HLA-B*3508 (blue, PDB code 1ZSD), and its conformation change upon TCR binding (pink, PDB code 2NX5). Peptide Cα backbone positions are denoted by P1-PΩ for Tp1<sub>214–224</sub>. (D) Mouse comparison: 9mer peptide (red, PBD code 1CE6) and 11mer peptide (blue, PBD code 1JPF) bound to H-2D<sup>b</sup>; 10mer peptide (brown, PBD code 1BII) bound to H-2D<sup>d</sup>; 8mer peptide (green, PBD code 1FO0) bound to H-2K<sup>b</sup>; 9mer peptide (pink, PBD code 1VGK) bound to H-2K<sup>d</sup>; 9mer peptide (yellow, PBD code 1ZT1) bound to H-2K<sup>k</sup>. (E) Mouse comparison: view onto the binding groove of <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1001149#ppat-1001149-g004\" target=\"_blank\">Fig. 4D</a>.</p>", "links"=>[], "tags"=>["biochemistry/protein chemistry", "immunology/antigen processing and recognition", "immunology/genetics of the immune system", "immunology/immunity to infections", "infectious diseases/protozoal infections"], "article_id"=>494705, "categories"=>["Biochemistry", "Immunology", "Physics"], "users"=>["Isabel K. Macdonald", "Maria Harkiolaki", "Lawrence Hunt", "Timothy Connelley", "A. Victoria Carroll", "Niall D. MacHugh", "Simon P. Graham", "E. Yvonne Jones", "W. Ivan Morrison", "Darren R. Flower", "Shirley A. Ellis"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001149.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_structures_/494705", "title"=>"Comparison of structures.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-10-14 01:18:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/410857", "https://ndownloader.figshare.com/files/410878", "https://ndownloader.figshare.com/files/410897", "https://ndownloader.figshare.com/files/410915", "https://ndownloader.figshare.com/files/410933", "https://ndownloader.figshare.com/files/410952", "https://ndownloader.figshare.com/files/410984", "https://ndownloader.figshare.com/files/411013"], "description"=>"<div><p>T cell receptor (TCR) recognition of peptide-MHC class I (pMHC) complexes is a crucial event in the adaptive immune response to pathogens. Peptide epitopes often display a strong dominance hierarchy, resulting in focusing of the response on a limited number of the most dominant epitopes. Such T cell responses may be additionally restricted by particular MHC alleles in preference to others. We have studied this poorly understood phenomenon using <em>Theileria parva</em>, a protozoan parasite that causes an often fatal lymphoproliferative disease in cattle. Despite its antigenic complexity, CD8<sup>+</sup> T cell responses induced by infection with the parasite show profound immunodominance, as exemplified by the Tp1<sub>214–224</sub> epitope presented by the common and functionally important MHC class I allele N*01301. We present a high-resolution crystal structure of this pMHC complex, demonstrating that the peptide is presented in a distinctive raised conformation. Functional studies using CD8<sup>+</sup> T cell clones show that this impacts significantly on TCR recognition. The unconventional structure is generated by a hydrophobic ridge within the MHC peptide binding groove, found in a set of cattle MHC alleles. Extremely rare in all other species, this feature is seen in a small group of mouse MHC class I molecules. The data generated in this analysis contribute to our understanding of the structural basis for T cell-dependent immune responses, providing insight into what determines a highly immunogenic p-MHC complex, and hence can be of value in prediction of antigenic epitopes and vaccine design.</p></div>", "links"=>[], "tags"=>["mhc", "bound", "immunodominant", "epitope", "demonstrates", "unconventional", "receptors"], "article_id"=>141168, "categories"=>["Biochemistry", "Immunology", "Physics"], "users"=>["Isabel K. Macdonald", "Maria Harkiolaki", "Lawrence Hunt", "Timothy Connelley", "A. Victoria Carroll", "Niall D. MacHugh", "Simon P. Graham", "E. Yvonne Jones", "W. Ivan Morrison", "Darren R. Flower", "Shirley A. Ellis"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1001149.s001", "https://dx.doi.org/10.1371/journal.ppat.1001149.s002", "https://dx.doi.org/10.1371/journal.ppat.1001149.s003", "https://dx.doi.org/10.1371/journal.ppat.1001149.s004", "https://dx.doi.org/10.1371/journal.ppat.1001149.s005", "https://dx.doi.org/10.1371/journal.ppat.1001149.s006", "https://dx.doi.org/10.1371/journal.ppat.1001149.s007", "https://dx.doi.org/10.1371/journal.ppat.1001149.s008"], "stats"=>{"downloads"=>13, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/MHC_Class_I_Bound_to_an_Immunodominant_Theileria_parva_Epitope_Demonstrates_Unconventional_Presentation_to_T_Cell_Receptors/141168", "title"=>"MHC Class I Bound to an Immunodominant <em>Theileria parva</em> Epitope Demonstrates Unconventional Presentation to T Cell Receptors", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-10-14 00:19:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/824247"], "description"=>"<p>Conformation of the bound peptide Tp1<sub>214–224</sub> shown from the α2 helix side of the binding groove, unless stated otherwise. (A) The corresponding <i>2F<sub>o</sub>-F<sub>c</sub></i> electron density is shown in mesh format. The peptide is in stick format with each amino acid labeled (B) View onto the binding groove (as in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1001149#ppat-1001149-g002\" target=\"_blank\">Fig. 2B</a>) additionally showing Trp3 and Glu9 of Tp1<sub>214–224</sub>, and Arg155 of N*01301. Hydrogen bonds are denoted by dotted grey lines (C) The peptide backbone is shown as a cartoon ribbon in gold. The Lys at position 5 of Tp1<sub>214–224</sub> and the Asn, Glu and Trp at positions 70, 97 and 73 respectively of N*01301 are shown in stick format.</p>", "links"=>[], "tags"=>["bound"], "article_id"=>494606, "categories"=>["Biochemistry", "Immunology", "Physics"], "users"=>["Isabel K. Macdonald", "Maria Harkiolaki", "Lawrence Hunt", "Timothy Connelley", "A. Victoria Carroll", "Niall D. MacHugh", "Simon P. Graham", "E. Yvonne Jones", "W. Ivan Morrison", "Darren R. Flower", "Shirley A. Ellis"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001149.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conformation_of_the_bound_peptide_/494606", "title"=>"Conformation of the bound peptide.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-10-14 01:16:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/824141"], "description"=>"<p>(A) The heavy chain is shown in cyan, β<sub>2</sub>m in purple, and the peptide in yellow (B) Top view of the binding platform showing the bound peptide Tp1<sub>214–224</sub> in stick format with residues labeled.</p>", "links"=>[], "tags"=>["biochemistry/protein chemistry", "immunology/antigen processing and recognition", "immunology/genetics of the immune system", "immunology/immunity to infections", "infectious diseases/protozoal infections"], "article_id"=>494489, "categories"=>["Biochemistry", "Immunology", "Physics"], "users"=>["Isabel K. Macdonald", "Maria Harkiolaki", "Lawrence Hunt", "Timothy Connelley", "A. Victoria Carroll", "Niall D. MacHugh", "Simon P. Graham", "E. Yvonne Jones", "W. Ivan Morrison", "Darren R. Flower", "Shirley A. Ellis"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001149.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overview_of_the_structure_of_N_01301_/494489", "title"=>"Overview of the structure of N*01301.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-10-14 01:14:49"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"9", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"1", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"2"}
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  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"1", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"15", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"6", "full-text"=>"14", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"1", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"14", "full-text"=>"8", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"3", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"6", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"10", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"6", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"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"=>"8"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}
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Relative Metric

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