The Expanded Kinesin-13 Repertoire of Trypanosomes Contains Only One Mitotic Kinesin Indicating Multiple Extra-Nuclear Roles
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{"title"=>"The expanded kinesin-13 repertoire of trypanosomes contains only one mitotic kinesin indicating multiple extra-nuclear roles", "type"=>"journal", "authors"=>[{"first_name"=>"Bill", "last_name"=>"Wickstead", "scopus_author_id"=>"6602380992"}, {"first_name"=>"Jamie T.", "last_name"=>"Carrington", "scopus_author_id"=>"56906024000"}, {"first_name"=>"Eva", "last_name"=>"Gluenz", "scopus_author_id"=>"16444376500"}, {"first_name"=>"Keith", "last_name"=>"Gull", "scopus_author_id"=>"7004312188"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"78649514149", "doi"=>"10.1371/journal.pone.0015020", "pui"=>"360051147", "pmid"=>"21124853", "scopus"=>"2-s2.0-78649514149", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)"}, "id"=>"c2457b72-bd05-3301-977e-dd05a64ac7ea", "abstract"=>"BACKGROUND: Kinesin-13 proteins have a critical role in animal cell mitosis, during which they regulate spindle microtubule dynamics through their depolymerisation activity. Much of what is known about Kinesin-13 function emanates from a relatively small sub-family of proteins containing MCAK and Kif2A/B. However, recent work on kinesins from the much more widely distributed, ancestral Kinesin-13 family, which includes human Kif24, have identified a second function in flagellum length regulation that may exist either alongside or instead of the mitotic role. METHODOLOGY/PRINCIPAL FINDINGS: The African trypanosome Trypanosoma brucei encodes 7 distinct Kinesin-13 proteins, allowing scope for extensive specialisation of roles. Here, we show that of all the trypanosomal Kinesin-13 proteins, only one is nuclear. This protein, TbKIN13-1, is present in the nucleoplasm throughout the cell cycle, but associates with the spindle during mitosis, which in trypanosomes is closed. TbKIN13-1 is necessary for the segregation of both large and mini-chromosomes in this organism and reduction in TbKIN13-1 levels mediated by RNA interference causes deflects in spindle disassembly with spindle-like structures persisting in non-mitotic cells. A second Kinesin-13 is localised to the flagellum tip, but the majority of the Kinesin-13 family members are in neither of these cellular locations. CONCLUSIONS/SIGNIFICANCE: These data show that the expanded Kinesin-13 repertoire of trypanosomes is not associated with diversification of spindle-associated roles. TbKIN13-1 is required for correct spindle function, but the extra-nuclear localisation of the remaining paralogues suggests that the biological roles of the Kinesin-13 family is wider than previously thought.", "link"=>"http://www.mendeley.com/research/expanded-kinesin13-repertoire-trypanosomes-contains-only-one-mitotic-kinesin-indicating-multiple-ext", "reader_count"=>35, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>7, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>14, "Student > Master"=>4, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>7, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>14, "Student > Master"=>4, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>28, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>28}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United Kingdom"=>1, "Switzerland"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/817091"], "description"=>"<p>Direct fluorescence signal from TbKIN13-1-GFP (green) and DAPI-stained DNA (red) are shown for representative cells at different stages of the cell-cycle (ordered from G1 to cytokinesis, top to bottom). All images were captured and processed with the same settings, such that fluorescence levels can be directly compared.</p>", "links"=>[], "tags"=>["nucleus"], "article_id"=>487469, "categories"=>["Cell Biology"], "users"=>["Bill Wickstead", "Jamie T. Carrington", "Eva Gluenz", "Keith Gull"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015020.g004", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TbKIN13_1_is_found_in_the_nucleus_throughout_the_cell_cycle_/487469", "title"=>"TbKIN13-1 is found in the nucleus throughout the cell-cycle.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-23 02:04:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/817384"], "description"=>"<p>A) Cell growth is reduced 24 h after the addition of tetracycline. B) Levels of TbKIN13-1 are similar in parental cells line (29-13) and RNAi cells before induction (0) but rapidly fall at post-induction (12, 24, 48, 72 h shown), as seen by Western blot using affinity-purified anti-TbKIN13-1 polyclonal antibody (α-KIN13-1). Monoclonal antibody L8C4 which detects a flagellar protein <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0015020#pone.0015020-Kohl1\" target=\"_blank\">[69]</a> was used as a loading control. C) Induction of RNAi is accompanied by an increase in anuclear ‘1K0N’ cells (K = kinetoplast, N = nucleus; each time point represents 500 cells). Indirect immunofluorescence using anti-β-tubulin monoclonal antibody KMX-1 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0015020#pone.0015020-Birkett1\" target=\"_blank\">[67]</a> (red) and DAPI (blue), before (D) and after (E) induction shows that RNAi results in cells with unevenly segregated nuclear DNA and abnormal tubulin distribution.</p>", "links"=>[], "tags"=>["rna-interference"], "article_id"=>487754, "categories"=>["Cell Biology"], "users"=>["Bill Wickstead", "Jamie T. Carrington", "Eva Gluenz", "Keith Gull"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015020.g006", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Induction_of_RNA_interference_against_TbKIN13_1_/487754", "title"=>"Induction of RNA-interference against <i>TbKIN13-1</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-23 02:09:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/816974"], "description"=>"<p>Images show signal from indirect immunofluorescence using affinity-purified polyclonal antisera against TbKIN13-1 or TbKIN13-3 (α-TbKIN13-1, α-Tb-KIN13-3) in cells expressing either TbKIN13-1-GFP or TbKIN13-3-GFP. Antibody and GFP co-localise when directed toward the same kinesin (A,D), but are specific to that kinesin (B,C). Both kinesins localise to the same cellular compartment whether tagged or untagged (A,C and B,D).</p>", "links"=>[], "tags"=>["subcellular", "locations", "tbkin13-1", "tbkin13-3", "unaffected", "c-terminal", "tagging"], "article_id"=>487336, "categories"=>["Cell Biology"], "users"=>["Bill Wickstead", "Jamie T. Carrington", "Eva Gluenz", "Keith Gull"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015020.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_subcellular_locations_of_TbKIN13_1_and_TbKIN13_3_are_unaffected_by_C_terminal_tagging_with_GFP_/487336", "title"=>"The subcellular locations of TbKIN13-1 and TbKIN13-3 are unaffected by C-terminal tagging with GFP.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-23 02:02:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/817481"], "description"=>"<p>Knockdown of <i>TbKIN13-1</i> results in a rapid accumulation in cells undergoing mitosis (A; as judged by the presence of a mitotic spindle). However, there is a concomitant decrease in the proportions of these spindles with a ‘diamond’ configuration characteristic of cells in early mitosis and an increase in abnormal spindle morphologies (B). All time points represent counts of 500 cells or spindles.</p>", "links"=>[], "tags"=>["rnai", "spindle"], "article_id"=>487856, "categories"=>["Cell Biology"], "users"=>["Bill Wickstead", "Jamie T. Carrington", "Eva Gluenz", "Keith Gull"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015020.g007", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_RNAi_against_TbKIN13_1_on_spindle_formation_/487856", "title"=>"Effect of RNAi against <i>TbKIN13-1</i> on spindle formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-23 02:10:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/816720"], "description"=>"<p>The result of a Bayesian tree inference based on an alignment of the motor domain region is shown alongside protein architecture schematics showing the positions of predicted Pfam-A domains and coiled-coils (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0015020#s4\" target=\"_blank\">Materials and Methods</a>). The expanded <i>Trypanosoma brucei</i> repertoire is highlighted (red). A small number of Kinesin-8 and Kinesin-14 sequences are included as an outgroup. Numbers beside nodes represent support from Bayesian posterior probabilities or maximum likelihood bootstrap values (PP/BV).</p>", "links"=>[], "tags"=>["kinesin-13", "members"], "article_id"=>487088, "categories"=>["Cell Biology"], "users"=>["Bill Wickstead", "Jamie T. Carrington", "Eva Gluenz", "Keith Gull"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015020.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_analysis_of_Kinesin_13_family_members_from_a_diverse_range_of_eukaryotes_/487088", "title"=>"Phylogenetic analysis of Kinesin-13 family members from a diverse range of eukaryotes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-23 01:58:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/817582"], "description"=>"<p>Shown is signal from <i>in situ</i> hybridisation using a 177 bp repeat specific to the mini-chromosomal population (green) and combined immunofluorescence using anti-β-tubulin monoclonal antibody KMX-1 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0015020#pone.0015020-Birkett1\" target=\"_blank\">[67]</a> (red). DAPI (blue) shows total DNA. In non-induced cells, minichromosomes progress rapidly to the spindle poles at the onset of anaphase, where they remain (A). Following induction of RNAi against <i>TbKIN13-1</i>, there are defects in the movement of both the small chromosome population and bulk DNA (B). Arrows highlight lagging DNA in anaphase cells.</p>", "links"=>[], "tags"=>["causes", "defects", "segregation"], "article_id"=>487950, "categories"=>["Cell Biology"], "users"=>["Bill Wickstead", "Jamie T. Carrington", "Eva Gluenz", "Keith Gull"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015020.g008", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Knockdown_of_TbKIN13_1_causes_defects_in_the_segregation_of_both_large_and_mini_chromosomes_/487950", "title"=>"Knockdown of <i>TbKIN13-1</i> causes defects in the segregation of both large and mini-chromosomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-23 02:12:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/816837"], "description"=>"<p>A) For each protein, direct fluorescence from C-terminal chimeras created by the insertion of <i>GFP</i> at the endogenous locus is shown (left panel), next to an overlay of signal from DAPI-stained DNA (blue) and phase-contrast image (right panel). Only TbKIN13-1 is nuclear. The accumulation of TbKIN13-2 at the flagellar tips is highlighted (arrows). All other Kinesin-13 family members in <i>Trypanosoma brucei</i> are found in the cytoplasm, or associated with the subpellicular array of microtubules. B) Levels of tagged protein in the cell lines seen in (A), demonstrated by Western blotting of whole cell lysates with α-GFP antibodies. Detection of the flagellar protein PFR2 by monoclonal antibody L8C4 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0015020#pone.0015020-Kohl1\" target=\"_blank\">[69]</a>, is shown as a loading control. C) Demonstration of near wild-type levels of protein expression produced by endogenous locus tagging with incorporation of endogenous UTRs (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0015020#s4\" target=\"_blank\">Materials and Methods</a>). Panels show whole cell lysates of cell lines containing TbKIN13-1-GFP or TbKIN13-3-GFP expressed from one of the two endogenous alleles, blotted with either α-GFP antibodies or affinity-purified polyclonal antisera against TbKIN13-1 or TbKIN13-3.</p>", "links"=>[], "tags"=>["cellular", "localisation", "kinesin-13"], "article_id"=>487210, "categories"=>["Cell Biology"], "users"=>["Bill Wickstead", "Jamie T. Carrington", "Eva Gluenz", "Keith Gull"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015020.g002", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_cellular_localisation_of_all_seven_Trypanosoma_brucei_Kinesin_13_family_members_/487210", "title"=>"The cellular localisation of all seven <i>Trypanosoma brucei</i> Kinesin-13 family members.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-23 02:00:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/407291", "https://ndownloader.figshare.com/files/407302", "https://ndownloader.figshare.com/files/407310", "https://ndownloader.figshare.com/files/407317", "https://ndownloader.figshare.com/files/407326"], "description"=>"<div><h3>Background</h3><p>Kinesin-13 proteins have a critical role in animal cell mitosis, during which they regulate spindle microtubule dynamics through their depolymerisation activity. Much of what is known about Kinesin-13 function emanates from a relatively small sub-family of proteins containing MCAK and Kif2A/B. However, recent work on kinesins from the much more widely distributed, ancestral Kinesin-13 family, which includes human Kif24, have identified a second function in flagellum length regulation that may exist either alongside or instead of the mitotic role.</p> <h3>Methodology/Principal Findings</h3><p>The African trypanosome <em>Trypanosoma brucei</em> encodes 7 distinct Kinesin-13 proteins, allowing scope for extensive specialisation of roles. Here, we show that of all the trypanosomal Kinesin-13 proteins, only one is nuclear. This protein, TbKIN13-1, is present in the nucleoplasm throughout the cell cycle, but associates with the spindle during mitosis, which in trypanosomes is closed. TbKIN13-1 is necessary for the segregation of both large and mini-chromosomes in this organism and reduction in TbKIN13-1 levels mediated by RNA interference causes deflects in spindle disassembly with spindle-like structures persisting in non-mitotic cells. A second Kinesin-13 is localised to the flagellum tip, but the majority of the Kinesin-13 family members are in neither of these cellular locations.</p> <h3>Conclusions/Significance</h3><p>These data show that the expanded Kinesin-13 repertoire of trypanosomes is not associated with diversification of spindle-associated roles. TbKIN13-1 is required for correct spindle function, but the extra-nuclear localisation of the remaining paralogues suggests that the biological roles of the Kinesin-13 family is wider than previously thought.</p> </div>", "links"=>[], "tags"=>["expanded", "kinesin-13", "repertoire", "trypanosomes", "contains", "mitotic", "kinesin", "indicating", "extra-nuclear", "roles"], "article_id"=>140472, "categories"=>["Cell Biology"], "users"=>["Bill Wickstead", "Jamie T. Carrington", "Eva Gluenz", "Keith Gull"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0015020.s001", "https://dx.doi.org/10.1371/journal.pone.0015020.s002", "https://dx.doi.org/10.1371/journal.pone.0015020.s003", "https://dx.doi.org/10.1371/journal.pone.0015020.s004", "https://dx.doi.org/10.1371/journal.pone.0015020.s005"], "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Expanded_Kinesin_13_Repertoire_of_Trypanosomes_Contains_Only_One_Mitotic_Kinesin_Indicating_Multiple_Extra_Nuclear_Roles/140472", "title"=>"The Expanded Kinesin-13 Repertoire of Trypanosomes Contains Only One Mitotic Kinesin Indicating Multiple Extra-Nuclear Roles", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-11-23 00:07:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/817264"], "description"=>"<p>Direct fluorescence signal from TbKIN13-1-GFP (green), and indirect immunofluorscence using the anti-β-tubulin monoclonal antibody KMX-1 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0015020#pone.0015020-Birkett1\" target=\"_blank\">[67]</a> (red) for ‘cytoskeletons’ made by extracting cells with non-ionic detergent in microtubule-stabilising buffer. Overlays of DAPI-stained DNA (blue) and phase-contrast images are also shown (right panel).</p>", "links"=>[], "tags"=>["mitotic"], "article_id"=>487635, "categories"=>["Cell Biology"], "users"=>["Bill Wickstead", "Jamie T. Carrington", "Eva Gluenz", "Keith Gull"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015020.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TbKIN13_1_is_associated_with_the_mitotic_spindle_/487635", "title"=>"TbKIN13-1 is associated with the mitotic spindle.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-23 02:07:15"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"2", "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"=>"12"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
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  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
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  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
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  • {"unique-ip"=>"10", "full-text"=>"12", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"14", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"13", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2021", "month"=>"1"}

Relative Metric

{"start_date"=>"2010-01-01T00:00:00Z", "end_date"=>"2010-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[288, 576, 733, 867, 984, 1087, 1182, 1267, 1346, 1424, 1501, 1577, 1646, 1711, 1778, 1841, 1908, 1970, 2034, 2102, 2162, 2227, 2296, 2359, 2422, 2482, 2550, 2610, 2679, 2747, 2820, 2887, 2955, 3009, 3067, 3130, 3200, 3257, 3322, 3379, 3443, 3507, 3571, 3632, 3683, 3753, 3822, 3877]}, {"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[290, 557, 702, 824, 930, 1032, 1119, 1197, 1276, 1347, 1410, 1477, 1539, 1603, 1678, 1741, 1801, 1866, 1930, 1988, 2060, 2117, 2185, 2239, 2300, 2358, 2429, 2486, 2548, 2613, 2693, 2758, 2824, 2891, 2950, 3019, 3093, 3163, 3224, 3284, 3355, 3421, 3486, 3552, 3622, 3684, 3749, 3799, 3859]}]}
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