Outward Rectification of Voltage-Gated K+ Channels Evolved at Least Twice in Life History
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{"title"=>"Outward rectification of voltage-gated K+channels evolved at least twice in life history", "type"=>"journal", "authors"=>[{"first_name"=>"Janin", "last_name"=>"Riedelsberger", "scopus_author_id"=>"35801279700"}, {"first_name"=>"Ingo", "last_name"=>"Dreyer", "scopus_author_id"=>"55918914300"}, {"first_name"=>"Wendy", "last_name"=>"Gonzalez", "scopus_author_id"=>"23481763900"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"606519671", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0137600", "scopus"=>"2-s2.0-84944755223", "pmid"=>"26356684", "sgr"=>"84944755223"}, "id"=>"a72b2464-a9a5-3bec-8458-ae0aaab16eab", "abstract"=>"Voltage-gated potassium (K+) channels are present in all living systems. Despite high structural similarities in the transmembrane domains (TMD), this K+ channel type segregates into at least two main functional categories-hyperpolarization-activated, inward-rectifying (Kin) and depolarization-activated, outward-rectifying (Kout) channels. Voltage-gated K+ channels sense the membrane voltage via a voltage-sensing domain that is connected to the conduction pathway of the channel. It has been shown that the voltage-sensing mechanism is the same in Kin and Kout channels, but its performance results in opposite pore conformations. It is not known how the different coupling of voltage-sensor and pore is implemented. Here, we studied sequence and structural data of voltage-gated K+ channels from animals and plants with emphasis on the property of opposite rectification. We identified structural hotspots that alone allow already the distinction between Kin and Kout channels. Among them is a loop between TMD S5 and the pore that is very short in animal Kout, longer in plant and animal Kin and the longest in plant Kout channels. In combination with further structural and phylogenetic analyses this finding suggests that outward-rectification evolved twice and independently in the animal and plant kingdom.", "link"=>"http://www.mendeley.com/research/outward-rectification-voltagegated-kchannels-evolved-least-twice-life-history", "reader_count"=>8, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>1, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>1, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Agricultural and Biological Sciences"=>6, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>6}, "Computer Science"=>{"Computer Science"=>1}, "Unspecified"=>{"Unspecified"=>1}}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2257921"], "description"=>"<p>Voltage-gated K<sup>+</sup> channel groups are defined according to the clades that arose from the phylogenetic analysis presented in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0137600#pone.0137600.g002\" target=\"_blank\">Fig 2</a>. The N-termini of these K<sup>+</sup> channels are sparsely conserved. Even within channel groups there is a high variability in length (represented by the white to black gradient). Some animal K<sub>out</sub> channels show an extended sequence between the first two TMDs. In contrast, all plant Kv-like and animal K<sub>in</sub> channels have an extended loop between TMD S2 and S3. Animal K<sub>in</sub> channels have the highest number of charged residues in S4, whereas the lowest number is present in plant Kv-like channels. In contrast, plant Kv-like channels feature the highest number of charged residues in the S4-S5 linker, while animal K<sub>out</sub> channels hardly possess charged residues in this linker. The most striking structural difference that correlates with channel function is a loop between TMD S5 and the pore region. This loop is only present in plant Kv-like and animal K<sub>in</sub> channels. In addition, a small stretch in the loop discriminates between plant K<sub>in</sub> and K<sub>out</sub> channels.</p>", "links"=>[], "tags"=>["Kout channels", "plant Kout channels", "channel type segregates", "kin", "TMD S 5"], "article_id"=>1539360, "categories"=>["Uncategorised"], "users"=>["Janin Riedelsberger", "Ingo Dreyer", "Wendy Gonzalez"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137600.g003", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Simplified_representation_of_structural_characteristics_of_voltage_gated_K_channel_groups_/1539360", "title"=>"Simplified representation of structural characteristics of voltage-gated K<sup>+</sup> channel groups.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-10 03:43:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/2257919"], "description"=>"<p>It moves towards the intracellular side of the membrane upon hyperpolarizing membrane voltages and towards the extracellular side upon membrane depolarization. The “down” movement of S4 causes K<sub>in</sub> channels to open, while the same S4 movement results in closure of K<sub>out</sub> channels. The opening of K<sub>out</sub> and closure of K<sub>in</sub> channels proceeds in the inverse manner in response to S4 “up” movements.</p>", "links"=>[], "tags"=>["Kout channels", "plant Kout channels", "channel type segregates", "kin", "TMD S 5"], "article_id"=>1539358, "categories"=>["Uncategorised"], "users"=>["Janin Riedelsberger", "Ingo Dreyer", "Wendy Gonzalez"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137600.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structure_and_function_of_voltage_gated_K_channels_A_Functional_voltage_gated_K_channels_form_tetramers_coloured_representation_Each_subunit_grey_representation_comprises_six_transmembrane_domains_S1_S6_and_a_selectivity_filter_between_S5_and_S6_The_firs/1539358", "title"=>"Structure and function of voltage-gated K<sup>+</sup> channels (A) Functional voltage-gated K<sup>+</sup> channels form tetramers (coloured representation). Each subunit (grey representation) comprises six transmembrane domains (S1-S6) and a selectivity filter between S5 and S6. The first four TMDs form the voltage sensor that is located in the periphery of the functional channel. The last two TMDs contribute to the channel pore in the centre of the channel. (B) TMD S4 of the voltage sensor translocates in response to the transmembrane voltage within the membrane and affects the channel conformation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-10 03:43:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/2257932", "https://ndownloader.figshare.com/files/2257933", "https://ndownloader.figshare.com/files/2257934"], "description"=>"<div><p>Voltage-gated potassium (K<sup>+</sup>) channels are present in all living systems. Despite high structural similarities in the transmembrane domains (TMD), this K<sup>+</sup> channel type segregates into at least two main functional categories—hyperpolarization-activated, inward-rectifying (K<sub>in</sub>) and depolarization-activated, outward-rectifying (K<sub>out</sub>) channels. Voltage-gated K<sup>+</sup> channels sense the membrane voltage via a voltage-sensing domain that is connected to the conduction pathway of the channel. It has been shown that the voltage-sensing mechanism is the same in K<sub>in</sub> and K<sub>out</sub> channels, but its performance results in opposite pore conformations. It is not known how the different coupling of voltage-sensor and pore is implemented. Here, we studied sequence and structural data of voltage-gated K<sup>+</sup> channels from animals and plants with emphasis on the property of opposite rectification. We identified structural hotspots that alone allow already the distinction between K<sub>in</sub> and K<sub>out</sub> channels. Among them is a loop between TMD S5 and the pore that is very short in animal K<sub>out</sub>, longer in plant and animal K<sub>in</sub> and the longest in plant K<sub>out</sub> channels. In combination with further structural and phylogenetic analyses this finding suggests that outward-rectification evolved twice and independently in the animal and plant kingdom.</p></div>", "links"=>[], "tags"=>["Kout channels", "plant Kout channels", "channel type segregates", "kin", "TMD S 5"], "article_id"=>1539368, "categories"=>["Uncategorised"], "users"=>["Janin Riedelsberger", "Ingo Dreyer", "Wendy Gonzalez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0137600.s001", "https://dx.doi.org/10.1371/journal.pone.0137600.s002", "https://dx.doi.org/10.1371/journal.pone.0137600.s003"], "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Outward_Rectification_of_Voltage_Gated_K_Channels_Evolved_at_Least_Twice_in_Life_History/1539368", "title"=>"Outward Rectification of Voltage-Gated K<sup>+</sup> Channels Evolved at Least Twice in Life History", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-09-10 03:43:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/2257927"], "description"=>"<p>Data derived from: + protein models</p><p>* crystal structures; E experiments; or S sequence analysis. ‘n.a.’ not available data due to lacking structure. E’ an interaction between the S4-S5 linker and the S6 end has been observed experimentally, but it is not clear in which state the interaction occurs.</p><p>M and C in the column ‘structure’ indicate availability of protein models (M) or crystal structures (C). Number given in brackets following the ‘C’ indicates PDB ID of the respective structure.</p><p>Overview of characteristic features found in voltage-gated K<sup>+</sup> channels of different taxa.</p>", "links"=>[], "tags"=>["Kout channels", "plant Kout channels", "channel type segregates", "kin", "TMD S 5"], "article_id"=>1539366, "categories"=>["Uncategorised"], "users"=>["Janin Riedelsberger", "Ingo Dreyer", "Wendy Gonzalez"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137600.t002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overview_of_characteristic_features_found_in_voltage_gated_K_channels_of_different_taxa_/1539366", "title"=>"Overview of characteristic features found in voltage-gated K<sup>+</sup> channels of different taxa.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-09-10 03:43:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/2257924"], "description"=>"<p>A maximum likelihood tree was calculated using the WAG model and a bootstrap value of 1000 with K<sup>+</sup> channel sequences from (i) bacteria (<i>Aeropyrum pernix</i>: <i>Ape</i>-KvAP (APE_0955); <i>Listeria monocytogenes</i>: <i>Lmo</i>-Kv (lmo2059); <i>Methanocaldococcus jannaschii</i>: <i>Mja</i>-Kv (MJ0139)), (ii) animals (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0137600#pone.0137600.t001\" target=\"_blank\">Table 1</a>; <i>Caenorhabditis elegans</i>: <i>Cel</i>-Kv (CELEg_ZK1321.2)), (iii) early land plants (<i>Selaginella</i> moellendorffii: <i>Smo</i>-Kout (scaffold_121_2_ORF2559)); <i>Physcomitrella patens</i>: <i>Ppa</i>-Kin1 (Pp1s3_156V6.1), <i>Ppa</i>-Kin2 (Pp1s2_170V6.1), <i>Ppa</i>-Kin3 (Pp1s22_165V6.1), <i>Ppa</i>-Kin4 (Pp1s283_74V6.1), (iv) eudicots (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0137600#pone.0137600.t001\" target=\"_blank\">Table 1</a>), and (vi) the early terrestrial alga <i>Klebsormidium</i> (<i>Kfl</i>-21-370 (kfl00021_0370), <i>Kfl</i>-21-430 (kfl00021_0430), <i>Kfl</i>-35-100 (kfl00035_0100), <i>Kfl</i>-43-330 (kfl00043_0330), <i>Kfl</i>-108-190 (kfl00108_0190), <i>Kfl</i>-119-90 (kfl00119_0090), <i>Kfl</i>-175-250 (kfl00175_0250), <i>Kfl</i>-373-10 (kfl00373_0010), <i>Kfl</i>-409-60 (kfl00409_0060), <i>Kfl</i>-437-30 (kfl00437_0030), <i>Kfl</i>-600-80 (kfl00600_0080)). The phylogenetic tree is mid-point rooted and displays the relationship of K<sup>+</sup> channels. The main K<sup>+</sup> channel families are grouped in separated clades. Plant K<sub>in</sub> and K<sub>out</sub> channels as well as animal K<sub>in</sub> and K<sub>out</sub> channels form individual clades. Thereby, bacterial and animal K<sub>out</sub> channels are separated from K<sup>+</sup> channels from green plants as well as animal K<sub>in</sub> channels. The K<sup>+</sup> channels from <i>Klebsormidium</i> are not grouped into one clade. Instead they spread over the entire tree indicating a broad diversity of different K<sup>+</sup> channels. Especially two, out of eleven, K<sup>+</sup> channels from <i>Klebsormidium</i> (marked by a square) are closely related to plant K<sub>in</sub> and plant K<sub>out</sub> channels.</p>", "links"=>[], "tags"=>["Kout channels", "plant Kout channels", "channel type segregates", "kin", "TMD S 5"], "article_id"=>1539363, "categories"=>["Uncategorised"], "users"=>["Janin Riedelsberger", "Ingo Dreyer", "Wendy Gonzalez"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137600.g006", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Two_Klebsormidium_voltage_gated_K_channels_are_closely_related_to_Kv_like_channels_of_higher_land_plants_/1539363", "title"=>"Two <i>Klebsormidium</i> voltage-gated K<sup>+</sup> channels are closely related to Kv-like channels of higher land plants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-10 03:43:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/2257923"], "description"=>"<p>Channel characteristics are illustrated for animal and plant Kv-like channels in the open and in the closed state. The representation of animal K<sub>in</sub> channels is grey shaded because no protein structures are available so far. In general, the voltage sensor is displayed in blue and the pore in orange. The pore opening at the intracellular side is according to the channel states wide or narrow. The width of this pore part correlates with the distance of the C-terminal S6 ends. S4 is marked within the voltage sensor in its up or down position, respectively. The S4-S5 linkers of all four subunits surround the inner part of the channel pore and form a kind of ring around it. Its diameter correlates with the S4 position and is larger when S4 is in the up position. A black dot at the extracellular side of Kv channels represents the occurrence of the connection of voltage sensor and pore. The loop between the C-terminal end of S5 and the pore TMD is displayed at the extracellular side of the pore in plant Kv-like and animal K<sub>in</sub> channels. The bending of S6 is illustrated within the pore. It is more bended in the closed states and straighter in the open states. Red stars in plant Kv-like and animal K<sub>out</sub> channels represent the interaction of the S4-S5 linker and S6. An interaction of these both structures has been described for animal K<sub>in</sub> channels as well. But it is not clear in which state it appears. Therefore, a yellow star is used to illustrate the interaction.</p>", "links"=>[], "tags"=>["Kout channels", "plant Kout channels", "channel type segregates", "kin", "TMD S 5"], "article_id"=>1539362, "categories"=>["Uncategorised"], "users"=>["Janin Riedelsberger", "Ingo Dreyer", "Wendy Gonzalez"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137600.g005", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Illustration_of_voltage_gated_K_channel_features_described_in_Table_2_/1539362", "title"=>"Illustration of voltage-gated K<sup>+</sup> channel features described in Table 2.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-10 03:43:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/2257926"], "description"=>"<p>Overview of voltage-gated K<sup>+</sup> channel sequences used in this study.</p>", "links"=>[], "tags"=>["Kout channels", "plant Kout channels", "channel type segregates", "kin", "TMD S 5"], "article_id"=>1539365, "categories"=>["Uncategorised"], "users"=>["Janin Riedelsberger", "Ingo Dreyer", "Wendy Gonzalez"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137600.t001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overview_of_voltage_gated_K_channel_sequences_used_in_this_study_/1539365", "title"=>"Overview of voltage-gated K<sup>+</sup> channel sequences used in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-09-10 03:43:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/2257925"], "description"=>"<p>The core channel parts S1 to S6 are displayed including features that are characteristic for these K<sup>+</sup> channel groups, like the extended S2-S3 and S5-P loops, conserved positive charges in S4 and the S4-S5 linker, and the selectivity filter motif TxxTxGYGD. Furthermore, two motifs in the transmembrane domains S1 and S6 are displayed. Outward-rectifying K<sup>+</sup> channels contain an SFFT motif in S1, where inward-rectifying channels contain an AWxx motif. In S6 the characteristic DMI (K<sub>out</sub> channels) and NLG (K<sub>in</sub> channels) motifs are illustrated. In Klebsormidium the S6 motif is not yet specified, while the motif in S1 is that of K<sub>in</sub> channels. The extended loop between S5 and P is two amino acids longer than in plant K<sub>in</sub> channels and six amino acids shorter than the corresponding loop in plant K<sub>out</sub> channels.</p>", "links"=>[], "tags"=>["Kout channels", "plant Kout channels", "channel type segregates", "kin", "TMD S 5"], "article_id"=>1539364, "categories"=>["Uncategorised"], "users"=>["Janin Riedelsberger", "Ingo Dreyer", "Wendy Gonzalez"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137600.g007", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Simplified_representation_of_structural_features_of_Kv_like_channels_from_higher_land_plants_and_Klebsormidium_/1539364", "title"=>"Simplified representation of structural features of Kv-like channels from higher land plants and <i>Klebsormidium</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-10 03:43:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/2257922"], "description"=>"<p>(A) The simplified tree that represents the average distance analysis of full-length K<sup>+</sup> channel sequences corresponds to the tree in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0137600#pone.0137600.g002\" target=\"_blank\">Fig 2</a>. (B) Arrows in the schematic channel representation mark separation points used for sequence fragmentation. Plant Kv-like and animal K<sub>in</sub> channels cluster in one clade if only those channel structures are considered that code for S1 to S4 (D), S5 to S6 (G), only S6 (H), and the C-terminus (I). If only the N-termini are considered plant Kv-like channels cluster together with only some of the animal K<sub>in</sub> channels (C). In contrast to the complete voltage sensor unit S1 to S4 (D), S4 alone does not differentiate between animal K<sub>in</sub> and K<sub>out</sub> channels (E). Here, animal K<sub>in</sub> and K<sub>out</sub> channels cluster together and plant Kv-like channels are present in a separated clade. The S4-S5 linker sequences are the only structural part that clusters plant Kv-like and animal K<sub>out</sub> channels in one clade, which is separated from animal K<sub>in</sub> channels (F).</p>", "links"=>[], "tags"=>["Kout channels", "plant Kout channels", "channel type segregates", "kin", "TMD S 5"], "article_id"=>1539361, "categories"=>["Uncategorised"], "users"=>["Janin Riedelsberger", "Ingo Dreyer", "Wendy Gonzalez"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137600.g004", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Simplified_mid_point_rooted_trees_based_on_average_distance_analyses_of_fragmented_voltage_gated_K_channel_sequences_/1539361", "title"=>"Simplified mid-point rooted trees based on average distance analyses of fragmented voltage-gated K<sup>+</sup> channel sequences.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-10 03:43:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/2257920"], "description"=>"<p>Phylogenetic analysis classifies voltage-gated K<sup>+</sup> channels according to their function and appearance. The maximum likelihood tree was calculated using the WAG model and a bootstrap value of 1000. Plant Kv-like channels, animal K<sub>in</sub> and animal K<sub>out</sub> channels are each classified into one clade. Thereby, plant Kv-like and animal K<sub>in</sub> channels belong to the same superior clade, while animal K<sub>out</sub> channels are organized into a second superior clade. Dashed lines indicate the two mayor clades. Please note: The mid-point rooted tree allows conclusions about channel relationships, but not about assumptions of the ancestors.</p>", "links"=>[], "tags"=>["Kout channels", "plant Kout channels", "channel type segregates", "kin", "TMD S 5"], "article_id"=>1539359, "categories"=>["Uncategorised"], "users"=>["Janin Riedelsberger", "Ingo Dreyer", "Wendy Gonzalez"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137600.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Plant_Kv_like_channels_are_closer_related_to_animal_K_in_than_to_animal_K_out_channels_/1539359", "title"=>"Plant Kv-like channels are closer related to animal K<sub>in</sub> than to animal K<sub>out</sub> channels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-10 03:43:00"}

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  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"9", "full-text"=>"6", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"19", "full-text"=>"17", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"11", "full-text"=>"9", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"15", "full-text"=>"17", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"18", "full-text"=>"15", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"22", "full-text"=>"22", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"17", "full-text"=>"16", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"21", "full-text"=>"21", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"20", "full-text"=>"30", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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