Triose Phosphate Isomerase Deficiency Is Caused by Altered Dimerization–Not Catalytic Inactivity–of the Mutant Enzymes
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{"title"=>"Triose phosphate isomerase deficiency is caused by altered dimerization-not catalytic inactivity-of the mutant enzymes", "type"=>"journal", "authors"=>[{"first_name"=>"Markus", "last_name"=>"Ralser", "scopus_author_id"=>"8836934400"}, {"first_name"=>"Gino", "last_name"=>"Heeren", "scopus_author_id"=>"6602569192"}, {"first_name"=>"Michael", "last_name"=>"Breitenbach", "scopus_author_id"=>"7005123663"}, {"first_name"=>"Hans", "last_name"=>"Lehrach", "scopus_author_id"=>"57050399800"}, {"first_name"=>"Sylvia", "last_name"=>"Krobitsch", "scopus_author_id"=>"8836934300"}], "year"=>2006, "source"=>"PLoS ONE", "identifiers"=>{"isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "issn"=>"19326203", "pui"=>"352589006", "pmid"=>"17183658", "doi"=>"10.1371/journal.pone.0000030", "sgr"=>"55149086824", "scopus"=>"2-s2.0-55149086824"}, "id"=>"5692f3cd-df47-3ef2-96ab-1b8ca76e93ab", "abstract"=>"Triosephosphate isomerase (TPI) deficiency is an autosomal recessive disorder caused by various mutations in the gene encoding the key glycolytic enzyme TPI. A drastic decrease in TPI activity and an increased level of its substrate, dihydroxyacetone phosphate, have been measured in unpurified cell extracts of affected individuals. These observations allowed concluding that the different mutations in the TPI alleles result in catalytically inactive enzymes. However, despite a high occurrence of TPI null alleles within several human populations, the frequency of this disorder is exceptionally rare. In order to address this apparent discrepancy, we generated a yeast model allowing us to perform comparative in vivo analyses of the enzymatic and functional properties of the different enzyme variants. We discovered that the majority of these variants exhibit no reduced catalytic activity per se. Instead, we observed, the dimerization behavior of TPI is influenced by the particular mutations investigated, and by the use of a potential alternative translation initiation site in the TPI gene. Additionally, we demonstrated that the overexpression of the most frequent TPI variant, Glu104Asp, which displays altered dimerization features, results in diminished endogenous TPI levels in mammalian cells. Thus, our results reveal that enzyme deregulation attributable to aberrant dimerization of TPI, rather than direct catalytic inactivation of the enzyme, underlies the pathogenesis of TPI deficiency. Finally, we discovered that yeast cells expressing a TPI variant exhibiting reduced catalytic activity are more resistant against oxidative stress caused by the thiol-oxidizing reagent diamide. This observed advantage might serve to explain the high allelic frequency of TPI null alleles detected among human populations.", "link"=>"http://www.mendeley.com/research/triose-phosphate-isomerase-deficiency-caused-altered-dimerizationnot-catalytic-inactivityof-mutant-e", "reader_count"=>47, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>11, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>4, "Student > Master"=>5, "Student > Bachelor"=>4, "Professor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>11, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>4, "Student > Master"=>5, "Student > Bachelor"=>4, "Professor"=>3}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>6, "Materials Science"=>1, "Agricultural and Biological Sciences"=>33, "Medicine and Dentistry"=>1, "Chemical Engineering"=>1, "Chemistry"=>3, "Computer Science"=>2}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>33}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"Austria"=>1, "United States"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/954569"], "description"=>"<div><p>\n <b>A)</b> The first 17 codons of the human TPI sequence and the netstart scores are presented. The introduced mutations are indicated in bold letters.</p>\n <p>\n <b>B)</b> MR100 <i>Δtpi1</i> yeast cells were transformed with the respective plasmids encoding TPI, TPI<sub>Met1_AAG</sub>, TPI<sub>Ser3_TER</sub> or the variant TPI<sub>2ndATG</sub>.</p>\n <p>Ethanol lysates were prepared from logarithmically growing yeast cultures and the expression level of the different TPI variants was analyzed by immunoblotting using polyclonal α-TPI serum.</p>\n <p>Please note that no sample was loaded in case of the lane marked with a dash.</p>\n <p>\n <b>C)</b> COS1 cells were transfected with the plasmids pEGFP-N1, pEGFP-N1-TPI, pEGFP-N1-TPI<sub>Met1_AAG</sub> or pEGFP-N1-TPI<sub>Ser3_TER</sub>.</p>\n <p>Cell lysates were prepared and the expression level of the different fusion proteins was analyzed by immunoblot using an α-GFP antibody.</p>\n <p>\n <b>D)</b> MR100 <i>Δtpi1</i> yeast was transformed with expression plasmids encoding wild-type TPI, TPI<sub>Met1_AAG</sub> or TPI<sub>2ndATG</sub>.</p>\n <p>Afterwards, single yeast clones were selected and grown on the respective SC<sup>-leu-ura</sup> plates for 3 days at 30°C as indicated.</p></div>", "links"=>[], "tags"=>["initiation", "tpi"], "article_id"=>624864, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Evolutionary Biology"], "users"=>["Markus Ralser", "Gino Heeren", "Michael Breitenbach", "Hans Lehrach", "Sylvia Krobitsch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000030.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_An_alternative_translation_initiation_start_site_within_the_TPI_mRNA_/624864", "title"=>"An alternative translation initiation start site within the TPI mRNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:59:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/470099"], "description"=>"<div><p>Triosephosphate isomerase (TPI) deficiency is an autosomal recessive disorder caused by various mutations in the gene encoding the key glycolytic enzyme TPI. A drastic decrease in TPI activity and an increased level of its substrate, dihydroxyacetone phosphate, have been measured in unpurified cell extracts of affected individuals. These observations allowed concluding that the different mutations in the TPI alleles result in catalytically inactive enzymes. However, despite a high occurrence of TPI null alleles within several human populations, the frequency of this disorder is exceptionally rare. In order to address this apparent discrepancy, we generated a yeast model allowing us to perform comparative <em>in vivo</em> analyses of the enzymatic and functional properties of the different enzyme variants. We discovered that the majority of these variants exhibit no reduced catalytic activity per se. Instead, we observed, the dimerization behavior of TPI is influenced by the particular mutations investigated, and by the use of a potential alternative translation initiation site in the TPI gene. Additionally, we demonstrated that the overexpression of the most frequent TPI variant, Glu104Asp, which displays altered dimerization features, results in diminished endogenous TPI levels in mammalian cells. Thus, our results reveal that enzyme deregulation attributable to aberrant dimerization of TPI, rather than direct catalytic inactivation of the enzyme, underlies the pathogenesis of TPI deficiency. Finally, we discovered that yeast cells expressing a TPI variant exhibiting reduced catalytic activity are more resistant against oxidative stress caused by the thiol-oxidizing reagent diamide. This observed advantage might serve to explain the high allelic frequency of TPI null alleles detected among human populations.</p> </div>", "links"=>[], "tags"=>["triose", "phosphate", "isomerase", "deficiency", "caused", "altered", "catalytic", "mutant", "enzymes"], "article_id"=>152643, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Evolutionary Biology"], "users"=>["Markus Ralser", "Gino Heeren", "Michael Breitenbach", "Hans Lehrach", "Sylvia Krobitsch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000030", "stats"=>{"downloads"=>8, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Triose_Phosphate_Isomerase_Deficiency_Is_Caused_by_Altered_Dimerization_Not_Catalytic_Inactivity_of_the_Mutant_Enzymes/152643", "title"=>"Triose Phosphate Isomerase Deficiency Is Caused by Altered Dimerization–Not Catalytic Inactivity–of the Mutant Enzymes", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2006-12-20 00:44:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/954856"], "description"=>"<div><p>MR100 <i>Δtpi1</i> yeast cells expressing wild-type as well as the pathogenic TPI variants Cys41Tyr, Glu104Asp, Gly122Arg, Ile170Val or Phe240Leu were grown to stationary phase, serially diluted to OD<sub>600</sub> values of 3.0, 1.0, 0.3, 0.1 and spotted onto SC medium plates containing different concentrations of diamide.</p>\n <p>Sensitivity/resistance was determined by comparing the growth between the different yeast strains after incubating the plates for 3 days at 28°C.</p></div>", "links"=>[], "tags"=>["yeast", "cells", "expressing", "ile170val", "tpi", "variant", "hyperresistant"], "article_id"=>625137, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Evolutionary Biology"], "users"=>["Markus Ralser", "Gino Heeren", "Michael Breitenbach", "Hans Lehrach", "Sylvia Krobitsch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000030.g007", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MR100_tpi1_yeast_cells_expressing_the_Ile170Val_TPI_variant_are_hyperresistant_to_diamide_/625137", "title"=>"MR100 Δ<i>tpi1</i> yeast cells expressing the Ile170Val TPI variant are hyperresistant to diamide.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 13:01:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/954677"], "description"=>"<div><p>\n <b>A)</b> The yeast two-hybrid strain L40ccua was co-transformed with plasmids encoding LexA-TPI, AD, AD-TPI or AD-TPI<sub>2ndATG</sub> as indicated.</p>\n <p>Afterwards, transformants were spotted on SC media lacking tryptophan and leucine, onto SC medium lacking tryptophan, leucine, histidine and uracil, or onto nylon membrane for analyzing the activity of the three reporter genes (left panel).</p>\n <p>For quantitative analysis of the <i>lacZ</i> reporter gene activity a liquid β-galactosidase assay was performed (middle panel).</p>\n <p>Each column represents the mean value of four measurements.</p>\n <p>Error bars indicate the standard deviation.</p>\n <p>The expression level of the respective bait and prey proteins was analyzed by immunoblot analysis using antibodies against lexA or gal4AD (right panel).</p>\n <p>\n <b>B)</b> Strain L40ccua was transformed with plasmids encoding LexA-TPI and AD-TPI or LexA-TPI and the pathogenic variants AD-Cys41Tyr, AD-Glu104Asp, AD-Gly122Arg, AD-Ile170Val or AD-Phe240Leu, respectively.</p>\n <p>In <b>C)</b> plasmids encoding the LexA-Glu104Asp protein and AD-WT or LexA-Glu104Asp and the variants AD-Cys41Tyr, AD-Glu104Asp, AD-Gly122Arg, AD-Ile170Val or AD-Phe240Leu, respectively, were used.</p>\n <p>\n <i>LacZ</i> reporter gene activity in <b>B)</b> and <b>C)</b> was measured using a liquid β-galactosidase assay.</p>\n <p>\n <b>D)</b> Dimerization behavior between wild-type TPI and TPI<sub>2ndATG</sub> variants comprising the corresponding amino acid exchanges was analyzed as described before.</p>\n <p>All experiments were repeated twice using yeast cells obtained from independent transformations.</p>\n <p>The intracellular level of the various bait or the prey proteins (in B–D) was monitored by immunoblot analysis using antibodies against lexA or gal4AD.</p></div>", "links"=>[], "tags"=>["wild-type", "pathogenic", "tpi"], "article_id"=>624969, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Evolutionary Biology"], "users"=>["Markus Ralser", "Gino Heeren", "Michael Breitenbach", "Hans Lehrach", "Sylvia Krobitsch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000030.g005", "stats"=>{"downloads"=>3, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dimerization_behavior_of_wild_type_and_pathogenic_TPI_variants_/624969", "title"=>"Dimerization behavior of wild-type and pathogenic TPI variants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 13:00:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/954391"], "description"=>"<div><p>\n <b>A)</b> MR100 yeast cells (<i>Δtpi1</i>) were transformed with the various p416GPD-based expression plasmids encoding wild-type human TPI as well as the pathogenic variants Met1_AAG, Cys41Tyr, Glu104Asp, Gly122Arg, Ile170Val or Phe240Leu, respectively, and plated on minimal SC <sup>-leu-ura</sup> medium supplemented with 3% ethanol/0.1% glucose.</p>\n <p>Afterwards, single yeast clones were selected and grown as represented by the schemes on SC <sup>-leu-ura</sup> medium plates supplemented either with 2% glucose or with 3% ethanol/0.1% glucose at 30°C. <b>B)</b> MR100 <i>Δtpi1</i> yeast cells expressing wild-type TPI or the different pathogenic TPI variants were grown until logarithmic phase.</p>\n <p>Then, the same cell number of each culture was spotted as 5-fold serial dilutions onto glucose media or onto glucose media supplemented with different concentrations of lithium chloride. </p>\n <p>Plates were incubated for 3 days at 30°C and growth of the different yeast strains was analyzed.</p></div>", "links"=>[], "tags"=>["wild-type", "pathogenic", "tpi", "variants", "substitute", "yeast"], "article_id"=>624683, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Evolutionary Biology"], "users"=>["Markus Ralser", "Gino Heeren", "Michael Breitenbach", "Hans Lehrach", "Sylvia Krobitsch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000030.g002", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Human_wild_type_and_pathogenic_TPI_variants_can_substitute_for_yeast_TPI1_/624683", "title"=>"Human wild-type and pathogenic TPI variants can substitute for yeast TPI1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:58:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/954304"], "description"=>"<div><p>The pathogenic TPI variants Cys41Tyr, Glu104Asp, Gly122Arg, Ile170Val and Phe240Leu were assigned to the crystal structure of human TPI generated by Kinoshita et al <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000030#pone.0000030-Kinoshita1\" target=\"_blank\">[38]</a>; NT: amino terminus. </p>\n <p>\n <b>(Lower panel)</b> Appearance of pathogenic TPI variants among TPI deficiency patients (c.h.: compound heterozygous; n.d.: not determined).</p></div>", "links"=>[], "tags"=>["Biochemistry", "cell biology", "Evolutionary biology", "molecular biology"], "article_id"=>624593, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Evolutionary Biology"], "users"=>["Markus Ralser", "Gino Heeren", "Michael Breitenbach", "Hans Lehrach", "Sylvia Krobitsch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000030.g001", "stats"=>{"downloads"=>4, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structural_model_of_human_TPI_Upper_panel_/624593", "title"=>"Structural model of human TPI. (Upper panel)", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:57:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/954502"], "description"=>"<div><p>MR100 <i>Δtpi1</i> yeast cells expressing wild-type as well as the pathogenic TPI variants Cys41Tyr, Glu104Asp, Gly122Arg, Ile170Val or Phe240Leu were grown until the logarithmic phase and equal cell numbers were collected.</p>\n <p>Afterwards, the enzymatic assay was performed as described in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000030#s2\" target=\"_blank\">Methods</a> section.</p>\n <p>The catalytic activity of each pathogenic TPI variant was compared to the activity of the wild-type enzyme.</p>\n <p>Each column represents the mean value of multiple measurements of 4 different yeast clones.</p>\n <p>Error bars indicate standard deviation.</p></div>", "links"=>[], "tags"=>["tpi", "variants", "catalytic"], "article_id"=>624792, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Evolutionary Biology"], "users"=>["Markus Ralser", "Gino Heeren", "Michael Breitenbach", "Hans Lehrach", "Sylvia Krobitsch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000030.g003", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pathogenic_TPI_variants_display_catalytic_activity_in_vivo_/624792", "title"=>"Pathogenic TPI variants display catalytic activity <i>in vivo</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:59:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/954765"], "description"=>"<div><p>COS1 cells were transfected with pTL-Flag-TPI-WT or pTL-Flag-TPI-Glu104Asp as indicated.</p>\n <p>After 48h, lysates were prepared and analyzed by immunoblotting as described in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000030#s2\" target=\"_blank\">Methods</a> section.</p>\n <p>Loading of equal protein concentrations was demonstrated by tubulin staining (lower panel).</p>\n <p>In addition, similar levels of FLAG-tagged wild-type TPI and FLAG-tagged Glu104Asp TPI was detected in the respective cell lysates (middle panel).</p></div>", "links"=>[], "tags"=>["glu104asp", "tpi", "variant", "reduced", "endogenous"], "article_id"=>625052, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Evolutionary Biology"], "users"=>["Markus Ralser", "Gino Heeren", "Michael Breitenbach", "Hans Lehrach", "Sylvia Krobitsch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000030.g006", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overexpression_of_the_Glu104Asp_TPI_variant_results_in_a_reduced_expression_level_of_endogenous_TPI_/625052", "title"=>"Overexpression of the Glu104Asp TPI variant results in a reduced expression level of endogenous TPI.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 13:00:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/954920"], "description"=>"<div><p>Homozygous mutations within TPI affecting enzyme dimerization cause TPI deficiency, whereas homozygous mutations resulting in an inactive <i>TPI</i> allele are lethal.</p>\n <p>Compound heterozygous individuals having inherited one inactive and one allele defective in dimerization properties will develop TPI deficiency, whereas heterozygote individuals having inherited a heterozygote null allele have an evolutionary advantage. (+: wild-type TPI; −: TPI with aberrant dimerization property; 0: allele encoding no or a catalytically inactive TPI).</p></div>", "links"=>[], "tags"=>["mutations"], "article_id"=>625213, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Evolutionary Biology"], "users"=>["Markus Ralser", "Gino Heeren", "Michael Breitenbach", "Hans Lehrach", "Sylvia Krobitsch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000030.g008", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Consequences_of_mutations_within_human_TPI_/625213", "title"=>"Consequences of mutations within human TPI.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 13:02:09"}

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  • {"unique-ip"=>"15", "full-text"=>"23", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"8"}
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  • {"unique-ip"=>"19", "full-text"=>"23", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"22", "full-text"=>"22", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
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  • {"unique-ip"=>"20", "full-text"=>"25", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"14", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"17", "full-text"=>"19", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"4"}
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  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
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  • {"unique-ip"=>"26", "full-text"=>"29", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"33", "full-text"=>"34", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"31", "full-text"=>"31", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
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  • {"unique-ip"=>"24", "full-text"=>"26", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"31", "full-text"=>"31", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
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  • {"unique-ip"=>"37", "full-text"=>"41", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2018", "month"=>"10"}
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  • {"unique-ip"=>"73", "full-text"=>"82", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
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  • {"unique-ip"=>"33", "full-text"=>"39", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
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  • {"unique-ip"=>"39", "full-text"=>"44", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"63", "full-text"=>"69", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"36", "full-text"=>"38", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
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  • {"unique-ip"=>"43", "full-text"=>"50", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"40", "full-text"=>"47", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"20", "full-text"=>"24", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"10", "full-text"=>"13", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"28", "full-text"=>"25", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
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Relative Metric

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