Lhx1 Is Required for Specification of the Renal Progenitor Cell Field
Publication Date
April 15, 2011
Journal
PLOS ONE
Authors
M. Cecilia Cirio, Zhao Hui, Caroline E. Haldin, Chiara Cianciolo Cosentino, et al
Volume
6
Issue
4
Pages
e18858
DOI
https://dx.plos.org/10.1371/journal.pone.0018858
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0018858
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21526205
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3078140
Europe PMC
http://europepmc.org/abstract/MED/21526205
Web of Science
000289578600036
Scopus
79954537128
Mendeley
http://www.mendeley.com/research/lhx1-required-specification-renal-progenitor-cell-field
Events
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Mendeley | Further Information

{"title"=>"Lhx1 is required for specification of the renal progenitor cell field", "type"=>"journal", "authors"=>[{"first_name"=>"M. Cecilia", "last_name"=>"Cirio", "scopus_author_id"=>"17134396100"}, {"first_name"=>"Zhao", "last_name"=>"Hui", "scopus_author_id"=>"37122125000"}, {"first_name"=>"Caroline E.", "last_name"=>"Haldin", "scopus_author_id"=>"6508161533"}, {"first_name"=>"Chiara Cianciolo", "last_name"=>"Cosentino", "scopus_author_id"=>"36155278700"}, {"first_name"=>"Carsten", "last_name"=>"Stuckenholz", "scopus_author_id"=>"23010820900"}, {"first_name"=>"Xiongfong", "last_name"=>"Chen", "scopus_author_id"=>"57192467833"}, {"first_name"=>"Sung Kook", "last_name"=>"Hong", "scopus_author_id"=>"37030293500"}, {"first_name"=>"Igor B.", "last_name"=>"Dawid", "scopus_author_id"=>"7102048818"}, {"first_name"=>"Neil A.", "last_name"=>"Hukriede", "scopus_author_id"=>"6603306879"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"79954537128", "doi"=>"10.1371/journal.pone.0018858", "pui"=>"361627589", "scopus"=>"2-s2.0-79954537128", "issn"=>"19326203", "pmid"=>"21526205"}, "id"=>"3ca7f2e6-db92-393a-a25b-8a9af8ba0be6", "abstract"=>"In the vertebrate embryo, the kidney is derived from the intermediate mesoderm. The LIM-class homeobox transcription factor lhx1 is expressed early in the intermediate mesoderm and is one of the first genes to be expressed in the nephric mesenchyme. In this study, we investigated the role of Lhx1 in specification of the kidney field by either overexpressing or depleting lhx1 in Xenopus embryos or depleting lhx1 in an explant culture system. By overexpressing a constitutively-active form of Lhx1, we established its capacity to expand the kidney field during the specification stage of kidney organogenesis. In addition, the ability of Lhx1 to expand the kidney field diminishes as kidney organogenesis transitions to the morphogenesis stage. In a complimentary set of experiments, we determined that embryos depleted of lhx1, show an almost complete loss of the kidney field. Using an explant culture system to induce kidney tissue, we confirmed that expression of genes from both proximal and distal kidney structures is affected by the absence of lhx1. Taken together our results demonstrate an essential role for Lhx1 in driving specification of the entire kidney field from the intermediate mesoderm.", "link"=>"http://www.mendeley.com/research/lhx1-required-specification-renal-progenitor-cell-field", "reader_count"=>25, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>4, "Librarian"=>1, "Researcher"=>6, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>4, "Librarian"=>1, "Researcher"=>6, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Medicine and Dentistry"=>4, "Agricultural and Biological Sciences"=>12, "Arts and Humanities"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>1}, "Arts and Humanities"=>{"Arts and Humanities"=>1}}, "reader_count_by_country"=>{"Argentina"=>1, "United States"=>1, "Portugal"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/782773"], "description"=>"<p>Embryos were injected (1xV2) with 200 pg of LL-VP16 mRNA at the 8-cell stage. Embryos were treated with hydroxyurea and aphidicolin (HUA) at stage 10.5/11. (<b>A–D</b>) <i>In situ</i> hybridization of embryos at stage 20 for <i>pax8</i>. (<b>A</b>) Uninjected embryo. (<b>B</b>) Uninjected embryo treated with HUA. (<b>C</b>) Injected embryo. Expansion of <i>pax8</i> expression was observed in 91% of the embryos (n = 35). (<b>D</b>) Injected embryo treated with HUA. Expansion of <i>pax8</i> expression was observed in 82% of the embryos (n = 33). (<b>E–H</b>) Whole-mount immunostaining analysis of proliferation with anti-phospho-Histone H3 antibody, αPH3. (<b>E</b>) Uninjected embryo. (<b>F</b>) Uninjected embryo treated with HUA. (<b>G</b>) Injected embryo. (<b>H</b>) Injected embryo treated with HUA. (<b>I–L</b>) <i>In situ</i> hybridization of embryos for the paraxial mesoderm marker <i>myoD</i>. (<b>I, J</b>) Uninjected and injected embryos at stage 20. Reduced <i>myoD</i> expression was observed in 63% of the embryos (n = 51). (<b>K, L</b>) Control and injected sides of the same embryo at stage 26. Reduced <i>myoD</i> expression was observed in 87% of the embryos (n = 30). Anterior somites are highlighted with black brackets. (<b>M–P</b>) <i>In situ</i> hybridization of embryos for the lateral plate mesoderm marker <i>scl</i>. (<b>M, N</b>) Uninjected and injected embryos at stage 20 (n = 45). Midline of the embryos is marked with a dotted line with anterior to the left. (<b>O, P</b>) Control and injected sides of the same embryo at stage 26 (n = 43). The injected side of the embryos is marked with an asterisk.</p>", "links"=>[], "tags"=>["causes"], "article_id"=>453135, "categories"=>["Developmental Biology"], "users"=>["M. Cecilia Cirio", "Zhao Hui", "Caroline E. Haldin", "Chiara Cianciolo Cosentino", "Carsten Stuckenholz", "Xiongfong Chen", "Sung-Kook Hong", "Igor B. Dawid", "Neil A. Hukriede"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018858.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ectopic_lhx1_expression_causes_a_fate_transformation_event_/453135", "title"=>"Ectopic <i>lhx1</i> expression causes a fate transformation event.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-15 00:52:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/783039"], "description"=>"<p>Venn diagram outlining the distribution of probe sets in the three organ culture treatments. Overlap between probe sets that showed a 4-fold or greater increase in expression in AcRA treated (AcRA) vs untreated (C) explants (pink), probe sets that presented a 2-fold or greater decrease in expression on <i>lhx1-AS</i>/AcRA vs AcRA explants (blue) and probe sets which expression showed less than a 0.5-fold increase/decrease in injected (<i>lhx1-AS</i>) vs C explants were considered unaffected (green).</p>", "links"=>[], "tags"=>["developmental biology"], "article_id"=>453405, "categories"=>["Developmental Biology"], "users"=>["M. Cecilia Cirio", "Zhao Hui", "Caroline E. Haldin", "Chiara Cianciolo Cosentino", "Carsten Stuckenholz", "Xiongfong Chen", "Sung-Kook Hong", "Igor B. Dawid", "Neil A. Hukriede"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018858.g005", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Microarray_analysis_of_lhx1_depletion_in_organ_culture_/453405", "title"=>"Microarray analysis of <i>lhx1</i>-depletion in organ culture.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-15 00:56:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/782937"], "description"=>"<p>Embryos were injected (1xV2) with 300 pg of <i>ctrl-AS</i> or <i>lhx1-AS</i> at the 8-cell stage. (<b>A, D, G, J</b>) Uninjected embryos. (<b>B, E, H, K</b>) Embryos injected with <i>ctrl-AS</i>. (<b>C, F, I, L</b>) Embryos injected with <i>lhx1-AS</i>. (<b>A–C</b>) <i>In situ</i> hybridization of embryos at stage 20 for the pronephric marker <i>pax8</i>. (<b>C</b>) Reduced or absent <i>pax8</i> expression was observed in 47% and 53% of the embryos, respectively (n = 34). (<b>D–F</b>) 3G8 whole-mount immunostaining was carried out at stage 32. (<b>E</b>) Reduced 3G8 staining was observed in 5% of the embryos (n = 41). (<b>F</b>) Reduced 3G8 staining was observed in 76% of the embryos (n = 34). Insets show enlargement of 3G8 staining of the proximal tubule. (<b>G–I</b>) 4A6 whole-mount immunostaining was carried out at stage 37/38. (<b>H</b>) Reduced 4A6 staining was observed in 9% of the embryos (n = 23). (<b>I</b>) Reduced 4A6 staining was observed in 91% of the embryos (n = 34). (<b>J–L</b>) <i>In situ</i> hybridization of embryos at stage 39 for <i>β1-NaK-ATPase</i>. (<b>L</b>) Reduced <i>β1-NaK-ATPase</i> expression was observed in 72% of the embryos (n = 29). (<b>M</b>) Bar graph with the percentage embryos injected with the different doses of <i>lhx1-AS</i> that showed presence, reduction or absence of <i>pax8</i> expression at stage 20. <i>Lhx1-AS</i> 100 pg: reduced <i>pax8</i> expression was observed in 89%, absence in 4% and presence in 7% of the embryos (n = 28). <i>Lhx1-AS</i> 200 pg: reduced <i>pax8</i> expression was observed in 93% and presence in 7% of the embryos (n = 27). <i>Lhx1-AS</i> 300 pg: reduced of <i>pax8</i> expression was observed in 47% and absent in 53% of the embryos (n = 34). <i>Lhx1-AS</i> 400 pg: reduced <i>pax8</i> expression was observed in 50% and absent in 50% of the embryos (n = 42). <i>Lhx1-AS</i> 300 pg+<i>zflhx1</i> mRNA 25 pg: presence of <i>pax8</i> expression was observed in 51% of the embryos (n = 41).</p>", "links"=>[], "tags"=>["pronephric"], "article_id"=>453305, "categories"=>["Developmental Biology"], "users"=>["M. Cecilia Cirio", "Zhao Hui", "Caroline E. Haldin", "Chiara Cianciolo Cosentino", "Carsten Stuckenholz", "Xiongfong Chen", "Sung-Kook Hong", "Igor B. Dawid", "Neil A. Hukriede"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018858.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Depletion_of_lhx1_results_in_a_loss_of_the_pronephric_kidney_/453305", "title"=>"Depletion of <i>lhx1</i> results in a loss of the pronephric kidney.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-15 00:55:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/783160"], "description"=>"<p>Embryos were injected (1xV2) with 300 pg of <i>lhx1-AS</i> at the 8-cell stage. (<b>A–O</b>) <i>In situ</i> hybridization of embryos at stage 32. (<b>A–C</b>) <i>In situ</i> hybridization for <i>follistatin (fst)</i>. (<b>A</b>) Uninjected embryo. (<b>B, C</b>) Control and injected sides of the same embryo are shown. (<b>C</b>) Reduced <i>fst</i> expression was observed in 57% of the embryos (n = 44). (<b>D–F</b>) <i>In situ</i> hybridization for <i>pax2</i>. (<b>D</b>) Uninjected embryo. (<b>E, F</b>) Control and injected sides of the same embryo are shown. (<b>F</b>) Reduced <i>pax2</i> expression was observed in 86% of the embryos (n = 32). (<b>G–I</b>) <i>In situ</i> hybridization for <i>hoxb7</i>. (<b>G</b>) Uninjected embryo. (<b>H, I</b>) Control and injected sides of the same embryo are shown. (<b>I</b>) Reduced <i>hoxb7</i> expression was observed in 92% of the embryos (n = 38). (<b>J–L</b>) <i>In situ</i> hybridization for <i>laminin-β1</i>. (<b>J</b>) Uninjected embryo. (<b>K, L</b>) Control and injected sides of the same embryo are shown. (<b>L</b>) Reduced <i>laminin-β1</i> expression was observed in 94% of the embryos (n = 32). (<b>M–O</b>) <i>In situ</i> hybridization for <i>neuropilin1 (nrp1)</i>. (<b>M</b>) Uninjected embryo. (<b>N, O</b>) Control and injected sides of the same embryo are shown. (<b>O</b>) Reduced <i>nrp1</i> expression was observed in 90% of the embryos (n = 40). (<b>P–U</b>) <i>In situ</i> hybridization of embryos at stage 24 for <i>wt1</i>. (<b>P, Q</b>) Uninjected embryo. (<b>R–U</b>) Control and injected sides of the same embryo are shown. (<b>T, U</b>) Reduced <i>wt1</i> expression was observed in 89% of the embryos (n = 37). (<b>Q, S, U</b>) Transverse sections of embryos in P and R/T, respectively. Arrows indicate plane of section in appropriate panels.</p>", "links"=>[], "tags"=>["affects", "domains", "pronephric"], "article_id"=>453528, "categories"=>["Developmental Biology"], "users"=>["M. Cecilia Cirio", "Zhao Hui", "Caroline E. Haldin", "Chiara Cianciolo Cosentino", "Carsten Stuckenholz", "Xiongfong Chen", "Sung-Kook Hong", "Igor B. Dawid", "Neil A. Hukriede"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018858.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Absence_of_lhx1_affects_all_the_domains_of_the_pronephric_kidney_/453528", "title"=>"Absence of <i>lhx1</i> affects all the domains of the pronephric kidney.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-15 00:58:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/782504"], "description"=>"<p>Embryos were injected (1xV2) with 200 pg of LL-VP16 mRNA at the 8-cell stage. (<b>A–C</b>) <i>In situ</i> hybridization of embryos at stage 20 for the early pronephric marker <i>pax8</i>. (<b>A</b>) Uninjected embryo. (<b>B–C</b>) Control and injected sides of the same embryo are shown. (<b>C</b>) Expansion of <i>pax8</i> expression was observed in 83% of the embryos (n = 33). Kidney fields are highlighted with black brackets. (<b>D–I</b>) 3G8 and 4A6 whole-mount immunostaining were carried out at stages 32 and 37/38, respectively. (<b>D, G</b>) Uninjected embryos. (<b>E, F, H, I</b>) Control and injected sides of the same embryo. (<b>F, I</b>) Larger tubule epithelium with 3G8 was observed in 81% of the embryos (n = 32) and expanded intermediate and distal tubules with 4A6 were observed in 80% of the embryos (n = 30). (<b>D–F</b>) Insets show enlargements of 3G8 staining of the proximal tubule. (<b>J–M</b>) 3G8, 4A6 double whole-mount immunostaining of stage 42 embryos. (<b>K</b>) Magnification of the pronephric kidney of uninjected embryo. (<b>M</b>) Magnification of the pronephric kidney of injected embryo. (<b>N</b>) Bar graph showing the percentage of embryos injected at the different doses of LL-VP16 that showed expansion of <i>pax8</i> expression. LL-VP16 mRNA 50 pg: expansion of <i>pax8</i> expression was observed in 35% of the embryos (n = 26). LL-VP16 mRNA 100 pg: expansion of <i>pax8</i> expression was observed in 53% of the embryos (n = 30). LL-VP16 mRNA 200 pg: expansion of <i>pax8</i> expression was observed in 70% of the embryos (n = 30). LL-VP16 mRNA 300 pg: expansion of <i>pax8</i> expression was observed in 93% of the embryos (n = 27).</p>", "links"=>[], "tags"=>["induces", "pronephric"], "article_id"=>452869, "categories"=>["Developmental Biology"], "users"=>["M. Cecilia Cirio", "Zhao Hui", "Caroline E. Haldin", "Chiara Cianciolo Cosentino", "Carsten Stuckenholz", "Xiongfong Chen", "Sung-Kook Hong", "Igor B. Dawid", "Neil A. Hukriede"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018858.g001", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Over_expression_of_lhx1_induces_expansion_of_the_pronephric_kidney_/452869", "title"=>"Over-expression of <i>lhx1</i> induces expansion of the pronephric kidney.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-15 00:47:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/392905", "https://ndownloader.figshare.com/files/392951", "https://ndownloader.figshare.com/files/392991", "https://ndownloader.figshare.com/files/393016", "https://ndownloader.figshare.com/files/393038", "https://ndownloader.figshare.com/files/393070", "https://ndownloader.figshare.com/files/393102", "https://ndownloader.figshare.com/files/393135"], "description"=>"<div><p>In the vertebrate embryo, the kidney is derived from the intermediate mesoderm. The LIM-class homeobox transcription factor <em>lhx1</em> is expressed early in the intermediate mesoderm and is one of the first genes to be expressed in the nephric mesenchyme. In this study, we investigated the role of Lhx1 in specification of the kidney field by either overexpressing or depleting <em>lhx1</em> in <em>Xenopus</em> embryos or depleting <em>lhx1</em> in an explant culture system. By overexpressing a constitutively-active form of Lhx1, we established its capacity to expand the kidney field during the specification stage of kidney organogenesis. In addition, the ability of Lhx1 to expand the kidney field diminishes as kidney organogenesis transitions to the morphogenesis stage. In a complimentary set of experiments, we determined that embryos depleted of <em>lhx1</em>, show an almost complete loss of the kidney field. Using an explant culture system to induce kidney tissue, we confirmed that expression of genes from both proximal and distal kidney structures is affected by the absence of <em>lhx1</em>. Taken together our results demonstrate an essential role for Lhx1 in driving specification of the entire kidney field from the intermediate mesoderm.</p> </div>", "links"=>[], "tags"=>["lhx1", "specification", "renal", "progenitor"], "article_id"=>137590, "categories"=>["Developmental Biology"], "users"=>["M. Cecilia Cirio", "Zhao Hui", "Caroline E. Haldin", "Chiara Cianciolo Cosentino", "Carsten Stuckenholz", "Xiongfong Chen", "Sung-Kook Hong", "Igor B. Dawid", "Neil A. Hukriede"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0018858.s001", "https://dx.doi.org/10.1371/journal.pone.0018858.s002", "https://dx.doi.org/10.1371/journal.pone.0018858.s003", "https://dx.doi.org/10.1371/journal.pone.0018858.s004", "https://dx.doi.org/10.1371/journal.pone.0018858.s005", "https://dx.doi.org/10.1371/journal.pone.0018858.s006", "https://dx.doi.org/10.1371/journal.pone.0018858.s007", "https://dx.doi.org/10.1371/journal.pone.0018858.s008"], "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Lhx1_Is_Required_for_Specification_of_the_Renal_Progenitor_Cell_Field/137590", "title"=>"Lhx1 Is Required for Specification of the Renal Progenitor Cell Field", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-04-15 02:06:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/782643"], "description"=>"<p>Embryos were injected (1xV2) with 200 pg of LL-VP16-GR mRNA at the 8-cell stage. (<b>A–L</b>) <i>In situ</i> hybridization for <i>pax8</i> of embryos at stage 31, followed by MZ15 whole-mount immunostaining. (<b>A, C, E, G, I, K</b>) Uninjected embryos. (<b>B, D, F, H, J, L</b>) Injected embryos. Activation of LL-VP16-GR was controlled by addition of dexamethasone (Dex) at specified stages. Dex was added to uninjected and injected embryos at: (<b>A, B</b>) stage 10; (<b>C, D</b>) stage 12.5; (<b>E, F</b>) stage 15; (<b>G, H</b>) stage 18; (<b>I, J</b>) stage 21; (<b>K, L</b>) stage 24. (<b>M</b>) Bar graph with the percentage of injected embryos that showed expansion after Dex treatment at different stages. Expansion of <i>pax8</i> expression was observed in 53% of the embryos for stage 10 (n = 36), 56% for stage 12.5 (n = 32), 84% for stage 15 (n = 32), 79% for stage 18 (n = 34), 40% for stage 21 (n = 45) and 24% for stage 24 (n = 21).</p>", "links"=>[], "tags"=>["activation", "defines", "temporal", "kidney"], "article_id"=>453010, "categories"=>["Developmental Biology"], "users"=>["M. Cecilia Cirio", "Zhao Hui", "Caroline E. Haldin", "Chiara Cianciolo Cosentino", "Carsten Stuckenholz", "Xiongfong Chen", "Sung-Kook Hong", "Igor B. Dawid", "Neil A. Hukriede"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018858.g002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Inducible_activation_of_Lhx1_defines_a_temporal_window_of_kidney_field_expansion_/453010", "title"=>"Inducible activation of Lhx1, defines a temporal window of kidney field expansion.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-15 00:50:10"}

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  • {"unique-ip"=>"1", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"5", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"4", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
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  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
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  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"3", "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"=>"10", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"12", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"11", "full-text"=>"13", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
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Relative Metric

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