Genome-Wide Mapping of Collier In Vivo Binding Sites Highlights Its Hierarchical Position in Different Transcription Regulatory Networks
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{"title"=>"Genome-wide mapping of Collier in vivo binding sites highlights its hierarchical position in different transcription regulatory networks", "type"=>"journal", "authors"=>[{"first_name"=>"Mathilde", "last_name"=>"De Taffin", "scopus_author_id"=>"54894575700"}, {"first_name"=>"Yannick", "last_name"=>"Carrier", "scopus_author_id"=>"56184056100"}, {"first_name"=>"Laurence", "last_name"=>"Dubois", "scopus_author_id"=>"7102611126"}, {"first_name"=>"Laetitia", "last_name"=>"Bataillé", "scopus_author_id"=>"6603187792"}, {"first_name"=>"Anaïs", "last_name"=>"Painset", "scopus_author_id"=>"56850338600"}, {"first_name"=>"Stéphanie", "last_name"=>"Le Gras", "scopus_author_id"=>"36450980800"}, {"first_name"=>"Bernard", "last_name"=>"Jost", "scopus_author_id"=>"7102126721"}, {"first_name"=>"Michèle", "last_name"=>"Crozatier", "scopus_author_id"=>"6603633150"}, {"first_name"=>"Alain", "last_name"=>"Vincent", "scopus_author_id"=>"7201634560"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "isbn"=>"10.1371/journal.pone.0133387", "doi"=>"10.1371/journal.pone.0133387", "pui"=>"606006471", "sgr"=>"84941790081", "pmid"=>"26204530", "scopus"=>"2-s2.0-84941790081"}, "id"=>"fe3505f7-5b21-3778-a1a5-75ae16bf1dc9", "abstract"=>"Collier, the single Drosophila COE (Collier/EBF/Olf-1) transcription factor, is required in several developmental processes, including head patterning and specification of muscle and neuron identity during embryogenesis. To identify direct Collier (Col) targets in different cell types, we used ChIP-seq to map Col binding sites throughout the genome, at mid-embryogenesis. In vivo Col binding peaks were associated to 415 potential direct target genes. Gene Ontology analysis revealed a strong enrichment in proteins with DNA binding and/or transcription-regulatory properties. Characterization of a selection of candidates, using transgenic CRM-reporter assays, identified direct Col targets in dorso-lateral somatic muscles and specific neuron types in the central nervous system. These data brought new evidence that Col direct control of the expression of the transcription regulators apterous and eyes-absent (eya) is critical to specifying neuronal identities. They also showed that cross-regulation between col and eya in muscle progenitor cells is required for specification of muscle identity, revealing a new parallel between the myogenic regulatory networks operating in Drosophila and vertebrates. Col regulation of eya, both in specific muscle and neuronal lineages, may illustrate one mechanism behind the evolutionary diversification of Col biological roles.", "link"=>"http://www.mendeley.com/research/genomewide-mapping-collier-vivo-binding-sites-highlights-hierarchical-position-different-transcripti", "reader_count"=>19, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>1, "Researcher"=>3, "Student > Ph. D. Student"=>9, "Student > Master"=>1, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>1, "Researcher"=>3, "Student > Ph. D. Student"=>9, "Student > Master"=>1, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>14, "Neuroscience"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Neuroscience"=>{"Neuroscience"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}}, "reader_count_by_country"=>{"Japan"=>1, "France"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2187732", "https://ndownloader.figshare.com/files/2187733", "https://ndownloader.figshare.com/files/2187734", "https://ndownloader.figshare.com/files/2187735", "https://ndownloader.figshare.com/files/2187736", "https://ndownloader.figshare.com/files/2187738", "https://ndownloader.figshare.com/files/2187739", "https://ndownloader.figshare.com/files/2187740", "https://ndownloader.figshare.com/files/2187741", "https://ndownloader.figshare.com/files/2187742"], "description"=>"<div><p>Collier, the single <i>Drosophila</i> COE (Collier/EBF/Olf-1) transcription factor, is required in several developmental processes, including head patterning and specification of muscle and neuron identity during embryogenesis. To identify direct Collier (Col) targets in different cell types, we used ChIP-seq to map Col binding sites throughout the genome, at mid-embryogenesis. <i>In vivo</i> Col binding peaks were associated to 415 potential direct target genes. Gene Ontology analysis revealed a strong enrichment in proteins with DNA binding and/or transcription-regulatory properties. Characterization of a selection of candidates, using transgenic CRM-reporter assays, identified direct Col targets in dorso-lateral somatic muscles and specific neuron types in the central nervous system. These data brought new evidence that Col direct control of the expression of the transcription regulators <i>apterous</i> and <i>eyes-absent</i> (<i>eya</i>) is critical to specifying neuronal identities. They also showed that cross-regulation between <i>col </i>and <i>eya</i> in muscle progenitor cells is required for specification of muscle identity, revealing a new parallel between the myogenic regulatory networks operating in <i>Drosophila</i> and vertebrates. Col regulation of <i>eya</i>, both in specific muscle and neuronal lineages, may illustrate one mechanism behind the evolutionary diversification of Col biological roles.</p></div>", "links"=>[], "tags"=>["Drosophila COE", "Different Transcription Regulatory Networks Collier", "gene ontology analysis", "Col regulation", "target genes", "vivo Col binding peaks", "head patterning", "Col targets", "Vivo Binding Sites Highlights", "neuron identity", "Hierarchical Position", "map Col binding sites", "eya", "neuron types", "DNA binding", "transcription regulators apterous", "muscle progenitor cells", "cell types", "muscle identity"], "article_id"=>1492717, "categories"=>["Biological Sciences"], "users"=>["Mathilde de Taffin", "Yannick Carrier", "Laurence Dubois", "Laetitia Bataillé", "Anaïs Painset", "Stéphanie Le Gras", "Bernard Jost", "Michèle Crozatier", "Alain Vincent"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0133387.s001", "https://dx.doi.org/10.1371/journal.pone.0133387.s002", "https://dx.doi.org/10.1371/journal.pone.0133387.s003", "https://dx.doi.org/10.1371/journal.pone.0133387.s004", "https://dx.doi.org/10.1371/journal.pone.0133387.s005", "https://dx.doi.org/10.1371/journal.pone.0133387.s006", "https://dx.doi.org/10.1371/journal.pone.0133387.s007", "https://dx.doi.org/10.1371/journal.pone.0133387.s008", "https://dx.doi.org/10.1371/journal.pone.0133387.s009", "https://dx.doi.org/10.1371/journal.pone.0133387.s010"], "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Genome_Wide_Mapping_of_Collier_In_Vivo_Binding_Sites_Highlights_Its_Hierarchical_Position_in_Different_Transcription_Regulatory_Networks/1492717", "title"=>"Genome-Wide Mapping of Collier <i>In Vivo</i> Binding Sites Highlights Its Hierarchical Position in Different Transcription Regulatory Networks", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-07-23 02:57:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/2187717"], "description"=>"<p>n.d.: not detected</p><p>Candidate Col direct targets and linked CRMs.</p>", "links"=>[], "tags"=>["Drosophila COE", "Different Transcription Regulatory Networks Collier", "gene ontology analysis", "Col regulation", "target genes", "vivo Col binding peaks", "head patterning", "Col targets", "Vivo Binding Sites Highlights", "neuron identity", "Hierarchical Position", "map Col binding sites", "eya", "neuron types", "DNA binding", "transcription regulators apterous", "muscle progenitor cells", "cell types", "muscle identity"], "article_id"=>1492702, "categories"=>["Biological Sciences"], "users"=>["Mathilde de Taffin", "Yannick Carrier", "Laurence Dubois", "Laetitia Bataillé", "Anaïs Painset", "Stéphanie Le Gras", "Bernard Jost", "Michèle Crozatier", "Alain Vincent"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0133387.t001", "stats"=>{"downloads"=>1, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Candidate_Col_direct_targets_and_linked_CRMs_/1492702", "title"=>"Candidate Col direct targets and linked CRMs.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-07-23 02:57:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/2187714"], "description"=>"<p>(A) <i>eya_</i>Col (GFP) expression in the DA3 muscle (arrows) in stage 15 embryos, is not detected for <i>eya_</i>Col<sup>mut</sup> (B). (C-E) Triple staining of st11 wt (C), <i>+;col</i><sup><i>eCRM</i></sup><i>-lacZ</i> (D) and <i>col</i><sup><i>1</i></sup><i>;col</i><sup><i>eCRM</i></sup><i>-lacZ</i> (E) embryos for Nau (blue), <i>eya</i> transcripts (red), and either Col (C) or β-galactosidase (D,E) (green), shows co-expression of Col, <i>col</i><sup>e-CRM</sup>-LacZ, Nau and <i>eya</i> in DL muscle PCs (white arrow). (C’-E’) only Nau and <i>eya</i> stainings are shown. <i>eya</i> transcription is specifically lost in DL PCs in <i>col</i><sup><i>1</i></sup> mutant embryos (E,E’); dorso-lateral view of the T2 and T3 segments is shown. (F) Schematic drawing of the dorsal, dorso-lateral and lateral transverse muscles in a stage 16 wt embryo, with the DA3 muscle in red and the LL1 muscle indicated by an arrow. (G, H) Staining of stage 16 wt (G) and (H), <i>eya</i><sup><i>cIi-IID</i></sup><i>/Df(2L)BSC354</i> (null) mutant embryos for Col (red) and β3-tubuliin (green). Lateral view of 3 segments. In absence of <i>eya</i>, Col expression is lost in most segments, the LL1 muscle is missing (white arrow) and the DA3 muscle (asterisk) malformed. White brackets indicate dorsal, unaffected muscles while the lateral transverse and ventral muscles (yellow brackets) are moderately affected. (I-J) Col immunostaining of st.16 wt (I), and (J) <i>eya</i> mutant embryos, showing the loss of Col muscle expression in most segments (see also G, H), in <i>eya</i> mutants. (K, L) promuscular Col expression, early stage 11, is reduced in <i>eya</i> mutant embryos (L), compared to wt (K).</p>", "links"=>[], "tags"=>["Drosophila COE", "Different Transcription Regulatory Networks Collier", "gene ontology analysis", "Col regulation", "target genes", "vivo Col binding peaks", "head patterning", "Col targets", "Vivo Binding Sites Highlights", "neuron identity", "Hierarchical Position", "map Col binding sites", "eya", "neuron types", "DNA binding", "transcription regulators apterous", "muscle progenitor cells", "cell types", "muscle identity"], "article_id"=>1492699, "categories"=>["Biological Sciences"], "users"=>["Mathilde de Taffin", "Yannick Carrier", "Laurence Dubois", "Laetitia Bataillé", "Anaïs Painset", "Stéphanie Le Gras", "Bernard Jost", "Michèle Crozatier", "Alain Vincent"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0133387.g005", "stats"=>{"downloads"=>0, "page_views"=>38, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cross_regulation_between_eya_and_col_is_required_to_specify_dorso_lateral_muscles_/1492699", "title"=>"Cross-regulation between <i>eya</i> and <i>col</i> is required to specify dorso-lateral muscles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-23 02:57:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/2187699"], "description"=>"<p>(A) Annotation of the Col peak in <i>cnc</i>, adapted from <i>Gene Browser</i> (GEO submission GSE67805). 39,5 kb of <i>cnc</i> genomic region are shown (Chr3R: 19.009.000–19.048.500) with the Flybase gene annotation indicated by bars (transcribed regions) and intervening blue lines (introns). Black arrows indicate the direction of transcription of <i>cnc</i> and <i>fuzzy onions</i> (<i>fzo</i>), <i>inwardly rectifying potassium channel 1</i> (<i>Irk1</i>). The <i>cnc</i> transcripts coding for the protein isoforms CncA and CncB are indicated. ChIP-seq data for Col (green) substracted from HA (mock) data (red) are shown on the bottom. The Col Dam-ID binding regions [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0133387#pone.0133387.ref059\" target=\"_blank\">59</a>] are indicated by yellow bars, top line. The summit of the ChIP-Col peak identified by SISSRs and position of the Col binding site(s) identified by MEME are indicated by blue and violet lines, respectively; the position of <i>cnc_</i>Col is represented by a black box; scale is indicated. (B-D) Ventral anterior views of stage 11 embryos. (B) Overlap between <i>cnc_</i>Col (GFP, green) and Col (red) expression in the HL (white arrow). (C) <i>cnc_</i>Col and (D) <i>cnc_</i>Col<sup>mut</sup> mRNA expression, showing down-regulation of <i>cnc_</i>Col<sup>mut</sup> in the mandibular segment (open arrow). (E,F) <i>Ama</i>_Col, (G,H) <i>Ama</i>_Col<sup>mut</sup> expression in stage 10 (E,G) and 11 (F,H) embryos. HL <i>Ama</i>_Col expression (arrow) is lost in <i>Ama</i>_Col<sup>mut</sup> (open arrow). (I, J) Overlap between <i>Ama</i> (red), Col (blue), and <i>col</i>2.6–0.9moeGFP (green) expression in the HL (white arrow) in stage 11 wt (I), and <i>col</i><sup><i>1</i></sup> mutant embryos (J). Separate signals for <i>Ama</i>, GFP (I, J) and Col (inset in I, left panel) are shown in black and white. <i>Ama</i> expression is specifically lost in the HL in <i>col</i><sup><i>1</i></sup> mutants. The asterisk in C, D, F, H, J indicates <i>Ama</i> and <i>cnc</i> expression independent on Col.</p>", "links"=>[], "tags"=>["Drosophila COE", "Different Transcription Regulatory Networks Collier", "gene ontology analysis", "Col regulation", "target genes", "vivo Col binding peaks", "head patterning", "Col targets", "Vivo Binding Sites Highlights", "neuron identity", "Hierarchical Position", "map Col binding sites", "eya", "neuron types", "DNA binding", "transcription regulators apterous", "muscle progenitor cells", "cell types", "muscle identity"], "article_id"=>1492684, "categories"=>["Biological Sciences"], "users"=>["Mathilde de Taffin", "Yannick Carrier", "Laurence Dubois", "Laetitia Bataillé", "Anaïs Painset", "Stéphanie Le Gras", "Bernard Jost", "Michèle Crozatier", "Alain Vincent"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0133387.g002", "stats"=>{"downloads"=>0, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Col_control_of_cnc_and_Ama_expression_in_the_head_/1492684", "title"=>"Col control of <i>cnc</i> and <i>Ama</i> expression in the head.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-23 02:57:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/2187694"], "description"=>"<p>(A) Col expression in stage 12 and stage 14 embryos, lateral view. In this and all subsequent figures, embryos are oriented anterior to the left. HL: hypopharyngeal lobe; PCs: dorso-lateral muscle progenitors; vnc: ventral nerve chord; lg: lymph gland; md: class IV multidendritic neuron. (B) Fold enrichment distribution of the 559 Col ChIP peaks selected using SISSRs. (C) Single most enriched sequence motif identified by MEME analysis in the 559 Col binding peaks. (D) Graphical representation of the position of Col-binding motifs relative to the center of Col binding peaks. The axis gives the number of motifs in each cluster. (E) GO clusters enriched in putative Col direct target genes. The p-Value of the top two clusters is given in brackets.</p>", "links"=>[], "tags"=>["Drosophila COE", "Different Transcription Regulatory Networks Collier", "gene ontology analysis", "Col regulation", "target genes", "vivo Col binding peaks", "head patterning", "Col targets", "Vivo Binding Sites Highlights", "neuron identity", "Hierarchical Position", "map Col binding sites", "eya", "neuron types", "DNA binding", "transcription regulators apterous", "muscle progenitor cells", "cell types", "muscle identity"], "article_id"=>1492681, "categories"=>["Biological Sciences"], "users"=>["Mathilde de Taffin", "Yannick Carrier", "Laurence Dubois", "Laetitia Bataillé", "Anaïs Painset", "Stéphanie Le Gras", "Bernard Jost", "Michèle Crozatier", "Alain Vincent"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0133387.g001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genome_wide_mapping_of_Col_binding_sites_/1492681", "title"=>"Genome-wide mapping of Col binding sites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-23 02:57:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/2187704"], "description"=>"<p>(A) Annotation of the Col peak in <i>ap</i>, same representation as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0133387#pone.0133387.g002\" target=\"_blank\">Fig 2A</a>; 35.8 kb of the <i>ap</i> genomic region are shown (Chr2R: 1.593.000–1.628.800); the previously described apC enhancer is represented by a blue box. (B) <i>ap</i>_Col (GFP) expression in the dAp (yellow arrow) and Tv1-Tv4 neurons (white arrow) in stage 15 embryos, ventral view. (C) <i>ap</i>_Col<sup>mut</sup> expression is severely reduced in dAP neurons and Tv neurons. (D,D’) Close up view of 4 segments of stage 16 embryos, showing the specific overlap between Col (red) and <i>ap</i>_Col (green) in the Tv1 and dAp neurons. (E) all Tv neurons express <i>ap</i>_Col and Eya. (F,G) <i>ap_</i>Col<sup>mut</sup> expression is lost in dAp and strongly reduced in Tv neurons.</p>", "links"=>[], "tags"=>["Drosophila COE", "Different Transcription Regulatory Networks Collier", "gene ontology analysis", "Col regulation", "target genes", "vivo Col binding peaks", "head patterning", "Col targets", "Vivo Binding Sites Highlights", "neuron identity", "Hierarchical Position", "map Col binding sites", "eya", "neuron types", "DNA binding", "transcription regulators apterous", "muscle progenitor cells", "cell types", "muscle identity"], "article_id"=>1492689, "categories"=>["Biological Sciences"], "users"=>["Mathilde de Taffin", "Yannick Carrier", "Laurence Dubois", "Laetitia Bataillé", "Anaïs Painset", "Stéphanie Le Gras", "Bernard Jost", "Michèle Crozatier", "Alain Vincent"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0133387.g003", "stats"=>{"downloads"=>0, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Col_direct_control_of_ap_expression_in_Ap_neurons_/1492689", "title"=>"Col direct control of <i>ap</i> expression in Ap neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-23 02:57:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/2187716"], "description"=>"<p>Col directly controls <i>ap</i>_Col and <i>eya</i>_Col CRM activity in the Tv and dAP neurons and <i>eya</i>_Col and <i>col</i>_Col CRM in the DA3 muscle lineage. The two Col binding sites in <i>eya</i>_Col CRM are not functionally equivalent (double arrow). <i>eya</i> and <i>col</i> cross-regulate each other in the DA3 PC. Control of <i>DopR</i> and <i>Nplp1</i> expression in Tv and dAP neurons (Baumgardt et al., 2007) could be indirect.</p>", "links"=>[], "tags"=>["Drosophila COE", "Different Transcription Regulatory Networks Collier", "gene ontology analysis", "Col regulation", "target genes", "vivo Col binding peaks", "head patterning", "Col targets", "Vivo Binding Sites Highlights", "neuron identity", "Hierarchical Position", "map Col binding sites", "eya", "neuron types", "DNA binding", "transcription regulators apterous", "muscle progenitor cells", "cell types", "muscle identity"], "article_id"=>1492701, "categories"=>["Biological Sciences"], "users"=>["Mathilde de Taffin", "Yannick Carrier", "Laurence Dubois", "Laetitia Bataillé", "Anaïs Painset", "Stéphanie Le Gras", "Bernard Jost", "Michèle Crozatier", "Alain Vincent"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0133387.g006", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Scheme_for_Col_direct_regulation_of_ap_and_eya_in_specific_neuron_and_muscle_lineages_/1492701", "title"=>"Scheme for Col direct regulation of <i>ap</i> and <i>eya</i> in specific neuron and muscle lineages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-23 02:57:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/2187710"], "description"=>"<p>(A) Annotation of the Col peaks in <i>eya</i>, same representation as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0133387#pone.0133387.g002\" target=\"_blank\">Fig 2A</a>; 24 kb of the <i>eya</i> genomic region are shown (Chr2L: 6.524.500–6.548.500); the summits of the two ChIP-Col peaks are numbered 1 and 2. (B, C) <i>eya_</i>Col (GFP) expression in the dAp (yellow arrow) and Tv1-Tv4 neurons (white arrow) in stage 16 embryos, ventral view. (C) Close up view of abdominal segments, showing the specific overlap between Col (red) and <i>eya_</i>Col (green) in the dAp (yellow arrow) and Tv1 neurons (white arrow). (D, E) <i>eya_</i>Col<sup>mut</sup> expression is lost in dAP neurons and reduced in TV neurons. (F, G) Mutation of the Col binding site 2 (G), but not site 1 (F) eliminates <i>eya_</i>Col (RFP) expression in dAp neurons (yellow arrow).</p>", "links"=>[], "tags"=>["Drosophila COE", "Different Transcription Regulatory Networks Collier", "gene ontology analysis", "Col regulation", "target genes", "vivo Col binding peaks", "head patterning", "Col targets", "Vivo Binding Sites Highlights", "neuron identity", "Hierarchical Position", "map Col binding sites", "eya", "neuron types", "DNA binding", "transcription regulators apterous", "muscle progenitor cells", "cell types", "muscle identity"], "article_id"=>1492695, "categories"=>["Biological Sciences"], "users"=>["Mathilde de Taffin", "Yannick Carrier", "Laurence Dubois", "Laetitia Bataillé", "Anaïs Painset", "Stéphanie Le Gras", "Bernard Jost", "Michèle Crozatier", "Alain Vincent"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0133387.g004", "stats"=>{"downloads"=>0, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Col_direct_control_of_eya_expression_in_Ap_neurons_/1492695", "title"=>"Col direct control of <i>eya</i> expression in Ap neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-23 02:57:32"}

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  • {"unique-ip"=>"8", "full-text"=>"11", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"26", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"10", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"25", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"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"=>"6"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"2", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"5", "pdf"=>"5", "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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