Fine Time Course Expression Analysis Identifies Cascades of Activation and Repression and Maps a Putative Regulator of Mammalian Sex Determination
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{"title"=>"Fine Time Course Expression Analysis Identifies Cascades of Activation and Repression and Maps a Putative Regulator of Mammalian Sex Determination", "type"=>"journal", "authors"=>[{"first_name"=>"Steven C.", "last_name"=>"Munger", "scopus_author_id"=>"16304855700"}, {"first_name"=>"Anirudh", "last_name"=>"Natarajan", "scopus_author_id"=>"55163003400"}, {"first_name"=>"Loren L.", "last_name"=>"Looger", "scopus_author_id"=>"6602848770"}, {"first_name"=>"Uwe", "last_name"=>"Ohler", "scopus_author_id"=>"14065036600"}, {"first_name"=>"Blanche", "last_name"=>"Capel", "scopus_author_id"=>"7003726720"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"doi"=>"10.1371/journal.pgen.1003630", "sgr"=>"84880845873", "isbn"=>"1553-7404", "pmid"=>"23874228", "issn"=>"15537390", "scopus"=>"2-s2.0-84880845873", "pui"=>"369438612"}, "id"=>"7581f9d1-7db3-322e-8d50-bb4dd2b17fe6", "abstract"=>"In vertebrates, primary sex determination refers to the decision within a bipotential organ precursor to differentiate as a testis or ovary. Bifurcation of organ fate begins between embryonic day (E) 11.0-E12.0 in mice and likely involves a dynamic transcription network that is poorly understood. To elucidate the first steps of sexual fate specification, we profiled the XX and XY gonad transcriptomes at fine granularity during this period and resolved cascades of gene activation and repression. C57BL/6J (B6) XY gonads showed a consistent ~5-hour delay in the activation of most male pathway genes and repression of female pathway genes relative to 129S1/SvImJ, which likely explains the sensitivity of the B6 strain to male-to-female sex reversal. Using this fine time course data, we predicted novel regulatory genes underlying expression QTLs (eQTLs) mapped in a previous study. To test predictions, we developed an in vitro gonad primary cell assay and optimized a lentivirus-based shRNA delivery method to silence candidate genes and quantify effects on putative targets. We provide strong evidence that Lmo4 (Lim-domain only 4) is a novel regulator of sex determination upstream of SF1 (Nr5a1), Sox9, Fgf9, and Col9a3. This approach can be readily applied to identify regulatory interactions in other systems.", "link"=>"http://www.mendeley.com/research/fine-time-course-expression-analysis-identifies-cascades-activation-repression-maps-putative-regulat", "reader_count"=>71, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Librarian"=>1, "Researcher"=>22, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>4, "Student > Master"=>8, "Other"=>4, "Student > Bachelor"=>7, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Librarian"=>1, "Researcher"=>22, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>4, "Student > Master"=>8, "Other"=>4, "Student > Bachelor"=>7, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>15, "Agricultural and Biological Sciences"=>38, "Medicine and Dentistry"=>5, "Philosophy"=>1, "Neuroscience"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1, "Social Sciences"=>1, "Computer Science"=>4, "Energy"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Energy"=>{"Energy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>38}, "Computer Science"=>{"Computer Science"=>4}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>15}, "Unspecified"=>{"Unspecified"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"United States"=>2, "China"=>1, "United Kingdom"=>1, "Slovenia"=>1, "Germany"=>1, "Spain"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1117267"], "description"=>"<p>Fold differences between XY and XX gonads at each time point in both strains were calculated for all probes passing the ANOVA filtering step. This data was then used to initialize and train the Hidden Markov Model (HMM) (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003630#s4\" target=\"_blank\">Materials and Methods</a>). The most probable (Viterbi) state path reflects possible dimorphic expression patterns between XX and XY gonads and was used to cluster genes. Heatmaps illustrate 3 clusters with state paths indicated by circles at the top of each heatmap.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "microarrays", "systems biology", "developmental biology", "Organism development", "organogenesis", "Cell differentiation", "Cell fate determination", "genetics", "Heredity", "Quantitative traits", "Trait locus", "Genome expression analysis", "Model organisms", "Animal models", "mouse", "markov", "patterns", "dimorphic", "gonad"], "article_id"=>744300, "categories"=>["Biological Sciences"], "users"=>["Steven C. Munger", "Anirudh Natarajan", "Loren L. Looger", "Uwe Ohler", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003630.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_Hidden_Markov_Model_HMM_to_identify_patterns_of_dimorphic_expression_in_the_gonad_transcriptome_/744300", "title"=>"A Hidden Markov Model (HMM) to identify patterns of dimorphic expression in the gonad transcriptome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 02:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117264"], "description"=>"<p>(A) Experimental design. Total transcript abundance was profiled in XX and XY gonads at six equally spaced intervals between E11.0–E12.0 capturing the critical transition in the gonad transcriptome from a bipotential to sexually-differentiated state. The analysis was conducted in two inbred strains, C57Bl/6J (B6) and 129S1/SvImJ (129S1), with well-characterized differences in their sensitivity to sex reversal. By including XX gonads and multiple time points in the analysis, the current study expands on an earlier strain comparison of B6 and 129S1 gonads at E11.5 <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003630#pgen.1003630-Munger1\" target=\"_blank\">[1]</a>. (B) Analysis of Variance (ANOVA) results. Nearly half of the probes on the array (n = 12,213), representing more than half of all genes (n = 9,254, shown in gray), were expressed above background levels at one or more time points between E11.0–E12.0 in XY or XX gonad samples. For a large proportion of expressed probes (n = 5,659), variation in gonad transcript abundance was significantly associated with additive effects from sex, developmental stage, and/or strain. A sex-by-stage interaction effect accounted for a significant proportion of the expression variation in 733 probes. (C) For many probes, variation in expression is driven by more than one experimental variable. A Venn diagram showing probes whose expression is affected by one or more of the additive effects of sex, stage, and strain. Values within each circle correspond to the number of probes that are significantly affected by that variable. Note that the overlaps in the Venn diagram do not capture interaction effects, but represent probes that are significantly affected by two or all three factors. For example, the 469 probes in the center region all exhibit variation in expression that can be attributed to differences in sex, stage, and strain independently, but not necessarily a sex*stage*strain effect (as occurs for 11 probes in the Anova analysis).</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "microarrays", "systems biology", "developmental biology", "Organism development", "organogenesis", "Cell differentiation", "Cell fate determination", "genetics", "Heredity", "Quantitative traits", "Trait locus", "Genome expression analysis", "Model organisms", "Animal models", "mouse", "gonad", "transcriptome", "24-hour", "encompassing"], "article_id"=>744297, "categories"=>["Biological Sciences"], "users"=>["Steven C. Munger", "Anirudh Natarajan", "Loren L. Looger", "Uwe Ohler", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003630.g001", "stats"=>{"downloads"=>1, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Time_course_analysis_of_the_gonad_transcriptome_during_the_24_hour_period_encompassing_sex_determination_/744297", "title"=>"Time course analysis of the gonad transcriptome during the 24-hour period encompassing sex determination.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 02:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117276", "https://ndownloader.figshare.com/files/1117277", "https://ndownloader.figshare.com/files/1117278", "https://ndownloader.figshare.com/files/1117281", "https://ndownloader.figshare.com/files/1117283", "https://ndownloader.figshare.com/files/1117286", "https://ndownloader.figshare.com/files/1117287", "https://ndownloader.figshare.com/files/1117288", "https://ndownloader.figshare.com/files/1117289", "https://ndownloader.figshare.com/files/1117292", "https://ndownloader.figshare.com/files/1117293", "https://ndownloader.figshare.com/files/1117295", "https://ndownloader.figshare.com/files/1117296", "https://ndownloader.figshare.com/files/1117298", "https://ndownloader.figshare.com/files/1117300"], "description"=>"<div><p>In vertebrates, primary sex determination refers to the decision within a bipotential organ precursor to differentiate as a testis or ovary. Bifurcation of organ fate begins between embryonic day (E) 11.0–E12.0 in mice and likely involves a dynamic transcription network that is poorly understood. To elucidate the first steps of sexual fate specification, we profiled the XX and XY gonad transcriptomes at fine granularity during this period and resolved cascades of gene activation and repression. C57BL/6J (B6) XY gonads showed a consistent ∼5-hour delay in the activation of most male pathway genes and repression of female pathway genes relative to 129S1/SvImJ, which likely explains the sensitivity of the B6 strain to male-to-female sex reversal. Using this fine time course data, we predicted novel regulatory genes underlying expression QTLs (eQTLs) mapped in a previous study. To test predictions, we developed an <i>in vitro</i> gonad primary cell assay and optimized a lentivirus-based shRNA delivery method to silence candidate genes and quantify effects on putative targets. We provide strong evidence that <i>Lmo4</i> (Lim-domain only 4) is a novel regulator of sex determination upstream of <i>SF1 (Nr5a1)</i>, <i>Sox9</i>, <i>Fgf9</i>, and <i>Col9a3</i>. This approach can be readily applied to identify regulatory interactions in other systems.</p></div>", "links"=>[], "tags"=>["Computational biology", "genomics", "microarrays", "systems biology", "developmental biology", "Organism development", "organogenesis", "Cell differentiation", "Cell fate determination", "genetics", "Heredity", "Quantitative traits", "Trait locus", "Genome expression analysis", "Model organisms", "Animal models", "mouse", "identifies", "cascades", "activation", "repression", "maps", "putative", "mammalian"], "article_id"=>744309, "categories"=>["Biological Sciences"], "users"=>["Steven C. Munger", "Anirudh Natarajan", "Loren L. Looger", "Uwe Ohler", "Blanche Capel"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003630.s001", "https://dx.doi.org/10.1371/journal.pgen.1003630.s002", "https://dx.doi.org/10.1371/journal.pgen.1003630.s003", "https://dx.doi.org/10.1371/journal.pgen.1003630.s004", "https://dx.doi.org/10.1371/journal.pgen.1003630.s005", "https://dx.doi.org/10.1371/journal.pgen.1003630.s006", "https://dx.doi.org/10.1371/journal.pgen.1003630.s007", "https://dx.doi.org/10.1371/journal.pgen.1003630.s008", "https://dx.doi.org/10.1371/journal.pgen.1003630.s009", "https://dx.doi.org/10.1371/journal.pgen.1003630.s010", "https://dx.doi.org/10.1371/journal.pgen.1003630.s011", "https://dx.doi.org/10.1371/journal.pgen.1003630.s012", "https://dx.doi.org/10.1371/journal.pgen.1003630.s013", "https://dx.doi.org/10.1371/journal.pgen.1003630.s014", "https://dx.doi.org/10.1371/journal.pgen.1003630.s015"], "stats"=>{"downloads"=>18, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fine_Time_Course_Expression_Analysis_Identifies_Cascades_of_Activation_and_Repression_and_Maps_a_Putative_Regulator_of_Mammalian_Sex_Determination_/744309", "title"=>"Fine Time Course Expression Analysis Identifies Cascades of Activation and Repression and Maps a Putative Regulator of Mammalian Sex Determination", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-07-11 02:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117271"], "description"=>"<p>(A) Expression of male- (top panel) and female-enriched (bottom panel) genes. Dimorphic expression for these genes is delayed by ∼5 hours in B6 compared to 129S1. (B) Heatmap showing dimorphic expression at E11.6 in 129S1 and comparison of same genes in B6. While a few genes show earlier dimorphic expression in B6 mice compared to 129S1, the dominant pattern shows a ∼5 hr delay between B6 and 129S1 mice. (C) Matrix showing the time of onset of dimorphism in 129S1 and B6 mice for male-enriched (top panel) and female-enriched (bottom panel) genes. For example, out of the 32 male-enriched probes that became dimorphically expressed at E11.4 in 129S1, 9 probes were also dimorphically expressed starting at E11.4 in B6 while 18 showed dimorphic expression starting at E11.6 in B6 mice. However, 4 genes are dimorphic in B6 XY gonads at E11.4, but not in 129S1 until E11.6. * indicates significant overlap with p<0.001 evaluated by a hypergeometric test. The highlighted diagonals show the number of genes showing similar onset of dimorphism in 129S1 and B6 mice. Note that some genes that are male- or female-enriched in one strain do not show dimorphism in the other strain.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "microarrays", "systems biology", "developmental biology", "Organism development", "organogenesis", "Cell differentiation", "Cell fate determination", "genetics", "Heredity", "Quantitative traits", "Trait locus", "Genome expression analysis", "Model organisms", "Animal models", "mouse", "male-", "female-enriched", "genes", "b6", "delayed", "compared", "129s1"], "article_id"=>744304, "categories"=>["Biological Sciences"], "users"=>["Steven C. Munger", "Anirudh Natarajan", "Loren L. Looger", "Uwe Ohler", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003630.g005", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dimorphic_expression_of_multiple_male_and_female_enriched_genes_in_B6_is_delayed_compared_to_129S1_mice_/744304", "title"=>"Dimorphic expression of multiple male- and female-enriched genes in B6 is delayed compared to 129S1 mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 02:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117269"], "description"=>"<p>(A) Examples of genes showing higher expression in XY (male-enriched genes, top panel) and XX gonads (female-enriched genes, bottom panel) from 129S1 mice. Blue and red vertical lines show the time point when dimorphic expression is significant. (B) Cascades of dimorphic gene expression identified by the HMM in XY (top panel) and XX gonads (bottom panel). Colors indicate the log fold change between XY and XX gonads at a specific time point for the 129S1 strain. The genes are arranged in order of time of onset of dimorphic expression. (C) Contribution to changes in expression between E12.0 and the time point before the onset of dimorphism are shown for each gene in (B) in XY (column 1) and XX (column 2) gonads. Top panel: male-enriched genes. Bottom panel: female-enriched genes. This analysis shows that male-enriched genes are mostly up-regulated in XY gonads while female-enriched genes are mostly down-regulated in XY gonads.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "microarrays", "systems biology", "developmental biology", "Organism development", "organogenesis", "Cell differentiation", "Cell fate determination", "genetics", "Heredity", "Quantitative traits", "Trait locus", "Genome expression analysis", "Model organisms", "Animal models", "mouse", "dimorphic", "involving", "activation", "repression", "xy"], "article_id"=>744302, "categories"=>["Biological Sciences"], "users"=>["Steven C. Munger", "Anirudh Natarajan", "Loren L. Looger", "Uwe Ohler", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003630.g004", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cascades_of_dimorphic_expression_involving_both_activation_and_repression_in_XY_gonads_/744302", "title"=>"Cascades of dimorphic expression involving both activation and repression in XY gonads.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 02:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117265"], "description"=>"<p>Gene expression in XY and XX gonads was compared at the beginning and end of the 24-hour developmental window. For probes that exhibited a 1.5-fold or greater change in expression in either sex between E11.0 and E12.0, log of the Fold Change in the XY gonad is plotted on the Y-axis, and log of the Fold Change in the XX gonad is plotted on the X-axis. Probes that are similarly up-regulated or down-regulated in both sexes appear in gray in the upper right and lower left quadrants, respectively. Probes that become enriched in XY gonads relative to XX are shown in blue, while genes that become enriched in XX gonads relative to XX are shown in red. Examples from each category are highlighted, and their expression patterns in XY (blue line) and XX (red line) gonads are displayed. From this perspective, it is clear that enrichment in one sex is achieved by activation, repression, or both regulatory mechanisms.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "microarrays", "systems biology", "developmental biology", "Organism development", "organogenesis", "Cell differentiation", "Cell fate determination", "genetics", "Heredity", "Quantitative traits", "Trait locus", "Genome expression analysis", "Model organisms", "Animal models", "mouse", "xx", "xy", "gonads"], "article_id"=>744298, "categories"=>["Biological Sciences"], "users"=>["Steven C. Munger", "Anirudh Natarajan", "Loren L. Looger", "Uwe Ohler", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003630.g002", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_XX_and_XY_gonads_contribute_to_expression_fold_change_between_E11_0_and_E12_0_/744298", "title"=>"Changes in XX and XY gonads contribute to expression fold change between E11.0 and E12.0.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 02:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117274"], "description"=>"<p>Strain differences in temporal gene expression are informative for predicting regulatory genes underlying trans-band eQTLs. Multiple criteria were established to identify the best candidate genes in the trans-band eQTLs mapped in Munger et al. <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003630#pgen.1003630-Munger1\" target=\"_blank\">[1]</a>. First, the putative regulatory gene must be expressed above background at or before E11.5 to exert any effects on downstream target genes. Genes implicated in the list of target genes that exhibited a sexually-dimorphic expression pattern consistent with the sexual differentiation pathway (male or female) were prioritized. Genes that met both of the above criteria, and exhibited strain expression differences (either in overall levels of transcript abundance or in timing of onset of sexual dimorphism) in a pattern consistent with the observed allelic effects for that eQTL, were prioritized as the highest candidates. A few eQTLs harbor genes in which abnormal sex determination phenotypes have been noted in the null mutant mouse, and these genes were given similar high priority. Using these criteria, confidence intervals containing 60–526 protein coding genes were narrowed down to eight or fewer high priority candidates.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "microarrays", "systems biology", "developmental biology", "Organism development", "organogenesis", "Cell differentiation", "Cell fate determination", "genetics", "Heredity", "Quantitative traits", "Trait locus", "Genome expression analysis", "Model organisms", "Animal models", "mouse", "genes", "trans-band", "eqtls"], "article_id"=>744307, "categories"=>["Biological Sciences"], "users"=>["Steven C. Munger", "Anirudh Natarajan", "Loren L. Looger", "Uwe Ohler", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003630.t001", "stats"=>{"downloads"=>3, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_candidate_genes_in_prominent_trans_band_eQTLs_based_on_dynamic_expression_patterns_/744307", "title"=>"Identification of candidate genes in prominent trans-band eQTLs based on dynamic expression patterns.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-07-11 02:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117273"], "description"=>"<p>(A) <i>Lmo4</i> exhibits an expression pattern indicative of a role in sex determination and consistent with expectations for a gene underlying a strain eQTL regulating early sex determination and male pathway genes. It is expressed at similar levels in XY and XX gonads before E11.6, becomes enriched in XY gonads as early as E11.6 in both strains, and shows reduced expression levels in B6 (dashed lines), consistent with the observed allelic effects of the Chromosome 3 eQTL. (B) E12.5 XY gonads were dissected free of the mesonephroi, pooled by sex, dissociated into single cell suspensions, plated on tissue culture plates at t = 0 with lentiviral particles containing shRNA targeted to the candidate gene of interest, and cultured for 72 hours. Quantitative RT-PCR was conducted to assay expression of predicted targets. (C) Lentiviral shRNA-mediated knockdown of Lmo4 in cultured XY primary gonadal cells resulted in the consistent down-regulation of multiple Chromosome 3 eQTL target genes relative to the nontargeting control (gray bar) using two different shRNA hairpins targeting Lmo4 (light/medium blue bars in graph). Expression was normalized to the housekeeping gene <i>Gapdh</i>. Both male pathway genes, <i>Fgf9</i> and <i>Col9a3</i>, were significantly down-regulated following Lmo4 knockdown with both clones. Similarly, one of the putative targets with a role in early gonadogenesis, <i>SF1/Nr5a1</i>, was significantly reduced, however expression of the other gene involved in early gonadogenesis, <i>Wt1</i>, was not significantly affected by <i>Lmo4</i> knockdown. The important male pathway regulator <i>Sox9</i> was found to be significantly down-regulated as a result of <i>Lmo4</i> knockdown. <i>Canx</i> (a second normalization gene not predicted to be a target of LMO4) showed no difference in expression compared to the control. Error bars show minimum and maximum expression. Significance was calculated by comparing control and data across all independent runs.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "microarrays", "systems biology", "developmental biology", "Organism development", "organogenesis", "Cell differentiation", "Cell fate determination", "genetics", "Heredity", "Quantitative traits", "Trait locus", "Genome expression analysis", "Model organisms", "Animal models", "mouse", "fetal"], "article_id"=>744306, "categories"=>["Biological Sciences"], "users"=>["Steven C. Munger", "Anirudh Natarajan", "Loren L. Looger", "Uwe Ohler", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003630.g006", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Validation_of_Lmo4_as_a_novel_regulator_of_gene_expression_in_the_fetal_gonad_/744306", "title"=>"Validation of <i>Lmo4</i> as a novel regulator of gene expression in the fetal gonad.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 02:47:42"}

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Relative Metric

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