A Regulatory Hierarchy Controls the Dynamic Transcriptional Response to Extreme Oxidative Stress in Archaea
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{"title"=>"A Regulatory Hierarchy Controls the Dynamic Transcriptional Response to Extreme Oxidative Stress in Archaea", "type"=>"journal", "authors"=>[{"first_name"=>"Peter D.", "last_name"=>"Tonner", "scopus_author_id"=>"56543020300"}, {"first_name"=>"Adrianne M C", "last_name"=>"Pittman", "scopus_author_id"=>"36847180800"}, {"first_name"=>"Jordan G.", "last_name"=>"Gulli", "scopus_author_id"=>"56543744100"}, {"first_name"=>"Kriti", "last_name"=>"Sharma", "scopus_author_id"=>"51764701900"}, {"first_name"=>"Amy K.", "last_name"=>"Schmid", "scopus_author_id"=>"8633642100"}], "year"=>2015, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"602890480", "sgr"=>"84924371175", "issn"=>"15537404", "pmid"=>"25569531", "scopus"=>"2-s2.0-84924371175", "doi"=>"10.1371/journal.pgen.1004912", "isbn"=>"1553-7390"}, "id"=>"ebe0f04f-5ed4-36d5-836e-90b854fc4540", "abstract"=>"Networks of interacting transcription factors are central to the regulation of cellular responses to abiotic stress. Although the architecture of many such networks has been mapped, their dynamic function remains unclear. Here we address this challenge in archaea, microorganisms possessing transcription factors that resemble those of both eukaryotes and bacteria. Using genome-wide DNA binding location analysis integrated with gene expression and cell physiological data, we demonstrate that a bacterial-type transcription factor (TF), called RosR, and five TFIIB proteins, homologs of eukaryotic TFs, combinatorially regulate over 100 target genes important for the response to extremely high levels of peroxide. These genes include 20 other transcription factors and oxidative damage repair genes. RosR promoter occupancy is surprisingly dynamic, with the pattern of target gene expression during the transition from rapid growth to stress correlating strongly with the pattern of dynamic binding. We conclude that a hierarchical regulatory network orchestrated by TFs of hybrid lineage enables dynamic response and survival under extreme stress in archaea. This raises questions regarding the evolutionary trajectory of gene networks in response to stress.", "link"=>"http://www.mendeley.com/research/regulatory-hierarchy-controls-dynamic-transcriptional-response-extreme-oxidative-stress-archaea", "reader_count"=>39, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>4, "Other"=>1, "Student > Master"=>3, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>4, "Other"=>1, "Student > Master"=>3, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Unspecified"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>17, "Agricultural and Biological Sciences"=>15, "Neuroscience"=>1, "Computer Science"=>1, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Neuroscience"=>{"Neuroscience"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>15}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>17}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>1}}, "group_count"=>6}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1863497"], "description"=>"<p>(A) The number of RosR-bound loci is plotted as a function of the number of different TFIIB (Tfb) proteins bound in combination. (B) Overlap between the number of sites co-bound by RosR and each Tfb protein. B, TfbB (VNG0734G, red ellipse); F, TfbF (VNG0315G, green ellipse); G, TfbG (VNG254G, blue ellipse); D, TfbD (VNG0869G, orange ellipse). <i>P</i>-values are given in the legend for significant enrichment in co-binding relative to total genome-wide RosR binding sites. Data for co-bound sites are listed in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen.1004912.s004\" target=\"_blank\">S4 Table</a>, including TfbA data, which was omitted from the figure for clarity given the small number of co-bound RosR-TfbA sites. (C) Gene network of RosR and Tfb coordinate control of other TF-encoding genes. Tfb designations and colors are as in (B). Arrows represent activation, bars represent repression. Each edge in the network is based on both gene expression and ChIP-chip or ChIP-seq data (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen.1004912.s002\" target=\"_blank\">S2 Table</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen.1004912-Seitzer1\" target=\"_blank\">[32]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen.1004912-Facciotti1\" target=\"_blank\">[33]</a>). (D) Comparison of RosR activity (GE-ChIP correlation) with the distance between RosR and Tfb binding loci. The negative log10 <i>p</i>-value of the significance of this comparison is given on the y-axis, and the absolute value of the distance cutoff is given on the X-axis. These correlations in the parent strain (black lines) are compared to the correlation in the Δ<i>rosR</i> mutant (grey lines) and random data with the same mean and standard deviation as the actual distribution at each distance cutoff (dark grey dotted lines).</p>", "links"=>[], "tags"=>["oxidative damage repair genes", "Regulatory Hierarchy Controls", "tfiib", "dna", "RosR promoter occupancy", "tf", "transcription factors", "response", "stress", "target gene expression", "Dynamic Transcriptional Response", "Extreme Oxidative Stress", "100 target genes"], "article_id"=>1286720, "categories"=>["Biological Sciences"], "users"=>["Peter D. Tonner", "Adrianne M. C. Pittman", "Jordan G. Gulli", "Kriti Sharma", "Amy K. Schmid"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004912.g006", "stats"=>{"downloads"=>0, "page_views"=>43, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Combinatorial_control_of_gene_expression_by_TFIIB_proteins_and_RosR_/1286720", "title"=>"Combinatorial control of gene expression by TFIIB proteins and RosR.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:38:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1863495"], "description"=>"<p>(A) Consensus sequence logo for the motif. Cis-regulatory sequences that make up this logo are listed in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen.1004912.s005\" target=\"_blank\">S5 Table</a>. Information content in bits is shown on the y-axis and the residue position is given on the x-axis. (B) Position of predicted cis-regulatory sequence and ChIP-chip hits relative to start codon of genes for which a motif was detected (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen.1004912.s005\" target=\"_blank\">S5 Table</a>). The vertical blue line indicates the average position of the binding location. The red line indicates the average position of the cis-regulatory sequence (18 bp from ATG). (C) Experimental validation of cis-regulatory motif sequence. Negative control (-) empty vector and positive control (+) with a strong constitutive promoter driving GFP expression are shown as a comparison to promoter activities of interest in each of the parent (grey bars) and Δ<i>rosR</i> (red bars) strains grown in the absence of stress. Error bars represent the standard error of the mean (minimum n = 12, at least five independent biological replicate measurements, each with 2–4 technical replicates). Filled circle within brackets represents t-test <i>p</i><0.05, open circle <i>p</i><0.01.</p>", "links"=>[], "tags"=>["oxidative damage repair genes", "Regulatory Hierarchy Controls", "tfiib", "dna", "RosR promoter occupancy", "tf", "transcription factors", "response", "stress", "target gene expression", "Dynamic Transcriptional Response", "Extreme Oxidative Stress", "100 target genes"], "article_id"=>1286718, "categories"=>["Biological Sciences"], "users"=>["Peter D. Tonner", "Adrianne M. C. Pittman", "Jordan G. Gulli", "Kriti Sharma", "Amy K. Schmid"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004912.g004", "stats"=>{"downloads"=>0, "page_views"=>37, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RosR_binds_to_an_imperfect_palindromic_cis_regulatory_sequence_/1286718", "title"=>"RosR binds to an imperfect palindromic cis-regulatory sequence.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:38:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1863492"], "description"=>"<p>(A) RosR binding peaks are plotted across the genome as a function of binding intensity. Locations of peak centers across the main chromosome are represented as vertical lines colored according to time point (see legend). Binding peak locations for the two megaplasmids are listed in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen.1004912.s002\" target=\"_blank\">S2 Table</a>. (B) Zoom-in of selected binding regions. For each binding site shown, vertical lines represent average enrichment intensity at the binding site predicted from the bootstrapped noise estimation fits to the raw data. Surrounding curves represent model fits to the raw data. Colors for each time point are as in (A). Peaks with solid lines in each region represent those binding sites that pass statistical filtering criteria (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#s4\" target=\"_blank\">Methods</a>); peaks with dotted lines do not. Gene strand designations are shown in the legend. Identification numbers or names are given for those genes immediately neighboring the binding sites.</p>", "links"=>[], "tags"=>["oxidative damage repair genes", "Regulatory Hierarchy Controls", "tfiib", "dna", "RosR promoter occupancy", "tf", "transcription factors", "response", "stress", "target gene expression", "Dynamic Transcriptional Response", "Extreme Oxidative Stress", "100 target genes"], "article_id"=>1286715, "categories"=>["Biological Sciences"], "users"=>["Peter D. Tonner", "Adrianne M. C. Pittman", "Jordan G. Gulli", "Kriti Sharma", "Amy K. Schmid"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004912.g001", "stats"=>{"downloads"=>0, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RosR_binds_to_DNA_dynamically_throughout_the_genome_in_response_to_H_2_O_2_/1286715", "title"=>"RosR binds to DNA dynamically throughout the genome in response to H<sub>2</sub>O<sub>2</sub>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:38:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1863500", "https://ndownloader.figshare.com/files/1863501", "https://ndownloader.figshare.com/files/1863502", "https://ndownloader.figshare.com/files/1863503", "https://ndownloader.figshare.com/files/1863504", "https://ndownloader.figshare.com/files/1863505"], "description"=>"<div><p>Networks of interacting transcription factors are central to the regulation of cellular responses to abiotic stress. Although the architecture of many such networks has been mapped, their dynamic function remains unclear. Here we address this challenge in archaea, microorganisms possessing transcription factors that resemble those of both eukaryotes and bacteria. Using genome-wide DNA binding location analysis integrated with gene expression and cell physiological data, we demonstrate that a bacterial-type transcription factor (TF), called RosR, and five TFIIB proteins, homologs of eukaryotic TFs, combinatorially regulate over 100 target genes important for the response to extremely high levels of peroxide. These genes include 20 other transcription factors and oxidative damage repair genes. RosR promoter occupancy is surprisingly dynamic, with the pattern of target gene expression during the transition from rapid growth to stress correlating strongly with the pattern of dynamic binding. We conclude that a hierarchical regulatory network orchestrated by TFs of hybrid lineage enables dynamic response and survival under extreme stress in archaea. This raises questions regarding the evolutionary trajectory of gene networks in response to stress.</p></div>", "links"=>[], "tags"=>["oxidative damage repair genes", "Regulatory Hierarchy Controls", "tfiib", "dna", "RosR promoter occupancy", "tf", "transcription factors", "response", "stress", "target gene expression", "Dynamic Transcriptional Response", "Extreme Oxidative Stress", "100 target genes"], "article_id"=>1286723, "categories"=>["Biological Sciences"], "users"=>["Peter D. Tonner", "Adrianne M. C. Pittman", "Jordan G. Gulli", "Kriti Sharma", "Amy K. Schmid"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004912.s001", "https://dx.doi.org/10.1371/journal.pgen.1004912.s002", "https://dx.doi.org/10.1371/journal.pgen.1004912.s003", "https://dx.doi.org/10.1371/journal.pgen.1004912.s004", "https://dx.doi.org/10.1371/journal.pgen.1004912.s005", "https://dx.doi.org/10.1371/journal.pgen.1004912.s006"], "stats"=>{"downloads"=>10, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_Regulatory_Hierarchy_Controls_the_Dynamic_Transcriptional_Response_to_Extreme_Oxidative_Stress_in_Archaea_/1286723", "title"=>"A Regulatory Hierarchy Controls the Dynamic Transcriptional Response to Extreme Oxidative Stress in Archaea", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-01-08 03:38:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1863499"], "description"=>"<p>*TFs contain a cis-regulatory sequence, RosR activated (A) or repressed (R) according to ChIP-GE correlations.</p><p>**VNG0751C promoter contains an additional cis sequence. See <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen.1004912.s005\" target=\"_blank\">S5 Table</a> for additional sequence.</p><p>TFs regulated by RosR.</p>", "links"=>[], "tags"=>["oxidative damage repair genes", "Regulatory Hierarchy Controls", "tfiib", "dna", "RosR promoter occupancy", "tf", "transcription factors", "response", "stress", "target gene expression", "Dynamic Transcriptional Response", "Extreme Oxidative Stress", "100 target genes"], "article_id"=>1286722, "categories"=>["Biological Sciences"], "users"=>["Peter D. Tonner", "Adrianne M. C. Pittman", "Jordan G. Gulli", "Kriti Sharma", "Amy K. Schmid"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004912.t002", "stats"=>{"downloads"=>0, "page_views"=>32, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TFs_regulated_by_RosR_/1286722", "title"=>"TFs regulated by RosR.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-01-08 03:38:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1863494"], "description"=>"<p>(A) Plots compare gene expression (pink lines) of genes nearby binding locations (grey lines) for RosR. Bolded red lines represent the mean gene expression profile in each cluster; bolded black lines represent the mean ChIP-chip binding profile. Data are mean and variance scaled. Genes with correlated gene expression and binding profiles during H<sub>2</sub>O<sub>2</sub> stress are shown on the left (C<sub>S</sub>≥0.6; “A” clusters), anticorrelations right (C<sub>S</sub>≤−0.6; “B” clusters). The cluster designations correspond to clusters shown in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen-1004912-g002\" target=\"_blank\">Fig. 2</a> and number of genes in each cluster (a subset of those in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen-1004912-g002\" target=\"_blank\">Fig. 2</a>) is indicated in the upper right corner of each graph. (B) GE-ChIP correlations trend significantly toward 0 when gene expression in the Δ<i>rosR</i> mutant background is compared to ChIP-chip profiles. Data from the same genes as in (A) make up the box plot distributions. P-values shown result from <i>t</i>-tests comparing distributions of parent to Δ<i>rosR</i> correlations (left) or anticorrelations (right).</p>", "links"=>[], "tags"=>["oxidative damage repair genes", "Regulatory Hierarchy Controls", "tfiib", "dna", "RosR promoter occupancy", "tf", "transcription factors", "response", "stress", "target gene expression", "Dynamic Transcriptional Response", "Extreme Oxidative Stress", "100 target genes"], "article_id"=>1286717, "categories"=>["Biological Sciences"], "users"=>["Peter D. Tonner", "Adrianne M. C. Pittman", "Jordan G. Gulli", "Kriti Sharma", "Amy K. Schmid"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004912.g003", "stats"=>{"downloads"=>0, "page_views"=>35, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RosR_is_a_bifunctional_regulator_and_a_large_fraction_of_hits_result_in_functional_effects_on_gene_expression_/1286717", "title"=>"RosR is a bifunctional regulator and a large fraction of hits result in functional effects on gene expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:38:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1863493"], "description"=>"<p>(A) Each boxplot displays the distribution of binding enrichment across promoters in each of the four clusters. In cluster 1 (top left), RosR disengages from DNA in the presence of H<sub>2</sub>O<sub>2</sub> and remains unbound for the duration of the time course. In cluster 2 (top right), RosR is released from DNA during H<sub>2</sub>O<sub>2</sub> stress but re-binds within 60 minutes. In cluster 3 (bottom left), RosR binds to DNA during H<sub>2</sub>O<sub>2</sub> stress. In cluster 4, RosR binding is dynamic and variable across the time course (bottom right). The number of genes in each cluster is indicated in the upper right corner of each boxplot. Upper and lower box borders represent the first and third quartiles, respectively. Whiskers represent the interquartile range. Black bar represents the median. Colors represent time points as in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen-1004912-g001\" target=\"_blank\">Fig. 1</a>. (B) ChIP-qPCR validation data are shown for representative promoter regions for cluster 2 (left, <i>VNG0180G</i>) and cluster 3 (right, <i>VNG1732C- VNG1734H-VNG1735C</i> operon). Error bars represent the standard error from the mean of 9 replicate samples.</p>", "links"=>[], "tags"=>["oxidative damage repair genes", "Regulatory Hierarchy Controls", "tfiib", "dna", "RosR promoter occupancy", "tf", "transcription factors", "response", "stress", "target gene expression", "Dynamic Transcriptional Response", "Extreme Oxidative Stress", "100 target genes"], "article_id"=>1286716, "categories"=>["Biological Sciences"], "users"=>["Peter D. Tonner", "Adrianne M. C. Pittman", "Jordan G. Gulli", "Kriti Sharma", "Amy K. Schmid"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004912.g002", "stats"=>{"downloads"=>0, "page_views"=>33, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RosR_occupies_different_promoters_with_four_types_of_dynamic_patterns_in_response_to_H_2_O_2_/1286716", "title"=>"RosR occupies different promoters with four types of dynamic patterns in response to H<sub>2</sub>O<sub>2</sub>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:38:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1863498"], "description"=>"<p>Enrichment of RosR-bound targets in arCOG categories.</p>", "links"=>[], "tags"=>["oxidative damage repair genes", "Regulatory Hierarchy Controls", "tfiib", "dna", "RosR promoter occupancy", "tf", "transcription factors", "response", "stress", "target gene expression", "Dynamic Transcriptional Response", "Extreme Oxidative Stress", "100 target genes"], "article_id"=>1286721, "categories"=>["Biological Sciences"], "users"=>["Peter D. Tonner", "Adrianne M. C. Pittman", "Jordan G. Gulli", "Kriti Sharma", "Amy K. Schmid"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004912.t001", "stats"=>{"downloads"=>1, "page_views"=>43, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Enrichment_of_RosR_bound_targets_in_arCOG_categories_/1286721", "title"=>"Enrichment of RosR-bound targets in arCOG categories.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-01-08 03:38:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1863496"], "description"=>"<p>(A) Comparison of binding and gene expression profiles of the seven of 21 TFs with cis-regulatory sequences and strong repression by RosR. Mean expression profiles are shown for TF-coding genes expressed in the early wave (red) and late wave (blue) in response to RosR binding dynamics (black lines, binding profiles for each of the 16 sites is shown). y-axis represents mean and variance scaled ChIP-chip and expression data. All expression and ChIP-chip data for these TFs are given in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen.1004912.s002\" target=\"_blank\">S2 Table</a>. (B) RosR dynamic regulation of TFs has functional consequences. Growth rate ratios for two strains deleted of TF-coding genes (Δ<i>VNG0194H</i> and Δ<i>hrg</i>) as well as <i>VNG0194H</i> and <i>hrg</i> complemented <i>in trans</i> on a plasmid are shown. Asterisks indicate <i>p</i>-value <0.05 in t-test comparisons of growth ratios between each mutant and the parent strain. Growth rates of complemented strains are not significantly different from that of the Δ<i>ura3</i> parent strain. Raw growth data are given in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen.1004912.s006\" target=\"_blank\">S6 Table</a>. Annotations for the strongly RosR-regulated TFs with cis-regulatory sequences are listed in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen-1004912-t002\" target=\"_blank\">Table 2</a>, with all 21 RosR-regulated TFs listed in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004912#pgen.1004912.s003\" target=\"_blank\">S3 Table</a>.</p>", "links"=>[], "tags"=>["oxidative damage repair genes", "Regulatory Hierarchy Controls", "tfiib", "dna", "RosR promoter occupancy", "tf", "transcription factors", "response", "stress", "target gene expression", "Dynamic Transcriptional Response", "Extreme Oxidative Stress", "100 target genes"], "article_id"=>1286719, "categories"=>["Biological Sciences"], "users"=>["Peter D. Tonner", "Adrianne M. C. Pittman", "Jordan G. Gulli", "Kriti Sharma", "Amy K. Schmid"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004912.g005", "stats"=>{"downloads"=>0, "page_views"=>42, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dynamic_RosR_regulation_of_other_TFs_has_functional_consequences_during_ROS_stress_/1286719", "title"=>"Dynamic RosR regulation of other TFs has functional consequences during ROS stress.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:38:45"}

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Relative Metric

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