Regulation of Clock-Controlled Genes in Mammals
Publication Date
March 16, 2009
Journal
PLOS ONE
Authors
Katarzyna Bozek, Angela Relógio, Szymon M. Kielbasa, Markus Heine, et al
Volume
4
Issue
3
Pages
e4882
DOI
https://dx.plos.org/10.1371/journal.pone.0004882
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0004882
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/19287494
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2654074
Europe PMC
http://europepmc.org/abstract/MED/19287494
Web of Science
000265496400021
Scopus
62849114200
Mendeley
http://www.mendeley.com/research/regulation-clockcontrolled-genes-mammals
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Mendeley | Further Information

{"title"=>"Regulation of clock-controlled genes in mammals", "type"=>"journal", "authors"=>[{"first_name"=>"Katarzyna", "last_name"=>"Bozek", "scopus_author_id"=>"24485444200"}, {"first_name"=>"Angela", "last_name"=>"Relógio", "scopus_author_id"=>"26421739400"}, {"first_name"=>"Szymon M.", "last_name"=>"Kielbasa", "scopus_author_id"=>"6603496867"}, {"first_name"=>"Markus", "last_name"=>"Heine", "scopus_author_id"=>"35579500600"}, {"first_name"=>"Christof", "last_name"=>"Dame", "scopus_author_id"=>"6701405383"}, {"first_name"=>"Achim", "last_name"=>"Kramer", "scopus_author_id"=>"26642995900"}, {"first_name"=>"Hanspeter", "last_name"=>"Herzel", "scopus_author_id"=>"7006726820"}], "year"=>2009, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"62849114200", "doi"=>"10.1371/journal.pone.0004882", "pui"=>"354352437", "pmid"=>"19287494", "scopus"=>"2-s2.0-62849114200", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "arxiv"=>"1203.2655"}, "id"=>"d7fe7e05-cfa8-38bc-8464-ae734a163d6a", "abstract"=>"The complexity of tissue- and day time-specific regulation of thousands of clock-controlled genes (CCGs) suggests that many regulatory mechanisms contribute to the transcriptional output of the circadian clock. We aim to predict these mechanisms using a large scale promoter analysis of CCGs.\\n\\nOur study is based on a meta-analysis of DNA-array data from rodent tissues. We searched in the promoter regions of 2065 CCGs for highly overrepresented transcription factor binding sites. In order to compensate the relatively high GC-content of CCG promoters, a novel background model to avoid a bias towards GC-rich motifs was employed. We found that many of the transcription factors with overrepresented binding sites in CCG promoters exhibit themselves circadian rhythms. Among the predicted factors are known regulators such as CLOCK∶BMAL1, DBP, HLF, E4BP4, CREB, RORα and the recently described regulators HSF1, STAT3, SP1 and HNF-4α. As additional promising candidates of circadian transcriptional regulators PAX-4, C/EBP, EVI-1, IRF, E2F, AP-1, HIF-1 and NF-Y were identified. Moreover, GC-rich motifs (SP1, EGR, ZF5, AP-2, WT1, NRF-1) and AT-rich motifs (MEF-2, HMGIY, HNF-1, OCT-1) are significantly overrepresented in promoter regions of CCGs. Putative tissue-specific binding sites such as HNF-3 for liver, NKX2.5 for heart or Myogenin for skeletal muscle were found. The regulation of the erythropoietin (Epo) gene was analysed, which exhibits many binding sites for circadian regulators. We provide experimental evidence for its circadian regulated expression in the adult murine kidney. Basing on a comprehensive literature search we integrate our predictions into a regulatory network of core clock and clock-controlled genes. Our large scale analysis of the CCG promoters reveals the complexity and extensiveness of the circadian regulation in mammals. Results of this study point to connections of the circadian clock to other functional systems including metabolism, endocrine regulation and pharmacokinetics.", "link"=>"http://www.mendeley.com/research/regulation-clockcontrolled-genes-mammals", "reader_count"=>122, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>13, "Student > Doctoral Student"=>8, "Researcher"=>35, "Student > Ph. D. Student"=>38, "Student > Postgraduate"=>3, "Student > Master"=>9, "Student > Bachelor"=>5, "Lecturer"=>4, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>13, "Student > Doctoral Student"=>8, "Researcher"=>35, "Student > Ph. D. Student"=>38, "Student > Postgraduate"=>3, "Student > Master"=>9, "Student > Bachelor"=>5, "Lecturer"=>4, "Professor"=>5}, "reader_count_by_subject_area"=>{"Unspecified"=>7, "Engineering"=>2, "Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>79, "Medicine and Dentistry"=>16, "Neuroscience"=>3, "Business, Management and Accounting"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Physics and Astronomy"=>1, "Chemistry"=>1, "Computer Science"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>16}, "Neuroscience"=>{"Neuroscience"=>3}, "Chemistry"=>{"Chemistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>79}, "Computer Science"=>{"Computer Science"=>2}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>7}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Argentina"=>1, "Czech Republic"=>1, "South Korea"=>1, "United States"=>2, "China"=>1, "Italy"=>2, "United Kingdom"=>2, "Chile"=>2}, "group_count"=>1}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/447833", "https://ndownloader.figshare.com/files/447899", "https://ndownloader.figshare.com/files/447936", "https://ndownloader.figshare.com/files/447976", "https://ndownloader.figshare.com/files/448007", "https://ndownloader.figshare.com/files/448081", "https://ndownloader.figshare.com/files/448181"], "description"=>"<div><p>The complexity of tissue- and day time-specific regulation of thousands of clock-controlled genes (CCGs) suggests that many regulatory mechanisms contribute to the transcriptional output of the circadian clock. We aim to predict these mechanisms using a large scale promoter analysis of CCGs.</p><p>Our study is based on a meta-analysis of DNA-array data from rodent tissues. We searched in the promoter regions of 2065 CCGs for highly overrepresented transcription factor binding sites. In order to compensate the relatively high GC-content of CCG promoters, a novel background model to avoid a bias towards GC-rich motifs was employed. We found that many of the transcription factors with overrepresented binding sites in CCG promoters exhibit themselves circadian rhythms. Among the predicted factors are known regulators such as CLOCK∶BMAL1, DBP, HLF, E4BP4, CREB, RORα and the recently described regulators HSF1, STAT3, SP1 and HNF-4α. As additional promising candidates of circadian transcriptional regulators PAX-4, C/EBP, EVI-1, IRF, E2F, AP-1, HIF-1 and NF-Y were identified. Moreover, GC-rich motifs (SP1, EGR, ZF5, AP-2, WT1, NRF-1) and AT-rich motifs (MEF-2, HMGIY, HNF-1, OCT-1) are significantly overrepresented in promoter regions of CCGs. Putative tissue-specific binding sites such as HNF-3 for liver, NKX2.5 for heart or Myogenin for skeletal muscle were found. The regulation of the erythropoietin (<em>Epo</em>) gene was analysed, which exhibits many binding sites for circadian regulators. We provide experimental evidence for its circadian regulated expression in the adult murine kidney. Basing on a comprehensive literature search we integrate our predictions into a regulatory network of core clock and clock-controlled genes. Our large scale analysis of the CCG promoters reveals the complexity and extensiveness of the circadian regulation in mammals. Results of this study point to connections of the circadian clock to other functional systems including metabolism, endocrine regulation and pharmacokinetics.</p></div>", "links"=>[], "tags"=>["clock-controlled", "genes", "mammals"], "article_id"=>148251, "categories"=>["Biological Sciences", "Genetics", "Cancer"], "users"=>["Katarzyna Bozek", "Angela Relógio", "Szymon M. Kielbasa", "Markus Heine", "Christof Dame", "Achim Kramer", "Hanspeter Herzel"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0004882.s001", "https://dx.doi.org/10.1371/journal.pone.0004882.s002", "https://dx.doi.org/10.1371/journal.pone.0004882.s003", "https://dx.doi.org/10.1371/journal.pone.0004882.s004", "https://dx.doi.org/10.1371/journal.pone.0004882.s005", "https://dx.doi.org/10.1371/journal.pone.0004882.s006", "https://dx.doi.org/10.1371/journal.pone.0004882.s007"], "stats"=>{"downloads"=>6, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Regulation_of_Clock_Controlled_Genes_in_Mammals/148251", "title"=>"Regulation of Clock-Controlled Genes in Mammals", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-03-16 02:17:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/904672"], "description"=>"<p>The data collection consisted of a CCG study search, meta-analysis of the genes and promoter sequence collection. The meta-analysis allowed hierarchical separation of the gene list into subsets of genes expressed in 4 different tissues (heart, liver, SCN, skeletal muscle) and within each tissue into genes with the peak of circadian expression falling into 1 of 4 defined time intervals. Together with the full list of genes and a subset of genes robustly oscillating, those 22 lists were used in a TFBS overrepresentation search. The total number of predicted sites in a promoter set of interest was compared to the mean number of predictions in an iteratively sampled background promoter set (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0004882#s4\" target=\"_blank\">Materials and Methods</a>). Z-score has been used as a measure of a motif overrepresentation.</p>", "links"=>[], "tags"=>["Computational biology", "computational biology/sequence motif analysis", "genetics and genomics/animal genetics", "genetics and genomics/gene function"], "article_id"=>575125, "categories"=>["Biological Sciences", "Genetics", "Virology"], "users"=>["Katarzyna Bozek", "Angela Relógio", "Szymon M. Kielbasa", "Markus Heine", "Christof Dame", "Achim Kramer", "Hanspeter Herzel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004882.g001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sequential_procedure_of_our_study_/575125", "title"=>"Sequential procedure of our study.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-16 01:25:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/905035"], "description"=>"<p>(A) Quantitative PCR analysis of circadian <i>Epo</i> and <i>Per2</i> mRNA expression in the adult murine kidney over a time period of 24 hours after release in constant darkness and normoxia. <i>Epo</i> mRNA (filled circles) and Per2 (open circles) mRNA transcript levels were normalized to Gapdh mRNA levels. Values are given as means±SD. (B) Analysis of the activity of a reporter gene construct harboring the 5′ promoter, first intron and 3′ enhancer of the human <i>Epo</i> gene (upper panel) or an E-Box reporter construct (lower panel) both co-transfected with Clock or Bmal1 alone or combined in human neuronal precursor (SH-SY5Y) cells. As positive control for the <i>Epo</i> reporter activation cells were also co-transfected with a HIF-1α expression plasmid (upper panel). A renilla luciferase vector was used for the normalization of transfection efficiencies. Values are shown as means±SD of three independent experiments, each performed in duplicate.</p>", "links"=>[], "tags"=>["circadian"], "article_id"=>575494, "categories"=>["Biological Sciences", "Genetics", "Virology"], "users"=>["Katarzyna Bozek", "Angela Relógio", "Szymon M. Kielbasa", "Markus Heine", "Christof Dame", "Achim Kramer", "Hanspeter Herzel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004882.g005", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_circadian_regulation_of_Epo_/575494", "title"=>"Analysis of circadian regulation of <i>Epo</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-16 01:31:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/905282"], "description"=>"<p>Numbers of genes in each group are indicated in parentheses. Phases are defined relative to <i>Per2</i> expression peak.</p>", "links"=>[], "tags"=>["overrepresented", "tissue-", "phase-specific"], "article_id"=>575729, "categories"=>["Biological Sciences", "Genetics", "Virology"], "users"=>["Katarzyna Bozek", "Angela Relógio", "Szymon M. Kielbasa", "Markus Heine", "Christof Dame", "Achim Kramer", "Hanspeter Herzel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004882.t002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Motifs_overrepresented_in_tissue_and_phase_specific_gene_groups_/575729", "title"=>"Motifs overrepresented in tissue- and phase-specific gene groups.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-03-16 01:35:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/904823"], "description"=>"<p>The histograms illustrate the distributions of number of predicted hits of several motifs in sampled background promoter sets with a GC-content matched to the selected subset of 167 CCGs. X-axis indicates numbers of predicted sites, the height of vertical bars corresponds to the percentage of sampled background sets containing the given number of predictions. The number of hits in the foreground set of 167 CCGs is marked with an arrow. All shown motifs are overrepresented in the analyzed CCG set (have z-scores over 2). The corresponding z-score values are given in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0004882#pone-0004882-t001\" target=\"_blank\">Tables 1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0004882#pone-0004882-t002\" target=\"_blank\">2</a>.</p>", "links"=>[], "tags"=>["Computational biology", "computational biology/sequence motif analysis", "genetics and genomics/animal genetics", "genetics and genomics/gene function"], "article_id"=>575274, "categories"=>["Biological Sciences", "Genetics", "Virology"], "users"=>["Katarzyna Bozek", "Angela Relógio", "Szymon M. Kielbasa", "Markus Heine", "Christof Dame", "Achim Kramer", "Hanspeter Herzel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004882.g003", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_the_number_of_predicted_TFBS_/575274", "title"=>"Distribution of the number of predicted TFBS.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-16 01:27:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/905150"], "description"=>"<p>The figure illustrates our computational predictions nested in other regulatory interactions reported in the literature. Solid line boxes contain transcription factors predicted by our study to regulate clock controlled genes. Dashed line boxes contain other factors involved in the regulation of clock controlled genes as provided by the literature. Transcription factors in bold letters are those reported to be clock controlled by at least one of the microarray studies mentioned in the main text or in other publications <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0004882#pone.0004882-Brewer1\" target=\"_blank\">[58]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0004882#pone.0004882-Nicols1\" target=\"_blank\">[59]</a>. Black arrows indicate activation, red dead-end lines inhibition and blue simple lines represent interaction. References to the literature reporting on particular interactions are indicated next to each connecting line. The full reference list can be found in the supplementary material. Several functional groups are highlighted: core clock proteins in green, proteins related to metabolism and detoxification in red, immune system related proteins in grey and muscle-specific in blue.</p>", "links"=>[], "tags"=>["putative", "circadian"], "article_id"=>575607, "categories"=>["Biological Sciences", "Genetics", "Virology"], "users"=>["Katarzyna Bozek", "Angela Relógio", "Szymon M. Kielbasa", "Markus Heine", "Christof Dame", "Achim Kramer", "Hanspeter Herzel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004882.g006", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_putative_network_of_circadian_regulation_/575607", "title"=>"A putative network of circadian regulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-16 01:33:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/904962"], "description"=>"<p>Both D-boxes and E-boxes (supplementary <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0004882#pone.0004882.s002\" target=\"_blank\">Figure S2</a>) are known to regulate clock genes and clock output pathways. Motifs highly similar to D-boxes and E-boxes are found to be overrepresented in the promoters of CCGs.</p>", "links"=>[], "tags"=>["logos", "binding", "sites"], "article_id"=>575414, "categories"=>["Biological Sciences", "Genetics", "Virology"], "users"=>["Katarzyna Bozek", "Angela Relógio", "Szymon M. Kielbasa", "Markus Heine", "Christof Dame", "Achim Kramer", "Hanspeter Herzel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004882.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sequence_logos_of_binding_sites_showing_strong_similarity_to_a_D_box_/575414", "title"=>"Sequence logos of binding sites showing strong similarity to a D-box.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-16 01:30:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/904755"], "description"=>"<p>Mean values of the GC-ratio and standard deviations of both distributions are indicated in the inserted box.</p>", "links"=>[], "tags"=>["subset", "167", "ccg", "promoters"], "article_id"=>575206, "categories"=>["Biological Sciences", "Genetics", "Virology"], "users"=>["Katarzyna Bozek", "Angela Relógio", "Szymon M. Kielbasa", "Markus Heine", "Christof Dame", "Achim Kramer", "Hanspeter Herzel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004882.g002", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GC_content_distribution_of_the_selected_subset_of_167_CCG_promoters_versus_all_mouse_gene_promoters_/575206", "title"=>"GC-content distribution of the selected subset of 167 CCG promoters versus all mouse gene promoters.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-16 01:26:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/905321"], "description"=>"<p>Motifs with a z-score above 3 in 2065 CCG promoters are shown. 8 additional factors that are overrepresented in the 167 selected gene promoters are listed below together with their z-scores from the corresponding background.</p>", "links"=>[], "tags"=>["overrepresented", "motifs", "clock-controlled"], "article_id"=>575775, "categories"=>["Biological Sciences", "Genetics", "Virology"], "users"=>["Katarzyna Bozek", "Angela Relógio", "Szymon M. Kielbasa", "Markus Heine", "Christof Dame", "Achim Kramer", "Hanspeter Herzel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004882.t001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Abundantly_overrepresented_cis_regulatory_motifs_in_clock_controlled_genes_/575775", "title"=>"Abundantly overrepresented <i>cis</i>-regulatory motifs in clock-controlled genes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-03-16 01:36:15"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2009-01-01T00:00:00Z", "end_date"=>"2009-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Chronobiology", "average_usage"=>[357, 777, 902, 1035, 1139, 1250, 1349, 1453, 1549, 1612, 1678, 1774, 1881, 1983, 2052, 2096, 2156, 2197, 2242, 2295, 2341, 2388, 2419, 2463, 2518, 2588, 2640, 2725, 2787, 2853, 2923, 2977, 3019, 3086, 3146, 3203, 3306, 3365, 3465, 3517, 3608, 3701, 3750, 3811, 3859, 3921, 3981, 4053, 4095, 4136, 4273, 4324, 4392, 4456, 4505, 4551, 4591, 4634, 4680, 4732, 4831, 4839]}, {"subject_area"=>"/Biology and life sciences/Genetics", "average_usage"=>[366, 637, 775, 896, 999, 1118, 1230, 1322, 1416, 1516, 1602, 1685, 1767, 1849, 1914, 1982, 2049, 2120, 2185, 2246, 2303, 2363, 2409, 2473, 2535, 2599, 2655, 2717, 2777, 2842, 2906, 2977, 3021, 3088, 3144, 3199, 3253, 3317, 3379, 3456, 3508, 3567, 3634, 3716, 3781, 3853, 3911, 3974, 4040, 4118, 4170, 4218, 4285, 4341, 4404, 4467, 4527, 4584, 4631, 4689, 4725]}]}
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