Transcription Factor Binding Site Analysis Identifies FOXO Transcription Factors as Regulators of the Cutaneous Wound Healing Process
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{"title"=>"Transcription factor binding site analysis identifies FOXO transcription factors as regulators of the cutaneous wound healing process", "type"=>"journal", "authors"=>[{"first_name"=>"Karl Markus", "last_name"=>"Roupé", "scopus_author_id"=>"14036155700"}, {"first_name"=>"Srinivas", "last_name"=>"Veerla", "scopus_author_id"=>"14326099000"}, {"first_name"=>"Joshua", "last_name"=>"Olson", "scopus_author_id"=>"55011027200"}, {"first_name"=>"Erica L.", "last_name"=>"Stone", "scopus_author_id"=>"11240036200"}, {"first_name"=>"Ole E.", "last_name"=>"Sørensen", "scopus_author_id"=>"7101713762"}, {"first_name"=>"Stephen M.", "last_name"=>"Hedrick", "scopus_author_id"=>"7006019924"}, {"first_name"=>"Victor", "last_name"=>"Nizet", "scopus_author_id"=>"7003353710"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"372565787", "sgr"=>"84895858633", "doi"=>"10.1371/journal.pone.0089274", "scopus"=>"2-s2.0-84895858633", "pmid"=>"24586650"}, "id"=>"abe6ce00-e9ee-3ea0-aa66-fe87fb6acd7a", "abstract"=>"The search for significantly overrepresented and co-occurring transcription factor binding sites in the promoter regions of the most differentially expressed genes in microarray data sets could be a powerful approach for finding key regulators of complex biological processes. To test this concept, two previously published independent data sets on wounded human epidermis were re-analyzed. The presence of co-occurring transcription factor binding sites for FOXO1, FOXO3 and FOXO4 in the majority of the promoter regions of the most significantly differentially expressed genes between non-wounded and wounded epidermis implied an important role for FOXO transcription factors during wound healing. Expression levels of FOXO transcription factors during wound healing in vivo in both human and mouse skin were analyzed and a decrease for all FOXOs in human wounded skin was observed, with FOXO3 having the highest expression level in non wounded skin. Impaired re-epithelialization was found in cultures of primary human keratinocytes expressing a constitutively active variant of FOXO3. Conversely knockdown of FOXO3 in keratinocytes had the opposite effect and in an in vivo mouse model with FOXO3 knockout mice we detected significantly accelerated wound healing. This article illustrates that the proposed approach is a viable method for identifying important regulators of complex biological processes using in vivo samples. FOXO3 has not previously been implicated as an important regulator of wound healing and its exact function in this process calls for further investigation.", "link"=>"http://www.mendeley.com/research/transcription-factor-binding-site-analysis-identifies-foxo-transcription-factors-regulators-cutaneou", "reader_count"=>17, "reader_count_by_academic_status"=>{"Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>5, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>5, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>1, "Medicine and Dentistry"=>3, "Agricultural and Biological Sciences"=>10, "Arts and Humanities"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>10}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Arts and Humanities"=>{"Arts and Humanities"=>1}}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1390736"], "description"=>"<p>List of significantly differentially expressed genes involved in regulation of FOXO3 expression/activity in the Roupé et al 2009 data set comparing human <i>in vivo</i> wounded skin with control.</p><p>*Change in expression is consistent with a decrease in FOXO3 activity/expression.</p><p>** Change in expression is not consistent with a decrease in FOXO3 activity/expression.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "skin", "Skin physiology", "Computational biology", "genomics", "Genome analysis tools", "Genetic networks", "transcriptomes", "Functional genomics", "Genome expression analysis", "Molecular genetics", "Gene regulation", "microarrays", "Regulatory networks", "systems biology", "genetics", "gene expression", "DNA transcription", "differentially", "regulators"], "article_id"=>938253, "categories"=>["Biological Sciences"], "users"=>["Karl Markus Roupé", "Srinivas Veerla", "Joshua Olson", "Erica L. Stone", "Ole E. Sørensen", "Stephen M. Hedrick", "Victor Nizet"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089274.t002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Significantly_differentially_expressed_regulators_of_FOXO3_/938253", "title"=>"Significantly differentially expressed regulators of FOXO3.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-02-19 02:43:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1390735"], "description"=>"<p>List of significantly differentially expressed known, potential and indirect target genes of FOXO3 in Roupé et al 2009 data set comparing human <i>in vivo</i> wounded skin with control. Genes known to be direct target genes of FOXO3 are <b>in bold</b>.</p><p>*Change in expression is consistent with a decrease in FOXO3 transcriptional activity.</p><p>**Change in expression not consistent with a decrease in FOXO3 transcriptional activity.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "skin", "Skin physiology", "Computational biology", "genomics", "Genome analysis tools", "Genetic networks", "transcriptomes", "Functional genomics", "Genome expression analysis", "Molecular genetics", "Gene regulation", "microarrays", "Regulatory networks", "systems biology", "genetics", "gene expression", "DNA transcription", "differentially", "genes"], "article_id"=>938252, "categories"=>["Biological Sciences"], "users"=>["Karl Markus Roupé", "Srinivas Veerla", "Joshua Olson", "Erica L. Stone", "Ole E. Sørensen", "Stephen M. Hedrick", "Victor Nizet"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089274.t001", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Significantly_differentially_expressed_target_genes_of_FOXO3_/938252", "title"=>"Significantly differentially expressed target genes of FOXO3.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-02-19 02:43:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1390732"], "description"=>"<p>A) The promoter sequences for the 100 most differentially expressed genes between wounded and non-wounded skin were probed for transcription factor binding sites and co-occurring transcription factor binding sites. The presence of co-occurring transcription factor binding sites of FOXO1, FOXO3 and FOXO4 found by the SMART software to be within 50 base pairs of each other is depicted in the promoter regions of the 70 genes out of 100 were they were found. The presence of co-occurring transcription factor binding sites of either FOXO1, FOXO3 or FOXO4 in these promoter regions are also depicted. Some of these sites are partially overlapping. Genes with a Pavlidis template matching correlation coefficient of 0.9 to FOXO3 expression are highlighted; yellow equals positive correlation and green negative correlation B) Hierarchical clustering and heat map of the 70 genes containing co-occurring FOXO1-FOXO3-FOXO4 transcription factor binding sites. C) Schematic of currently known and annotated interactions between the 70 genes containing co-occurring FOXO1-FOXO3-FOXO4 binding sites generated by ingenuity pathway analysis software. FOXO1, FOXO3 and FOXO4 were also added to visualize how they interact with the selected genes. Only genes with at least one known connection to FOXO1, FOXO3, FOXO4, or one of the other 70 genes were included. D) PCA plots of the 100 selected genes depicting the remaining variance between the samples on the left and a synchronized PCA plot of the variables (gene expression) giving rise to the variance on the right. Genes were selected by first removing all genes having a q-value>0.05 based on a two group comparison analysis between wounded and non-wounded samples. Remaining genes were then filtered by variance till the top 100 genes remained with a p-value≤0.008. The selected genes stood for 23% of the total amount of variance in the data set. E) The normalized hybridization levels of FOXO transcription factor transcripts from the micro array data set from Roupé et. al. 2010 are depicted. A two-tailed Student's t-test confirmed a differential expression of FOXO1, FOXO3 and FOXO6 when comparing non-wounded and <i>in vivo</i> wounded human skin (*<i>P</i><0.05, **<i>P</i><0.01, ***<i>P</i><0.001). Error bar denotes mean ±SD (n = 3). F) Flowchart giving an overview over the analysis approach (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089274#s2\" target=\"_blank\">methods</a> section for more details.)</p>", "links"=>[], "tags"=>["Anatomy and physiology", "skin", "Skin physiology", "Computational biology", "genomics", "Genome analysis tools", "Genetic networks", "transcriptomes", "Functional genomics", "Genome expression analysis", "Molecular genetics", "Gene regulation", "microarrays", "Regulatory networks", "systems biology", "genetics", "gene expression", "DNA transcription", "microarray", "non", "wounded"], "article_id"=>938249, "categories"=>["Biological Sciences"], "users"=>["Karl Markus Roupé", "Srinivas Veerla", "Joshua Olson", "Erica L. Stone", "Ole E. Sørensen", "Stephen M. Hedrick", "Victor Nizet"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089274.g001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Re_analysis_of_a_microarray_data_set_from_14_on_non_wounded_and_in_vivo_wounded_human_skin_samples_/938249", "title"=>"Re-analysis of a microarray data set from [14] on non wounded and <i>in vivo</i> wounded human skin samples.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-19 02:43:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1390740", "https://ndownloader.figshare.com/files/1390741", "https://ndownloader.figshare.com/files/1390742", "https://ndownloader.figshare.com/files/1390743", "https://ndownloader.figshare.com/files/1390744", "https://ndownloader.figshare.com/files/1390745", "https://ndownloader.figshare.com/files/1390746", "https://ndownloader.figshare.com/files/1390747"], "description"=>"<div><p>The search for significantly overrepresented and co-occurring transcription factor binding sites in the promoter regions of the most differentially expressed genes in microarray data sets could be a powerful approach for finding key regulators of complex biological processes. To test this concept, two previously published independent data sets on wounded human epidermis were re-analyzed. The presence of co-occurring transcription factor binding sites for FOXO1, FOXO3 and FOXO4 in the majority of the promoter regions of the most significantly differentially expressed genes between non-wounded and wounded epidermis implied an important role for FOXO transcription factors during wound healing. Expression levels of FOXO transcription factors during wound healing <i>in vivo</i> in both human and mouse skin were analyzed and a decrease for all FOXOs in human wounded skin was observed, with FOXO3 having the highest expression level in non wounded skin. Impaired re-epithelialization was found in cultures of primary human keratinocytes expressing a constitutively active variant of FOXO3. Conversely knockdown of FOXO3 in keratinocytes had the opposite effect and in an <i>in vivo</i> mouse model with FOXO3 knockout mice we detected significantly accelerated wound healing. This article illustrates that the proposed approach is a viable method for identifying important regulators of complex biological processes using <i>in vivo</i> samples. FOXO3 has not previously been implicated as an important regulator of wound healing and its exact function in this process calls for further investigation.</p></div>", "links"=>[], "tags"=>["Anatomy and physiology", "skin", "Skin physiology", "Computational biology", "genomics", "Genome analysis tools", "Genetic networks", "transcriptomes", "Functional genomics", "Genome expression analysis", "Molecular genetics", "Gene regulation", "microarrays", "Regulatory networks", "systems biology", "genetics", "gene expression", "DNA transcription", "binding", "identifies", "foxo", "transcription", "regulators", "cutaneous", "healing"], "article_id"=>938257, "categories"=>["Biological Sciences"], "users"=>["Karl Markus Roupé", "Srinivas Veerla", "Joshua Olson", "Erica L. Stone", "Ole E. Sørensen", "Stephen M. Hedrick", "Victor Nizet"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0089274.s001", "https://dx.doi.org/10.1371/journal.pone.0089274.s002", "https://dx.doi.org/10.1371/journal.pone.0089274.s003", "https://dx.doi.org/10.1371/journal.pone.0089274.s004", "https://dx.doi.org/10.1371/journal.pone.0089274.s005", "https://dx.doi.org/10.1371/journal.pone.0089274.s006", "https://dx.doi.org/10.1371/journal.pone.0089274.s007", "https://dx.doi.org/10.1371/journal.pone.0089274.s008"], "stats"=>{"downloads"=>18, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transcription_Factor_Binding_Site_Analysis_Identifies_FOXO_Transcription_Factors_as_Regulators_of_the_Cutaneous_Wound_Healing_Process_/938257", "title"=>"Transcription Factor Binding Site Analysis Identifies FOXO Transcription Factors as Regulators of the Cutaneous Wound Healing Process", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-02-19 02:43:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1390734"], "description"=>"<p>A) Quantitative RT-PCR using mRNA from non-wounded and <i>in vivo</i> wounded mouse skin was performed. All data was normalized to GAPDH expression (Glyceraldehyde 3-phosphate dehydrogenase) that was used as housekeeping gene. A one-way analysis of variance was performed. Significant differences were found day 1 after wounding for FOXO3 and FOXO4 when performing a Dunnett's Multiple Comparison Test against non-wounded control. (*<i>P</i><0.05, **<i>P</i><0.01). Error bar denotes mean ±SD (n = 3). B) Graph displays wound size in mm<sup>2</sup> over time. Values from each mouse represent an average of 4 wounds induced by 6 mm punches through folded dorsal skin. A two-way ANOVA was performed to detect differences over time between FOXO3 knock out mice and C57bl/6 control mice using Bonferroni post-testing to detect differences at each time point. An overall difference was detected over time <i>P</i><0.023 and post-testing generated significant results for day 1 to day 4. (*<i>P</i><0.05, **<i>P</i><0.01, ***<i>P</i><0.001) (n = 4) C) Bacterial loads in the wound beds day 10 after wounding. D) Wound healing rate in FOXO3 LysM-cre mice and control mice over time. E) Group A streptococcal (GAS) survival in neutrophil killing assays using neutrophils isolated from either FOXO3 LysM-cre mice or C57bl/6 control mice. Percent survival is expressed relative to GAS survival with no neutrophils present.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "skin", "Skin physiology", "Computational biology", "genomics", "Genome analysis tools", "Genetic networks", "transcriptomes", "Functional genomics", "Genome expression analysis", "Molecular genetics", "Gene regulation", "microarrays", "Regulatory networks", "systems biology", "genetics", "gene expression", "DNA transcription", "healing", "foxo3", "lysm-cre", "knockout", "mice", "compared"], "article_id"=>938251, "categories"=>["Biological Sciences"], "users"=>["Karl Markus Roupé", "Srinivas Veerla", "Joshua Olson", "Erica L. Stone", "Ole E. Sørensen", "Stephen M. Hedrick", "Victor Nizet"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089274.g003", "stats"=>{"downloads"=>7, "page_views"=>45, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Wound_healing_rate_in_FOXO3_and_FOXO3_LysM_cre_knockout_mice_compared_to_control_/938251", "title"=>"Wound healing rate in FOXO3 and FOXO3 LysM-cre knockout mice compared to control.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-19 02:43:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1390733"], "description"=>"<p>A) Immunohistochemistry was performed on <i>in vivo</i> wounded human skin four days post wounding as well as on normal skin from the same donor. An anti-pFOXO antibody and a secondary fluorescently labeled antibody was used to detect the levels of phosphorylated FOXO transcription factors in the samples. Notice the increase in fluorescence intensity in the cytoplasm of keratinocytes closest to the front of the migrating epidermal tongue moving in under the wound crust at day 4. B–D) Scratch assays were performed on cultures of primary human keratinocytes transduced with either GFP control or FOXO3 AAA using adenoviral vectors and re-epithelialization was monitored over 24 h. B) Bar graph depicts the percent remaining of the original scratch width after 24 h (n = 9). C) Representative image of scratches from each condition at 0, 12 and 24 h. D) RT-PCR was run on isolated mRNA from scratched wells after 24 h. MMP-9, IL-8 and IL-6 gene expression was normalized using GAPDH (Glyceraldehyde 3-phosphate dehydrogenase) as housekeeping gene. E) Scratch assays were performed on cultures of primary human keratinocytes transduced with either negative shRNA control or shRNA targeting FOXO3 using lentiviral vectors and re-epithelialization was monitored over 48 hours. Bar graph depicts the percent remaining of the original scratch width after 24 h (n = 12).</p>", "links"=>[], "tags"=>["Anatomy and physiology", "skin", "Skin physiology", "Computational biology", "genomics", "Genome analysis tools", "Genetic networks", "transcriptomes", "Functional genomics", "Genome expression analysis", "Molecular genetics", "Gene regulation", "microarrays", "Regulatory networks", "systems biology", "genetics", "gene expression", "DNA transcription", "phosphorylated", "foxo", "transcription", "wounded", "scratched", "keratinocytes", "expressing", "constitutively", "foxo3", "shrna", "targeting"], "article_id"=>938250, "categories"=>["Biological Sciences"], "users"=>["Karl Markus Roupé", "Srinivas Veerla", "Joshua Olson", "Erica L. Stone", "Ole E. Sørensen", "Stephen M. Hedrick", "Victor Nizet"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089274.g002", "stats"=>{"downloads"=>0, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Immunohistochemistry_on_phosphorylated_FOXO_transcription_factors_in_wounded_human_skin_and_scratched_human_primary_keratinocytes_expressing_either_a_constitutively_active_form_of_FOXO3_or_shRNA_targeting_FOXO3_/938250", "title"=>"Immunohistochemistry on phosphorylated FOXO transcription factors in wounded human skin and scratched human primary keratinocytes expressing either a constitutively active form of FOXO3 or shRNA targeting FOXO3.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-19 02:43:42"}

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Relative Metric

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