Identification of Pou5f1, Sox2, and Nanog downstream target genes with statistical confidence by applying a novel algorithm to time course microarray and genome-wide chromatin immunoprecipitation data

Background Target genes of a transcription factor (TF) Pou5f1 ( Oct3/4 or Oct4 ), which is essential for pluripotency maintenance and self-renewal of embryonic stem (ES) cells, have previously been identified based on their response to Pou5f1 manipulation and occurrence of Chromatin-immunoprecipitat...

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Veröffentlicht in:	BMC genomics Jg. 9; H. 1; S. 269
Hauptverfasser:	Sharov, Alexei A, Masui, Shinji, Sharova, Lioudmila V, Piao, Yulan, Aiba, Kazuhiro, Matoba, Ryo, Xin, Li, Niwa, Hitoshi, Ko, Minoru SH
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	London BioMed Central 03.06.2008 BioMed Central Ltd BMC
Schlagworte:	Algorithms Analysis Animal Genetics and Genomics Animals Binding Sites Biomedical and Life Sciences Chromatin Chromatin Immunoprecipitation - methods DNA binding proteins DNA microarrays DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Embryonic Stem Cells - metabolism Genetic aspects Genome Health aspects HMGB Proteins - genetics HMGB Proteins - metabolism Homeodomain Proteins - genetics Homeodomain Proteins - metabolism Humans Life Sciences Mice Microarrays Microbial Genetics and Genomics Nanog Homeobox Protein Octamer Transcription Factor-3 - genetics Octamer Transcription Factor-3 - metabolism Oligonucleotide Array Sequence Analysis Plant Genetics and Genomics Proteomics Research Article SOXB1 Transcription Factors Time Factors Transcription Factors - genetics Transcription Factors - metabolism United States False Discovery Rate Trophoblast Stem Cell Trophoblast Stem Embryonic Stem Cell ChIP Data
ISSN:	1471-2164, 1471-2164
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Abstract	Background Target genes of a transcription factor (TF) Pou5f1 ( Oct3/4 or Oct4 ), which is essential for pluripotency maintenance and self-renewal of embryonic stem (ES) cells, have previously been identified based on their response to Pou5f1 manipulation and occurrence of Chromatin-immunoprecipitation (ChIP)-binding sites in promoters. However, many responding genes with binding sites may not be direct targets because response may be mediated by other genes and ChIP-binding site may not be functional in terms of transcription regulation. Results To reduce the number of false positives, we propose to separate responding genes into groups according to direction, magnitude, and time of response, and to apply the false discovery rate (FDR) criterion to each group individually. Using this novel algorithm with stringent statistical criteria (FDR < 0.2) to a compendium of published and new microarray data (3, 6, 12, and 24 hr after Pou5f1 suppression) and published ChIP data, we identified 420 tentative target genes (TTGs) for Pou5f1 . The majority of TTGs (372) were down-regulated after Pou5f1 suppression, indicating that the Pou5f1 functions as an activator of gene expression when it binds to promoters. Interestingly, many activated genes are potent suppressors of transcription, which include polycomb genes, zinc finger TFs, chromatin remodeling factors, and suppressors of signaling. Similar analysis showed that Sox2 and Nanog also function mostly as transcription activators in cooperation with Pou5f1 . Conclusion We have identified the most reliable sets of direct target genes for key pluripotency genes – Pou5f1 , Sox2 , and Nanog , and found that they predominantly function as activators of downstream gene expression. Thus, most genes related to cell differentiation are suppressed indirectly.
AbstractList	Abstract Background Target genes of a transcription factor (TF) Pou5f1 (Oct3/4 or Oct4), which is essential for pluripotency maintenance and self-renewal of embryonic stem (ES) cells, have previously been identified based on their response to Pou5f1 manipulation and occurrence of Chromatin-immunoprecipitation (ChIP)-binding sites in promoters. However, many responding genes with binding sites may not be direct targets because response may be mediated by other genes and ChIP-binding site may not be functional in terms of transcription regulation. Results To reduce the number of false positives, we propose to separate responding genes into groups according to direction, magnitude, and time of response, and to apply the false discovery rate (FDR) criterion to each group individually. Using this novel algorithm with stringent statistical criteria (FDR < 0.2) to a compendium of published and new microarray data (3, 6, 12, and 24 hr after Pou5f1 suppression) and published ChIP data, we identified 420 tentative target genes (TTGs) for Pou5f1. The majority of TTGs (372) were down-regulated after Pou5f1 suppression, indicating that the Pou5f1 functions as an activator of gene expression when it binds to promoters. Interestingly, many activated genes are potent suppressors of transcription, which include polycomb genes, zinc finger TFs, chromatin remodeling factors, and suppressors of signaling. Similar analysis showed that Sox2 and Nanog also function mostly as transcription activators in cooperation with Pou5f1. Conclusion We have identified the most reliable sets of direct target genes for key pluripotency genes – Pou5f1, Sox2, and Nanog, and found that they predominantly function as activators of downstream gene expression. Thus, most genes related to cell differentiation are suppressed indirectly. Background Target genes of a transcription factor (TF) Pou5f1 ( Oct3/4 or Oct4 ), which is essential for pluripotency maintenance and self-renewal of embryonic stem (ES) cells, have previously been identified based on their response to Pou5f1 manipulation and occurrence of Chromatin-immunoprecipitation (ChIP)-binding sites in promoters. However, many responding genes with binding sites may not be direct targets because response may be mediated by other genes and ChIP-binding site may not be functional in terms of transcription regulation. Results To reduce the number of false positives, we propose to separate responding genes into groups according to direction, magnitude, and time of response, and to apply the false discovery rate (FDR) criterion to each group individually. Using this novel algorithm with stringent statistical criteria (FDR < 0.2) to a compendium of published and new microarray data (3, 6, 12, and 24 hr after Pou5f1 suppression) and published ChIP data, we identified 420 tentative target genes (TTGs) for Pou5f1 . The majority of TTGs (372) were down-regulated after Pou5f1 suppression, indicating that the Pou5f1 functions as an activator of gene expression when it binds to promoters. Interestingly, many activated genes are potent suppressors of transcription, which include polycomb genes, zinc finger TFs, chromatin remodeling factors, and suppressors of signaling. Similar analysis showed that Sox2 and Nanog also function mostly as transcription activators in cooperation with Pou5f1 . Conclusion We have identified the most reliable sets of direct target genes for key pluripotency genes – Pou5f1 , Sox2 , and Nanog , and found that they predominantly function as activators of downstream gene expression. Thus, most genes related to cell differentiation are suppressed indirectly. Background Target genes of a transcription factor (TF) Pou5f1 (Oct3/4 or Oct4), which is essential for pluripotency maintenance and self-renewal of embryonic stem (ES) cells, have previously been identified based on their response to Pou5f1 manipulation and occurrence of Chromatin-immunoprecipitation (ChIP)-binding sites in promoters. However, many responding genes with binding sites may not be direct targets because response may be mediated by other genes and ChIP-binding site may not be functional in terms of transcription regulation. Results To reduce the number of false positives, we propose to separate responding genes into groups according to direction, magnitude, and time of response, and to apply the false discovery rate (FDR) criterion to each group individually. Using this novel algorithm with stringent statistical criteria (FDR & 0.2) to a compendium of published and new microarray data (3, 6, 12, and 24 hr after Pou5f1 suppression) and published ChIP data, we identified 420 tentative target genes (TTGs) for Pou5f1. The majority of TTGs (372) were down-regulated after Pou5f1 suppression, indicating that the Pou5f1 functions as an activator of gene expression when it binds to promoters. Interestingly, many activated genes are potent suppressors of transcription, which include polycomb genes, zinc finger TFs, chromatin remodeling factors, and suppressors of signaling. Similar analysis showed that Sox2 and Nanog also function mostly as transcription activators in cooperation with Pou5f1. Conclusion We have identified the most reliable sets of direct target genes for key pluripotency genes - Pou5f1, Sox2, and Nanog, and found that they predominantly function as activators of downstream gene expression. Thus, most genes related to cell differentiation are suppressed indirectly. Target genes of a transcription factor (TF) Pou5f1 (Oct3/4 or Oct4), which is essential for pluripotency maintenance and self-renewal of embryonic stem (ES) cells, have previously been identified based on their response to Pou5f1 manipulation and occurrence of Chromatin-immunoprecipitation (ChIP)-binding sites in promoters. However, many responding genes with binding sites may not be direct targets because response may be mediated by other genes and ChIP-binding site may not be functional in terms of transcription regulation.BACKGROUNDTarget genes of a transcription factor (TF) Pou5f1 (Oct3/4 or Oct4), which is essential for pluripotency maintenance and self-renewal of embryonic stem (ES) cells, have previously been identified based on their response to Pou5f1 manipulation and occurrence of Chromatin-immunoprecipitation (ChIP)-binding sites in promoters. However, many responding genes with binding sites may not be direct targets because response may be mediated by other genes and ChIP-binding site may not be functional in terms of transcription regulation.To reduce the number of false positives, we propose to separate responding genes into groups according to direction, magnitude, and time of response, and to apply the false discovery rate (FDR) criterion to each group individually. Using this novel algorithm with stringent statistical criteria (FDR < 0.2) to a compendium of published and new microarray data (3, 6, 12, and 24 hr after Pou5f1 suppression) and published ChIP data, we identified 420 tentative target genes (TTGs) for Pou5f1. The majority of TTGs (372) were down-regulated after Pou5f1 suppression, indicating that the Pou5f1 functions as an activator of gene expression when it binds to promoters. Interestingly, many activated genes are potent suppressors of transcription, which include polycomb genes, zinc finger TFs, chromatin remodeling factors, and suppressors of signaling. Similar analysis showed that Sox2 and Nanog also function mostly as transcription activators in cooperation with Pou5f1.RESULTSTo reduce the number of false positives, we propose to separate responding genes into groups according to direction, magnitude, and time of response, and to apply the false discovery rate (FDR) criterion to each group individually. Using this novel algorithm with stringent statistical criteria (FDR < 0.2) to a compendium of published and new microarray data (3, 6, 12, and 24 hr after Pou5f1 suppression) and published ChIP data, we identified 420 tentative target genes (TTGs) for Pou5f1. The majority of TTGs (372) were down-regulated after Pou5f1 suppression, indicating that the Pou5f1 functions as an activator of gene expression when it binds to promoters. Interestingly, many activated genes are potent suppressors of transcription, which include polycomb genes, zinc finger TFs, chromatin remodeling factors, and suppressors of signaling. Similar analysis showed that Sox2 and Nanog also function mostly as transcription activators in cooperation with Pou5f1.We have identified the most reliable sets of direct target genes for key pluripotency genes - Pou5f1, Sox2, and Nanog, and found that they predominantly function as activators of downstream gene expression. Thus, most genes related to cell differentiation are suppressed indirectly.CONCLUSIONWe have identified the most reliable sets of direct target genes for key pluripotency genes - Pou5f1, Sox2, and Nanog, and found that they predominantly function as activators of downstream gene expression. Thus, most genes related to cell differentiation are suppressed indirectly. Target genes of a transcription factor (TF) Pou5f1 (Oct3/4 or Oct4), which is essential for pluripotency maintenance and self-renewal of embryonic stem (ES) cells, have previously been identified based on their response to Pou5f1 manipulation and occurrence of Chromatin-immunoprecipitation (ChIP)-binding sites in promoters. However, many responding genes with binding sites may not be direct targets because response may be mediated by other genes and ChIP-binding site may not be functional in terms of transcription regulation. To reduce the number of false positives, we propose to separate responding genes into groups according to direction, magnitude, and time of response, and to apply the false discovery rate (FDR) criterion to each group individually. Using this novel algorithm with stringent statistical criteria (FDR < 0.2) to a compendium of published and new microarray data (3, 6, 12, and 24 hr after Pou5f1 suppression) and published ChIP data, we identified 420 tentative target genes (TTGs) for Pou5f1. The majority of TTGs (372) were down-regulated after Pou5f1 suppression, indicating that the Pou5f1 functions as an activator of gene expression when it binds to promoters. Interestingly, many activated genes are potent suppressors of transcription, which include polycomb genes, zinc finger TFs, chromatin remodeling factors, and suppressors of signaling. Similar analysis showed that Sox2 and Nanog also function mostly as transcription activators in cooperation with Pou5f1. We have identified the most reliable sets of direct target genes for key pluripotency genes - Pou5f1, Sox2, and Nanog, and found that they predominantly function as activators of downstream gene expression. Thus, most genes related to cell differentiation are suppressed indirectly.
ArticleNumber	269
Audience	Academic
Author	Piao, Yulan Matoba, Ryo Aiba, Kazuhiro Sharov, Alexei A Sharova, Lioudmila V Niwa, Hitoshi Ko, Minoru SH Xin, Li Masui, Shinji
AuthorAffiliation	1 Developmental Genomics and Aging Section, Laboratory of Genetics, National Institute on Aging, NIH, Baltimore, MD 21224, USA 2 Laboratory of Pluripotent Cell Studies, RIKEN Center for Developmental Biology, Kobe 650-0047, Japan
AuthorAffiliation_xml	– name: 1 Developmental Genomics and Aging Section, Laboratory of Genetics, National Institute on Aging, NIH, Baltimore, MD 21224, USA – name: 2 Laboratory of Pluripotent Cell Studies, RIKEN Center for Developmental Biology, Kobe 650-0047, Japan
Author_xml	– sequence: 1 givenname: Alexei A surname: Sharov fullname: Sharov, Alexei A organization: Developmental Genomics and Aging Section, Laboratory of Genetics, National Institute on Aging, NIH – sequence: 2 givenname: Shinji surname: Masui fullname: Masui, Shinji organization: Laboratory of Pluripotent Cell Studies, RIKEN Center for Developmental Biology – sequence: 3 givenname: Lioudmila V surname: Sharova fullname: Sharova, Lioudmila V organization: Developmental Genomics and Aging Section, Laboratory of Genetics, National Institute on Aging, NIH – sequence: 4 givenname: Yulan surname: Piao fullname: Piao, Yulan organization: Developmental Genomics and Aging Section, Laboratory of Genetics, National Institute on Aging, NIH – sequence: 5 givenname: Kazuhiro surname: Aiba fullname: Aiba, Kazuhiro organization: Developmental Genomics and Aging Section, Laboratory of Genetics, National Institute on Aging, NIH – sequence: 6 givenname: Ryo surname: Matoba fullname: Matoba, Ryo organization: Developmental Genomics and Aging Section, Laboratory of Genetics, National Institute on Aging, NIH – sequence: 7 givenname: Li surname: Xin fullname: Xin, Li organization: Developmental Genomics and Aging Section, Laboratory of Genetics, National Institute on Aging, NIH – sequence: 8 givenname: Hitoshi surname: Niwa fullname: Niwa, Hitoshi organization: Laboratory of Pluripotent Cell Studies, RIKEN Center for Developmental Biology – sequence: 9 givenname: Minoru SH surname: Ko fullname: Ko, Minoru SH email: kom@mail.nih.gov organization: Developmental Genomics and Aging Section, Laboratory of Genetics, National Institute on Aging, NIH
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/18522731$$D View this record in MEDLINE/PubMed
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Keywords	False Discovery Rate Trophoblast Stem Cell Trophoblast Stem Embryonic Stem Cell ChIP Data
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Snippet	Background Target genes of a transcription factor (TF) Pou5f1 ( Oct3/4 or Oct4 ), which is essential for pluripotency maintenance and self-renewal of embryonic... Target genes of a transcription factor (TF) Pou5f1 (Oct3/4 or Oct4), which is essential for pluripotency maintenance and self-renewal of embryonic stem (ES)... Background Target genes of a transcription factor (TF) Pou5f1 (Oct3/4 or Oct4), which is essential for pluripotency maintenance and self-renewal of embryonic... Abstract Background Target genes of a transcription factor (TF) Pou5f1 (Oct3/4 or Oct4), which is essential for pluripotency maintenance and self-renewal of...
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SubjectTerms	Algorithms Analysis Animal Genetics and Genomics Animals Binding Sites Biomedical and Life Sciences Chromatin Chromatin Immunoprecipitation - methods DNA binding proteins DNA microarrays DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Embryonic Stem Cells - metabolism Genetic aspects Genome Health aspects HMGB Proteins - genetics HMGB Proteins - metabolism Homeodomain Proteins - genetics Homeodomain Proteins - metabolism Humans Life Sciences Mice Microarrays Microbial Genetics and Genomics Nanog Homeobox Protein Octamer Transcription Factor-3 - genetics Octamer Transcription Factor-3 - metabolism Oligonucleotide Array Sequence Analysis Plant Genetics and Genomics Proteomics Research Article SOXB1 Transcription Factors Time Factors Transcription Factors - genetics Transcription Factors - metabolism
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Title	Identification of Pou5f1, Sox2, and Nanog downstream target genes with statistical confidence by applying a novel algorithm to time course microarray and genome-wide chromatin immunoprecipitation data
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