Distinct DNA Binding Sites Contribute to the TCF Transcriptional Switch in C. elegans and Drosophila
Regulation of gene expression by signaling pathways often occurs through a transcriptional switch, where the transcription factor responsible for signal-dependent gene activation represses the same targets in the absence of signaling. T-cell factors (TCFs) are transcription factors in the Wnt/ß-cate...
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| Published in | PLoS genetics Vol. 10; no. 2; p. e1004133 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.02.2014
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7404 1553-7390 1553-7404 |
| DOI | 10.1371/journal.pgen.1004133 |
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| Abstract | Regulation of gene expression by signaling pathways often occurs through a transcriptional switch, where the transcription factor responsible for signal-dependent gene activation represses the same targets in the absence of signaling. T-cell factors (TCFs) are transcription factors in the Wnt/ß-catenin pathway, which control numerous cell fate specification events in metazoans. The TCF transcriptional switch is mediated by many co-regulators that contribute to repression or activation of Wnt target genes. It is typically assumed that DNA recognition by TCFs is important for target gene location, but plays no role in the actual switch. TCF/Pangolin (the fly TCF) and some vertebrate TCF isoforms bind DNA through two distinct domains, a High Mobility Group (HMG) domain and a C-clamp, which recognize DNA motifs known as HMG and Helper sites, respectively. Here, we demonstrate that POP-1 (the C. elegans TCF) also activates target genes through HMG and Helper site interactions. Helper sites enhanced the ability of a synthetic enhancer to detect Wnt/ß-catenin signaling in several tissues and revealed an unsuspected role for POP-1 in regulating the C. elegans defecation cycle. Searching for HMG-Helper site clusters allowed the identification of a new POP-1 target gene active in the head muscles and gut. While Helper sites and the C-clamp are essential for activation of worm and fly Wnt targets, they are dispensable for TCF-dependent repression of targets in the absence of Wnt signaling. These data suggest that a fundamental change in TCF-DNA binding contributes to the transcriptional switch that occurs upon Wnt stimulation. |
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| AbstractList | Regulation of gene expression by signaling pathways often occurs through a transcriptional switch, where the transcription factor responsible for signal-dependent gene activation represses the same targets in the absence of signaling. T-cell factors (TCFs) are transcription factors in the Wnt/β- catenin pathway, which control numerous cell fate specification events in metazoans. The TCF transcriptional switch is mediated by many co-regulators that contribute to repression or activation of Wnt target genes. It is typically assumed that DNA recognition by TCFs is important for target gene location, but plays no role in the actual switch. TCF/Pangolin (the fly TCF) and some vertebrate TCF isoforms bind DNA through two distinct domains, a High Mobility Group (HMG) domain and a C-clamp, which recognize DNA motifs known as HMG and Helper sites, respectively. Here, we demonstrate that POP-1 (the C. elegans TCF) also activates target genes through HMG and Helper site interactions. Helper sites enhanced the ability of a synthetic enhancer to detect Wnt/β-catenin signaling in several tissues and revealed an unsuspected role for POP-1 in regulating the C. elegans defecation cycle. Searching for HMGHelper site clusters allowed the identification of a new POP-1 target gene active in the head muscles and gut. While Helper sites and the C-clamp are essential for activation of worm and fly Wnt targets, they are dispensable for TCF-dependent repression of targets in the absence of Wnt signaling. These data suggest that a fundamental change in TCF-DNA binding contributes to the transcriptional switch that occurs upon Wnt stimulation. Regulation of gene expression by signaling pathways often occurs through a transcriptional switch, where the transcription factor responsible for signal-dependent gene activation represses the same targets in the absence of signaling. T-cell factors (TCFs) are transcription factors in the Wnt/ß-catenin pathway, which control numerous cell fate specification events in metazoans. The TCF transcriptional switch is mediated by many co-regulators that contribute to repression or activation of Wnt target genes. It is typically assumed that DNA recognition by TCFs is important for target gene location, but plays no role in the actual switch. TCF/Pangolin (the fly TCF) and some vertebrate TCF isoforms bind DNA through two distinct domains, a High Mobility Group (HMG) domain and a C-clamp, which recognize DNA motifs known as HMG and Helper sites, respectively. Here, we demonstrate that POP-1 (the C. elegans TCF) also activates target genes through HMG and Helper site interactions. Helper sites enhanced the ability of a synthetic enhancer to detect Wnt/ß-catenin signaling in several tissues and revealed an unsuspected role for POP-1 in regulating the C. elegans defecation cycle. Searching for HMG-Helper site clusters allowed the identification of a new POP-1 target gene active in the head muscles and gut. While Helper sites and the C-clamp are essential for activation of worm and fly Wnt targets, they are dispensable for TCF-dependent repression of targets in the absence of Wnt signaling. These data suggest that a fundamental change in TCF-DNA binding contributes to the transcriptional switch that occurs upon Wnt stimulation. Regulation of gene expression by signaling pathways often occurs through a transcriptional switch, where the transcription factor responsible for signal-dependent gene activation represses the same targets in the absence of signaling. T-cell factors (TCFs) are transcription factors in the Wnt/ß-catenin pathway, which control numerous cell fate specification events in metazoans. The TCF transcriptional switch is mediated by many co-regulators that contribute to repression or activation of Wnt target genes. It is typically assumed that DNA recognition by TCFs is important for target gene location, but plays no role in the actual switch. TCF/Pangolin (the fly TCF) and some vertebrate TCF isoforms bind DNA through two distinct domains, a High Mobility Group (HMG) domain and a C-clamp, which recognize DNA motifs known as HMG and Helper sites, respectively. Here, we demonstrate that POP-1 (the C. elegans TCF) also activates target genes through HMG and Helper site interactions. Helper sites enhanced the ability of a synthetic enhancer to detect Wnt/ß-catenin signaling in several tissues and revealed an unsuspected role for POP-1 in regulating the C. elegans defecation cycle. Searching for HMG-Helper site clusters allowed the identification of a new POP-1 target gene active in the head muscles and gut. While Helper sites and the C-clamp are essential for activation of worm and fly Wnt targets, they are dispensable for TCF-dependent repression of targets in the absence of Wnt signaling. These data suggest that a fundamental change in TCF-DNA binding contributes to the transcriptional switch that occurs upon Wnt stimulation. Regulation of gene expression by signaling pathways often occurs through a transcriptional switch, where the transcription factor responsible for signal-dependent gene activation represses the same targets in the absence of signaling. T-cell factors (TCFs) are transcription factors in the Wnt/ß-catenin pathway, which control numerous cell fate specification events in metazoans. The TCF transcriptional switch is mediated by many co-regulators that contribute to repression or activation of Wnt target genes. It is typically assumed that DNA recognition by TCFs is important for target gene location, but plays no role in the actual switch. TCF/Pangolin (the fly TCF) and some vertebrate TCF isoforms bind DNA through two distinct domains, a High Mobility Group (HMG) domain and a C-clamp, which recognize DNA motifs known as HMG and Helper sites, respectively. Here, we demonstrate that POP-1 (the C. elegans TCF) also activates target genes through HMG and Helper site interactions. Helper sites enhanced the ability of a synthetic enhancer to detect Wnt/ß-catenin signaling in several tissues and revealed an unsuspected role for POP-1 in regulating the C. elegans defecation cycle. Searching for HMG-Helper site clusters allowed the identification of a new POP-1 target gene active in the head muscles and gut. While Helper sites and the C-clamp are essential for activation of worm and fly Wnt targets, they are dispensable for TCF-dependent repression of targets in the absence of Wnt signaling. These data suggest that a fundamental change in TCF-DNA binding contributes to the transcriptional switch that occurs upon Wnt stimulation.Regulation of gene expression by signaling pathways often occurs through a transcriptional switch, where the transcription factor responsible for signal-dependent gene activation represses the same targets in the absence of signaling. T-cell factors (TCFs) are transcription factors in the Wnt/ß-catenin pathway, which control numerous cell fate specification events in metazoans. The TCF transcriptional switch is mediated by many co-regulators that contribute to repression or activation of Wnt target genes. It is typically assumed that DNA recognition by TCFs is important for target gene location, but plays no role in the actual switch. TCF/Pangolin (the fly TCF) and some vertebrate TCF isoforms bind DNA through two distinct domains, a High Mobility Group (HMG) domain and a C-clamp, which recognize DNA motifs known as HMG and Helper sites, respectively. Here, we demonstrate that POP-1 (the C. elegans TCF) also activates target genes through HMG and Helper site interactions. Helper sites enhanced the ability of a synthetic enhancer to detect Wnt/ß-catenin signaling in several tissues and revealed an unsuspected role for POP-1 in regulating the C. elegans defecation cycle. Searching for HMG-Helper site clusters allowed the identification of a new POP-1 target gene active in the head muscles and gut. While Helper sites and the C-clamp are essential for activation of worm and fly Wnt targets, they are dispensable for TCF-dependent repression of targets in the absence of Wnt signaling. These data suggest that a fundamental change in TCF-DNA binding contributes to the transcriptional switch that occurs upon Wnt stimulation. Regulation of gene expression by signaling pathways often occurs through a transcriptional switch, where the transcription factor responsible for signal-dependent gene activation represses the same targets in the absence of signaling. T-cell factors (TCFs) are transcription factors in the Wnt/ß-catenin pathway, which control numerous cell fate specification events in metazoans. The TCF transcriptional switch is mediated by many co-regulators that contribute to repression or activation of Wnt target genes. It is typically assumed that DNA recognition by TCFs is important for target gene location, but plays no role in the actual switch. TCF/Pangolin (the fly TCF) and some vertebrate TCF isoforms bind DNA through two distinct domains, a High Mobility Group (HMG) domain and a C-clamp, which recognize DNA motifs known as HMG and Helper sites, respectively. Here, we demonstrate that POP-1 (the C. elegans TCF) also activates target genes through HMG and Helper site interactions. Helper sites enhanced the ability of a synthetic enhancer to detect Wnt/ß-catenin signaling in several tissues and revealed an unsuspected role for POP-1 in regulating the C. elegans defecation cycle. Searching for HMG-Helper site clusters allowed the identification of a new POP-1 target gene active in the head muscles and gut. While Helper sites and the C-clamp are essential for activation of worm and fly Wnt targets, they are dispensable for TCF-dependent repression of targets in the absence of Wnt signaling. These data suggest that a fundamental change in TCF-DNA binding contributes to the transcriptional switch that occurs upon Wnt stimulation. The DNA of cells must be correctly “read” so that the proper genes are expressed. Transcription factors are the primary “DNA readers”, and these proteins bind to specific DNA sequences. Using nematodes as a model system, we investigated the rules of DNA binding for a particular transcription factor, called POP-1, which mediates Wnt signaling, an important cell-cell communication pathway. In addition to its known DNA binding site, we found that POP-1 recognizes additional sequences, termed Helper sites, which are essential for activation of Wnt targets. We used this knowledge to discover that Wnt signaling is active in pacemaker cells in the nematode intestine, which control defecation, a rhythmic behavior with parallels to the vertebrate heartbeat. POP-1 has a dual role in regulating Wnt targets, repressing target genes in the absence of signaling and activating them upon signal stimulation. Surprisingly, we found that Helper sites are only required for activation and not repression, and that this is also the case in the fruit fly Drosophila . This work thus reveals an unexpected complexity in POP-1 DNA binding, which is likely to be relevant for its human counterparts, which play important roles in stem cell biology and cancer. |
| Audience | Academic |
| Author | Ravindranath, Aditi J. Yang, Yaxuan X. Korswagen, Hendrik C. Betist, Marco C. Bhambhani, Chandan Koushika, Sandhya P. Chang, Mikyung V. Cadigan, Ken M. Mentink, Remco A. |
| AuthorAffiliation | Harvard University, United States of America 2 Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences and University Medical Center Utrecht, Utrecht, The Netherlands 1 Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, Michigan, United States of America 3 Department of Biological Sciences, Tata Institute of Fundamental Research, Colaba, Mumbai, India |
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| Author_xml | – sequence: 1 givenname: Chandan surname: Bhambhani fullname: Bhambhani, Chandan – sequence: 2 givenname: Aditi J. surname: Ravindranath fullname: Ravindranath, Aditi J. – sequence: 3 givenname: Remco A. surname: Mentink fullname: Mentink, Remco A. – sequence: 4 givenname: Mikyung V. surname: Chang fullname: Chang, Mikyung V. – sequence: 5 givenname: Marco C. surname: Betist fullname: Betist, Marco C. – sequence: 6 givenname: Yaxuan X. surname: Yang fullname: Yang, Yaxuan X. – sequence: 7 givenname: Sandhya P. surname: Koushika fullname: Koushika, Sandhya P. – sequence: 8 givenname: Hendrik C. surname: Korswagen fullname: Korswagen, Hendrik C. – sequence: 9 givenname: Ken M. surname: Cadigan fullname: Cadigan, Ken M. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24516405$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2014 Public Library of Science 2014 Bhambhani et al 2014 Bhambhani et al 2014 Bhambhani et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Bhambhani C, Ravindranath AJ, Mentink RA, Chang MV, Betist MC, et al. (2014) Distinct DNA Binding Sites Contribute to the TCF Transcriptional Switch in C. elegans and Drosophila. PLoS Genet 10(2): e1004133. doi:10.1371/journal.pgen.1004133 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: CB AJR MVC HCK KMC. Performed the experiments: CB AJR MVC RAM MCB YXY KMC. Analyzed the data: CB AJR MVC RAM YXY HCK KMC. Contributed reagents/materials/analysis tools: SPK. Wrote the paper: CB KMC. The authors have declared that no competing interests exist. |
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| SubjectTerms | Animals Binding Sites Biology Caenorhabditis elegans - genetics Caenorhabditis elegans - metabolism Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Deoxyribonucleic acid DNA DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism DNA-ligand interactions Drosophila Drosophila - genetics Drosophila - metabolism Drosophila Proteins - genetics Drosophila Proteins - metabolism Experiments Gene expression Gene Expression Regulation Genetic aspects Genetic transcription Genomics High Mobility Group Proteins - genetics High Mobility Group Proteins - metabolism HMG-Box Domains - genetics Insects Mutation Nematodes Nucleotide Motifs - genetics Protein Binding Repressor Proteins - genetics Repressor Proteins - metabolism Signal Transduction - genetics Transcription factors Wnt Signaling Pathway - genetics |
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| Title | Distinct DNA Binding Sites Contribute to the TCF Transcriptional Switch in C. elegans and Drosophila |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/24516405 https://www.proquest.com/docview/1499150628 https://pubmed.ncbi.nlm.nih.gov/PMC3916239 https://doaj.org/article/8a64b1389d3949cba82f92d6ddde5849 http://dx.doi.org/10.1371/journal.pgen.1004133 |
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