Transcriptional regulation of Wnt inhibitory factor-1 by Miz-1 c-Myc
The Wnt signaling pathway is capable of self-regulation through positive and negative feedback mechanisms. For example, the oncoprotein c-Myc, which is upregulated by Wnt signaling activity, participates in a positive feedback loop of canonical Wnt signaling through repression of Wnt antagonists DKK...
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| Published in: | Oncogene Vol. 29; no. 44; pp. 5923 - 5934 |
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| Main Authors: | , , , , , , |
| Format: | Journal Article |
| Language: | English |
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04-11-2010
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| Abstract | The Wnt signaling pathway is capable of self-regulation through positive and negative feedback mechanisms. For example, the oncoprotein c-Myc, which is upregulated by Wnt signaling activity, participates in a positive feedback loop of canonical Wnt signaling through repression of Wnt antagonists
DKK1
and
SFRP1
. In this study, we investigated the mechanism of Wnt inhibitory factor-1 (
WIF-1
) silencing. Mapping of CpG island methylation of the
WIF-1
promoter reveals regional methylation (−295 to −95 bp from the transcription start site) that correlates with transcriptional silencing. We identified Miz-1 as a direct activator of
WIF-1
transcriptional activity, which is found at
WIF-1
promoter. In addition, we show that c-Myc contributes to
WIF-1
transcriptional repression in a Miz-1-dependent manner. Although the transient repression mediated by Miz-1/c-Myc is independent of
de novo
methylation, the stable repression by this complex is associated with CpG island methylation of the critical −295 to −95-bp region of the
WIF-1
promoter. Importantly, Miz-1 and c-Myc are found at
WIF-1
promoter in
WIF-1
non-expressing cell lines DLD-1 and 209
myc
. Transient knockdown or somatic knockout of c-Myc in DLD-1 failed to restore
WIF-1
expression suggesting that c-Myc is involved in initiating rather than maintaining
WIF-1
epigenetic silencing. In a genome-wide screen,
DNAJA4
,
TGFβ-induced
and
TRIM59
were repressed by c-Myc overexpression and DNA promoter hypermethylation. Our data reveal novel insights into c-Myc-mediated DNA methylation-dependent transcriptional silencing, a mechanism that might contribute to the dysregulation of Wnt signaling in cancer. |
|---|---|
| AbstractList | The Wnt signaling pathway is capable of self-regulation through positive and negative feedback mechanisms. For example, the oncoprotein c-Myc, which is upregulated by Wnt signaling activity, participates in a positive feedback loop of canonical Wnt signaling through repression of Wnt antagonists
DKK1
and
SFRP1
. In this study, we investigated the mechanism of Wnt inhibitory factor-1 (
WIF-1
) silencing. Mapping of CpG island methylation of the
WIF-1
promoter reveals regional methylation (–295 to –95 bp from the transcription start site) that correlates with transcriptional silencing. We identified Miz-1 as a direct activator of
WIF-1
transcriptional activity, which is found at
WIF-1
promoter. In addition, we show that c-Myc contributes to
WIF-1
transcriptional repression in a Miz-1-dependent manner. Although the transient repression mediated by Miz-1/c-Myc is independent of
de novo
methylation, the stable repression by this complex is associated with CpG island methylation of the critical –295 to –95-bp region of the
WIF-1
promoter. Importantly, Miz-1 and c-Myc are found at
WIF-1
promoter in
WIF-1
non-expressing cell lines DLD-1 and 209
myc
. Transient knockdown or somatic knockout of c-Myc in DLD-1 failed to restore
WIF-1
expression suggesting that c-Myc is involved in initiating rather than maintaining
WIF-1
epigenetic silencing. In a genome-wide screen,
DNAJA4, TGFβ-induced
and
TRIM59
were repressed by c-Myc overexpression and DNA promoter hypermethylation. Our data reveal novel insights into c-Myc-mediated DNA methylation-dependent transcriptional silencing, a mechanism that might contribute to the dysregulation of Wnt signaling in cancer. The Wnt signaling pathway is capable of self-regulation through positive and negative feedback mechanisms. For example, the oncoprotein c-Myc, which is upregulated by Wnt signaling activity, participates in a positive feedback loop of canonical Wnt signaling through repression of Wnt antagonists DKK1 and SFRP1 . In this study, we investigated the mechanism of Wnt inhibitory factor-1 ( WIF-1 ) silencing. Mapping of CpG island methylation of the WIF-1 promoter reveals regional methylation (−295 to −95 bp from the transcription start site) that correlates with transcriptional silencing. We identified Miz-1 as a direct activator of WIF-1 transcriptional activity, which is found at WIF-1 promoter. In addition, we show that c-Myc contributes to WIF-1 transcriptional repression in a Miz-1-dependent manner. Although the transient repression mediated by Miz-1/c-Myc is independent of de novo methylation, the stable repression by this complex is associated with CpG island methylation of the critical −295 to −95-bp region of the WIF-1 promoter. Importantly, Miz-1 and c-Myc are found at WIF-1 promoter in WIF-1 non-expressing cell lines DLD-1 and 209 myc . Transient knockdown or somatic knockout of c-Myc in DLD-1 failed to restore WIF-1 expression suggesting that c-Myc is involved in initiating rather than maintaining WIF-1 epigenetic silencing. In a genome-wide screen, DNAJA4 , TGFβ-induced and TRIM59 were repressed by c-Myc overexpression and DNA promoter hypermethylation. Our data reveal novel insights into c-Myc-mediated DNA methylation-dependent transcriptional silencing, a mechanism that might contribute to the dysregulation of Wnt signaling in cancer. The Wnt signaling pathway is capable of self-regulation through positive and negative feedback mechanisms. For example, the oncoprotein c-Myc, which is upregulated by Wnt signaling activity, participates in a positive feedback loop of canonical Wnt signaling through repression of Wnt antagonists DKK1 and SFRP1. In this study, we investigated the mechanism of Wnt inhibitory factor-1 (WIF-1) silencing. Mapping of CpG island methylation of the WIF-1 promoter reveals regional methylation (-295 to -95bp from the transcription start site) that correlates with transcriptional silencing. We identified Miz-1 as a direct activator of WIF-1 transcriptional activity, which is found at WIF-1 promoter. In addition, we show that c-Myc contributes to WIF-1 transcriptional repression in a Miz-1-dependent manner. Although the transient repression mediated by Miz-1/c-Myc is independent of de novo methylation, the stable repression by this complex is associated with CpG island methylation of the critical -295 to -95-bp region of the WIF-1 promoter. Importantly, Miz-1 and c-Myc are found at WIF-1 promoter in WIF-1 non-expressing cell lines DLD-1 and 209myc. Transient knockdown or somatic knockout of c-Myc in DLD-1 failed to restore WIF-1 expression suggesting that c-Myc is involved in initiating rather than maintaining WIF-1 epigenetic silencing. In a genome-wide screen, DNAJA4, TGF beta -induced and TRIM59 were repressed by c-Myc overexpression and DNA promoter hypermethylation. Our data reveal novel insights into c-Myc-mediated DNA methylation-dependent transcriptional silencing, a mechanism that might contribute to the dysregulation of Wnt signaling in cancer. The Wnt signaling pathway is capable of self-regulation through positive and negative feedback mechanisms. For example, the oncoprotein c-Myc, which is upregulated by Wnt signaling activity, participates in a positive feedback loop of canonical Wnt signaling through repression of Wnt antagonists DKK1 and SFRP1. In this study, we investigated the mechanism of Wnt inhibitory factor-1 (WIF-1) silencing. Mapping of CpG island methylation of the WIF-1 promoter reveals regional methylation (-295 to -95 bp from the transcription start site) that correlates with transcriptional silencing. We identified Miz-1 as a direct activator of WIF-1 transcriptional activity, which is found at WIF-1 promoter. In addition, we show that c-Myc contributes to WIF-1 transcriptional repression in a Miz-1-dependent manner. Although the transient repression mediated by Miz-1/c-Myc is independent of de novo methylation, the stable repression by this complex is associated with CpG island methylation of the critical -295 to -95-bp region of the WIF-1 promoter. Importantly, Miz-1 and c-Myc are found at WIF-1 promoter in WIF-1 non-expressing cell lines DLD-1 and 209myc. Transient knockdown or somatic knockout of c-Myc in DLD-1 failed to restore WIF-1 expression suggesting that c-Myc is involved in initiating rather than maintaining WIF-1 epigenetic silencing. In a genome-wide screen, DNAJA4, TGFβ-induced and TRIM59 were repressed by c-Myc overexpression and DNA promoter hypermethylation. Our data reveal novel insights into c-Myc-mediated DNA methylation-dependent transcriptional silencing, a mechanism that might contribute to the dysregulation of Wnt signaling in cancer. [PUBLICATION ABSTRACT] The Wnt signaling pathway is capable of self-regulation through positive and negative feedback mechanisms. For example, the oncoprotein c-Myc, which is upregulated by Wnt signaling activity, participates in a positive feedback loop of canonical Wnt signaling through repression of Wnt antagonists DKK1 and SFRP1. In this study, we investigated the mechanism of Wnt inhibitory factor-1 (WIF-1) silencing. Mapping of CpG island methylation of the WIF-1 promoter reveals regional methylation ( 295 to -95 bp from the transcription start site) that correlates with transcriptional silencing. We identified Miz-1 as a direct activator of WIF-1 transcriptional activity, which is found at WIF-1 promoter. In addition, we show that c-Myc contributes to WIF-1 transcriptional repression in a Miz-1-dependent manner. Although the transient repression mediated by Miz-1/c-Myc is independent of de novo methylation, the stable repression by this complex is associated with CpG island methylation of the critical -295 to -95-bp region of the WIF-1 promoter. Importantly, Miz-1 and c-Myc are found at WIF-1 promoter in WIF-1 non-expressing cell lines DLD-1 and 209myc. Transient knockdown or somatic knockout of c-Myc in DLD-1 failed to restore WIF-1 expression suggesting that c-Myc is involved in initiating rather than maintaining WIF-1 epigenetic silencing. In a genome-wide screen, DNAJA4, TGFji-induced and TRIM59 were repressed by c-Myc overexpression and DNA promoter hypermethylation. Our data reveal novel insights into c-Myc-mediated DNA methylation-dependent transcriptional silencing, a mechanism that might contribute to the dysregulation of Wnt signaling in cancer. The Wnt signaling pathway is capable of self-regulation through positive and negative feedback mechanisms. For example, the oncoprotein c-Myc, which is upregulated by Wnt signaling activity, participates in a positive feedback loop of canonical Wnt signaling through repression of Wnt antagonists DKK1 and SFRP1. In this study, we investigated the mechanism of Wnt inhibitory factor-1 (WIF-1) silencing. Mapping of CpG island methylation of the WIF-1 promoter reveals regional methylation ( 295 to -95 bp from the transcription start site) that correlates with transcriptional silencing. We identified Miz-1 as a direct activator of WIF-1 transcriptional activity, which is found at WIF-1 promoter. In addition, we show that c-Myc contributes to WIF-1 transcriptional repression in a Miz-1-dependent manner. Although the transient repression mediated by Miz-1/c-Myc is independent of de novo methylation, the stable repression by this complex is associated with CpG island methylation of the critical -295 to -95-bp region of the WIF-1 promoter. Importantly, Miz-1 and c-Myc are found at WIF-1 promoter in WIF-1 non-expressing cell lines DLD-1 and 209myc. Transient knockdown or somatic knockout of c-Myc in DLD-1 failed to restore WIF-1 expression suggesting that c-Myc is involved in initiating rather than maintaining WIF-1 epigenetic silencing. In a genome-wide screen, DNAJA4, TGFji-induced and TRIM59 were repressed by c-Myc overexpression and DNA promoter hypermethylation. Our data reveal novel insights into c-Myc-mediated DNA methylation-dependent transcriptional silencing, a mechanism that might contribute to the dysregulation of Wnt signaling in cancer. Oncogene (2010) 29, 5923-5934; doi: 10.1038/onc.2010.322; published online 9 August 2010 Keywords: WIF-1; Wnt signaling; c-Myc; Miz-1; DNA methylation The Wnt signaling pathway is capable of self-regulation through positive and negative feedback mechanisms. For example, the oncoprotein c-Myc, which is upregulated by Wnt signaling activity, participates in a positive feedback loop of canonical Wnt signaling through repression of Wnt antagonists DKK1 and SFRP1. In this study, we investigated the mechanism of Wnt inhibitory factor-1 (WIF-1) silencing. Mapping of CpG island methylation of the WIF-1 promoter reveals regional methylation (-295 to -95 bp from the transcription start site) that correlates with transcriptional silencing. We identified Miz-1 as a direct activator of WIF-1 transcriptional activity, which is found at WIF-1 promoter. In addition, we show that c-Myc contributes to WIF-1 transcriptional repression in a Miz-1-dependent manner. Although the transient repression mediated by Miz-1/c-Myc is independent of de novo methylation, the stable repression by this complex is associated with CpG island methylation of the critical -295 to -95-bp region of the WIF-1 promoter. Importantly, Miz-1 and c-Myc are found at WIF-1 promoter in WIF-1 non-expressing cell lines DLD-1 and 209myc. Transient knockdown or somatic knockout of c-Myc in DLD-1 failed to restore WIF-1 expression suggesting that c-Myc is involved in initiating rather than maintaining WIF-1 epigenetic silencing. In a genome-wide screen, DNAJA4, TGFβ-induced and TRIM59 were repressed by c-Myc overexpression and DNA promoter hypermethylation. Our data reveal novel insights into c-Myc-mediated DNA methylation-dependent transcriptional silencing, a mechanism that might contribute to the dysregulation of Wnt signaling in cancer. The Wnt signaling pathway is capable of self-regulation through positive and negative feedback mechanisms. For example, the oncoprotein c-Myc, which is upregulated by Wnt signaling activity, participates in a positive feedback loop of canonical Wnt signaling through repression of Wnt antagonists DKK1 and SFRP1. In this study, we investigated the mechanism of Wnt inhibitory factor-1 (WIF-1) silencing. Mapping of CpG island methylation of the WIF-1 promoter reveals regional methylation (−295 to −95 bp from the transcription start site) that correlates with transcriptional silencing. We identified Miz-1 as a direct activator of WIF-1 transcriptional activity, which is found at WIF-1 promoter. In addition, we show that c-Myc contributes to WIF-1 transcriptional repression in a Miz-1-dependent manner. Although the transient repression mediated by Miz-1/c-Myc is independent of de novo methylation, the stable repression by this complex is associated with CpG island methylation of the critical −295 to −95-bp region of the WIF-1 promoter. Importantly, Miz-1 and c-Myc are found at WIF-1 promoter in WIF-1 non-expressing cell lines DLD-1 and 209myc. Transient knockdown or somatic knockout of c-Myc in DLD-1 failed to restore WIF-1 expression suggesting that c-Myc is involved in initiating rather than maintaining WIF-1 epigenetic silencing. In a genome-wide screen, DNAJA4, TGFβ-induced and TRIM59 were repressed by c-Myc overexpression and DNA promoter hypermethylation. Our data reveal novel insights into c-Myc-mediated DNA methylation-dependent transcriptional silencing, a mechanism that might contribute to the dysregulation of Wnt signaling in cancer. |
| Audience | Academic |
| Author | Cope, L Licchesi, J D F Van Neste, L Lin, X Baylin, S B Herman, J G Tiwari, V K |
| AuthorAffiliation | 3 Department of Molecular Biotechnology, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium 1 Cancer Biology Program, The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD, USA 2 MRC Laboratory of Molecular Biology, Cambridge, UK 4 Department of Applied Mathematics and Statistics, Whiting School of Engineering, Johns Hopkins University, Baltimore, MD, USA |
| AuthorAffiliation_xml | – name: 2 MRC Laboratory of Molecular Biology, Cambridge, UK – name: 1 Cancer Biology Program, The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD, USA – name: 4 Department of Applied Mathematics and Statistics, Whiting School of Engineering, Johns Hopkins University, Baltimore, MD, USA – name: 3 Department of Molecular Biotechnology, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium |
| Author_xml | – sequence: 1 givenname: J D F surname: Licchesi fullname: Licchesi, J D F email: jlicchesi@yahoo.com organization: Cancer Biology Program, The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, MRC Laboratory of Molecular Biology – sequence: 2 givenname: L surname: Van Neste fullname: Van Neste, L organization: Department of Molecular Biotechnology, Faculty of Bioscience Engineering, Ghent University – sequence: 3 givenname: V K surname: Tiwari fullname: Tiwari, V K organization: Cancer Biology Program, The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins – sequence: 4 givenname: L surname: Cope fullname: Cope, L organization: Cancer Biology Program, The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins – sequence: 5 givenname: X surname: Lin fullname: Lin, X organization: Department of Applied Mathematics and Statistics, Whiting School of Engineering, Johns Hopkins University – sequence: 6 givenname: S B surname: Baylin fullname: Baylin, S B organization: Cancer Biology Program, The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins – sequence: 7 givenname: J G surname: Herman fullname: Herman, J G email: hermanji@jhmi.edu organization: Cancer Biology Program, The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins |
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| Copyright | Macmillan Publishers Limited 2010 2015 INIST-CNRS COPYRIGHT 2010 Nature Publishing Group Macmillan Publishers Limited 2010. Copyright Nature Publishing Group Nov 4, 2010 2010 Macmillan Publishers Limited All rights reserved 2010 |
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| Keywords | DNA methylation Wnt signaling Miz-1 c-Myc Transcription Carcinogenesis Cell signaling Signal transduction Regulation(control) WIF-1 DNA C-Onc gene Methylation Protooncogene |
| Language | English |
| License | CC BY 4.0 |
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| OpenAccessLink | http://dx.doi.org/10.1038/onc.2010.322 |
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| PublicationDate | 11-4-2010 |
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| PublicationTitle | Oncogene |
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| PublicationYear | 2010 |
| Publisher | Nature Publishing Group UK Nature Publishing Group |
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| Snippet | The Wnt signaling pathway is capable of self-regulation through positive and negative feedback mechanisms. For example, the oncoprotein c-Myc, which is... |
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| SubjectTerms | 631/208/176/1988 631/337/176/2016 631/337/572 Adaptor Proteins, Signal Transducing - genetics Anopheles Antagonists Apoptosis Biological and medical sciences c-Myc protein Cancer Care and treatment Cell Biology Cell Line, Tumor Cell physiology Cell transformation and carcinogenesis. Action of oncogenes and antioncogenes Cellular biology Chromatin Immunoprecipitation CpG islands Dkk1 protein DNA DNA Methylation Epigenetics Feedback Frizzled-related protein 1 Fundamental and applied biological sciences. Psychology Gene expression Gene Expression Regulation - physiology Gene mapping Gene regulation Gene Silencing Genetic aspects Genomes Human Genetics Humans Internal Medicine Kruppel-Like Transcription Factors - physiology Medicine Medicine & Public Health Methylation Molecular and cellular biology Molecular genetics Myc protein Oncology original-article Promoter Regions, Genetic Proteins Proto-Oncogene Proteins c-myc - physiology Repressor Proteins - genetics Reverse Transcriptase Polymerase Chain Reaction Signal transduction Transcription, Genetic - physiology Transcription. Transcription factor. Splicing. Rna processing Wnt protein |
| Title | Transcriptional regulation of Wnt inhibitory factor-1 by Miz-1 c-Myc |
| URI | http://dx.doi.org/10.1038/onc.2010.322 https://link.springer.com/article/10.1038/onc.2010.322 https://www.ncbi.nlm.nih.gov/pubmed/20697356 https://www.proquest.com/docview/2641412599 https://www.proquest.com/docview/762713181 https://search.proquest.com/docview/762483612 https://search.proquest.com/docview/864954288 https://pubmed.ncbi.nlm.nih.gov/PMC3230129 |
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