The role of GRHL2 and epigenetic remodeling in epithelial–mesenchymal plasticity in ovarian cancer cells

Cancer cells exhibit phenotypic plasticity during epithelial–mesenchymal transition (EMT) and mesenchymal–epithelial transition (MET) involving intermediate states. To study genome-wide epigenetic remodeling associated with EMT plasticity, we integrate the analyses of DNA methylation, ChIP-sequencin...

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Published inCommunications biology Vol. 2; no. 1; p. 272
Main Authors Chung, Vin Yee, Tan, Tuan Zea, Ye, Jieru, Huang, Rui-Lan, Lai, Hung-Cheng, Kappei, Dennis, Wollmann, Heike, Guccione, Ernesto, Huang, Ruby Yun-Ju
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 24.07.2019
Nature Publishing Group
Subjects
45/91
631/136/142
631/208/176
631/67/1517/1709
Binding sites
Biology
Biomedical and Life Sciences
Cell Line, Tumor
CpG Islands
DNA Methylation
DNA sequencing
DNA-Binding Proteins - genetics
DNA-Binding Proteins - physiology
Epigenesis, Genetic - physiology
Epigenetics
Epithelial-Mesenchymal Transition - genetics
Epithelial-Mesenchymal Transition - physiology
Female
Gene expression
Gene Knockdown Techniques
Genomes
Histones - metabolism
Humans
Life Sciences
Mesenchyme
Ovarian cancer
Ovarian Neoplasms - pathology
Phenotypic plasticity
Promoters
Transcription Factors - genetics
Transcription Factors - physiology
Epigenetics
Differentiation
Ovarian cancer
Online AccessGet full text

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Abstract Cancer cells exhibit phenotypic plasticity during epithelial–mesenchymal transition (EMT) and mesenchymal–epithelial transition (MET) involving intermediate states. To study genome-wide epigenetic remodeling associated with EMT plasticity, we integrate the analyses of DNA methylation, ChIP-sequencing of five histone marks (H3K4me1, H3K4me3, H3K27Ac, H3K27me3 and H3K9me3) and transcriptome profiling performed on ovarian cancer cells with different epithelial/mesenchymal states and on a knockdown model of EMT suppressor Grainyhead-like 2 (GRHL2). We have identified differentially methylated CpG sites associated with EMT, found at promoters of epithelial genes and GRHL2 binding sites. GRHL2 knockdown results in CpG methylation gain and nucleosomal remodeling (reduction in permissive marks H3K4me3 and H3K27ac; elevated repressive mark H3K27me3), resembling the changes observed across progressive EMT states. Epigenetic-modifying agents such as 5-azacitidine, GSK126 and mocetinostat further reveal cell state-dependent plasticity upon GRHL2 overexpression. Overall, we demonstrate that epithelial genes are subject to epigenetic control during intermediate phases of EMT/MET involving GRHL2. Vin Yee Chung et al. identify differentially methylated CpG sites in the promoters of epithelial genes and GRHL2 binding sites in ovarian cancer cells during the epithelial–mesenchymal transition. They find that GRHL2 knockdown or overexpression affects methylation, suggesting a role for this transcription factor in epigenetic remodeling.
AbstractList Cancer cells exhibit phenotypic plasticity during epithelial-mesenchymal transition (EMT) and mesenchymal-epithelial transition (MET) involving intermediate states. To study genome-wide epigenetic remodeling associated with EMT plasticity, we integrate the analyses of DNA methylation, ChIP-sequencing of five histone marks (H3K4me1, H3K4me3, H3K27Ac, H3K27me3 and H3K9me3) and transcriptome profiling performed on ovarian cancer cells with different epithelial/mesenchymal states and on a knockdown model of EMT suppressor Grainyhead-like 2 (GRHL2). We have identified differentially methylated CpG sites associated with EMT, found at promoters of epithelial genes and GRHL2 binding sites. GRHL2 knockdown results in CpG methylation gain and nucleosomal remodeling (reduction in permissive marks H3K4me3 and H3K27ac; elevated repressive mark H3K27me3), resembling the changes observed across progressive EMT states. Epigenetic-modifying agents such as 5-azacitidine, GSK126 and mocetinostat further reveal cell state-dependent plasticity upon GRHL2 overexpression. Overall, we demonstrate that epithelial genes are subject to epigenetic control during intermediate phases of EMT/MET involving GRHL2.
Cancer cells exhibit phenotypic plasticity during epithelial–mesenchymal transition (EMT) and mesenchymal–epithelial transition (MET) involving intermediate states. To study genome-wide epigenetic remodeling associated with EMT plasticity, we integrate the analyses of DNA methylation, ChIP-sequencing of five histone marks (H3K4me1, H3K4me3, H3K27Ac, H3K27me3 and H3K9me3) and transcriptome profiling performed on ovarian cancer cells with different epithelial/mesenchymal states and on a knockdown model of EMT suppressor Grainyhead-like 2 (GRHL2). We have identified differentially methylated CpG sites associated with EMT, found at promoters of epithelial genes and GRHL2 binding sites. GRHL2 knockdown results in CpG methylation gain and nucleosomal remodeling (reduction in permissive marks H3K4me3 and H3K27ac; elevated repressive mark H3K27me3), resembling the changes observed across progressive EMT states. Epigenetic-modifying agents such as 5-azacitidine, GSK126 and mocetinostat further reveal cell state-dependent plasticity upon GRHL2 overexpression. Overall, we demonstrate that epithelial genes are subject to epigenetic control during intermediate phases of EMT/MET involving GRHL2. Vin Yee Chung et al. identify differentially methylated CpG sites in the promoters of epithelial genes and GRHL2 binding sites in ovarian cancer cells during the epithelial–mesenchymal transition. They find that GRHL2 knockdown or overexpression affects methylation, suggesting a role for this transcription factor in epigenetic remodeling.
Cancer cells exhibit phenotypic plasticity during epithelial–mesenchymal transition (EMT) and mesenchymal–epithelial transition (MET) involving intermediate states. To study genome-wide epigenetic remodeling associated with EMT plasticity, we integrate the analyses of DNA methylation, ChIP-sequencing of five histone marks (H3K4me1, H3K4me3, H3K27Ac, H3K27me3 and H3K9me3) and transcriptome profiling performed on ovarian cancer cells with different epithelial/mesenchymal states and on a knockdown model of EMT suppressor Grainyhead-like 2 (GRHL2). We have identified differentially methylated CpG sites associated with EMT, found at promoters of epithelial genes and GRHL2 binding sites. GRHL2 knockdown results in CpG methylation gain and nucleosomal remodeling (reduction in permissive marks H3K4me3 and H3K27ac; elevated repressive mark H3K27me3), resembling the changes observed across progressive EMT states. Epigenetic-modifying agents such as 5-azacitidine, GSK126 and mocetinostat further reveal cell state-dependent plasticity upon GRHL2 overexpression. Overall, we demonstrate that epithelial genes are subject to epigenetic control during intermediate phases of EMT/MET involving GRHL2.Vin Yee Chung et al. identify differentially methylated CpG sites in the promoters of epithelial genes and GRHL2 binding sites in ovarian cancer cells during the epithelial–mesenchymal transition. They find that GRHL2 knockdown or overexpression affects methylation, suggesting a role for this transcription factor in epigenetic remodeling.
Cancer cells exhibit phenotypic plasticity during epithelial-mesenchymal transition (EMT) and mesenchymal-epithelial transition (MET) involving intermediate states. To study genome-wide epigenetic remodeling associated with EMT plasticity, we integrate the analyses of DNA methylation, ChIP-sequencing of five histone marks (H3K4me1, H3K4me3, H3K27Ac, H3K27me3 and H3K9me3) and transcriptome profiling performed on ovarian cancer cells with different epithelial/mesenchymal states and on a knockdown model of EMT suppressor Grainyhead-like 2 (GRHL2). We have identified differentially methylated CpG sites associated with EMT, found at promoters of epithelial genes and GRHL2 binding sites. GRHL2 knockdown results in CpG methylation gain and nucleosomal remodeling (reduction in permissive marks H3K4me3 and H3K27ac; elevated repressive mark H3K27me3), resembling the changes observed across progressive EMT states. Epigenetic-modifying agents such as 5-azacitidine, GSK126 and mocetinostat further reveal cell state-dependent plasticity upon GRHL2 overexpression. Overall, we demonstrate that epithelial genes are subject to epigenetic control during intermediate phases of EMT/MET involving GRHL2.Cancer cells exhibit phenotypic plasticity during epithelial-mesenchymal transition (EMT) and mesenchymal-epithelial transition (MET) involving intermediate states. To study genome-wide epigenetic remodeling associated with EMT plasticity, we integrate the analyses of DNA methylation, ChIP-sequencing of five histone marks (H3K4me1, H3K4me3, H3K27Ac, H3K27me3 and H3K9me3) and transcriptome profiling performed on ovarian cancer cells with different epithelial/mesenchymal states and on a knockdown model of EMT suppressor Grainyhead-like 2 (GRHL2). We have identified differentially methylated CpG sites associated with EMT, found at promoters of epithelial genes and GRHL2 binding sites. GRHL2 knockdown results in CpG methylation gain and nucleosomal remodeling (reduction in permissive marks H3K4me3 and H3K27ac; elevated repressive mark H3K27me3), resembling the changes observed across progressive EMT states. Epigenetic-modifying agents such as 5-azacitidine, GSK126 and mocetinostat further reveal cell state-dependent plasticity upon GRHL2 overexpression. Overall, we demonstrate that epithelial genes are subject to epigenetic control during intermediate phases of EMT/MET involving GRHL2.
ArticleNumber 272
Author Kappei, Dennis
Wollmann, Heike
Huang, Ruby Yun-Ju
Chung, Vin Yee
Tan, Tuan Zea
Ye, Jieru
Lai, Hung-Cheng
Huang, Rui-Lan
Guccione, Ernesto
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  surname: Tan
  fullname: Tan, Tuan Zea
  organization: Cancer Science Institute of Singapore, National University of Singapore
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  givenname: Jieru
  surname: Ye
  fullname: Ye, Jieru
  organization: Cancer Science Institute of Singapore, National University of Singapore
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  surname: Huang
  fullname: Huang, Rui-Lan
  organization: Department of Obstetrics and Gynecology, Shuang Ho Hospital, Taipei Medical University
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  surname: Wollmann
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  organization: Institute of Molecular and Cell Biology, ASTAR
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  organization: Institute of Molecular and Cell Biology, ASTAR
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  givenname: Ruby Yun-Ju
  surname: Huang
  fullname: Huang, Ruby Yun-Ju
  email: csihyjr@nus.edu.sg, rubyhuang@ntu.edu.tw
  organization: Cancer Science Institute of Singapore, National University of Singapore, School of Medicine, College of Medicine, National Taiwan University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31372511$$D View this record in MEDLINE/PubMed
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Issue 1
Keywords Epigenetics
Differentiation
Ovarian cancer
Language English
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Snippet Cancer cells exhibit phenotypic plasticity during epithelial–mesenchymal transition (EMT) and mesenchymal–epithelial transition (MET) involving intermediate...
Cancer cells exhibit phenotypic plasticity during epithelial-mesenchymal transition (EMT) and mesenchymal-epithelial transition (MET) involving intermediate...
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SubjectTerms 45/91
631/136/142
631/208/176
631/67/1517/1709
Binding sites
Biology
Biomedical and Life Sciences
Cell Line, Tumor
CpG Islands
DNA Methylation
DNA sequencing
DNA-Binding Proteins - genetics
DNA-Binding Proteins - physiology
Epigenesis, Genetic - physiology
Epigenetics
Epithelial-Mesenchymal Transition - genetics
Epithelial-Mesenchymal Transition - physiology
Female
Gene expression
Gene Knockdown Techniques
Genomes
Histones - metabolism
Humans
Life Sciences
Mesenchyme
Ovarian cancer
Ovarian Neoplasms - pathology
Phenotypic plasticity
Promoters
Transcription Factors - genetics
Transcription Factors - physiology
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Title The role of GRHL2 and epigenetic remodeling in epithelial–mesenchymal plasticity in ovarian cancer cells
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