Zeb1 potentiates genome‐wide gene transcription with Lef1 to promote glioblastoma cell invasion

Glioblastoma is the most common and aggressive brain tumor, with a subpopulation of stem‐like cells thought to mediate its recurring behavior and therapeutic resistance. The epithelial–mesenchymal transition (EMT) inducing factor Zeb1 was linked to tumor initiation, invasion, and resistance to thera...

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Published inThe EMBO journal Vol. 37; no. 15
Main Authors Rosmaninho, Pedro, Mükusch, Susanne, Piscopo, Valerio, Teixeira, Vera, Raposo, Alexandre ASF, Warta, Rolf, Bennewitz, Romina, Tang, Yeman, Herold‐Mende, Christel, Stifani, Stefano, Momma, Stefan, Castro, Diogo S
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.08.2018
Springer Nature B.V
John Wiley and Sons Inc
Subjects
Activation
Binding
Brain
Brain cancer
Brain tumors
cancer stem‐like cells
Cell migration
Cell Movement - genetics
Chromatin
Deoxyribonucleic acid
DNA
DNA-Binding Proteins - genetics
EMBO03
EMBO37
EMBO44
Epithelial-Mesenchymal Transition - genetics
Gene expression
Gene mapping
Gene silencing
Genes
Genomes
Glioblastoma
Glioblastoma - genetics
Glioblastoma - mortality
Glioblastoma - pathology
Glioblastoma cells
glioblastoma multiforme
Guanine
Guanine nucleotide exchange factor
Guanine Nucleotide Exchange Factors - genetics
Guanine Nucleotide Exchange Factors - metabolism
Humans
Invasiveness
Lef1 gene
Lymphoid Enhancer-Binding Factor 1 - genetics
Mesenchyme
Neoplasm Invasiveness - genetics
Recruitment
Regulators
Regulatory mechanisms (biology)
Regulatory sequences
Repressors
Signaling
Stem cells
transcription
Transcription factors
Transcription, Genetic - genetics
Transcriptional Activation - genetics
Tumors
Wnt protein
Wnt signaling
Wnt Signaling Pathway - genetics
Zeb1
Zinc Finger E-box-Binding Homeobox 1 - genetics
Zinc Finger E-box-Binding Homeobox 1 - metabolism
cancer stem‐like cells
Zeb1
glioblastoma multiforme
Wnt signaling
transcription
Online AccessGet full text

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Abstract Glioblastoma is the most common and aggressive brain tumor, with a subpopulation of stem‐like cells thought to mediate its recurring behavior and therapeutic resistance. The epithelial–mesenchymal transition (EMT) inducing factor Zeb1 was linked to tumor initiation, invasion, and resistance to therapy in glioblastoma, but how Zeb1 functions at molecular level and what genes it regulates remain poorly understood. Contrary to the common view that EMT factors act as transcriptional repressors, here we show that genome‐wide binding of Zeb1 associates with both activation and repression of gene expression in glioblastoma stem‐like cells. Transcriptional repression requires direct DNA binding of Zeb1, while indirect recruitment to regulatory regions by the Wnt pathway effector Lef1 results in gene activation, independently of Wnt signaling. Amongst glioblastoma genes activated by Zeb1 are predicted mediators of tumor cell migration and invasion, including the guanine nucleotide exchange factor Prex1, whose elevated expression is predictive of shorter glioblastoma patient survival. Prex1 promotes invasiveness of glioblastoma cells in vivo highlighting the importance of Zeb1/Lef1 gene regulatory mechanisms in gliomagenesis. Synopsis Genome‐wide characterization of Zeb1 transcriptional targets in glioblastoma stem cells reveals how Zeb1 coordinately regulates an EMT‐like program, simultaneously promoting gene activation and repression via two different mechanisms. ChIP‐seq mapping correlates transcriptional repression with direct Zeb1 binding to gene regulatory regions. Indirect recruitment mediated by Lef/Tcf factors potentiates gene expression independent of Wnt signaling. Activated genes include regulators of cell migration and invasion that correlate with Zeb1 expression in tumors. Zeb1 activates Prex1 to promote glioblastoma cell invasion in vivo . Graphical Abstract Genome‐wide binding reveals that the EMT‐inducer Zeb1, best‐known as a transcriptional repressor, can team up with a transcriptional activator to indirectly enhance gene expression.
AbstractList Glioblastoma is the most common and aggressive brain tumor, with a subpopulation of stem‐like cells thought to mediate its recurring behavior and therapeutic resistance. The epithelial–mesenchymal transition (EMT) inducing factor Zeb1 was linked to tumor initiation, invasion, and resistance to therapy in glioblastoma, but how Zeb1 functions at molecular level and what genes it regulates remain poorly understood. Contrary to the common view that EMT factors act as transcriptional repressors, here we show that genome‐wide binding of Zeb1 associates with both activation and repression of gene expression in glioblastoma stem‐like cells. Transcriptional repression requires direct DNA binding of Zeb1, while indirect recruitment to regulatory regions by the Wnt pathway effector Lef1 results in gene activation, independently of Wnt signaling. Amongst glioblastoma genes activated by Zeb1 are predicted mediators of tumor cell migration and invasion, including the guanine nucleotide exchange factor Prex1, whose elevated expression is predictive of shorter glioblastoma patient survival. Prex1 promotes invasiveness of glioblastoma cells in vivo highlighting the importance of Zeb1/Lef1 gene regulatory mechanisms in gliomagenesis. Synopsis Genome‐wide characterization of Zeb1 transcriptional targets in glioblastoma stem cells reveals how Zeb1 coordinately regulates an EMT‐like program, simultaneously promoting gene activation and repression via two different mechanisms. ChIP‐seq mapping correlates transcriptional repression with direct Zeb1 binding to gene regulatory regions. Indirect recruitment mediated by Lef/Tcf factors potentiates gene expression independent of Wnt signaling. Activated genes include regulators of cell migration and invasion that correlate with Zeb1 expression in tumors. Zeb1 activates Prex1 to promote glioblastoma cell invasion in vivo . Graphical Abstract Genome‐wide binding reveals that the EMT‐inducer Zeb1, best‐known as a transcriptional repressor, can team up with a transcriptional activator to indirectly enhance gene expression.
Glioblastoma is the most common and aggressive brain tumor, with a subpopulation of stem‐like cells thought to mediate its recurring behavior and therapeutic resistance. The epithelial–mesenchymal transition (EMT) inducing factor Zeb1 was linked to tumor initiation, invasion, and resistance to therapy in glioblastoma, but how Zeb1 functions at molecular level and what genes it regulates remain poorly understood. Contrary to the common view that EMT factors act as transcriptional repressors, here we show that genome‐wide binding of Zeb1 associates with both activation and repression of gene expression in glioblastoma stem‐like cells. Transcriptional repression requires direct DNA binding of Zeb1, while indirect recruitment to regulatory regions by the Wnt pathway effector Lef1 results in gene activation, independently of Wnt signaling. Amongst glioblastoma genes activated by Zeb1 are predicted mediators of tumor cell migration and invasion, including the guanine nucleotide exchange factor Prex1, whose elevated expression is predictive of shorter glioblastoma patient survival. Prex1 promotes invasiveness of glioblastoma cells in vivo highlighting the importance of Zeb1/Lef1 gene regulatory mechanisms in gliomagenesis.
Glioblastoma is the most common and aggressive brain tumor, with a subpopulation of stem-like cells thought to mediate its recurring behavior and therapeutic resistance. The epithelial-mesenchymal transition (EMT) inducing factor Zeb1 was linked to tumor initiation, invasion, and resistance to therapy in glioblastoma, but how Zeb1 functions at molecular level and what genes it regulates remain poorly understood. Contrary to the common view that EMT factors act as transcriptional repressors, here we show that genome-wide binding of Zeb1 associates with both activation and repression of gene expression in glioblastoma stem-like cells. Transcriptional repression requires direct DNA binding of Zeb1, while indirect recruitment to regulatory regions by the Wnt pathway effector Lef1 results in gene activation, independently of Wnt signaling. Amongst glioblastoma genes activated by Zeb1 are predicted mediators of tumor cell migration and invasion, including the guanine nucleotide exchange factor Prex1, whose elevated expression is predictive of shorter glioblastoma patient survival. Prex1 promotes invasiveness of glioblastoma cells in vivo highlighting the importance of Zeb1/Lef1 gene regulatory mechanisms in gliomagenesis.Glioblastoma is the most common and aggressive brain tumor, with a subpopulation of stem-like cells thought to mediate its recurring behavior and therapeutic resistance. The epithelial-mesenchymal transition (EMT) inducing factor Zeb1 was linked to tumor initiation, invasion, and resistance to therapy in glioblastoma, but how Zeb1 functions at molecular level and what genes it regulates remain poorly understood. Contrary to the common view that EMT factors act as transcriptional repressors, here we show that genome-wide binding of Zeb1 associates with both activation and repression of gene expression in glioblastoma stem-like cells. Transcriptional repression requires direct DNA binding of Zeb1, while indirect recruitment to regulatory regions by the Wnt pathway effector Lef1 results in gene activation, independently of Wnt signaling. Amongst glioblastoma genes activated by Zeb1 are predicted mediators of tumor cell migration and invasion, including the guanine nucleotide exchange factor Prex1, whose elevated expression is predictive of shorter glioblastoma patient survival. Prex1 promotes invasiveness of glioblastoma cells in vivo highlighting the importance of Zeb1/Lef1 gene regulatory mechanisms in gliomagenesis.
Glioblastoma is the most common and aggressive brain tumor, with a subpopulation of stem-like cells thought to mediate its recurring behavior and therapeutic resistance. The epithelial-mesenchymal transition (EMT) inducing factor Zeb1 was linked to tumor initiation, invasion, and resistance to therapy in glioblastoma, but how Zeb1 functions at molecular level and what genes it regulates remain poorly understood. Contrary to the common view that EMT factors act as transcriptional repressors, here we show that genome-wide binding of Zeb1 associates with both activation and repression of gene expression in glioblastoma stem-like cells. Transcriptional repression requires direct DNA binding of Zeb1, while indirect recruitment to regulatory regions by the Wnt pathway effector Lef1 results in gene activation, independently of Wnt signaling. Amongst glioblastoma genes activated by Zeb1 are predicted mediators of tumor cell migration and invasion, including the guanine nucleotide exchange factor Prex1, whose elevated expression is predictive of shorter glioblastoma patient survival. Prex1 promotes invasiveness of glioblastoma cells highlighting the importance of Zeb1/Lef1 gene regulatory mechanisms in gliomagenesis.
Glioblastoma is the most common and aggressive brain tumor, with a subpopulation of stem‐like cells thought to mediate its recurring behavior and therapeutic resistance. The epithelial–mesenchymal transition ( EMT ) inducing factor Zeb1 was linked to tumor initiation, invasion, and resistance to therapy in glioblastoma, but how Zeb1 functions at molecular level and what genes it regulates remain poorly understood. Contrary to the common view that EMT factors act as transcriptional repressors, here we show that genome‐wide binding of Zeb1 associates with both activation and repression of gene expression in glioblastoma stem‐like cells. Transcriptional repression requires direct DNA binding of Zeb1, while indirect recruitment to regulatory regions by the Wnt pathway effector Lef1 results in gene activation, independently of Wnt signaling. Amongst glioblastoma genes activated by Zeb1 are predicted mediators of tumor cell migration and invasion, including the guanine nucleotide exchange factor Prex1, whose elevated expression is predictive of shorter glioblastoma patient survival. Prex1 promotes invasiveness of glioblastoma cells in vivo highlighting the importance of Zeb1/Lef1 gene regulatory mechanisms in gliomagenesis.
Glioblastoma is the most common and aggressive brain tumor, with a subpopulation of stem‐like cells thought to mediate its recurring behavior and therapeutic resistance. The epithelial–mesenchymal transition (EMT) inducing factor Zeb1 was linked to tumor initiation, invasion, and resistance to therapy in glioblastoma, but how Zeb1 functions at molecular level and what genes it regulates remain poorly understood. Contrary to the common view that EMT factors act as transcriptional repressors, here we show that genome‐wide binding of Zeb1 associates with both activation and repression of gene expression in glioblastoma stem‐like cells. Transcriptional repression requires direct DNA binding of Zeb1, while indirect recruitment to regulatory regions by the Wnt pathway effector Lef1 results in gene activation, independently of Wnt signaling. Amongst glioblastoma genes activated by Zeb1 are predicted mediators of tumor cell migration and invasion, including the guanine nucleotide exchange factor Prex1, whose elevated expression is predictive of shorter glioblastoma patient survival. Prex1 promotes invasiveness of glioblastoma cells in vivo highlighting the importance of Zeb1/Lef1 gene regulatory mechanisms in gliomagenesis. Synopsis Genome‐wide characterization of Zeb1 transcriptional targets in glioblastoma stem cells reveals how Zeb1 coordinately regulates an EMT‐like program, simultaneously promoting gene activation and repression via two different mechanisms. ChIP‐seq mapping correlates transcriptional repression with direct Zeb1 binding to gene regulatory regions. Indirect recruitment mediated by Lef/Tcf factors potentiates gene expression independent of Wnt signaling. Activated genes include regulators of cell migration and invasion that correlate with Zeb1 expression in tumors. Zeb1 activates Prex1 to promote glioblastoma cell invasion in vivo. Genome‐wide binding reveals that the EMT‐inducer Zeb1, best‐known as a transcriptional repressor, can team up with a transcriptional activator to indirectly enhance gene expression.
Author Bennewitz, Romina
Momma, Stefan
Teixeira, Vera
Tang, Yeman
Stifani, Stefano
Rosmaninho, Pedro
Warta, Rolf
Piscopo, Valerio
Herold‐Mende, Christel
Mükusch, Susanne
Raposo, Alexandre ASF
Castro, Diogo S
AuthorAffiliation 2 Institute of Neurology (Edinger Institute) Frankfurt University Medical School Frankfurt Germany
4 Department of Neurology and Neurosurgery Montreal Neurological Institute McGill University Montreal QC Canada
3 German Cancer Consortium (DKTK) German Cancer Research Center (DKFZ) Heidelberg Germany
5 Division of Experimental Neurosurgery Department of Neurosurgery University Hospital of Heidelberg Heidelberg Germany
1 Molecular Neurobiology Laboratory Instituto Gulbenkian de Ciência Oeiras Portugal
AuthorAffiliation_xml – name: 1 Molecular Neurobiology Laboratory Instituto Gulbenkian de Ciência Oeiras Portugal
– name: 4 Department of Neurology and Neurosurgery Montreal Neurological Institute McGill University Montreal QC Canada
– name: 2 Institute of Neurology (Edinger Institute) Frankfurt University Medical School Frankfurt Germany
– name: 5 Division of Experimental Neurosurgery Department of Neurosurgery University Hospital of Heidelberg Heidelberg Germany
– name: 3 German Cancer Consortium (DKTK) German Cancer Research Center (DKFZ) Heidelberg Germany
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  organization: Molecular Neurobiology Laboratory, Instituto Gulbenkian de Ciência
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29903919$$D View this record in MEDLINE/PubMed
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Issue 15
Keywords cancer stem‐like cells
Zeb1
glioblastoma multiforme
Wnt signaling
transcription
Language English
License 2018 The Authors.
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Snippet Glioblastoma is the most common and aggressive brain tumor, with a subpopulation of stem‐like cells thought to mediate its recurring behavior and therapeutic...
Glioblastoma is the most common and aggressive brain tumor, with a subpopulation of stem-like cells thought to mediate its recurring behavior and therapeutic...
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SourceType Open Access Repository
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SubjectTerms Activation
Binding
Brain
Brain cancer
Brain tumors
cancer stem‐like cells
Cell migration
Cell Movement - genetics
Chromatin
Deoxyribonucleic acid
DNA
DNA-Binding Proteins - genetics
EMBO03
EMBO37
EMBO44
Epithelial-Mesenchymal Transition - genetics
Gene expression
Gene mapping
Gene silencing
Genes
Genomes
Glioblastoma
Glioblastoma - genetics
Glioblastoma - mortality
Glioblastoma - pathology
Glioblastoma cells
glioblastoma multiforme
Guanine
Guanine nucleotide exchange factor
Guanine Nucleotide Exchange Factors - genetics
Guanine Nucleotide Exchange Factors - metabolism
Humans
Invasiveness
Lef1 gene
Lymphoid Enhancer-Binding Factor 1 - genetics
Mesenchyme
Neoplasm Invasiveness - genetics
Recruitment
Regulators
Regulatory mechanisms (biology)
Regulatory sequences
Repressors
Signaling
Stem cells
transcription
Transcription factors
Transcription, Genetic - genetics
Transcriptional Activation - genetics
Tumors
Wnt protein
Wnt signaling
Wnt Signaling Pathway - genetics
Zeb1
Zinc Finger E-box-Binding Homeobox 1 - genetics
Zinc Finger E-box-Binding Homeobox 1 - metabolism
Title Zeb1 potentiates genome‐wide gene transcription with Lef1 to promote glioblastoma cell invasion
URI https://link.springer.com/article/10.15252/embj.201797115
https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembj.201797115
https://www.ncbi.nlm.nih.gov/pubmed/29903919
https://www.proquest.com/docview/2080565370
https://www.proquest.com/docview/2056397206
https://pubmed.ncbi.nlm.nih.gov/PMC6068449
Volume 37
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