Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal

The co-occupancy of Tcf3 with Oct4, Sox2 and Nanog on embryonic stem cell (ESC) chromatin indicated that Tcf3 has been suggested to play an integral role in a poorly understood mechanism underlying Wnt-dependent stimulation of mouse ESC self-renewal of mouse ESCs. Although the conventional view of T...

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Published inNature cell biology Vol. 13; no. 7; pp. 762 - 770
Main Authors Merrill, Bradley J, Yi, Fei, Pereira, Laura, Hoffman, Jackson A, Shy, Brian R, Yuen, Courtney M, Liu, David R
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.07.2011
Nature Publishing Group
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Abstract The co-occupancy of Tcf3 with Oct4, Sox2 and Nanog on embryonic stem cell (ESC) chromatin indicated that Tcf3 has been suggested to play an integral role in a poorly understood mechanism underlying Wnt-dependent stimulation of mouse ESC self-renewal of mouse ESCs. Although the conventional view of Tcf proteins as the β-catenin-binding effectors of Wnt signalling suggested Tcf3–β-catenin activation of target genes would stimulate self-renewal, here we show that an antagonistic relationship between Wnt3a and Tcf3 on gene expression regulates ESC self-renewal. Genetic ablation of Tcf3 replaced the requirement for exogenous Wnt3a or GSK3 inhibition for ESC self-renewal, demonstrating that inhibition of Tcf3 repressor is the necessary downstream effect of Wnt signalling. Interestingly, both Tcf3–β-catenin and Tcf1–β-catenin interactions contributed to Wnt stimulation of self-renewal and gene expression, and the combination of Tcf3 and Tcf1 recruited Wnt-stabilized β-catenin to Oct4 binding sites on ESC chromatin. This work elucidates the molecular link between the effects of Wnt and the regulation of the Oct4/Sox2/Nanog network. Inhibition of the repressor function of the Wnt3a effector β-catenin–TCF3 is shown to be required to maintain pluripotency in cooperation with the activating role of the second Wnt effector β-catenin–TCF1. Both Tcf3 and Tcf1 are involved in the recruitment of β-catenin to Oct4 binding sites in embryonic stem cell chromatin.
AbstractList The observation that Tcf3 (MGI name: Tcf7l1) bound the same genes as core stem cell transcription factors, Oct4 (MGI name:Pou5f1), Sox2 and Nanog, revealed a potentially important aspect of the poorly understood mechanism whereby Wnts stimulate self renewal of pluripotent mouse embryonic stem (ES) cells. Although the conventional view of Tcf proteins as the β-catenin-binding effectors of Wnt signaling suggested Tcf3-β-catenin mediated activation of target genes would stimulate ES cell self renewal, here we show that an antagonistic relationship between Wnt3a and Tcf3 on gene expression is important for regulating ES cell self renewal. Genetic ablation of Tcf3 replaced the requirement for exogenous Wnt3a or GSK3-inhibition for self renewal of ES cells, demonstrating that inhibition of Tcf3-repressor is the necessary downstream effect of Wnt signaling. Interestingly, the molecular mechanism underlying Wnt’s effects required both Tcf3-β-catenin and Tcf1-β-catenin interactions, as they each contributed to Wnt stimulation of self renewal and gene expression. Finally, the combination of Tcf3 and Tcf1 was necessary to recruit Wnt-stabilized β-catenin to Oct4 binding sites in ES cell chromatin. These results elucidate the molecular link between the effects of Wnt and the regulation of the Oct4/Sox2/Nanog network.
The co-occupancy of Tcf3 with Oct4, Sox2 and Nanog on embryonic stem cell (ESC) chromatin indicated that Tcf3 has been suggested to play an integral role in a poorly understood mechanism underlying Wnt-dependent stimulation of mouse ESC self-renewal of mouse ESCs. Although the conventional view of Tcf proteins as the β-catenin-binding effectors of Wnt signalling suggested Tcf3-β-catenin activation of target genes would stimulate self-renewal, here we show that an antagonistic relationship between Wnt3a and Tcf3 on gene expression regulates ESC self-renewal. Genetic ablation of Tcf3 replaced the requirement for exogenous Wnt3a or GSK3 inhibition for ESC self-renewal, demonstrating that inhibition of Tcf3 repressor is the necessary downstream effect of Wnt signalling. Interestingly, both Tcf3-β-catenin and Tcf1-β-catenin interactions contributed to Wnt stimulation of self-renewal and gene expression, and the combination of Tcf3 and Tcf1 recruited Wnt-stabilized β-catenin to Oct4 binding sites on ESC chromatin. This work elucidates the molecular link between the effects of Wnt and the regulation of the Oct4/Sox2/Nanog network.
The co-occupancy of Tcf3 with Oct4, Sox2 and Nanog on embryonic stem cell (ESC) chromatin indicated that Tcf3 has been suggested to play an integral role in a poorly understood mechanism underlying Wnt-dependent stimulation of mouse ESC self-renewal of mouse ESCs. Although the conventional view of Tcf proteins as the [beta]-catenin-binding effectors of Wnt signalling suggested Tcf3-[beta]-catenin activation of target genes would stimulate self-renewal, here we show that an antagonistic relationship between Wnt3a and Tcf3 on gene expression regulates ESC self-renewal. Genetic ablation of Tcf3 replaced the requirement for exogenous Wnt3a or GSK3 inhibition for ESC self-renewal, demonstrating that inhibition of Tcf3 repressor is the necessary downstream effect of Wnt signalling. Interestingly, both Tcf3-[beta]-catenin and Tcf1-[beta]-catenin interactions contributed to Wnt stimulation of self-renewal and gene expression, and the combination of Tcf3 and Tcf1 recruited Wnt-stabilized [beta]-catenin to Oct4 binding sites on ESC chromatin. This work elucidates the molecular link between the effects of Wnt and the regulation of the Oct4/Sox2/Nanog network.
The co-occupancy of Tcf3 with Oct4, Sox2 and Nanog on embryonic stem cell (ESC) chromatin indicated that Tcf3 has been suggested to play an integral role in a poorly understood mechanism underlying Wnt-dependent stimulation of mouse ESC self-renewal of mouse ESCs. Although the conventional view of Tcf proteins as the β-catenin-binding effectors of Wnt signalling suggested Tcf3–β-catenin activation of target genes would stimulate self-renewal, here we show that an antagonistic relationship between Wnt3a and Tcf3 on gene expression regulates ESC self-renewal. Genetic ablation of Tcf3 replaced the requirement for exogenous Wnt3a or GSK3 inhibition for ESC self-renewal, demonstrating that inhibition of Tcf3 repressor is the necessary downstream effect of Wnt signalling. Interestingly, both Tcf3–β-catenin and Tcf1–β-catenin interactions contributed to Wnt stimulation of self-renewal and gene expression, and the combination of Tcf3 and Tcf1 recruited Wnt-stabilized β-catenin to Oct4 binding sites on ESC chromatin. This work elucidates the molecular link between the effects of Wnt and the regulation of the Oct4/Sox2/Nanog network. Inhibition of the repressor function of the Wnt3a effector β-catenin–TCF3 is shown to be required to maintain pluripotency in cooperation with the activating role of the second Wnt effector β-catenin–TCF1. Both Tcf3 and Tcf1 are involved in the recruitment of β-catenin to Oct4 binding sites in embryonic stem cell chromatin.
Audience Academic
Author Pereira, Laura
Yuen, Courtney M
Yi, Fei
Merrill, Bradley J
Shy, Brian R
Liu, David R
Hoffman, Jackson A
AuthorAffiliation 3 Howard Hughes Medical Institute, Department of Chemistry and Chemical Biology, Harvard University, 12 Oxford Street, Cambridge, MA 02138
1 Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago, Chicago, IL 60607
AuthorAffiliation_xml – name: 1 Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago, Chicago, IL 60607
– name: 3 Howard Hughes Medical Institute, Department of Chemistry and Chemical Biology, Harvard University, 12 Oxford Street, Cambridge, MA 02138
Author_xml – sequence: 1
  givenname: Bradley J
  surname: Merrill
  fullname: Merrill, Bradley J
  organization: Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago
– sequence: 2
  givenname: Fei
  surname: Yi
  fullname: Yi, Fei
  organization: Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago
– sequence: 3
  givenname: Laura
  surname: Pereira
  fullname: Pereira, Laura
  organization: Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago
– sequence: 4
  givenname: Jackson A
  surname: Hoffman
  fullname: Hoffman, Jackson A
  organization: Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago
– sequence: 5
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  surname: Shy
  fullname: Shy, Brian R
  organization: Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago
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  surname: Yuen
  fullname: Yuen, Courtney M
  organization: Howard Hughes Medical Institute, Department of Chemistry and Chemical Biology, Harvard University
– sequence: 7
  givenname: David R
  surname: Liu
  fullname: Liu, David R
  organization: Howard Hughes Medical Institute, Department of Chemistry and Chemical Biology, Harvard University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/21685894$$D View this record in MEDLINE/PubMed
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Copyright Springer Nature Limited 2011
COPYRIGHT 2011 Nature Publishing Group
Copyright Nature Publishing Group Jul 2011
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Snippet The co-occupancy of Tcf3 with Oct4, Sox2 and Nanog on embryonic stem cell (ESC) chromatin indicated that Tcf3 has been suggested to play an integral role in a...
The observation that Tcf3 (MGI name: Tcf7l1) bound the same genes as core stem cell transcription factors, Oct4 (MGI name:Pou5f1), Sox2 and Nanog, revealed a...
SourceID pubmedcentral
proquest
gale
crossref
pubmed
springer
nature
SourceType Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 762
SubjectTerms 631/208/199
631/532/2117
631/532/2441
631/80/86
Ablation
Animals
Basic Helix-Loop-Helix Transcription Factors - genetics
Basic Helix-Loop-Helix Transcription Factors - metabolism
beta Catenin - genetics
beta Catenin - metabolism
Biomedical and Life Sciences
Cancer Research
Cell Biology
Cell cycle
Cell Line
Cell Proliferation - drug effects
Chromatin
Developmental Biology
Embryonic stem cells
Embryonic Stem Cells - drug effects
Embryonic Stem Cells - metabolism
Gene expression
Gene Expression Regulation, Developmental
Genetic aspects
Glycogen Synthase Kinase 3 - antagonists & inhibitors
Glycogen Synthase Kinase 3 - metabolism
Hepatocyte Nuclear Factor 1-alpha - genetics
Hepatocyte Nuclear Factor 1-alpha - metabolism
Homeodomain Proteins - genetics
Homeodomain Proteins - metabolism
Kinases
Life Sciences
Mice
Nanog Homeobox Protein
Octamer Transcription Factor-3 - genetics
Octamer Transcription Factor-3 - metabolism
Phosphatase
Physiological aspects
Protein Kinase Inhibitors - pharmacology
Proteins
RNA Interference
Signal Transduction - drug effects
Signal Transduction - genetics
SOXB1 Transcription Factors - genetics
SOXB1 Transcription Factors - metabolism
Stem Cells
Transcription factors
Transcription, Genetic
Transfection
Wnt Proteins - genetics
Wnt Proteins - metabolism
Wnt3 Protein
Wnt3A Protein
Title Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal
URI http://dx.doi.org/10.1038/ncb2283
https://link.springer.com/article/10.1038/ncb2283
https://www.ncbi.nlm.nih.gov/pubmed/21685894
https://www.proquest.com/docview/894312528
https://pubmed.ncbi.nlm.nih.gov/PMC3129424
Volume 13
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