Wnt signaling regulates the lineage differentiation potential of mouse embryonic stem cells through Tcf3 down-regulation
Canonical Wnt signaling plays a rate-limiting role in regulating self-renewal and differentiation in mouse embryonic stem cells (ESCs). We have previously shown that mutation in the Apc (adenomatous polyposis coli) tumor suppressor gene constitutively activates Wnt signaling in ESCs and inhibits the...
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| Published in | PLoS genetics Vol. 9; no. 5; p. e1003424 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.05.2013
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Canonical Wnt signaling plays a rate-limiting role in regulating self-renewal and differentiation in mouse embryonic stem cells (ESCs). We have previously shown that mutation in the Apc (adenomatous polyposis coli) tumor suppressor gene constitutively activates Wnt signaling in ESCs and inhibits their capacity to differentiate towards ecto-, meso-, and endodermal lineages. However, the underlying molecular and cellular mechanisms through which Wnt regulates lineage differentiation in mouse ESCs remain to date largely unknown. To this aim, we have derived and studied the gene expression profiles of several Apc-mutant ESC lines encoding for different levels of Wnt signaling activation. We found that down-regulation of Tcf3, a member of the Tcf/Lef family and a key player in the control of self-renewal and pluripotency, represents a specific and primary response to Wnt activation in ESCs. Accordingly, rescuing Tcf3 expression partially restored the neural defects observed in Apc-mutant ESCs, suggesting that Tcf3 down-regulation is a necessary step towards Wnt-mediated suppression of neural differentiation. We found that Tcf3 down-regulation in the context of constitutively active Wnt signaling does not result from promoter DNA methylation but is likely to be caused by a plethora of mechanisms at both the RNA and protein level as shown by the observed decrease in activating histone marks (H3K4me3 and H3-acetylation) and the upregulation of miR-211, a novel Wnt-regulated microRNA that targets Tcf3 and attenuates early neural differentiation in mouse ESCs. Our data show for the first time that Wnt signaling down-regulates Tcf3 expression, possibly at both the transcriptional and post-transcriptional levels, and thus highlight a novel mechanism through which Wnt signaling inhibits neuro-ectodermal lineage differentiation in mouse embryonic stem cells. |
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| AbstractList | Canonical Wnt signaling plays a rate-limiting role in regulating self-renewal and differentiation in mouse embryonic stem cells (ESCs). We have previously shown that mutation in the Apc (adenomatous polyposis coli) tumor suppressor gene constitutively activates Wnt signaling in ESCs and inhibits their capacity to differentiate towards ecto-, meso-, and endodermal lineages. However, the underlying molecular and cellular mechanisms through which Wnt regulates lineage differentiation in mouse ESCs remain to date largely unknown. To this aim, we have derived and studied the gene expression profiles of several Apc-mutant ESC lines encoding for different levels of Wnt signaling activation. We found that down-regulation of Tcf3, a member of the Tcf/Lef family and a key player in the control of self-renewal and pluripotency, represents a specific and primary response to Wnt activation in ESCs. Accordingly, rescuing Tcf3 expression partially restored the neural defects observed in Apc-mutant ESCs, suggesting that Tcf3 down-regulation is a necessary step towards Wnt-mediated suppression of neural differentiation. We found that Tcf3 down-regulation in the context of constitutively active Wnt signaling does not result from promoter DNA methylation but is likely to be caused by a plethora of mechanisms at both the RNA and protein level as shown by the observed decrease in activating histone marks (H3K4me3 and H3-acetylation) and the upregulation of miR-211, a novel Wnt-regulated microRNA that targets Tcf3 and attenuates early neural differentiation in mouse ESCs. Our data show for the first time that Wnt signaling down-regulates Tcf3 expression, possibly at both the transcriptional and post-transcriptional levels, and thus highlight a novel mechanism through which Wnt signaling inhibits neuro-ectodermal lineage differentiation in mouse embryonic stem cells. Canonical Wnt signaling plays a rate-limiting role in regulating self-renewal and differentiation in mouse embryonic stem cells (ESCs). We have previously shown that mutation in the Apc (adenomatous polyposis coli) tumor suppressor gene constitutively activates Wnt signaling in ESCs and inhibits their capacity to differentiate towards ecto-, meso-, and endodermal lineages. However, the underlying molecular and cellular mechanisms through which Wnt regulates lineage differentiation in mouse ESCs remain to date largely unknown. To this aim, we have derived and studied the gene expression profiles of several Apc-mutant ESC lines encoding for different levels of Wnt signaling activation. We found that down-regulation of Tcf3, a member of the Tcf/Lef family and a key player in the control of self-renewal and pluripotency, represents a specific and primary response to Wnt activation in ESCs. Accordingly, rescuing Tcf3 expression partially restored the neural defects observed in Apc-mutant ESCs, suggesting that Tcf3 down-regulation is a necessary step towards Wnt-mediated suppression of neural differentiation. We found that Tcf3 down-regulation in the context of constitutively active Wnt signaling does not result from promoter DNA methylation but is likely to be caused by a plethora of mechanisms at both the RNA and protein level as shown by the observed decrease in activating histone marks (H3K4me3 and H3acetylation) and the upregulation of miR-211, a novel Wnt-regulated microRNA that targets Tcf3 and attenuates early neural differentiation in mouse ESCs. Our data show for the first time that Wnt signaling down-regulates Tcf3 expression, possibly at both the transcriptional and post-transcriptional levels, and thus highlight a novel mechanism through which Wnt signaling inhibits neuro-ectodermal lineage differentiation in mouse embryonic stem cells. Canonical Wnt signaling plays a rate-limiting role in regulating self-renewal and differentiation in mouse embryonic stem cells (ESCs). We have previously shown that mutation in the Apc (adenomatous polyposis coli) tumor suppressor gene constitutively activates Wnt signaling in ESCs and inhibits their capacity to differentiate towards ecto-, meso-, and endodermal lineages. However, the underlying molecular and cellular mechanisms through which Wnt regulates lineage differentiation in mouse ESCs remain to date largely unknown. To this aim, we have derived and studied the gene expression profiles of several Apc-mutant ESC lines encoding for different levels of Wnt signaling activation. We found that down-regulation of Tcf3, a member of the Tcf/Lef family and a key player in the control of self-renewal and pluripotency, represents a specific and primary response to Wnt activation in ESCs. Accordingly, rescuing Tcf3 expression partially restored the neural defects observed in Apc-mutant ESCs, suggesting that Tcf3 down-regulation is a necessary step towards Wnt-mediated suppression of neural differentiation. We found that Tcf3 down-regulation in the context of constitutively active Wnt signaling does not result from promoter DNA methylation but is likely to be caused by a plethora of mechanisms at both the RNA and protein level as shown by the observed decrease in activating histone marks (H3K4me3 and H3-acetylation) and the upregulation of miR-211, a novel Wnt-regulated microRNA that targets Tcf3 and attenuates early neural differentiation in mouse ESCs. Our data show for the first time that Wnt signaling down-regulates Tcf3 expression, possibly at both the transcriptional and post-transcriptional levels, and thus highlight a novel mechanism through which Wnt signaling inhibits neuro-ectodermal lineage differentiation in mouse embryonic stem cells. Canonical Wnt signaling plays a rate-limiting role in regulating self-renewal and differentiation in mouse embryonic stem cells (ESCs). We have previously shown that mutation in the Apc (adenomatous polyposis coli) tumor suppressor gene constitutively activates Wnt signaling in ESCs and inhibits their capacity to differentiate towards ecto-, meso-, and endodermal lineages. However, the underlying molecular and cellular mechanisms through which Wnt regulates lineage differentiation in mouse ESCs remain to date largely unknown. To this aim, we have derived and studied the gene expression profiles of several Apc -mutant ESC lines encoding for different levels of Wnt signaling activation. We found that down-regulation of Tcf3 , a member of the Tcf/Lef family and a key player in the control of self-renewal and pluripotency, represents a specific and primary response to Wnt activation in ESCs. Accordingly, rescuing Tcf3 expression partially restored the neural defects observed in Apc -mutant ESCs, suggesting that Tcf3 down-regulation is a necessary step towards Wnt-mediated suppression of neural differentiation. We found that Tcf3 down-regulation in the context of constitutively active Wnt signaling does not result from promoter DNA methylation but is likely to be caused by a plethora of mechanisms at both the RNA and protein level as shown by the observed decrease in activating histone marks (H3K4me3 and H3-acetylation) and the upregulation of miR-211, a novel Wnt-regulated microRNA that targets Tcf3 and attenuates early neural differentiation in mouse ESCs. Our data show for the first time that Wnt signaling down-regulates Tcf3 expression, possibly at both the transcriptional and post-transcriptional levels, and thus highlight a novel mechanism through which Wnt signaling inhibits neuro-ectodermal lineage differentiation in mouse embryonic stem cells. The future successes of regenerative medicine largely rely on our knowledge of, and our capacity to manipulate, the cellular and molecular mechanisms governing stem cell differentiation. A growing body of evidence suggests that, in mouse embryonic stem cells, canonical Wnt/β-catenin signaling not only enhances self-renewal but also directs the cell fate decision towards non-neuroectodermal lineages. However, little is known about the mechanisms underlying the differentiation defects caused by constitutive active Wnt signaling. Using a set of Apc -mutant ESCs harbouring different levels of Wnt signaling, we found that, among others, down-regulation of Tcf3 , a key member of the pluripotency circuit, as well as induction of a novel Wnt-regulated microRNA, miR-211, represent two important downstream effects through which Wnt signaling inhibits neural differentiation in mouse ESCs. We also provide a more detailed picture on how Wnt signaling counteracts Tcf3 function in stem cells by showing that Tcf3 repression, in the context of active Wnt signaling, involves histone modifications at the Tcf3 promoter and the activation of miR-211, which post-transcriptionally stabilizes Tcf3 downregulation. Understanding the downstream effects of Wnt signaling in ESCs is of both fundamental and translational relevance, as it may be exploited to manipulate ESC differentiation towards specific cell lineages. |
| Audience | Academic |
| Author | Fodde, Riccardo Calin, George A Franken, Patrick Mahmoudi, Tokameh Gaspar, Claudia Decraene, Charles Merrill, Bradley J Rafati, Haleh Atlasi, Yaser Sacchetti, Andrea Noori, Rubina |
| AuthorAffiliation | 4 CNRS, UMR144, Paris, France 2 Department of Biochemistry, Erasmus MC, Rotterdam, The Netherlands University of Michigan, United States of America 5 Department of Experimental Therapeutics and Center for RNA Interference and Non-Coding RNAs, MD Anderson Cancer Center, Houston, Texas, United States of America 6 Department of Biochemistry and Molecular Genetics, University of Illinois, Chicago, Illinois, United States of America 1 Department of Pathology, Josephine Nefkens Institute, Erasmus MC, Rotterdam, The Netherlands 3 Translational Research Department, Institut Curie, Centre de Recherche, Paris, France |
| AuthorAffiliation_xml | – name: 5 Department of Experimental Therapeutics and Center for RNA Interference and Non-Coding RNAs, MD Anderson Cancer Center, Houston, Texas, United States of America – name: 4 CNRS, UMR144, Paris, France – name: 6 Department of Biochemistry and Molecular Genetics, University of Illinois, Chicago, Illinois, United States of America – name: University of Michigan, United States of America – name: 3 Translational Research Department, Institut Curie, Centre de Recherche, Paris, France – name: 1 Department of Pathology, Josephine Nefkens Institute, Erasmus MC, Rotterdam, The Netherlands – name: 2 Department of Biochemistry, Erasmus MC, Rotterdam, The Netherlands |
| Author_xml | – sequence: 1 givenname: Yaser surname: Atlasi fullname: Atlasi, Yaser organization: Department of Pathology, Josephine Nefkens Institute, Erasmus MC, Rotterdam, The Netherlands – sequence: 2 givenname: Rubina surname: Noori fullname: Noori, Rubina – sequence: 3 givenname: Claudia surname: Gaspar fullname: Gaspar, Claudia – sequence: 4 givenname: Patrick surname: Franken fullname: Franken, Patrick – sequence: 5 givenname: Andrea surname: Sacchetti fullname: Sacchetti, Andrea – sequence: 6 givenname: Haleh surname: Rafati fullname: Rafati, Haleh – sequence: 7 givenname: Tokameh surname: Mahmoudi fullname: Mahmoudi, Tokameh – sequence: 8 givenname: Charles surname: Decraene fullname: Decraene, Charles – sequence: 9 givenname: George A surname: Calin fullname: Calin, George A – sequence: 10 givenname: Bradley J surname: Merrill fullname: Merrill, Bradley J – sequence: 11 givenname: Riccardo surname: Fodde fullname: Fodde, Riccardo |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23658527$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2013 Public Library of Science 2013 Atlasi et al 2013 Atlasi et al 2013 Atlasi 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: Atlasi Y, Noori R, Gaspar C, Franken P, Sacchetti A, et al. (2013) Wnt Signaling Regulates the Lineage Differentiation Potential of Mouse Embryonic Stem Cells through Tcf3 Down-Regulation. PLoS Genet 9(5): e1003424. doi:10.1371/journal.pgen.1003424 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current address: Faculdade de Medicina de Lisboa, Instituto de Medicina Molecular, Lisboa, Portugal Conceived and designed the experiments: YA CG RF GAC BJM TM. Performed the experiments: YA RN PF CG AS HR. Analyzed the data: YA CG AS CD TM BJM GAC RF. Contributed reagents/materials/analysis tools: AS CD TM BJM GAC. Wrote the paper: YA RF. The authors have declared that no competing interests exist. |
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| Snippet | Canonical Wnt signaling plays a rate-limiting role in regulating self-renewal and differentiation in mouse embryonic stem cells (ESCs). We have previously... Canonical Wnt signaling plays a rate-limiting role in regulating self-renewal and differentiation in mouse embryonic stem cells (ESCs). We have previously... |
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| SubjectTerms | Adenomatous Polyposis Coli Protein - genetics Animals Basic Helix-Loop-Helix Transcription Factors - genetics Basic Helix-Loop-Helix Transcription Factors - metabolism Biology Cell Differentiation Cell Lineage Cloning Colleges & universities DNA Methylation Down-Regulation Embryonic stem cells Embryonic Stem Cells - cytology Embryonic Stem Cells - physiology Gene expression Gene Expression Regulation, Developmental Genetic aspects Genetic engineering Kinases Methylation Mice Mutation Physiological aspects Proteins Stem cells Transcription, Genetic Wnt Signaling Pathway |
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| Title | Wnt signaling regulates the lineage differentiation potential of mouse embryonic stem cells through Tcf3 down-regulation |
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