Stage-Specific Regulation of Reprogramming to Induced Pluripotent Stem Cells by Wnt Signaling and T Cell Factor Proteins
Wnt signaling is intrinsic to mouse embryonic stem cell self-renewal. Therefore, it is surprising that reprogramming of somatic cells to induced pluripotent stem cells (iPSCs) is not strongly enhanced by Wnt signaling. Here, we demonstrate that active Wnt signaling inhibits the early stage of reprog...
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Published in | Cell reports (Cambridge) Vol. 3; no. 6; pp. 2113 - 2126 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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27.06.2013
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Abstract | Wnt signaling is intrinsic to mouse embryonic stem cell self-renewal. Therefore, it is surprising that reprogramming of somatic cells to induced pluripotent stem cells (iPSCs) is not strongly enhanced by Wnt signaling. Here, we demonstrate that active Wnt signaling inhibits the early stage of reprogramming to iPSCs, whereas it is required and even stimulating during the late stage. Mechanistically, this biphasic effect of Wnt signaling is accompanied by a change in the requirement of all four of its transcriptional effectors: T cell factor 1 (Tcf1), Lef1, Tcf3, and Tcf4. For example, Tcf3 and Tcf4 are stimulatory early but inhibitory late in the reprogramming process. Accordingly, ectopic expression of Tcf3 early in reprogramming combined with its loss of function late enables efficient reprogramming in the absence of ectopic Sox2. Together, our data indicate that the stepwise process of reprogramming to iPSCs is critically dependent on the stage-specific control and action of all four Tcfs and Wnt signaling.
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•Wnt signaling switches from a negative to a positive regulator during reprogramming•Tcf3/Tcf4 promote the early but inhibit the late reprogramming stage•Tcf1/Lef1 and active Wnt signaling inhibit early but promote late reprogramming steps•Stage-specific modulation of Tcf3 levels enables efficient reprogramming without Sox2
Reprogramming of differentiated cells to induced pluripotent stem cells is a stepwise process of transcriptional changes. Here, Merrill, Plath, and colleagues demonstrate that reprogramming signals can be biphasic, using the Wnt pathway as an example. The data point to opposing effects of Wnt signaling and its downstream regulators, the Tcf proteins, early and late in the reprogramming process, indicating that events promoting one phase can be inhibitory for a subsequent phase. These observations should encourage the development of dynamic reprogramming approaches. |
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AbstractList | Wnt signaling is intrinsic to mouse embryonic stem cell self-renewal. Therefore, it is surprising that reprogramming of somatic cells to induced pluripotent stem cells (iPSCs) is not strongly enhanced by Wnt signaling. Here, we demonstrate that active Wnt signaling inhibits the early stage of reprogramming to iPSCs, whereas it is required and even stimulating during the late stage. Mechanistically, this biphasic effect of Wnt signaling is accompanied by a change in the requirement of all four of its transcriptional effectors: T cell factor 1 (Tcf1), Lef1, Tcf3, and Tcf4. For example, Tcf3 and Tcf4 are stimulatory early but inhibitory late in the reprogramming process. Accordingly, ectopic expression of Tcf3 early in reprogramming combined with its loss of function late enables efficient reprogramming in the absence of ectopic Sox2. Together, our data indicate that the stepwise process of reprogramming to iPSCs is critically dependent on the stage-specific control and action of all four Tcfs and Wnt signaling. Wnt signaling is intrinsic to mouse embryonic stem cell self-renewal. Therefore, it is surprising that reprogramming of somatic cells to induced pluripotent stem cells (iPSCs) is not strongly enhanced by Wnt signaling. Here, we demonstrate that active Wnt signaling inhibits the early stage of reprogramming to iPSCs, whereas it is required and even stimulating during the late stage. Mechanistically, this biphasic effect of Wnt signaling is accompanied by a change in the requirement of all four of its transcriptional effectors: T cell factor 1 (Tcf1), Lef1, Tcf3, and Tcf4. For example, Tcf3 and Tcf4 are stimulatory early but inhibitory late in the reprogramming process. Accordingly, ectopic expression of Tcf3 early in reprogramming combined with its loss of function late enables efficient reprogramming in the absence of ectopic Sox2. Together, our data indicate that the stepwise process of reprogramming to iPSCs is critically dependent on the stage-specific control and action of all four Tcfs and Wnt signaling. [Display omitted] •Wnt signaling switches from a negative to a positive regulator during reprogramming•Tcf3/Tcf4 promote the early but inhibit the late reprogramming stage•Tcf1/Lef1 and active Wnt signaling inhibit early but promote late reprogramming steps•Stage-specific modulation of Tcf3 levels enables efficient reprogramming without Sox2 Reprogramming of differentiated cells to induced pluripotent stem cells is a stepwise process of transcriptional changes. Here, Merrill, Plath, and colleagues demonstrate that reprogramming signals can be biphasic, using the Wnt pathway as an example. The data point to opposing effects of Wnt signaling and its downstream regulators, the Tcf proteins, early and late in the reprogramming process, indicating that events promoting one phase can be inhibitory for a subsequent phase. These observations should encourage the development of dynamic reprogramming approaches. |
Author | Papp, Bernadett Hoffman, Jackson A. Plath, Kathrin Ho, Ritchie Merrill, Bradley J. |
Author_xml | – sequence: 1 givenname: Ritchie surname: Ho fullname: Ho, Ritchie organization: Department of Biological Chemistry, Jonsson Comprehensive Cancer Center, Molecular Biology Institute, Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research, David Geffen School of Medicine, University of California Los Angeles, 615 Charles E. Young Drive South, Los Angeles, CA 90024, USA – sequence: 2 givenname: Bernadett surname: Papp fullname: Papp, Bernadett organization: Department of Biological Chemistry, Jonsson Comprehensive Cancer Center, Molecular Biology Institute, Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research, David Geffen School of Medicine, University of California Los Angeles, 615 Charles E. Young Drive South, Los Angeles, CA 90024, USA – sequence: 3 givenname: Jackson A. surname: Hoffman fullname: Hoffman, Jackson A. organization: Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago, Chicago, IL 60607, USA – sequence: 4 givenname: Bradley J. surname: Merrill fullname: Merrill, Bradley J. email: merrillb@uic.edu organization: Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago, Chicago, IL 60607, USA – sequence: 5 givenname: Kathrin surname: Plath fullname: Plath, Kathrin email: kplath@mednet.ucla.edu organization: Department of Biological Chemistry, Jonsson Comprehensive Cancer Center, Molecular Biology Institute, Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research, David Geffen School of Medicine, University of California Los Angeles, 615 Charles E. Young Drive South, Los Angeles, CA 90024, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23791530$$D View this record in MEDLINE/PubMed |
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Snippet | Wnt signaling is intrinsic to mouse embryonic stem cell self-renewal. Therefore, it is surprising that reprogramming of somatic cells to induced pluripotent... |
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SubjectTerms | Animals Gene Expression Regulation, Developmental Induced Pluripotent Stem Cells - cytology Induced Pluripotent Stem Cells - metabolism Mice T Cell Transcription Factor 1 - genetics T Cell Transcription Factor 1 - metabolism Wnt Signaling Pathway |
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Title | Stage-Specific Regulation of Reprogramming to Induced Pluripotent Stem Cells by Wnt Signaling and T Cell Factor Proteins |
URI | https://dx.doi.org/10.1016/j.celrep.2013.05.015 https://www.ncbi.nlm.nih.gov/pubmed/23791530 https://search.proquest.com/docview/1373437336 https://doaj.org/article/3b09acecabd7405e8969e6a4921fd5f3 |
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