An Alternative Splicing Switch Regulates Embryonic Stem Cell Pluripotency and Reprogramming

Alternative splicing (AS) is a key process underlying the expansion of proteomic diversity and the regulation of gene expression. Here, we identify an evolutionarily conserved embryonic stem cell (ESC)-specific AS event that changes the DNA-binding preference of the forkhead family transcription fac...

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Published inCell Vol. 147; no. 1; pp. 132 - 146
Main Authors Gabut, Mathieu, Samavarchi-Tehrani, Payman, Wang, Xinchen, Slobodeniuc, Valentina, O'Hanlon, Dave, Sung, Hoon-Ki, Alvarez, Manuel, Talukder, Shaheynoor, Pan, Qun, Mazzoni, Esteban O., Nedelec, Stephane, Wichterle, Hynek, Woltjen, Knut, Hughes, Timothy R., Zandstra, Peter W., Nagy, Andras, Wrana, Jeffrey L., Blencowe, Benjamin J.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 30.09.2011
Elsevier
Subjects
Alternative Splicing
Animals
Cellular Reprogramming
Differentiation
DNA - metabolism
Embryo cells
embryonic stem cells
Embryonic Stem Cells - cytology
Embryonic Stem Cells - metabolism
Evolution
Forkhead protein
Forkhead Transcription Factors - metabolism
Foxp1 protein
Gene expression
Gene Expression Regulation, Developmental
genes
Genes, Homeobox
Humans
induced pluripotent stem cells
Life Sciences
Mice
Oct-4 protein
Pluripotent Stem Cells - cytology
Pluripotent Stem Cells - metabolism
Protein Isoforms - metabolism
proteomics
Repressor Proteins - metabolism
Somatic cells
Stem cells
transcription (genetics)
Transcription factors
Online AccessGet full text
ISSN0092-8674
1097-4172
1097-4172
DOI10.1016/j.cell.2011.08.023

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Abstract Alternative splicing (AS) is a key process underlying the expansion of proteomic diversity and the regulation of gene expression. Here, we identify an evolutionarily conserved embryonic stem cell (ESC)-specific AS event that changes the DNA-binding preference of the forkhead family transcription factor FOXP1. We show that the ESC-specific isoform of FOXP1 stimulates the expression of transcription factor genes required for pluripotency, including OCT4, NANOG, NR5A2, and GDF3, while concomitantly repressing genes required for ESC differentiation. This isoform also promotes the maintenance of ESC pluripotency and contributes to efficient reprogramming of somatic cells into induced pluripotent stem cells. These results reveal a pivotal role for an AS event in the regulation of pluripotency through the control of critical ESC-specific transcriptional programs. [Display omitted] ► An ESC-specific splicing switch in FOXP1 transcripts produces the FOXP1-ES isoform ► FOXP1-ES has distinct DNA-binding properties compared to the canonical FOXP1 isoform ► FOXP1-ES stimulates key pluripotency genes and represses many differentiation genes ► FOXP1-ES is required for ESC pluripotency and efficient iPSC reprogramming Alternative splicing produces an ESC-specific isoform of FOXP1 that represses genes responsible for differentiation and directly stimulates production of pluripotency genes, including Oct4 and Nanog
AbstractList Alternative splicing (AS) is a key process underlying the expansion of proteomic diversity and the regulation of gene expression. Here, we identify an evolutionarily conserved embryonic stem cell (ESC)-specific AS event that changes the DNA-binding preference of the forkhead family transcription factor FOXP1. We show that the ESC-specific isoform of FOXP1 stimulates the expression of transcription factor genes required for pluripotency, including OCT4, NANOG, NR5A2, and GDF3, while concomitantly repressing genes required for ESC differentiation. This isoform also promotes the maintenance of ESC pluripotency and contributes to efficient reprogramming of somatic cells into induced pluripotent stem cells. These results reveal a pivotal role for an AS event in the regulation of pluripotency through the control of critical ESC-specific transcriptional programs.
Alternative splicing (AS) is a key process underlying the expansion of proteomic diversity and the regulation of gene expression. Here, we identify an evolutionarily conserved embryonic stem cell (ESC)-specific AS event that changes the DNA-binding preference of the forkhead family transcription factor FOXP1. We show that the ESC-specific isoform of FOXP1 stimulates the expression of transcription factor genes required for pluripotency, including OCT4, NANOG, NR5A2, and GDF3, while concomitantly repressing genes required for ESC differentiation. This isoform also promotes the maintenance of ESC pluripotency and contributes to efficient reprogramming of somatic cells into induced pluripotent stem cells. These results reveal a pivotal role for an AS event in the regulation of pluripotency through the control of critical ESC-specific transcriptional programs.Alternative splicing (AS) is a key process underlying the expansion of proteomic diversity and the regulation of gene expression. Here, we identify an evolutionarily conserved embryonic stem cell (ESC)-specific AS event that changes the DNA-binding preference of the forkhead family transcription factor FOXP1. We show that the ESC-specific isoform of FOXP1 stimulates the expression of transcription factor genes required for pluripotency, including OCT4, NANOG, NR5A2, and GDF3, while concomitantly repressing genes required for ESC differentiation. This isoform also promotes the maintenance of ESC pluripotency and contributes to efficient reprogramming of somatic cells into induced pluripotent stem cells. These results reveal a pivotal role for an AS event in the regulation of pluripotency through the control of critical ESC-specific transcriptional programs.
Alternative splicing (AS) is a key process underlying the expansion of proteomic diversity and the regulation of gene expression. Here, we identify an evolutionarily conserved embryonic stem cell (ESC)-specific AS event that changes the DNA-binding preference of the forkhead family transcription factor FOXP1. We show that the ESC-specific isoform of FOXP1 stimulates the expression of transcription factor genes required for pluripotency, including OCT4, NANOG, NR5A2, and GDF3, while concomitantly repressing genes required for ESC differentiation. This isoform also promotes the maintenance of ESC pluripotency and contributes to efficient reprogramming of somatic cells into induced pluripotent stem cells. These results reveal a pivotal role for an AS event in the regulation of pluripotency through the control of critical ESC-specific transcriptional programs. [Display omitted] ► An ESC-specific splicing switch in FOXP1 transcripts produces the FOXP1-ES isoform ► FOXP1-ES has distinct DNA-binding properties compared to the canonical FOXP1 isoform ► FOXP1-ES stimulates key pluripotency genes and represses many differentiation genes ► FOXP1-ES is required for ESC pluripotency and efficient iPSC reprogramming Alternative splicing produces an ESC-specific isoform of FOXP1 that represses genes responsible for differentiation and directly stimulates production of pluripotency genes, including Oct4 and Nanog
Author Slobodeniuc, Valentina
Blencowe, Benjamin J.
Hughes, Timothy R.
Wrana, Jeffrey L.
Sung, Hoon-Ki
Wang, Xinchen
Nedelec, Stephane
Talukder, Shaheynoor
Gabut, Mathieu
Mazzoni, Esteban O.
Woltjen, Knut
Zandstra, Peter W.
Pan, Qun
Alvarez, Manuel
O'Hanlon, Dave
Nagy, Andras
Wichterle, Hynek
Samavarchi-Tehrani, Payman
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  surname: Gabut
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  surname: Samavarchi-Tehrani
  fullname: Samavarchi-Tehrani, Payman
  organization: Center for Systems Biology, Samuel Lunenfeld Research Institute, Mount Sinai Hospital, 600 University Avenue, Toronto, Ontario M5G 1X5, Canada
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  surname: Nagy
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  organization: Banting and Best Department of Medical Research, University of Toronto, 160 College Street, Toronto, Ontario M5S 3E1, Canada
BackLink https://www.ncbi.nlm.nih.gov/pubmed/21924763$$D View this record in MEDLINE/PubMed
https://hal.science/hal-03830239$$DView record in HAL
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Snippet Alternative splicing (AS) is a key process underlying the expansion of proteomic diversity and the regulation of gene expression. Here, we identify an...
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StartPage 132
SubjectTerms Alternative Splicing
Animals
Cellular Reprogramming
Differentiation
DNA - metabolism
Embryo cells
embryonic stem cells
Embryonic Stem Cells - cytology
Embryonic Stem Cells - metabolism
Evolution
Forkhead protein
Forkhead Transcription Factors - metabolism
Foxp1 protein
Gene expression
Gene Expression Regulation, Developmental
genes
Genes, Homeobox
Humans
induced pluripotent stem cells
Life Sciences
Mice
Oct-4 protein
Pluripotent Stem Cells - cytology
Pluripotent Stem Cells - metabolism
Protein Isoforms - metabolism
proteomics
Repressor Proteins - metabolism
Somatic cells
Stem cells
transcription (genetics)
Transcription factors
Title An Alternative Splicing Switch Regulates Embryonic Stem Cell Pluripotency and Reprogramming
URI https://dx.doi.org/10.1016/j.cell.2011.08.023
https://www.ncbi.nlm.nih.gov/pubmed/21924763
https://www.proquest.com/docview/2000021665
https://www.proquest.com/docview/896219248
https://www.proquest.com/docview/907176449
https://hal.science/hal-03830239
Volume 147
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