TRIM28 Is an Epigenetic Barrier to Induced Pluripotent Stem Cell Reprogramming

Since the discovery of induced pluripotent stem cells there has been intense interest in understanding the mechanisms that allow a somatic cell to be reprogrammed back to a pluripotent state. Several groups have studied the alterations in gene expression that occur as somatic cells modify their geno...

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Published in:	Stem cells (Dayton, Ohio) Vol. 35; no. 1; pp. 147 - 157
Main Authors:	Miles, Denise Catherine, de Vries, Nienke Alexandra, Gisler, Santiago, Lieftink, Cor, Akhtar, Waseem, Gogola, Ewa, Pawlitzky, Inka, Hulsman, Danielle, Tanger, Ellen, Koppens, Martijn, Beijersbergen, Roderick Leonardus, van Lohuizen, Maarten
Format:	Journal Article
Language:	English
Published:	United States Oxford University Press 01.01.2017
Subjects:	Animals Cell Proliferation Cellular Reprogramming - genetics Chromatin Chromatin - metabolism Domains Endogenous retroviruses Endogenous Retroviruses - metabolism Epigenesis, Genetic Epigenetics Gene expression Gene Knockdown Techniques Genomes Histone-Lysine N-Methyltransferase Histones - metabolism Induced pluripotent stem cells Lysine - metabolism Methylation Mice, Transgenic Models, Biological Pluripotency Pluripotent Stem Cells - cytology Pluripotent Stem Cells - metabolism Reprogramming Retroviridae RNA, Small Interfering - metabolism Somatic cells Stem cells Trim28 Tripartite Motif-Containing Protein 28 - metabolism Up-Regulation - genetics Epigenetics Reprogramming Induced pluripotent stem cells Trim28
ISSN:	1066-5099, 1549-4918, 1549-4918
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Abstract	Since the discovery of induced pluripotent stem cells there has been intense interest in understanding the mechanisms that allow a somatic cell to be reprogrammed back to a pluripotent state. Several groups have studied the alterations in gene expression that occur as somatic cells modify their genome to that of an embryonic stem cell. Underpinning many of the gene expression changes are modifications to the epigenetic profile of the associated chromatin. We have used a large‐scale shRNA screen to identify epigenetic modifiers that act as barriers to reprogramming. We have uncovered an important role for TRIM28 in cells resisting transition between somatic and pluripotent states. TRIM28 achieves this by maintaining the H3K9me3 repressed state and keeping endogenous retroviruses (ERVs) silenced. We propose that knockdown of TRIM28 during reprogramming results in more plastic H3K9me3 domains, dysregulation of genes nearby H3K9me3 marks, and up regulation of ERVs, thus facilitating the transition through reprogramming. Stem Cells 2017;35:147–157 Model of TRIM28 function during reprogramming A) Ectopic expression of Oct4, Sox2, Klf4 and c‐Myc (OSKM) induces the reprogramming of somatic cells into induced pluripotent stem cells at a low efficiency B) Ectopic expression of OSKM along with knock down of TRIM28 increases the expression of genes nearby H3K9me3, and induces the expression of endogenous retroviruses. This decondensed chromatin state increases the reprogramming efficiency.
AbstractList	Since the discovery of induced pluripotent stem cells there has been intense interest in understanding the mechanisms that allow a somatic cell to be reprogrammed back to a pluripotent state. Several groups have studied the alterations in gene expression that occur as somatic cells modify their genome to that of an embryonic stem cell. Underpinning many of the gene expression changes are modifications to the epigenetic profile of the associated chromatin. We have used a large-scale shRNA screen to identify epigenetic modifiers that act as barriers to reprogramming. We have uncovered an important role for TRIM28 in cells resisting transition between somatic and pluripotent states. TRIM28 achieves this by maintaining the H3K9me3 repressed state and keeping endogenous retroviruses (ERVs) silenced. We propose that knockdown of TRIM28 during reprogramming results in more plastic H3K9me3 domains, dysregulation of genes nearby H3K9me3 marks, and up regulation of ERVs, thus facilitating the transition through reprogramming. Stem Cells 2017;35:147-157.Since the discovery of induced pluripotent stem cells there has been intense interest in understanding the mechanisms that allow a somatic cell to be reprogrammed back to a pluripotent state. Several groups have studied the alterations in gene expression that occur as somatic cells modify their genome to that of an embryonic stem cell. Underpinning many of the gene expression changes are modifications to the epigenetic profile of the associated chromatin. We have used a large-scale shRNA screen to identify epigenetic modifiers that act as barriers to reprogramming. We have uncovered an important role for TRIM28 in cells resisting transition between somatic and pluripotent states. TRIM28 achieves this by maintaining the H3K9me3 repressed state and keeping endogenous retroviruses (ERVs) silenced. We propose that knockdown of TRIM28 during reprogramming results in more plastic H3K9me3 domains, dysregulation of genes nearby H3K9me3 marks, and up regulation of ERVs, thus facilitating the transition through reprogramming. Stem Cells 2017;35:147-157. Since the discovery of induced pluripotent stem cells there has been intense interest in understanding the mechanisms that allow a somatic cell to be reprogrammed back to a pluripotent state. Several groups have studied the alterations in gene expression that occur as somatic cells modify their genome to that of an embryonic stem cell. Underpinning many of the gene expression changes are modifications to the epigenetic profile of the associated chromatin. We have used a large‐scale shRNA screen to identify epigenetic modifiers that act as barriers to reprogramming. We have uncovered an important role for TRIM28 in cells resisting transition between somatic and pluripotent states. TRIM28 achieves this by maintaining the H3K9me3 repressed state and keeping endogenous retroviruses (ERVs) silenced. We propose that knockdown of TRIM28 during reprogramming results in more plastic H3K9me3 domains, dysregulation of genes nearby H3K9me3 marks, and up regulation of ERVs, thus facilitating the transition through reprogramming. Stem Cells 2017;35:147–157 Since the discovery of induced pluripotent stem cells there has been intense interest in understanding the mechanisms that allow a somatic cell to be reprogrammed back to a pluripotent state. Several groups have studied the alterations in gene expression that occur as somatic cells modify their genome to that of an embryonic stem cell. Underpinning many of the gene expression changes are modifications to the epigenetic profile of the associated chromatin. We have used a large-scale shRNA screen to identify epigenetic modifiers that act as barriers to reprogramming. We have uncovered an important role for TRIM28 in cells resisting transition between somatic and pluripotent states. TRIM28 achieves this by maintaining the H3K9me3 repressed state and keeping endogenous retroviruses (ERVs) silenced. We propose that knockdown of TRIM28 during reprogramming results in more plastic H3K9me3 domains, dysregulation of genes nearby H3K9me3 marks, and up regulation of ERVs, thus facilitating the transition through reprogramming. Stem Cells 2017; 35:147-157 Model of TRIM28 function during reprogramming A) Ectopic expression of Oct4, Sox2, Klf4 and c-Myc (OSKM) induces the reprogramming of somatic cells into induced pluripotent stem cells at a low efficiency B) Ectopic expression of OSKM along with knock down of TRIM28 increases the expression of genes nearby H3K9me3, and induces the expression of endogenous retroviruses. This decondensed chromatin state increases the reprogramming efficiency. Since the discovery of induced pluripotent stem cells there has been intense interest in understanding the mechanisms that allow a somatic cell to be reprogrammed back to a pluripotent state. Several groups have studied the alterations in gene expression that occur as somatic cells modify their genome to that of an embryonic stem cell. Underpinning many of the gene expression changes are modifications to the epigenetic profile of the associated chromatin. We have used a large-scale shRNA screen to identify epigenetic modifiers that act as barriers to reprogramming. We have uncovered an important role for TRIM28 in cells resisting transition between somatic and pluripotent states. TRIM28 achieves this by maintaining the H3K9me3 repressed state and keeping endogenous retroviruses (ERVs) silenced. We propose that knockdown of TRIM28 during reprogramming results in more plastic H3K9me3 domains, dysregulation of genes nearby H3K9me3 marks, and up regulation of ERVs, thus facilitating the transition through reprogramming. Stem Cells 2017;35:147-157. Since the discovery of induced pluripotent stem cells there has been intense interest in understanding the mechanisms that allow a somatic cell to be reprogrammed back to a pluripotent state. Several groups have studied the alterations in gene expression that occur as somatic cells modify their genome to that of an embryonic stem cell. Underpinning many of the gene expression changes are modifications to the epigenetic profile of the associated chromatin. We have used a large-scale shRNA screen to identify epigenetic modifiers that act as barriers to reprogramming. We have uncovered an important role for TRIM28 in cells resisting transition between somatic and pluripotent states. TRIM28 achieves this by maintaining the H3K9me3 repressed state and keeping endogenous retroviruses (ERVs) silenced. We propose that knockdown of TRIM28 during reprogramming results in more plastic H3K9me3 domains, dysregulation of genes nearby H3K9me3 marks, and up regulation of ERVs, thus facilitating the transition through reprogramming. Since the discovery of induced pluripotent stem cells there has been intense interest in understanding the mechanisms that allow a somatic cell to be reprogrammed back to a pluripotent state. Several groups have studied the alterations in gene expression that occur as somatic cells modify their genome to that of an embryonic stem cell. Underpinning many of the gene expression changes are modifications to the epigenetic profile of the associated chromatin. We have used a large‐scale shRNA screen to identify epigenetic modifiers that act as barriers to reprogramming. We have uncovered an important role for TRIM28 in cells resisting transition between somatic and pluripotent states. TRIM28 achieves this by maintaining the H3K9me3 repressed state and keeping endogenous retroviruses (ERVs) silenced. We propose that knockdown of TRIM28 during reprogramming results in more plastic H3K9me3 domains, dysregulation of genes nearby H3K9me3 marks, and up regulation of ERVs, thus facilitating the transition through reprogramming. Stem Cells 2017;35:147–157 Model of TRIM28 function during reprogramming A) Ectopic expression of Oct4, Sox2, Klf4 and c‐Myc (OSKM) induces the reprogramming of somatic cells into induced pluripotent stem cells at a low efficiency B) Ectopic expression of OSKM along with knock down of TRIM28 increases the expression of genes nearby H3K9me3, and induces the expression of endogenous retroviruses. This decondensed chromatin state increases the reprogramming efficiency.
Author	van Lohuizen, Maarten de Vries, Nienke Alexandra Koppens, Martijn Akhtar, Waseem Gogola, Ewa Hulsman, Danielle Beijersbergen, Roderick Leonardus Pawlitzky, Inka Tanger, Ellen Miles, Denise Catherine Gisler, Santiago Lieftink, Cor
Author_xml	– sequence: 1 givenname: Denise Catherine surname: Miles fullname: Miles, Denise Catherine email: miles.d@wehi.edu.au organization: NKI Robotics and Screening Center, The Netherlands Cancer Institute – sequence: 2 givenname: Nienke Alexandra surname: de Vries fullname: de Vries, Nienke Alexandra organization: NKI Robotics and Screening Center, The Netherlands Cancer Institute – sequence: 3 givenname: Santiago surname: Gisler fullname: Gisler, Santiago organization: NKI Robotics and Screening Center, The Netherlands Cancer Institute – sequence: 4 givenname: Cor surname: Lieftink fullname: Lieftink, Cor organization: NKI Robotics and Screening Center, The Netherlands Cancer Institute – sequence: 5 givenname: Waseem surname: Akhtar fullname: Akhtar, Waseem organization: NKI Robotics and Screening Center, The Netherlands Cancer Institute – sequence: 6 givenname: Ewa surname: Gogola fullname: Gogola, Ewa organization: The Netherlands Cancer Institute – sequence: 7 givenname: Inka surname: Pawlitzky fullname: Pawlitzky, Inka organization: NKI Robotics and Screening Center, The Netherlands Cancer Institute – sequence: 8 givenname: Danielle surname: Hulsman fullname: Hulsman, Danielle organization: NKI Robotics and Screening Center, The Netherlands Cancer Institute – sequence: 9 givenname: Ellen surname: Tanger fullname: Tanger, Ellen organization: NKI Robotics and Screening Center, The Netherlands Cancer Institute – sequence: 10 givenname: Martijn surname: Koppens fullname: Koppens, Martijn organization: NKI Robotics and Screening Center, The Netherlands Cancer Institute – sequence: 11 givenname: Roderick Leonardus surname: Beijersbergen fullname: Beijersbergen, Roderick Leonardus organization: NKI Robotics and Screening Center, The Netherlands Cancer Institute – sequence: 12 givenname: Maarten surname: van Lohuizen fullname: van Lohuizen, Maarten email: m.v.lohuizen@nki.nl organization: Cancer Genomics Centre (CGC.nl)
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Keywords	Epigenetics Reprogramming Induced pluripotent stem cells Trim28
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Snippet	Since the discovery of induced pluripotent stem cells there has been intense interest in understanding the mechanisms that allow a somatic cell to be...
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SubjectTerms	Animals Cell Proliferation Cellular Reprogramming - genetics Chromatin Chromatin - metabolism Domains Endogenous retroviruses Endogenous Retroviruses - metabolism Epigenesis, Genetic Epigenetics Gene expression Gene Knockdown Techniques Genomes Histone-Lysine N-Methyltransferase Histones - metabolism Induced pluripotent stem cells Lysine - metabolism Methylation Mice, Transgenic Models, Biological Pluripotency Pluripotent Stem Cells - cytology Pluripotent Stem Cells - metabolism Reprogramming Retroviridae RNA, Small Interfering - metabolism Somatic cells Stem cells Trim28 Tripartite Motif-Containing Protein 28 - metabolism Up-Regulation - genetics
Title	TRIM28 Is an Epigenetic Barrier to Induced Pluripotent Stem Cell Reprogramming
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