PLZF targets developmental enhancers for activation during osteogenic differentiation of human mesenchymal stem cells

The PLZF transcription factor is essential for osteogenic differentiation of hMSCs; however, its regulation and molecular function during this process is not fully understood. Here, we revealed that the ZBTB16 locus encoding PLZF, is repressed by Polycomb (PcG) and H3K27me3 in naive hMSCs. At the pr...

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Published ineLife Vol. 8
Main Authors Agrawal Singh, Shuchi, Lerdrup, Mads, Gomes, Ana-Luisa R, van de Werken, Harmen JG, Vilstrup Johansen, Jens, Andersson, Robin, Sandelin, Albin, Helin, Kristian, Hansen, Klaus
Format Journal Article
LanguageEnglish
Published England eLife Sciences Publications Ltd 23.01.2019
eLife Sciences Publications, Ltd
Subjects
Acetylation
Biology
Cancer
Cell Differentiation - genetics
Cell Lineage - genetics
Chromatin - metabolism
Chromosomes and Gene Expression
developmental enhancer
Embryonic Development - genetics
Enhancer Elements, Genetic - genetics
Enhancers
Epigenesis, Genetic
Epigenetics
Event-related potentials
Gene expression
Gene loci
Genetic Loci
Genomes
histone H3 lysine 27 tri-methylation
Histones - metabolism
human mesenchymal stem cells
Humans
Hypothesis testing
Lysine - metabolism
Mesenchymal stem cells
Mesenchymal Stem Cells - cytology
Mesenchymal Stem Cells - metabolism
Mesenchyme
Methyltransferase
Mineralization
N-Methyltransferase
Nicotinamide
Nicotinamide N-methyltransferase
Nicotinamide N-Methyltransferase - genetics
Nicotinamide N-Methyltransferase - metabolism
Osteoblastogenesis
osteogenesis
Osteogenesis - genetics
PLZF
Polycomb group proteins
Polycomb proteins
Promoter Regions, Genetic
Promyelocytic Leukemia Zinc Finger Protein - genetics
Promyelocytic Leukemia Zinc Finger Protein - metabolism
Protein Binding
Proteins
RNA - genetics
Stem cells
Transcription factors
Transcriptome - genetics
Denmark
New York
Netherlands
United States > US
Copenhagen Denmark
developmental enhancer
histone H3 lysine 27 tri-methylation
human mesenchymal stem cells
ZBTB16
chromosomes
osteogenesis
PLZF
human
Polycomb proteins
gene expression
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Abstract The PLZF transcription factor is essential for osteogenic differentiation of hMSCs; however, its regulation and molecular function during this process is not fully understood. Here, we revealed that the ZBTB16 locus encoding PLZF, is repressed by Polycomb (PcG) and H3K27me3 in naive hMSCs. At the pre-osteoblast stage of differentiation, the locus lost PcG binding and H3K27me3, gained JMJD3 recruitment, and H3K27ac resulting in high expression of PLZF. Subsequently, PLZF was recruited to osteogenic enhancers, influencing H3K27 acetylation and expression of nearby genes important for osteogenic function. Furthermore, we identified a latent enhancer within the ZBTB16/PLZF locus itself that became active, gained PLZF, p300 and Mediator binding and looped to the promoter of the nicotinamide N-methyltransferase (NNMT) gene. The increased expression of NNMT correlated with a decline in SAM levels, which is dependent on PLZF and is required for osteogenic differentiation.
AbstractList The PLZF transcription factor is essential for osteogenic differentiation of hMSCs; however, its regulation and molecular function during this process is not fully understood. Here, we revealed that the ZBTB16 locus encoding PLZF, is repressed by Polycomb (PcG) and H3K27me3 in naive hMSCs. At the pre-osteoblast stage of differentiation, the locus lost PcG binding and H3K27me3, gained JMJD3 recruitment, and H3K27ac resulting in high expression of PLZF. Subsequently, PLZF was recruited to osteogenic enhancers, influencing H3K27 acetylation and expression of nearby genes important for osteogenic function. Furthermore, we identified a latent enhancer within the ZBTB16/PLZF locus itself that became active, gained PLZF, p300 and Mediator binding and looped to the promoter of the nicotinamide N-methyltransferase (NNMT) gene. The increased expression of NNMT correlated with a decline in SAM levels, which is dependent on PLZF and is required for osteogenic differentiation.
The PLZF transcription factor is essential for osteogenic differentiation of hMSCs; however, its regulation and molecular function during this process is not fully understood. Here, we revealed that the ZBTB16 locus encoding PLZF, is repressed by Polycomb (PcG) and H3K27me3 in naive hMSCs. At the pre-osteoblast stage of differentiation, the locus lost PcG binding and H3K27me3, gained JMJD3 recruitment, and H3K27ac resulting in high expression of PLZF. Subsequently, PLZF was recruited to osteogenic enhancers, influencing H3K27 acetylation and expression of nearby genes important for osteogenic function. Furthermore, we identified a latent enhancer within the ZBTB16/PLZF locus itself that became active, gained PLZF, p300 and Mediator binding and looped to the promoter of the nicotinamide N-methyltransferase ( NNMT ) gene. The increased expression of NNMT correlated with a decline in SAM levels, which is dependent on PLZF and is required for osteogenic differentiation.
The PLZF transcription factor is essential for osteogenic differentiation of hMSCs; however, its regulation and molecular function during this process is not fully understood. Here, we revealed that the ZBTB16 locus encoding PLZF, is repressed by Polycomb (PcG) and H3K27me3 in naive hMSCs. At the pre-osteoblast stage of differentiation, the locus lost PcG binding and H3K27me3, gained JMJD3 recruitment, and H3K27ac resulting in high expression of PLZF. Subsequently, PLZF was recruited to osteogenic enhancers, influencing H3K27 acetylation and expression of nearby genes important for osteogenic function. Furthermore, we identified a latent enhancer within the ZBTB16/PLZF locus itself that became active, gained PLZF, p300 and Mediator binding and looped to the promoter of the nicotinamide N-methyltransferase (NNMT) gene. The increased expression of NNMT correlated with a decline in SAM levels, which is dependent on PLZF and is required for osteogenic differentiation.The PLZF transcription factor is essential for osteogenic differentiation of hMSCs; however, its regulation and molecular function during this process is not fully understood. Here, we revealed that the ZBTB16 locus encoding PLZF, is repressed by Polycomb (PcG) and H3K27me3 in naive hMSCs. At the pre-osteoblast stage of differentiation, the locus lost PcG binding and H3K27me3, gained JMJD3 recruitment, and H3K27ac resulting in high expression of PLZF. Subsequently, PLZF was recruited to osteogenic enhancers, influencing H3K27 acetylation and expression of nearby genes important for osteogenic function. Furthermore, we identified a latent enhancer within the ZBTB16/PLZF locus itself that became active, gained PLZF, p300 and Mediator binding and looped to the promoter of the nicotinamide N-methyltransferase (NNMT) gene. The increased expression of NNMT correlated with a decline in SAM levels, which is dependent on PLZF and is required for osteogenic differentiation.
The PLZF transcription factor is essential for osteogenic differentiation of hMSCs; however, its regulation and molecular function during this process is not fully understood. Here, we revealed that the locus encoding PLZF, is repressed by Polycomb (PcG) and H3K27me3 in naive hMSCs. At the pre-osteoblast stage of differentiation, the locus lost PcG binding and H3K27me3, gained JMJD3 recruitment, and H3K27ac resulting in high expression of PLZF. Subsequently, PLZF was recruited to osteogenic enhancers, influencing H3K27 acetylation and expression of nearby genes important for osteogenic function. Furthermore, we identified a latent enhancer within the locus itself that became active, gained PLZF, p300 and Mediator binding and looped to the promoter of the nicotinamide N-methyltransferase ( ) gene. The increased expression of NNMT correlated with a decline in SAM levels, which is dependent on PLZF and is required for osteogenic differentiation.
Author Sandelin, Albin
Lerdrup, Mads
Gomes, Ana-Luisa R
Vilstrup Johansen, Jens
Helin, Kristian
van de Werken, Harmen JG
Agrawal Singh, Shuchi
Andersson, Robin
Hansen, Klaus
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  surname: Gomes
  fullname: Gomes, Ana-Luisa R
  organization: Biotech Research and Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark, Centre for Epigenetics, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
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  surname: van de Werken
  fullname: van de Werken, Harmen JG
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  surname: Andersson
  fullname: Andersson, Robin
  organization: Biotech Research and Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark, Centre for Epigenetics, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark, Department of Biology, The Bioinformatics Centre, University of Copenhagen, Copenhagen, Denmark
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  organization: Biotech Research and Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark, Centre for Epigenetics, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark, Department of Biology, The Bioinformatics Centre, University of Copenhagen, Copenhagen, Denmark
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  surname: Helin
  fullname: Helin, Kristian
  organization: The Novo Nordisk Center for Stem Cell Biology, Faculty of Health and Medical Sciences University of Copenhagen, Copenhagen, Denmark, Cell Biology Program, Memorial Sloan Kettering Cancer Center, New York, United States, Center for Epigenetics Research, Memorial Sloan Kettering Cancer Center, New York, United States
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  givenname: Klaus
  orcidid: 0000-0001-9657-8816
  surname: Hansen
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  organization: Biotech Research and Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark, Centre for Epigenetics, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30672466$$D View this record in MEDLINE/PubMed
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2019, Agrawal Singh et al. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Keywords developmental enhancer
histone H3 lysine 27 tri-methylation
human mesenchymal stem cells
ZBTB16
chromosomes
osteogenesis
PLZF
human
Polycomb proteins
gene expression
Language English
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2019, Agrawal Singh et al.
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Snippet The PLZF transcription factor is essential for osteogenic differentiation of hMSCs; however, its regulation and molecular function during this process is not...
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SubjectTerms Acetylation
Biology
Cancer
Cell Differentiation - genetics
Cell Lineage - genetics
Chromatin - metabolism
Chromosomes and Gene Expression
developmental enhancer
Embryonic Development - genetics
Enhancer Elements, Genetic - genetics
Enhancers
Epigenesis, Genetic
Epigenetics
Event-related potentials
Gene expression
Gene loci
Genetic Loci
Genomes
histone H3 lysine 27 tri-methylation
Histones - metabolism
human mesenchymal stem cells
Humans
Hypothesis testing
Lysine - metabolism
Mesenchymal stem cells
Mesenchymal Stem Cells - cytology
Mesenchymal Stem Cells - metabolism
Mesenchyme
Methyltransferase
Mineralization
N-Methyltransferase
Nicotinamide
Nicotinamide N-methyltransferase
Nicotinamide N-Methyltransferase - genetics
Nicotinamide N-Methyltransferase - metabolism
Osteoblastogenesis
osteogenesis
Osteogenesis - genetics
PLZF
Polycomb group proteins
Polycomb proteins
Promoter Regions, Genetic
Promyelocytic Leukemia Zinc Finger Protein - genetics
Promyelocytic Leukemia Zinc Finger Protein - metabolism
Protein Binding
Proteins
RNA - genetics
Stem cells
Transcription factors
Transcriptome - genetics
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Title PLZF targets developmental enhancers for activation during osteogenic differentiation of human mesenchymal stem cells
URI https://www.ncbi.nlm.nih.gov/pubmed/30672466
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https://pubmed.ncbi.nlm.nih.gov/PMC6344081
https://doaj.org/article/2c7c464f81894c2a99ba1da3eb3405fb
Volume 8
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