The Histone Methyltransferase KMT2B Is Required for RNA Polymerase II Association and Protection from DNA Methylation at the MagohB CpG Island Promoter

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Published in:Molecular and Cellular Biology Vol. 33; no. 7; pp. 1383 - 1393
Main Authors: Ladopoulos, Vasileios, Hofemeister, Helmut, Hoogenkamp, Maarten, Riggs, Arthur D., Stewart, A. Francis, Bonifer, Constanze
Format: Journal Article
Language:English
Published: United States American Society for Microbiology 01.04.2013
Taylor & Francis
Subjects:
Animals
Cell Line
chromatin
Chromatin - genetics
Chromatin - metabolism
CpG Islands
DNA Methylation
DNA-directed RNA polymerase
Down-Regulation
embryogenesis
Embryonic Stem Cells - metabolism
Gene Silencing
genes
genomic islands
Histone Methyltransferases
Histone-Lysine N-Methyltransferase - genetics
Histone-Lysine N-Methyltransferase - metabolism
histones
Kinetics
lysine
methyltransferases
Mice
Myeloid-Lymphoid Leukemia Protein - genetics
Myeloid-Lymphoid Leukemia Protein - metabolism
Nuclear Proteins - genetics
Nuclear Proteins - metabolism
Promoter Regions, Genetic
RNA Polymerase II - genetics
RNA Polymerase II - metabolism
transcription (genetics)
ISSN:0270-7306, 1098-5549, 1098-5549
Online Access:Get full text
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Abstract Article Usage Stats Services MCB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue Spotlights in the Current Issue MCB About MCB Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy MCB RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0270-7306 Online ISSN: 1098-5549 Copyright © 2014 by the American Society for Microbiology.   For an alternate route to MCB .asm.org, visit: MCB       
AbstractList KMT2B (MLL2/WBP7) is a member of the MLL subfamily of H3K4-specific histone lysine methyltransferases (KMT2) and is vital for normal embryonic development in the mouse. To gain insight into the molecular mechanism underlying KMT2B function, we focused on MagohB, which is controlled by a CpG island promoter. We show that in cells lacking Mll2—the gene encoding KMT2B—the MagohB promoter resides in inaccessible chromatin and is methylated. To dissect the molecular events leading to the establishment of silencing, we performed kinetic studies in Mll2-conditional-knockout embryonic stem cells. KMT2B depletion was followed by the loss of the active chromatin marks and progressive loss of RNA polymerase II binding with a concomitant downregulation of MagohB expression. Once the active chromatin marks were lost, the MagohB promoter was rapidly methylated. We demonstrate that in the presence of KMT2B, neither transcription elongation nor RNA polymerase II binding is required to maintain H3K4 trimethylation at the MagohB promoter and protect it from DNA methylation. Reexpression of KMT2B was sufficient to reinstate an active MagohB promoter. Our study provides a paradigm for the idea that KMT2 proteins are crucial components for establishing and maintaining the transcriptionally active and unmethylated state of CpG island promoters.
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KMT2B (MLL2/WBP7) is a member of the MLL subfamily of H3K4-specific histone lysine methyltransferases (KMT2) and is vital for normal embryonic development in the mouse. To gain insight into the molecular mechanism underlying KMT2B function, we focused on MagohB, which is controlled by a CpG island promoter. We show that in cells lacking Mll2-the gene encoding KMT2B-the MagohB promoter resides in inaccessible chromatin and is methylated. To dissect the molecular events leading to the establishment of silencing, we performed kinetic studies in Mll2-conditional-knockout embryonic stem cells. KMT2B depletion was followed by the loss of the active chromatin marks and progressive loss of RNA polymerase II binding with a concomitant downregulation of MagohB expression. Once the active chromatin marks were lost, the MagohB promoter was rapidly methylated. We demonstrate that in the presence of KMT2B, neither transcription elongation nor RNA polymerase II binding is required to maintain H3K4 trimethylation at the MagohB promoter and protect it from DNA methylation. Reexpression of KMT2B was sufficient to reinstate an active MagohB promoter. Our study provides a paradigm for the idea that KMT2 proteins are crucial components for establishing and maintaining the transcriptionally active and unmethylated state of CpG island promoters.KMT2B (MLL2/WBP7) is a member of the MLL subfamily of H3K4-specific histone lysine methyltransferases (KMT2) and is vital for normal embryonic development in the mouse. To gain insight into the molecular mechanism underlying KMT2B function, we focused on MagohB, which is controlled by a CpG island promoter. We show that in cells lacking Mll2-the gene encoding KMT2B-the MagohB promoter resides in inaccessible chromatin and is methylated. To dissect the molecular events leading to the establishment of silencing, we performed kinetic studies in Mll2-conditional-knockout embryonic stem cells. KMT2B depletion was followed by the loss of the active chromatin marks and progressive loss of RNA polymerase II binding with a concomitant downregulation of MagohB expression. Once the active chromatin marks were lost, the MagohB promoter was rapidly methylated. We demonstrate that in the presence of KMT2B, neither transcription elongation nor RNA polymerase II binding is required to maintain H3K4 trimethylation at the MagohB promoter and protect it from DNA methylation. Reexpression of KMT2B was sufficient to reinstate an active MagohB promoter. Our study provides a paradigm for the idea that KMT2 proteins are crucial components for establishing and maintaining the transcriptionally active and unmethylated state of CpG island promoters.
Author Helmut Hofemeister
Vasileios Ladopoulos
A. Francis Stewart
Constanze Bonifer
Arthur D. Riggs
Maarten Hoogenkamp
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Snippet Article Usage Stats Services MCB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley...
KMT2B (MLL2/WBP7) is a member of the MLL subfamily of H3K4-specific histone lysine methyltransferases (KMT2) and is vital for normal embryonic development in...
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StartPage 1383
SubjectTerms Animals
Cell Line
chromatin
Chromatin - genetics
Chromatin - metabolism
CpG Islands
DNA Methylation
DNA-directed RNA polymerase
Down-Regulation
embryogenesis
Embryonic Stem Cells - metabolism
Gene Silencing
genes
genomic islands
Histone Methyltransferases
Histone-Lysine N-Methyltransferase - genetics
Histone-Lysine N-Methyltransferase - metabolism
histones
Kinetics
lysine
methyltransferases
Mice
Myeloid-Lymphoid Leukemia Protein - genetics
Myeloid-Lymphoid Leukemia Protein - metabolism
Nuclear Proteins - genetics
Nuclear Proteins - metabolism
Promoter Regions, Genetic
RNA Polymerase II - genetics
RNA Polymerase II - metabolism
transcription (genetics)
Title The Histone Methyltransferase KMT2B Is Required for RNA Polymerase II Association and Protection from DNA Methylation at the MagohB CpG Island Promoter
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