DNA methylation of intragenic CpG islands depends on their transcriptional activity during differentiation and disease

The human genome contains ∼30,000 CpG islands (CGIs). While CGIs associated with promoters nearly always remain unmethylated, many of the ∼9,000 CGIs lying within gene bodies become methylated during development and differentiation. Both promoter and intragenic CGIs may also become abnormally methyl...

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Published in:Proceedings of the National Academy of Sciences - PNAS 2017-09, Vol.114 (36), p.E7526-E7535
Main Authors: Jeziorska, Danuta M., Murray, Robert J. S., De Gobbi, Marco, Gaentzsch, Ricarda, Garrick, David, Ayyub, Helena, Chen, Taiping, Li, En, Telenius, Jelena, Lynch, Magnus, Graham, Bryony, Smith, Andrew J. H., Lund, Jonathan N., Hughes, Jim R., Higgs, Douglas R., Tufarelli, Cristina
Format: Article
Language:English
Subjects:
Animals
Biological Sciences
Cell Differentiation - genetics
Cell Line
Chromatin
CpG islands
CpG Islands - genetics
Deoxyribonucleic acid
Differentiation
DNA
DNA methylation
DNA Methylation - genetics
DNA methyltransferase
Epigenesis, Genetic - genetics
Epigenetics
Genome, Human - genetics
Genomes
Humans
Islands
Malignancy
Mice
PNAS Plus
Promoter Regions, Genetic - genetics
Promoters
Sequence Analysis, DNA - methods
Studies
Transcription, Genetic - genetics
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cited_by cdi_FETCH-LOGICAL-c443t-9ac563e41a9682d23d976628f674b64a626829b8ab5fa83818176f12ead13daf3
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creator Jeziorska, Danuta M.
Murray, Robert J. S.
De Gobbi, Marco
Gaentzsch, Ricarda
Garrick, David
Ayyub, Helena
Chen, Taiping
Li, En
Telenius, Jelena
Lynch, Magnus
Graham, Bryony
Smith, Andrew J. H.
Lund, Jonathan N.
Hughes, Jim R.
Higgs, Douglas R.
Tufarelli, Cristina
description The human genome contains ∼30,000 CpG islands (CGIs). While CGIs associated with promoters nearly always remain unmethylated, many of the ∼9,000 CGIs lying within gene bodies become methylated during development and differentiation. Both promoter and intragenic CGIs may also become abnormally methylated as a result of genome rearrangements and in malignancy. The epigenetic mechanisms by which some CGIs become methylated but others, in the same cell, remain unmethylated in these situations are poorly understood. Analyzing specific loci and using a genome-wide analysis, we show that transcription running across CGIs, associated with specific chromatin modifications, is required for DNA methyltransferase 3B (DNMT3B)-mediated DNA methylation of many naturally occurring intragenic CGIs. Importantly, we also show that a subgroup of intragenic CGIs is not sensitive to this process of transcription-mediated methylation and that this correlates with their individual intrinsic capacity to initiate transcription in vivo. We propose a general model of how transcription could act as a primary determinant of the patterns of CGI methylation in normal development and differentiation, and in human disease.
doi_str_mv 10.1073/pnas.1703087114
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The epigenetic mechanisms by which some CGIs become methylated but others, in the same cell, remain unmethylated in these situations are poorly understood. Analyzing specific loci and using a genome-wide analysis, we show that transcription running across CGIs, associated with specific chromatin modifications, is required for DNA methyltransferase 3B (DNMT3B)-mediated DNA methylation of many naturally occurring intragenic CGIs. Importantly, we also show that a subgroup of intragenic CGIs is not sensitive to this process of transcription-mediated methylation and that this correlates with their individual intrinsic capacity to initiate transcription in vivo. 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S.</au><au>De Gobbi, Marco</au><au>Gaentzsch, Ricarda</au><au>Garrick, David</au><au>Ayyub, Helena</au><au>Chen, Taiping</au><au>Li, En</au><au>Telenius, Jelena</au><au>Lynch, Magnus</au><au>Graham, Bryony</au><au>Smith, Andrew J. 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Bird, University of Edinburgh, Edinburgh, United Kingdom, and approved July 28, 2017 (received for review February 23, 2017)</notes><notes>3Present address: Seven Bridges Genomics, London NW1 2RA, United Kingdom.</notes><notes>1Present address: Human Development and Health, Institute of Developmental Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom.</notes><abstract>The human genome contains ∼30,000 CpG islands (CGIs). While CGIs associated with promoters nearly always remain unmethylated, many of the ∼9,000 CGIs lying within gene bodies become methylated during development and differentiation. Both promoter and intragenic CGIs may also become abnormally methylated as a result of genome rearrangements and in malignancy. The epigenetic mechanisms by which some CGIs become methylated but others, in the same cell, remain unmethylated in these situations are poorly understood. Analyzing specific loci and using a genome-wide analysis, we show that transcription running across CGIs, associated with specific chromatin modifications, is required for DNA methyltransferase 3B (DNMT3B)-mediated DNA methylation of many naturally occurring intragenic CGIs. Importantly, we also show that a subgroup of intragenic CGIs is not sensitive to this process of transcription-mediated methylation and that this correlates with their individual intrinsic capacity to initiate transcription in vivo. We propose a general model of how transcription could act as a primary determinant of the patterns of CGI methylation in normal development and differentiation, and in human disease.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>28827334</pmid><doi>10.1073/pnas.1703087114</doi><orcidid>https://orcid.org/0000-0002-1053-4618</orcidid><oa>free_for_read</oa></addata></record>
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source JSTOR Archival Journals and Primary Sources Collection; PubMed Central
subjects Animals
Biological Sciences
Cell Differentiation - genetics
Cell Line
Chromatin
CpG islands
CpG Islands - genetics
Deoxyribonucleic acid
Differentiation
DNA
DNA methylation
DNA Methylation - genetics
DNA methyltransferase
Epigenesis, Genetic - genetics
Epigenetics
Genome, Human - genetics
Genomes
Humans
Islands
Malignancy
Mice
PNAS Plus
Promoter Regions, Genetic - genetics
Promoters
Sequence Analysis, DNA - methods
Studies
Transcription, Genetic - genetics
title DNA methylation of intragenic CpG islands depends on their transcriptional activity during differentiation and disease
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