Linking aberrant chromatin features in chronic lymphocytic leukemia to transcription factor networks

Abstract In chronic lymphocytic leukemia (CLL), a diverse set of genetic mutations is embedded in a deregulated epigenetic landscape that drives cancerogenesis. To elucidate the role of aberrant chromatin features, we mapped DNA methylation, seven histone modifications, nucleosome positions, chromat...

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Main Authors: Jan‐Philipp Mallm, Murat Iskar, Naveed Ishaque, Lara C Klett, Sabrina J Kugler, Jose M Muino, Vladimir B Teif, Alexandra M Poos, Sebastian Großmann, Fabian Erdel, Daniele Tavernari, Sandra D Koser, Sabrina Schumacher, Benedikt Brors, Rainer König, Daniel Remondini, Martin Vingron, Stephan Stilgenbauer, Peter Lichter, Marc Zapatka, Daniel Mertens, Karsten Rippe
Format: Article
Language:English
Published: Springer Nature 2019-05-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.15252/msb.20188339
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author Jan‐Philipp Mallm
Murat Iskar
Naveed Ishaque
Lara C Klett
Sabrina J Kugler
Jose M Muino
Vladimir B Teif
Alexandra M Poos
Sebastian Großmann
Fabian Erdel
Daniele Tavernari
Sandra D Koser
Sabrina Schumacher
Benedikt Brors
Rainer König
Daniel Remondini
Martin Vingron
Stephan Stilgenbauer
Peter Lichter
Marc Zapatka
Daniel Mertens
Karsten Rippe
author_facet Jan‐Philipp Mallm
Murat Iskar
Naveed Ishaque
Lara C Klett
Sabrina J Kugler
Jose M Muino
Vladimir B Teif
Alexandra M Poos
Sebastian Großmann
Fabian Erdel
Daniele Tavernari
Sandra D Koser
Sabrina Schumacher
Benedikt Brors
Rainer König
Daniel Remondini
Martin Vingron
Stephan Stilgenbauer
Peter Lichter
Marc Zapatka
Daniel Mertens
Karsten Rippe
author_sort Jan‐Philipp Mallm
collection DOAJ
description Abstract In chronic lymphocytic leukemia (CLL), a diverse set of genetic mutations is embedded in a deregulated epigenetic landscape that drives cancerogenesis. To elucidate the role of aberrant chromatin features, we mapped DNA methylation, seven histone modifications, nucleosome positions, chromatin accessibility, binding of EBF1 and CTCF, as well as the transcriptome of B cells from CLL patients and healthy donors. A globally increased histone deacetylase activity was detected and half of the genome comprised transcriptionally downregulated partially DNA methylated domains demarcated by CTCF. CLL samples displayed a H3K4me3 redistribution and nucleosome gain at promoters as well as changes of enhancer activity and enhancer linkage to target genes. A DNA binding motif analysis identified transcription factors that gained or lost binding in CLL at sites with aberrant chromatin features. These findings were integrated into a gene regulatory enhancer containing network enriched for B‐cell receptor signaling pathway components. Our study predicts novel molecular links to targets of CLL therapies and provides a valuable resource for further studies on the epigenetic contribution to the disease.
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publishDate 2019-05-01
publisher Springer Nature
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series Molecular Systems Biology
spelling doaj-art-d531e1d3965044bc9b7dc0b0a7049c9a2025-08-20T03:46:37ZengSpringer NatureMolecular Systems Biology1744-42922019-05-0115512010.15252/msb.20188339Linking aberrant chromatin features in chronic lymphocytic leukemia to transcription factor networksJan‐Philipp Mallm0Murat Iskar1Naveed Ishaque2Lara C Klett3Sabrina J Kugler4Jose M Muino5Vladimir B Teif6Alexandra M Poos7Sebastian Großmann8Fabian Erdel9Daniele Tavernari10Sandra D Koser11Sabrina Schumacher12Benedikt Brors13Rainer König14Daniel Remondini15Martin Vingron16Stephan Stilgenbauer17Peter Lichter18Marc Zapatka19Daniel Mertens20Karsten Rippe21Division of Chromatin Networks, German Cancer Research Center (DKFZ) and BioquantDivision of Molecular Genetics, German Cancer Research Center (DKFZ)Division of Theoretical Bioinformatics and Heidelberg Center for Personalized Oncology, German Cancer Research Center (DKFZ)Division of Chromatin Networks, German Cancer Research Center (DKFZ) and BioquantMechanisms of Leukemogenesis, German Cancer Research Center (DKFZ)Department of Computational Molecular Biology, Max Planck Institute for Molecular GeneticsSchool of Biological Sciences, University of EssexDivision of Chromatin Networks, German Cancer Research Center (DKFZ) and BioquantDivision of Chromatin Networks, German Cancer Research Center (DKFZ) and BioquantDivision of Chromatin Networks, German Cancer Research Center (DKFZ) and BioquantDivision of Chromatin Networks, German Cancer Research Center (DKFZ) and BioquantDivision of Applied Bioinformatics, German Cancer Research Center (DKFZ)Division of Chromatin Networks, German Cancer Research Center (DKFZ) and BioquantDivision of Applied Bioinformatics, German Cancer Research Center (DKFZ)Integrated Research and Treatment Center, Center for Sepsis Control and Care (CSCC), Jena University HospitalDepartment of Physics and Astronomy, Bologna UniversityDepartment of Computational Molecular Biology, Max Planck Institute for Molecular GeneticsDepartment of Internal Medicine III, University Hospital UlmDivision of Molecular Genetics, German Cancer Research Center (DKFZ)Division of Molecular Genetics, German Cancer Research Center (DKFZ)Mechanisms of Leukemogenesis, German Cancer Research Center (DKFZ)Division of Chromatin Networks, German Cancer Research Center (DKFZ) and BioquantAbstract In chronic lymphocytic leukemia (CLL), a diverse set of genetic mutations is embedded in a deregulated epigenetic landscape that drives cancerogenesis. To elucidate the role of aberrant chromatin features, we mapped DNA methylation, seven histone modifications, nucleosome positions, chromatin accessibility, binding of EBF1 and CTCF, as well as the transcriptome of B cells from CLL patients and healthy donors. A globally increased histone deacetylase activity was detected and half of the genome comprised transcriptionally downregulated partially DNA methylated domains demarcated by CTCF. CLL samples displayed a H3K4me3 redistribution and nucleosome gain at promoters as well as changes of enhancer activity and enhancer linkage to target genes. A DNA binding motif analysis identified transcription factors that gained or lost binding in CLL at sites with aberrant chromatin features. These findings were integrated into a gene regulatory enhancer containing network enriched for B‐cell receptor signaling pathway components. Our study predicts novel molecular links to targets of CLL therapies and provides a valuable resource for further studies on the epigenetic contribution to the disease.https://doi.org/10.15252/msb.20188339bivalent promoterDNA methylationenhancergene regulatory networkshistone modifications
spellingShingle Jan‐Philipp Mallm
Murat Iskar
Naveed Ishaque
Lara C Klett
Sabrina J Kugler
Jose M Muino
Vladimir B Teif
Alexandra M Poos
Sebastian Großmann
Fabian Erdel
Daniele Tavernari
Sandra D Koser
Sabrina Schumacher
Benedikt Brors
Rainer König
Daniel Remondini
Martin Vingron
Stephan Stilgenbauer
Peter Lichter
Marc Zapatka
Daniel Mertens
Karsten Rippe
Linking aberrant chromatin features in chronic lymphocytic leukemia to transcription factor networks
Molecular Systems Biology
bivalent promoter
DNA methylation
enhancer
gene regulatory networks
histone modifications
title Linking aberrant chromatin features in chronic lymphocytic leukemia to transcription factor networks
title_full Linking aberrant chromatin features in chronic lymphocytic leukemia to transcription factor networks
title_fullStr Linking aberrant chromatin features in chronic lymphocytic leukemia to transcription factor networks
title_full_unstemmed Linking aberrant chromatin features in chronic lymphocytic leukemia to transcription factor networks
title_short Linking aberrant chromatin features in chronic lymphocytic leukemia to transcription factor networks
title_sort linking aberrant chromatin features in chronic lymphocytic leukemia to transcription factor networks
topic bivalent promoter
DNA methylation
enhancer
gene regulatory networks
histone modifications
url https://doi.org/10.15252/msb.20188339
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