Mutant EZH2 alters the epigenetic network and increases epigenetic heterogeneity in B cell lymphoma.

Diffuse large B cell lymphomas and follicular lymphomas show recurrent mutations in epigenetic regulators; among these are loss-of-function mutations in KMT2D and gain-of-function mutations in EZH2. To systematically explore the effects of these mutations on the wiring of the epigenetic network, we...

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Main Authors: Ofir Griess, Noa Furth, Nofar Harpaz, Nicoletta Di Bernardo, Tomer-Meir Salame, Bareket Dassa, Ioannis Karagiannidis, Yusuke Isshiki, Menachem Gross, Ari M Melnick, Wendy Béguelin, Guy Ron, Efrat Shema
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-06-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3003191
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author Ofir Griess
Noa Furth
Nofar Harpaz
Nicoletta Di Bernardo
Tomer-Meir Salame
Bareket Dassa
Ioannis Karagiannidis
Yusuke Isshiki
Menachem Gross
Ari M Melnick
Wendy Béguelin
Guy Ron
Efrat Shema
author_facet Ofir Griess
Noa Furth
Nofar Harpaz
Nicoletta Di Bernardo
Tomer-Meir Salame
Bareket Dassa
Ioannis Karagiannidis
Yusuke Isshiki
Menachem Gross
Ari M Melnick
Wendy Béguelin
Guy Ron
Efrat Shema
author_sort Ofir Griess
collection DOAJ
description Diffuse large B cell lymphomas and follicular lymphomas show recurrent mutations in epigenetic regulators; among these are loss-of-function mutations in KMT2D and gain-of-function mutations in EZH2. To systematically explore the effects of these mutations on the wiring of the epigenetic network, we applied a single-cell approach to probe a wide array of histone modifications. We show that mutant-EZH2 elicits extensive effects on the epigenome of lymphomas, beyond alterations to H3K27 methylations, and is epistatic over KMT2D mutations. Utilizing the single-cell data, we present computational methods to measure epigenetic heterogeneity. We identify an unexpected characteristic of mutant-EZH2, but not KMT2D, in increasing heterogeneity, shedding light on a novel oncogenic mechanism mediated by this mutation. Finally, we present tools to reconstruct known interactions within the epigenetic network, as well as reveal potential novel cross talk between various modifications, supported by functional perturbations. Our work highlights novel roles for mutant-EZH2 in lymphomagenesis and establishes new concepts for measuring epigenetic heterogeneity and intra-chromatin connectivity in cancer cells.
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issn 1544-9173
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spelling doaj-art-15f7583d3cbf4310a01e4792b2539c182025-08-20T02:35:44ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852025-06-01236e300319110.1371/journal.pbio.3003191Mutant EZH2 alters the epigenetic network and increases epigenetic heterogeneity in B cell lymphoma.Ofir GriessNoa FurthNofar HarpazNicoletta Di BernardoTomer-Meir SalameBareket DassaIoannis KaragiannidisYusuke IsshikiMenachem GrossAri M MelnickWendy BéguelinGuy RonEfrat ShemaDiffuse large B cell lymphomas and follicular lymphomas show recurrent mutations in epigenetic regulators; among these are loss-of-function mutations in KMT2D and gain-of-function mutations in EZH2. To systematically explore the effects of these mutations on the wiring of the epigenetic network, we applied a single-cell approach to probe a wide array of histone modifications. We show that mutant-EZH2 elicits extensive effects on the epigenome of lymphomas, beyond alterations to H3K27 methylations, and is epistatic over KMT2D mutations. Utilizing the single-cell data, we present computational methods to measure epigenetic heterogeneity. We identify an unexpected characteristic of mutant-EZH2, but not KMT2D, in increasing heterogeneity, shedding light on a novel oncogenic mechanism mediated by this mutation. Finally, we present tools to reconstruct known interactions within the epigenetic network, as well as reveal potential novel cross talk between various modifications, supported by functional perturbations. Our work highlights novel roles for mutant-EZH2 in lymphomagenesis and establishes new concepts for measuring epigenetic heterogeneity and intra-chromatin connectivity in cancer cells.https://doi.org/10.1371/journal.pbio.3003191
spellingShingle Ofir Griess
Noa Furth
Nofar Harpaz
Nicoletta Di Bernardo
Tomer-Meir Salame
Bareket Dassa
Ioannis Karagiannidis
Yusuke Isshiki
Menachem Gross
Ari M Melnick
Wendy Béguelin
Guy Ron
Efrat Shema
Mutant EZH2 alters the epigenetic network and increases epigenetic heterogeneity in B cell lymphoma.
PLoS Biology
title Mutant EZH2 alters the epigenetic network and increases epigenetic heterogeneity in B cell lymphoma.
title_full Mutant EZH2 alters the epigenetic network and increases epigenetic heterogeneity in B cell lymphoma.
title_fullStr Mutant EZH2 alters the epigenetic network and increases epigenetic heterogeneity in B cell lymphoma.
title_full_unstemmed Mutant EZH2 alters the epigenetic network and increases epigenetic heterogeneity in B cell lymphoma.
title_short Mutant EZH2 alters the epigenetic network and increases epigenetic heterogeneity in B cell lymphoma.
title_sort mutant ezh2 alters the epigenetic network and increases epigenetic heterogeneity in b cell lymphoma
url https://doi.org/10.1371/journal.pbio.3003191
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