Histone H1 loss drives lymphoma by disrupting 3D chromatin architecture.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
01 2021
Historique:
received: 02 01 2020
accepted: 08 10 2020
pubmed: 11 12 2020
medline: 26 2 2021
entrez: 10 12 2020
Statut: ppublish

Résumé

Linker histone H1 proteins bind to nucleosomes and facilitate chromatin compaction

Identifiants

pubmed: 33299181
doi: 10.1038/s41586-020-3017-y
pii: 10.1038/s41586-020-3017-y
pmc: PMC7855728
mid: NIHMS1636448
doi:

Substances chimiques

Chromatin 0
Histones 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

299-305

Subventions

Organisme : NCI NIH HHS
ID : R01 CA252239
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA196539
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM108569
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA060553
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM138386
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA195732
Pays : United States
Organisme : NIH HHS
ID : S10 OD025194
Pays : United States
Organisme : NCI NIH HHS
ID : U54 CA193419
Pays : United States
Organisme : NCI NIH HHS
ID : R35 CA220499
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA229086
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM122562
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA228528
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM116143
Pays : United States
Organisme : NIGMS NIH HHS
ID : R44 GM116584
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA234561
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA194547
Pays : United States
Organisme : NIDCR NIH HHS
ID : R44 DE029633
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA260028
Pays : United States

Commentaires et corrections

Type : CommentIn

Références

Fyodorov, D. V., Zhou, B. R., Skoultchi, A. I. & Bai, Y. Emerging roles of linker histones in regulating chromatin structure and function. Nat. Rev. Mol. Cell Biol. 19, 192–206 (2018).
doi: 10.1038/nrm.2017.94
Fan, Y. et al. Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123, 1199–1212 (2005).
doi: 10.1016/j.cell.2005.10.028
Cao, K. et al. High-resolution mapping of H1 linker histone variants in embryonic stem cells. PLoS Genet. 9, e1003417 (2013).
doi: 10.1371/journal.pgen.1003417
Zhang, Y. et al. Histone H1 depletion impairs embryonic stem cell differentiation. PLoS Genet. 8, e1002691 (2012).
doi: 10.1371/journal.pgen.1002691
Nacev, B. A. et al. The expanding landscape of ‘oncohistone’ mutations in human cancers. Nature 567, 473–478 (2019).
doi: 10.1038/s41586-019-1038-1
Bennett, R. L. et al. A mutation in histone H2B represents a new class of oncogenic driver. Cancer Discov. 9, 1438–1451 (2019).
doi: 10.1158/2159-8290.CD-19-0393
Okosun, J. et al. Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat. Genet. 46, 176–181 (2014).
doi: 10.1038/ng.2856
Li, H. et al. Mutations in linker histone genes HIST1H1 B, C, D, and E; OCT2 (POU2F2); IRF8; and ARID1A underlying the pathogenesis of follicular lymphoma. Blood 123, 1487–1498 (2014).
doi: 10.1182/blood-2013-05-500264
Reichel, J. et al. Flow sorting and exome sequencing reveal the oncogenome of primary Hodgkin and Reed-Sternberg cells. Blood 125, 1061–1072 (2015).
doi: 10.1182/blood-2014-11-610436
Mesin, L., Ersching, J. & Victora, G. D. Germinal center B Cell dynamics. Immunity 45, 471–482 (2016).
doi: 10.1016/j.immuni.2016.09.001
Chapuy, B. et al. Molecular subtypes of diffuse large B cell lymphoma are associated with distinct pathogenic mechanisms and outcomes. Nat. Med. 24, 679–690 (2018).
doi: 10.1038/s41591-018-0016-8
Fan, Y. et al. H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Mol. Cell. Biol. 23, 4559–4572 (2003).
doi: 10.1128/MCB.23.13.4559-4572.2003
Wright, G. W. et al. A probabilistic classification tool for genetic subtypes of diffuse large B cell lymphoma with therapeutic implications. Cancer Cell 37, 551–568 (2020).
doi: 10.1016/j.ccell.2020.03.015
Zhou, B. R. et al. Structural mechanisms of nucleosome recognition by linker histones. Mol. Cell 59, 628–638 (2015).
doi: 10.1016/j.molcel.2015.06.025
Lu, C. et al. Histone H3K36 mutations promote sarcomagenesis through altered histone methylation landscape. Science 352, 844–849 (2016).
doi: 10.1126/science.aac7272
Swaroop, A. et al. An activating mutation of the NSD2 histone methyltransferase drives oncogenic reprogramming in acute lymphocytic leukemia. Oncogene 38, 671–686 (2019).
doi: 10.1038/s41388-018-0474-y
Béguelin, W. et al. EZH2 is required for germinal center formation and somatic EZH2 mutations promote lymphoid transformation. Cancer Cell 23, 677–692 (2013).
doi: 10.1016/j.ccr.2013.04.011
Ortega-Molina, A. et al. The histone lysine methyltransferase KMT2D sustains a gene expression program that represses B cell lymphoma development. Nat. Med. 21, 1199–1208 (2015).
doi: 10.1038/nm.3943
Eagen, K. P. Principles of chromosome architecture revealed by Hi-C. Trends Biochem. Sci. 43, 469–478 (2018).
doi: 10.1016/j.tibs.2018.03.006
Rao, S. S. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665–1680 (2014).
doi: 10.1016/j.cell.2014.11.021
Izzo, A. et al. The genomic landscape of the somatic linker histone subtypes H1.1 to H1.5 in human cells. Cell Rep. 3, 2142–2154 (2013).
doi: 10.1016/j.celrep.2013.05.003
Bascom, G. D., Myers, C. G. & Schlick, T. Mesoscale modeling reveals formation of an epigenetically driven HOXC gene hub. Proc. Natl Acad. Sci. USA 116, 4955–4962 (2019).
doi: 10.1073/pnas.1816424116
Kim, J. M. et al. Linker histone H1.2 establishes chromatin compaction and gene silencing through recognition of H3K27me3. Sci. Rep. 5, 16714 (2015).
doi: 10.1038/srep16714
Lhoumaud, P. et al. NSD2 overexpression drives clustered chromatin and transcriptional changes in a subset of insulated domains. Nat. Commun. 10, 4843 (2019).
doi: 10.1038/s41467-019-12811-4
Ezponda, T. et al. The histone methyltransferase MMSET/WHSC1 activates TWIST1 to promote an epithelial–mesenchymal transition and invasive properties of prostate cancer. Oncogene 32, 2882–2890 (2013).
doi: 10.1038/onc.2012.297
Mulder, T. A., Wahlin, B. E., Österborg, A. & Palma, M. Targeting the immune microenvironment in lymphomas of B cell origin: from biology to clinical application. Cancers 11, 915 (2019).
doi: 10.3390/cancers11070915
Yang, S. M., Kim, B. J., Norwood Toro, L. & Skoultchi, A. I. H1 linker histone promotes epigenetic silencing by regulating both DNA methylation and histone H3 methylation. Proc. Natl Acad. Sci. USA 110, 1708–1713 (2013).
doi: 10.1073/pnas.1213266110
Geeven, G. et al. Local compartment changes and regulatory landscape alterations in histone H1-depleted cells. Genome Biol. 16, 289 (2015).
doi: 10.1186/s13059-015-0857-0
Wilcockson, M. et al. H1 histones control the epigenetic landscape by local chromatin compaction. Nature https://doi.org/10.1038/s41586-020-3032-z (2020).
Eminli, S. et al. Differentiation stage determines potential of hematopoietic cells for reprogramming into induced pluripotent stem cells. Nat. Genet. 41, 968–976 (2009).
doi: 10.1038/ng.428
Wong, D. J. et al. Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2, 333–344 (2008).
doi: 10.1016/j.stem.2008.02.009
Stadhouders, R. et al. Transcription factors orchestrate dynamic interplay between genome topology and gene regulation during cell reprogramming. Nat. Genet. 50, 238–249 (2018).
doi: 10.1038/s41588-017-0030-7

Auteurs

Nevin Yusufova (N)

Division of Hematology and Medical Oncology, Sanford I. Weill Department of Medicine, Weill Cornell Medicine, New York, NY, USA.
Cell and Molecular Biology Graduate Program, Weill Cornell Medicine, New York, NY, USA.

Andreas Kloetgen (A)

Department of Pathology, NYU School of Medicine, New York, NY, USA.
Department of Computational Biology of Infection Research, Helmholtz Centre for Infection Research, Braunschweig, Germany.

Matt Teater (M)

Division of Hematology and Medical Oncology, Sanford I. Weill Department of Medicine, Weill Cornell Medicine, New York, NY, USA.

Adewola Osunsade (A)

Chemical Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Tri-Institutional PhD Program in Chemical Biology, New York, NY, USA.

Jeannie M Camarillo (JM)

Department of Chemistry, Northwestern University, Evanston, IL, USA.
Department of Molecular Biosciences, Northwestern University, Evanston, IL, USA.
Proteomics Center of Excellence, Northwestern University, Evanston, IL, USA.

Christopher R Chin (CR)

Department of Physiology and Biophysics, Weill Cornell Medicine, New York, NY, USA.
Tri-Institutional PhD Program in Computational Biomedicine, New York, NY, USA.

Ashley S Doane (AS)

Tri-Institutional PhD Program in Computational Biomedicine, New York, NY, USA.
Institute for Computational Biomedicine, Department of Physiology and Biophysics, Weill Cornell Medicine, New York, NY, USA.

Bryan J Venters (BJ)

EpiCypher, Durham, NC, USA.

Stephanie Portillo-Ledesma (S)

Department of Chemistry, New York University, New York, NY, USA.

Joseph Conway (J)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY, USA.

Jude M Phillip (JM)

Division of Hematology and Medical Oncology, Sanford I. Weill Department of Medicine, Weill Cornell Medicine, New York, NY, USA.

Olivier Elemento (O)

Department of Physiology and Biophysics, Weill Cornell Medicine, New York, NY, USA.

David W Scott (DW)

Centre for Lymphoid Cancer, BC Cancer, Vancouver, British Columbia, Canada.

Wendy Béguelin (W)

Division of Hematology and Medical Oncology, Sanford I. Weill Department of Medicine, Weill Cornell Medicine, New York, NY, USA.

Jonathan D Licht (JD)

University of Florida Health Cancer Center, The University of Florida Cancer and Genetics Research Complex, Gainesville, FL, USA.

Neil L Kelleher (NL)

Department of Chemistry, Northwestern University, Evanston, IL, USA.
Department of Molecular Biosciences, Northwestern University, Evanston, IL, USA.
Proteomics Center of Excellence, Northwestern University, Evanston, IL, USA.

Louis M Staudt (LM)

Lymphoid Malignancies Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Arthur I Skoultchi (AI)

Department of Cell Biology, Albert Einstein College of Medicine, New York, NY, USA.

Effie Apostolou (E)

Sanford I. Weill Department of Medicine, Weill Cornell Medicine, New York, NY, USA.
Sandra and Edward Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.

Christopher E Mason (CE)

Department of Physiology and Biophysics, Weill Cornell Medicine, New York, NY, USA.
The WorldQuant Initiative for Quantitative Prediction, Weill Cornell Medicine, New York, NY, USA.
The Feil Family Brain and Mind Research Institute, Weill Cornell Medicine, New York, NY, USA.

Marcin Imielinski (M)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY, USA.

Tamar Schlick (T)

Department of Chemistry, New York University, New York, NY, USA.
Courant Institute of Mathematical Sciences, New York University, New York, NY, USA.
New York University-East China Normal University Center for Computational Chemistry at New York University Shanghai, Shanghai, China.

Yael David (Y)

Chemical Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Tri-Institutional PhD Program in Chemical Biology, New York, NY, USA.

Aristotelis Tsirigos (A)

Department of Pathology, NYU School of Medicine, New York, NY, USA.
Institute for Computational Medicine, NYU School of Medicine, New York, NY, USA.

C David Allis (CD)

Laboratory of Chromatin Biology and Epigenetics, The Rockefeller University, New York, NY, USA.

Alexey A Soshnev (AA)

Laboratory of Chromatin Biology and Epigenetics, The Rockefeller University, New York, NY, USA. asoshnev@rockefeller.edu.

Ethel Cesarman (E)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY, USA. ecesarm@med.cornell.edu.

Ari M Melnick (AM)

Division of Hematology and Medical Oncology, Sanford I. Weill Department of Medicine, Weill Cornell Medicine, New York, NY, USA. amm2014@med.cornell.edu.

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