Aging of preleukemic thymocytes drives CpG island hypermethylation in T-cell acute lymphoblastic leukemia.


Journal

Blood cancer discovery
ISSN: 2643-3249
Titre abrégé: Blood Cancer Discov
Pays: United States
ID NLM: 101764786

Informations de publication

Date de publication:
11 2020
Historique:
entrez: 12 11 2020
pubmed: 13 11 2020
medline: 13 11 2020
Statut: ppublish

Résumé

Cancer cells display DNA hypermethylation at specific CpG islands in comparison to their normal healthy counterparts, but the mechanism that drives this so-called CpG island methylator phenotype (CIMP) remains poorly understood. Here, we show that CpG island methylation in human T-cell acute lymphoblastic leukemia (T-ALL) mainly occurs at promoters of Polycomb Repressor Complex 2 (PRC2) target genes that are not expressed in normal or malignant T-cells and which display a reciprocal association with H3K27me3 binding. In addition, we revealed that this aberrant methylation profile reflects the epigenetic history of T-ALL and is established already in pre-leukemic, self-renewing thymocytes that precede T-ALL development. Finally, we unexpectedly uncover that this age-related CpG island hypermethylation signature in T-ALL is completely resistant to the FDA-approved hypomethylating agent Decitabine. Altogether, we here provide conceptual evidence for the involvement of a pre-leukemic phase characterized by self-renewing thymocytes in the pathogenesis of human T-ALL.

Identifiants

pubmed: 33179015
doi: 10.1158/2643-3230.BCD-20-0059
pmc: PMC7116343
mid: EMS102743
pii: 2643-3230.BCD-20-0059
doi:

Types de publication

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

Langues

eng

Pagination

274-289

Subventions

Organisme : Blood Cancer UK
ID : 17002
Pays : United Kingdom
Organisme : European Research Council
ID : 639784
Pays : International
Organisme : BLRD VA
ID : I01 BX001799
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA207530
Pays : United States

Déclaration de conflit d'intérêts

Conflicts of Interest The authors declare no potential conflicts of interest.

Références

Sci Rep. 2017 Mar 07;7:43345
pubmed: 28266526
BMC Bioinformatics. 2013 Apr 15;14:128
pubmed: 23586463
Nat Commun. 2020 Jan 21;11(1):402
pubmed: 31964861
Leukemia. 2020 Apr;34(4):1163-1168
pubmed: 31732719
Nat Methods. 2015 Oct;12(10):963-965
pubmed: 26280331
Genome Biol. 2013;14(10):R115
pubmed: 24138928
Nat Rev Cancer. 2004 Dec;4(12):988-93
pubmed: 15573120
EMBO Mol Med. 2018 Dec;10(12):
pubmed: 30389682
Methods Mol Biol. 2013;1067:105-24
pubmed: 23975789
Onco Targets Ther. 2019 Aug 29;12:7039-7044
pubmed: 31507324
Haematologica. 2018 Dec;103(12):e585-e589
pubmed: 29954933
Cell Metab. 2017 Apr 4;25(4):954-960.e6
pubmed: 28380383
Nat Protoc. 2009;4(1):44-57
pubmed: 19131956
EMBO Rep. 2020 May 6;21(5):e49006
pubmed: 32255245
Genome Biol. 2016 Oct 3;17(1):205
pubmed: 27716309
Cell Rep. 2016 Mar 1;14(8):1953-65
pubmed: 26904942
Cell Stem Cell. 2013 Apr 4;12(4):413-25
pubmed: 23415915
Cancer Med. 2019 Jan;8(1):311-324
pubmed: 30575306
Genome Biol. 2014;15(12):550
pubmed: 25516281
Nat Immunol. 2020 Oct;21(10):1280-1292
pubmed: 32719521
Mol Cell. 2017 Jun 1;66(5):711-720.e3
pubmed: 28529057
Br J Haematol. 2014 Nov;167(3):356-65
pubmed: 25066676
Bone Marrow Transplant. 2017 Nov;52(11):1583-1584
pubmed: 28892087
J Clin Invest. 2012 Oct;122(10):3398-406
pubmed: 23023710
PLoS One. 2013 Jun 06;8(6):e65373
pubmed: 23762353
Oncotarget. 2017 Aug 10;8(44):76898-76920
pubmed: 29100357
Nat Genet. 2017 Aug;49(8):1211-1218
pubmed: 28671688
Nature. 2014 Nov 20;515(7527):402-5
pubmed: 25409831
Nucleic Acids Res. 2019 Jul 26;47(13):6699-6713
pubmed: 31127282
Int J Hematol. 2019 Aug;110(2):161-169
pubmed: 31020568
EMBO Rep. 2018 Dec;19(12):
pubmed: 30413482
Nat Rev Mol Cell Biol. 2019 Oct;20(10):573-589
pubmed: 31270442
Am J Hematol. 2019 Nov;94(11):E307-E310
pubmed: 31432528
Nat Commun. 2019 Dec 11;10(1):5649
pubmed: 31827082
Nature. 2006 Feb 16;439(7078):871-4
pubmed: 16357870
Am J Hematol. 2019 Apr;94(4):E93-E96
pubmed: 30614545
Nat Genet. 2003 Jul;34(3):267-73
pubmed: 12808457
Cancer Cell. 2002 Feb;1(1):75-87
pubmed: 12086890
BMC Genomics. 2018 May 23;19(1):390
pubmed: 29792182
Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50
pubmed: 16199517
Haematologica. 2020 Jun;105(6):1575-1581
pubmed: 31537687
Pediatr Blood Cancer. 2016 Jul;63(7):1185-92
pubmed: 26928953
PLoS One. 2014 Jan 21;9(1):e85883
pubmed: 24465765
Nucleic Acids Res. 2009 Jan;37(1):1-13
pubmed: 19033363
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
Haematologica. 2020 Jan 9;:
pubmed: 31919081
Curr Top Microbiol Immunol. 2012;360:75-97
pubmed: 22692833
J Huazhong Univ Sci Technolog Med Sci. 2017 Oct;37(5):693-698
pubmed: 29058281
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W187-91
pubmed: 24799436
Cell Cycle. 2011 Aug 1;10(15):2428-36
pubmed: 21750410
Nat Methods. 2014 Nov;11(11):1138-1140
pubmed: 25262207
Nucleic Acids Res. 2016 Jul 8;44(W1):W90-7
pubmed: 27141961
Case Rep Hematol. 2018 Aug 26;2018:6092646
pubmed: 30225152
J Clin Invest. 2018 Aug 31;128(9):3872-3886
pubmed: 30080177
Hematol Oncol Stem Cell Ther. 2020 Mar 19;:
pubmed: 32199933
Bioinformatics. 2011 Jun 1;27(11):1571-2
pubmed: 21493656
Mol Med Rep. 2016 Mar;13(3):2777-84
pubmed: 26861642
Proc Natl Acad Sci U S A. 2014 Nov 18;111(46):E4946-53
pubmed: 25369933
Cell Syst. 2019 Oct 23;9(4):321-337.e9
pubmed: 31629685
Genome Res. 2014 Aug;24(8):1285-95
pubmed: 24812327
Dev Cell. 2016 Jan 11;36(1):9-23
pubmed: 26766440
Cancer Cell. 2011 Apr 12;19(4):484-97
pubmed: 21481790
Genome Biol. 2016 Mar 31;17:61
pubmed: 27036880
Nucleic Acids Res. 2017 Feb 28;45(4):e22
pubmed: 27924034
Nature. 2012 Jan 11;481(7380):157-63
pubmed: 22237106

Auteurs

Juliette Roels (J)

Department of Biomolecular Medicine, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent (CRIG), Ghent, Belgium.

Morgan Thénoz (M)

Department of Biomolecular Medicine, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent (CRIG), Ghent, Belgium.

Bronisława Szarzyńska (B)

Institute of Human Genetics, Polish Academy of Sciences, Poznań, Poland.

Mattias Landfors (M)

Department of Medical Biosciences, Umeå University, Umeå, Sweden.

Stien De Coninck (S)

Department of Biomolecular Medicine, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent (CRIG), Ghent, Belgium.

Lisa Demoen (L)

Department of Biomolecular Medicine, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent (CRIG), Ghent, Belgium.

Lien Provez (L)

Department of Biomolecular Medicine, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent (CRIG), Ghent, Belgium.

Anna Kuchmiy (A)

Cancer Research Institute Ghent (CRIG), Ghent, Belgium.
Department of Diagnostic Sciences, Ghent University, Ghent, Belgium.

Steven Strubbe (S)

Department of Diagnostic Sciences, Ghent University, Ghent, Belgium.

Lindy Reunes (L)

Department of Biomolecular Medicine, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent (CRIG), Ghent, Belgium.

Tim Pieters (T)

Department of Biomolecular Medicine, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent (CRIG), Ghent, Belgium.

Filip Matthijssens (F)

Department of Biomolecular Medicine, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent (CRIG), Ghent, Belgium.

Wouter Van Loocke (W)

Department of Biomolecular Medicine, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent (CRIG), Ghent, Belgium.

Büşra Erarslan-Uysal (B)

Department of Pediatric Oncology, Hematology, and Immunology, University of Heidelberg, and Hopp Children's Cancer Center at NCT Heidelberg, Heidelberg, Germany.
Molecular Medicine Partnership Unit (MMPU), European Molecular Biology Laboratory (EMBL), University of Heidelberg, Heidelberg, Germany.

Paulina Richter-Pechańska (P)

Department of Pediatric Oncology, Hematology, and Immunology, University of Heidelberg, and Hopp Children's Cancer Center at NCT Heidelberg, Heidelberg, Germany.
Molecular Medicine Partnership Unit (MMPU), European Molecular Biology Laboratory (EMBL), University of Heidelberg, Heidelberg, Germany.

Ken Declerck (K)

Laboratory of Protein Chemistry, Proteomics and Epigenetic Signaling (PPES) and Integrated Personalized and Precision Oncology Network (IPPON), Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.

Tim Lammens (T)

Cancer Research Institute Ghent (CRIG), Ghent, Belgium.
Department of Pediatric Hematology-Oncology and Stem Cell Transplantation, Ghent University Hospital, Ghent, Belgium.

Barbara De Moerloose (B)

Cancer Research Institute Ghent (CRIG), Ghent, Belgium.
Department of Pediatric Hematology-Oncology and Stem Cell Transplantation, Ghent University Hospital, Ghent, Belgium.

Dieter Deforce (D)

Laboratory of Pharmaceutical Biotechnology, Ghent University, Ghent, Belgium.

Filip Van Nieuwerburgh (F)

Laboratory of Pharmaceutical Biotechnology, Ghent University, Ghent, Belgium.

Laurence C Cheung (LC)

Telethon Kids Cancer Centre, Telethon Kids Institute, University of Western Australia, Perth, Western Australia.
School of Pharmacy and Biomedical Sciences, Curtin University, Perth, Western Australia.

Rishi S Kotecha (RS)

Telethon Kids Cancer Centre, Telethon Kids Institute, University of Western Australia, Perth, Western Australia.
School of Pharmacy and Biomedical Sciences, Curtin University, Perth, Western Australia.

Marc R Mansour (MR)

Department of Haematology, University College London Cancer Institute, London, England.

Bart Ghesquière (B)

Metabolomics Expertise Center, VIB Center for Cancer Biology, Leuven, Belgium.

Guy Van Camp (G)

Center of Medical Genetics, University of Antwerp, Antwerp, Belgium.

Wim Vanden Berghe (WV)

Laboratory of Protein Chemistry, Proteomics and Epigenetic Signaling (PPES) and Integrated Personalized and Precision Oncology Network (IPPON), Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.

Jerzy R Kowalczyk (JR)

Department of Pediatric Hematology, Oncology and Transplantology, Medical University of Lublin, Lublin, Poland.

Tomasz Szczepański (T)

Department of Pediatric Hematology and Oncology, Zabrze, Medical University of Silesia, Katowice, Poland.

Utpal P Davé (UP)

Roudebush Veterans Affairs Medical Center and Indiana University School of Medicine, Indianapolis, Indiana.

Andreas E Kulozik (AE)

Department of Pediatric Oncology, Hematology, and Immunology, University of Heidelberg, and Hopp Children's Cancer Center at NCT Heidelberg, Heidelberg, Germany.
Molecular Medicine Partnership Unit (MMPU), European Molecular Biology Laboratory (EMBL), University of Heidelberg, Heidelberg, Germany.

Steven Goossens (S)

Department of Biomolecular Medicine, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent (CRIG), Ghent, Belgium.
Department of Diagnostic Sciences, Ghent University, Ghent, Belgium.

David J Curtis (DJ)

Australian Centre for Blood Diseases (ACBD), Monash University, Melbourne, Australia.

Tom Taghon (T)

Department of Diagnostic Sciences, Ghent University, Ghent, Belgium.

Małgorzata Dawidowska (M)

Institute of Human Genetics, Polish Academy of Sciences, Poznań, Poland.

Sofie Degerman (S)

Department of Medical Biosciences, Umeå University, Umeå, Sweden.
Department of Clinical Microbiology, Umeå University, Umeå, Sweden.

Pieter Van Vlierberghe (P)

Department of Biomolecular Medicine, Ghent University, Ghent, Belgium. pieter.vanvlierberghe@ugent.be.
Cancer Research Institute Ghent (CRIG), Ghent, Belgium.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH