Bcl11b PiggyBac cancer evolution genetic screening genomics leukemia lymphoma mouse non-coding genome quasi-insufficiency

Journal

Cell genomics
ISSN: 2666-979X
Titre abrégé: Cell Genom
Pays: United States
ID NLM: 9918284260106676

Informations de publication

Date de publication:
08 Mar 2023
Historique:
received: 10 03 2022
revised: 05 09 2022
accepted: 08 02 2023
entrez: 23 3 2023
pubmed: 24 3 2023
medline: 24 3 2023
Statut: epublish

Résumé

In contrast to mono- or biallelic loss of tumor-suppressor function, effects of discrete gene dysregulations, as caused by non-coding (epi)genome alterations, are poorly understood. Here, by perturbing the regulatory genome in mice, we uncover pervasive roles of subtle gene expression variation in cancer evolution. Genome-wide screens characterizing 1,450 tumors revealed that such quasi-insufficiency is extensive across entities and displays diverse context dependencies, such as distinct cell-of-origin associations in T-ALL subtypes. We compile catalogs of non-coding regions linked to quasi-insufficiency, show their enrichment with human cancer risk variants, and provide functional insights by engineering regulatory alterations in mice. As such, kilo-/megabase deletions in a

Identifiants

pubmed: 36950387
doi: 10.1016/j.xgen.2023.100276
pii: S2666-979X(23)00036-8
pmc: PMC10025556
doi:

Types de publication

Journal Article

Langues

eng

Pagination

100276

Informations de copyright

© 2023 The Authors.

Déclaration de conflit d'intérêts

The authors declare no competing interests.

Références

Genome Biol. 2014;15(12):550
pubmed: 25516281
Nat Genet. 2017 Aug;49(8):1211-1218
pubmed: 28671688
Nature. 2020 Feb;578(7793):82-93
pubmed: 32025007
Proc Natl Acad Sci U S A. 1971 Apr;68(4):820-3
pubmed: 5279523
Nat Cell Biol. 2007 May;9(5):493-505
pubmed: 17450133
Blood. 2021 Feb 11;137(6):801-811
pubmed: 32812017
Sci Rep. 2019 Sep 20;9(1):13613
pubmed: 31541121
Nature. 2010 Nov 25;468(7323):572-5
pubmed: 21107428
PLoS Comput Biol. 2006 Dec 8;2(12):e166
pubmed: 17154714
Mol Cell. 2013 Aug 8;51(3):310-25
pubmed: 23932714
Nature. 1992 Mar 19;356(6366):215-21
pubmed: 1552940
Sci Rep. 2017 Mar 07;7:43345
pubmed: 28266526
Cell. 2016 May 19;165(5):1120-1133
pubmed: 27156451
Nature. 2013 Jul 11;499(7457):214-218
pubmed: 23770567
Blood. 2013 Aug 8;122(6):902-11
pubmed: 23741008
Cancer Cell. 2018 Feb 12;33(2):274-291.e8
pubmed: 29438697
Nat Genet. 2016 Dec;48(12):1481-1489
pubmed: 27776115
Nat Protoc. 2022 Sep;17(9):1903-1925
pubmed: 35840661
J Exp Med. 1997 Apr 21;185(8):1467-79
pubmed: 9126927
Blood. 2017 Jun 15;129(24):3264-3268
pubmed: 28408461
Oncogene. 2014 Jan 23;33(4):403-10
pubmed: 23435431
Nat Immunol. 2013 Jul;14(7):756-63
pubmed: 23708252
PLoS Comput Biol. 2013;9(8):e1003118
pubmed: 23950696
Nature. 2010 Nov 25;468(7323):567-71
pubmed: 21107427
Nat Commun. 2019 Sep 6;10(1):4059
pubmed: 31492853
Haematologica. 2014 Jan;99(1):94-102
pubmed: 23975177
Nat Commun. 2019 Mar 29;10(1):1415
pubmed: 30926791
Nature. 2011 Aug 10;476(7359):163-9
pubmed: 21833082
Nat Genet. 2015 Jan;47(1):47-56
pubmed: 25485836
Proc Natl Acad Sci U S A. 2006 Nov 28;103(48):18261-6
pubmed: 17114293
Genome Res. 2015 Apr;25(4):504-13
pubmed: 25677180
Cancer Res. 2007 Feb 15;67(4):1461-71
pubmed: 17308084
Cell. 2015 May 21;161(5):1202-1214
pubmed: 26000488
Nat Genet. 2007 May;39(5):593-5
pubmed: 17435759
Nat Cell Biol. 2018 Dec;20(12):1410-1420
pubmed: 30397315
Leuk Lymphoma. 2017 Dec;58(12):2895-2904
pubmed: 28482719
Mol Cell. 2017 Sep 21;67(6):1049-1058.e6
pubmed: 28938092
Hemasphere. 2018 May 11;2(3):e43
pubmed: 31723771
Cell. 2018 Apr 5;173(2):371-385.e18
pubmed: 29625053
Science. 2012 Dec 14;338(6113):1435-9
pubmed: 23239728
Mol Cell Biol. 2013 Apr;33(7):1317-30
pubmed: 23358416
Nat Rev Cancer. 2021 Aug;21(8):500-509
pubmed: 34230647
Nat Rev Genet. 2016 Feb;17(2):93-108
pubmed: 26781813
Blood. 2002 Jul 1;100(1):246-58
pubmed: 12070034
Nature. 1986 Oct 16-22;323(6089):643-6
pubmed: 2877398
J Pathol. 2011 Jan;223(2):137-46
pubmed: 21125671
Nat Genet. 2004 Aug;36(8):867-71
pubmed: 15235602
Nature. 1992 Sep 24;359(6393):288-94
pubmed: 1406932
Nat Commun. 2022 Jan 12;13(1):281
pubmed: 35022408
Cell. 2017 Sep 21;171(1):103-119.e18
pubmed: 28938112
Haematologica. 2012 Sep;97(9):1405-13
pubmed: 22491738
Blood. 2006 Dec 15;108(13):4198-201
pubmed: 16926283
Nature. 2005 Jul 14;436(7048):221-6
pubmed: 16015321
Cancer Cell. 2008 Dec 9;14(6):447-57
pubmed: 19061836
Bioinformatics. 2019 Jun 1;35(12):2084-2092
pubmed: 30395178
Nat Rev Cancer. 2020 Oct;20(10):573-593
pubmed: 32636489
EMBO J. 1998 Aug 17;17(16):4657-67
pubmed: 9707425
Leukemia. 2018 Jun;32(6):1358-1369
pubmed: 29740158
Nat Immunol. 2017 Apr;18(4):433-441
pubmed: 28250424
Nat Genet. 2014 Apr;46(4):364-70
pubmed: 24584072
Nat Commun. 2017 Feb 09;8:14385
pubmed: 28181482
Nat Genet. 2017 May;49(5):730-741
pubmed: 28319090
Nature. 2017 Dec 7;552(7683):121-125
pubmed: 29143824
Science. 2014 Aug 22;345(6199):943-9
pubmed: 25103404
Nature. 2014 Nov 20;515(7527):355-64
pubmed: 25409824
Science. 2016 Mar 25;351(6280):1454-1458
pubmed: 26940867
Cell. 2019 Feb 7;176(4):897-912.e20
pubmed: 30686579
Blood. 2012 May 10;119(19):4476-9
pubmed: 22438252
Nat Med. 2014 Oct;20(10):1130-7
pubmed: 25194570
Cancer Cell. 2013 Jul 8;24(1):15-29
pubmed: 23845441
Cell. 2011 Jan 21;144(2):296-309
pubmed: 21241896
Lancet Oncol. 2009 Feb;10(2):147-56
pubmed: 19147408
Nat Rev Cancer. 2016 Jul 25;16(8):494-507
pubmed: 27451956
Nat Genet. 2010 May;42(5):454-8
pubmed: 20400965
Nature. 2005 Jul 14;436(7048):272-6
pubmed: 16015333
Nucleic Acids Res. 2017 Nov 16;45(20):12054
pubmed: 29036333
Sci Rep. 2016 May 09;6:25533
pubmed: 27156886
Nucleic Acids Res. 2021 Feb 22;49(3):e15
pubmed: 33275159
Nature. 2009 Apr 9;458(7239):719-24
pubmed: 19360079
Mol Cancer. 2017 Aug 23;16(1):142
pubmed: 28830551
Nature. 2018 Oct;562(7728):526-531
pubmed: 30333627
Cell. 2017 Oct 5;171(2):481-494.e15
pubmed: 28985567
Cancer Discov. 2021 Dec 1;11(12):3158-3177
pubmed: 34282029
Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50
pubmed: 16199517
Blood. 2016 May 19;127(20):2391-405
pubmed: 27069254
Genes Dev. 2017 Dec 1;31(23-24):2343-2360
pubmed: 29326336
Sci Rep. 2017 Mar 02;7:43613
pubmed: 28252665
Mol Cell. 2010 May 28;38(4):576-89
pubmed: 20513432
Nat Methods. 2012 Feb 28;9(3):215-6
pubmed: 22373907
Cell. 2017 Feb 9;168(4):629-643
pubmed: 28187285
Immunity. 2018 Feb 20;48(2):227-242.e8
pubmed: 29466755
Science. 1999 Sep 24;285(5436):2122-5
pubmed: 10497129
Science. 2010 Nov 19;330(6007):1104-7
pubmed: 20947725
Immunity. 2011 Aug 26;35(2):299-311
pubmed: 21867929
Nucleic Acids Res. 2017 Jan 4;45(D1):D896-D901
pubmed: 27899670
Cell. 2022 Feb 3;185(3):563-575.e11
pubmed: 35120664
PLoS Genet. 2014 Apr 10;10(4):e1004250
pubmed: 24721906
Blood. 2009 Jul 16;114(3):647-50
pubmed: 19458356
Leuk Lymphoma. 2011 Feb;52(2):290-7
pubmed: 21261500
Blood. 2016 Apr 14;127(15):1863-9
pubmed: 26747249
Front Cell Neurosci. 2017 Mar 29;11:89
pubmed: 28424591
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W187-91
pubmed: 24799436
Nature. 2014 Jul 31;511(7511):616-20
pubmed: 25043025
Mol Ther. 2016 Mar;24(3):592-606
pubmed: 26755332
Nature. 2020 Feb;578(7793):102-111
pubmed: 32025015
Nat Genet. 2019 Dec;51(12):1664-1669
pubmed: 31784727
Nat Med. 2007 Oct;13(10):1203-10
pubmed: 17873882
Leukemia. 2017 Oct;31(10):2057-2064
pubmed: 28260788
Blood Cancer Discov. 2021 Jan;2(1):92-109
pubmed: 33458694
Nature. 2018 Feb 1;554(7690):62-68
pubmed: 29364867
Curr Opin Hematol. 2013 Jul;20(4):369-73
pubmed: 23695450
Bioinformatics. 2015 Nov 1;31(21):3555-7
pubmed: 26139635
Immunity. 2018 Feb 20;48(2):243-257.e10
pubmed: 29466756
Nat Protoc. 2017 Feb;12(2):289-309
pubmed: 28079877
Nucleic Acids Res. 2023 Feb 28;51(4):e21
pubmed: 36617985
Cancer Cell. 2011 Apr 12;19(4):484-97
pubmed: 21481790
Genome Res. 2010 May;20(5):623-35
pubmed: 20308636
Science. 2014 Dec 12;346(6215):1373-7
pubmed: 25394790
Nat Immunol. 2020 Sep;21(9):1010-1021
pubmed: 32661362
Nature. 2012 Jan 11;481(7380):157-63
pubmed: 22237106

Auteurs

Anja Fischer (A)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany.

Robert Lersch (R)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.

Niklas de Andrade Krätzig (N)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.

Alexander Strong (A)

The Wellcome Trust Sanger Institute, Genome Campus, Hinxton, Cambridge, UK.

Mathias J Friedrich (MJ)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.
Department of Medicine II, Klinikum rechts der Isar, School of Medicine, Technische Universität München, 81675 Munich, Germany.

Julia Weber (J)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.

Thomas Engleitner (T)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.

Rupert Öllinger (R)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.

Hsi-Yu Yen (HY)

German Cancer Consortium (DKTK), Heidelberg, Germany.
Comparative Experimental Pathology, School of Medicine, Technische Universität München, 81675 Munich, Germany.

Ursula Kohlhofer (U)

Institute of Pathology and Comprehensive Cancer Center, Eberhard Karls Universität Tübingen, 72076 Tübingen, Germany.

Irene Gonzalez-Menendez (I)

Institute of Pathology and Comprehensive Cancer Center, Eberhard Karls Universität Tübingen, 72076 Tübingen, Germany.

David Sailer (D)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.

Liz Kogan (L)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.

Mari Lahnalampi (M)

Institute of Biomedicine, School of Medicine, University of Eastern Finland, Kuopio, Finland.

Saara Laukkanen (S)

Faculty of Medicine and Health Technology, Tampere Center for Child, Adolescent and Maternal Health Research and Tays Cancer Center, Tampere University, Tampere, Finland.

Thorsten Kaltenbacher (T)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.

Christine Klement (C)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.

Majdaddin Rezaei (M)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.

Tim Ammon (T)

Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.
Institute of Experimental Hematology, TUM School of Medicine, Technical University of Munich, 81675 Munich, Germany.

Juan J Montero (JJ)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.

Günter Schneider (G)

Department of Medicine II, Klinikum rechts der Isar, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Department of General, Visceral and Pediatric Surgery, University Medical Center Göttingen, 37075 Göttingen, Germany.

Julia Mayerle (J)

Medical Department II, University Hospital, LMU Munich, Munich, Germany.

Mathias Heikenwälder (M)

German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.
Division of Chronic Inflammation and Cancer, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.

Marc Schmidt-Supprian (M)

Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany.
Institute of Experimental Hematology, TUM School of Medicine, Technical University of Munich, 81675 Munich, Germany.

Leticia Quintanilla-Martinez (L)

Institute of Pathology and Comprehensive Cancer Center, Eberhard Karls Universität Tübingen, 72076 Tübingen, Germany.

Katja Steiger (K)

German Cancer Consortium (DKTK), Heidelberg, Germany.
Comparative Experimental Pathology, School of Medicine, Technische Universität München, 81675 Munich, Germany.

Pentao Liu (P)

The Wellcome Trust Sanger Institute, Genome Campus, Hinxton, Cambridge, UK.
Li Ka Shing Faculty of Medicine, Stem Cell and Regenerative Medicine Consortium, School of Biomedical Sciences, University of Hong Kong, Hong Kong, China.

Juan Cadiñanos (J)

Instituto de Medicina Oncológica y Molecular de Asturias (IMOMA), 33193 Oviedo, Spain.

George S Vassiliou (GS)

The Wellcome Trust Sanger Institute, Genome Campus, Hinxton, Cambridge, UK.
Wellcome Trust-MRC Stem Cell Institute, Cambridge Biomedical Campus, University of Cambridge, Cambridge CB2 0XY, UK.
Department of Haematology, Cambridge University Hospitals NHS Trust, Cambridge CB2 0PT, UK.

Dieter Saur (D)

Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.
Department of Medicine II, Klinikum rechts der Isar, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Institute for Experimental Cancer Therapy, School of Medicine, Technische Universität München, 81675 Munich, Germany.

Olli Lohi (O)

Faculty of Medicine and Health Technology, Tampere Center for Child, Adolescent and Maternal Health Research and Tays Cancer Center, Tampere University, Tampere, Finland.

Merja Heinäniemi (M)

Institute of Biomedicine, School of Medicine, University of Eastern Finland, Kuopio, Finland.

Nathalie Conte (N)

The Wellcome Trust Sanger Institute, Genome Campus, Hinxton, Cambridge, UK.

Allan Bradley (A)

The Wellcome Trust Sanger Institute, Genome Campus, Hinxton, Cambridge, UK.
Cambridge Institute of Therapeutic Immunology & Infectious Disease (CITIID), University of Cambridge, Puddicombe Way, Cambridge CB2 0AW, UK.

Lena Rad (L)

Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.
Institute for Experimental Cancer Therapy, School of Medicine, Technische Universität München, 81675 Munich, Germany.

Roland Rad (R)

Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, 81675 Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technische Universität München, 81675 Munich, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany.
Department of Medicine II, Klinikum rechts der Isar, School of Medicine, Technische Universität München, 81675 Munich, Germany.

Classifications MeSH