Loss of phosphatase CTDNEP1 potentiates aggressive medulloblastoma by triggering MYC amplification and genomic instability.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
10 02 2023
Historique:
received: 26 04 2022
accepted: 30 01 2023
pubmed: 11 2 2023
medline: 15 2 2023
entrez: 10 2 2023
Statut: epublish

Résumé

MYC-driven medulloblastomas are highly aggressive childhood brain tumors, however, the molecular and genetic events triggering MYC amplification and malignant transformation remain elusive. Here we report that mutations in CTDNEP1, a CTD nuclear-envelope-phosphatase, are the most significantly enriched recurrent alterations in MYC-driven medulloblastomas, and define high-risk subsets with poorer prognosis. Ctdnep1 ablation promotes the transformation of murine cerebellar progenitors into Myc-amplified medulloblastomas, resembling their human counterparts. CTDNEP1 deficiency stabilizes and activates MYC activity by elevating MYC serine-62 phosphorylation, and triggers chromosomal instability to induce p53 loss and Myc amplifications. Further, phosphoproteomics reveals that CTDNEP1 post-translationally modulates the activities of key regulators for chromosome segregation and mitotic checkpoint regulators including topoisomerase TOP2A and checkpoint kinase CHEK1. Co-targeting MYC and CHEK1 activities synergistically inhibits CTDNEP1-deficient MYC-amplified tumor growth and prolongs animal survival. Together, our studies demonstrate that CTDNEP1 is a tumor suppressor in highly aggressive MYC-driven medulloblastomas by controlling MYC activity and mitotic fidelity, pointing to a CTDNEP1-dependent targetable therapeutic vulnerability.

Identifiants

pubmed: 36765089
doi: 10.1038/s41467-023-36400-8
pii: 10.1038/s41467-023-36400-8
pmc: PMC9918503
doi:

Substances chimiques

Phosphoric Monoester Hydrolases EC 3.1.3.2
Proto-Oncogene Proteins c-myc 0
CTDNEP1 protein, human EC 3.1.3.16
Phosphoprotein Phosphatases EC 3.1.3.16

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

762

Subventions

Organisme : NCI NIH HHS
ID : P01 CA096832
Pays : United States
Organisme : NCI NIH HHS
ID : T32 CA117846
Pays : United States

Informations de copyright

© 2023. The Author(s).

Références

Cold Spring Harb Perspect Med. 2013 Nov 01;3(11):
pubmed: 24186490
Cold Spring Harb Perspect Med. 2014 Apr 01;4(4):a014373
pubmed: 24692190
Cell Rep. 2013 May 30;3(5):1339-45
pubmed: 23665218
Biochem Biophys Res Commun. 2002 Jul 5;295(1):85-91
pubmed: 12083771
Int J Proteomics. 2013;2013:756039
pubmed: 23401775
Oncotarget. 2017 Jul 27;8(39):64685-64697
pubmed: 29029386
Genes Dev. 2021 Aug 1;35(15-16):1093-1108
pubmed: 34266887
Proc Natl Acad Sci U S A. 2007 Apr 17;104(16):6596-601
pubmed: 17420445
Cancer Cell. 2017 Jun 12;31(6):737-754.e6
pubmed: 28609654
Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2147-52
pubmed: 10051609
Proc Natl Acad Sci U S A. 2011 Jan 11;108(2):632-7
pubmed: 21187408
Int J Biochem Cell Biol. 2013 Mar;45(3):711-23
pubmed: 23247197
Genes Dev. 2018 Nov 1;32(21-22):1398-1419
pubmed: 30366908
Cancer Cell. 2012 Feb 14;21(2):155-67
pubmed: 22340590
Cold Spring Harb Perspect Med. 2014 Oct 01;4(10):
pubmed: 25274755
Genes Cancer. 2011 Apr;2(4):466-74
pubmed: 21779514
Clin Cancer Res. 2018 Jul 15;24(14):3263-3272
pubmed: 29643063
Autophagy. 2021 Mar;17(3):796-813
pubmed: 32573315
Nat Genet. 2019 Dec;51(12):1723-1731
pubmed: 31784729
Annu Rev Genet. 2014;48:215-36
pubmed: 25292359
Cancer Cell. 2015 Jul 13;28(1):129-40
pubmed: 26175417
Dev Cell. 2021 Dec 20;56(24):3364-3379.e10
pubmed: 34852214
Dev Cell. 2006 Dec;11(6):763-74
pubmed: 17141153
Oncogene. 2015 Jul 30;34(31):4019-31
pubmed: 25328138
Cancer Chemother Pharmacol. 2020 Jan;85(1):9-20
pubmed: 31512029
Nat Rev Mol Cell Biol. 2002 Jun;3(6):430-40
pubmed: 12042765
Nat Commun. 2017 Mar 28;8:14864
pubmed: 28348404
Oncotarget. 2013 Nov;4(11):2080-95
pubmed: 24231268
Oncotarget. 2016 Aug 16;7(33):53881-53894
pubmed: 27449089
Neuro Oncol. 2021 Feb 25;23(2):226-239
pubmed: 32822486
Eur J Pharm Sci. 2020 Jan 15;142:105106
pubmed: 31669383
Cancer Cell. 2018 Mar 12;33(3):435-449.e6
pubmed: 29533784
Proc Natl Acad Sci U S A. 2019 Jun 25;116(26):12986-12995
pubmed: 31182587
Cancer Cell. 2019 Sep 16;36(3):302-318.e7
pubmed: 31474569
Nature. 2016 Jan 21;529(7586):351-7
pubmed: 26760213
Mol Cell. 2016 Oct 6;64(1):25-36
pubmed: 27642049
Nature. 2017 Jul 19;547(7663):311-317
pubmed: 28726821
Cell Rep. 2015 Aug 11;12(6):1019-31
pubmed: 26235622
Nature. 1998 Nov 12;396(6707):177-80
pubmed: 9823898
J Bone Miner Res. 2015 May;30(5):947
pubmed: 25879424
Cell Rep. 2020 Mar 10;30(10):3368-3382.e7
pubmed: 32160543
Nature. 2012 Aug 2;488(7409):100-5
pubmed: 22832583
Mol Oncol. 2017 Aug;11(8):945-964
pubmed: 28383788
Ann N Y Acad Sci. 2005 Nov;1059:145-59
pubmed: 16382050
Cold Spring Harb Perspect Med. 2016 Jun 01;6(6):
pubmed: 27252396
J Cell Biochem. 2012 Feb;113(2):433-9
pubmed: 22006292
Mol Biol Rep. 2019 Feb;46(1):1487-1497
pubmed: 30535769
Acta Neuropathol. 2012 Apr;123(4):473-84
pubmed: 22358457
Mol Cell Biol. 2007 Apr;27(7):2572-81
pubmed: 17242188
Oncotarget. 2016 Oct 11;7(41):66809-66821
pubmed: 27572308
Curr Protoc Mol Biol. 2015 Jan 05;109:21.29.1-21.29.9
pubmed: 25559105
J Neuropathol Exp Neurol. 2003 Jun;62(6):627-32
pubmed: 12834107
Lancet Oncol. 2018 Feb;19(2):207-215
pubmed: 29361470
Cell Cycle. 2009 May 1;8(9):1303
pubmed: 19342882
Nature. 2012 Aug 2;488(7409):43-8
pubmed: 22722829
Genes (Basel). 2017 Jun 07;8(6):
pubmed: 28590415
N Engl J Med. 1984 Mar 1;310(9):550-3
pubmed: 6694706
Acta Neuropathol. 2012 Apr;123(4):465-72
pubmed: 22134537
Proc Natl Acad Sci U S A. 2022 Jan 25;119(4):
pubmed: 35042798
Cancer Res. 2019 Apr 15;79(8):1967-1980
pubmed: 30862721
Nat Rev Mol Cell Biol. 2005 Aug;6(8):635-45
pubmed: 16064138
Nat Genet. 1999 Sep;23(1):99-103
pubmed: 10471508
Front Cell Dev Biol. 2021 Feb 18;9:634056
pubmed: 33681213
Cancer Cell. 2016 May 9;29(5):669-683
pubmed: 27165742
Nat Neurosci. 2005 Jun;8(6):723-9
pubmed: 15908947
Cancer Cell. 2018 Sep 10;34(3):396-410.e8
pubmed: 30205044
Cancer Cell. 2003 May;3(5):421-9
pubmed: 12781359
Mol Cell Biol. 1985 Jan;5(1):114-26
pubmed: 3872410
Pharmacol Res Perspect. 2015 Jun;3(3):e00149
pubmed: 26171228
J Cell Biol. 2019 Nov 4;218(11):3597-3611
pubmed: 31537708
Nature. 2014 Jul 24;511(7510):428-34
pubmed: 25043047
J Biotechnol. 2016 Oct 20;236:10-25
pubmed: 27498314
Cell. 2020 Mar 19;180(6):1212-1227.e14
pubmed: 32169215
Nature. 2019 Aug;572(7767):74-79
pubmed: 31341285
Cold Spring Harb Perspect Med. 2014 Jun 02;4(6):
pubmed: 24890833
Cancer Cell. 2012 Feb 14;21(2):168-80
pubmed: 22340591
Clin Cancer Res. 2014 Feb 15;20(4):912-25
pubmed: 24297863
Cell Div. 2012 Feb 28;7(1):6
pubmed: 22373487
Nature. 2012 Aug 2;488(7409):106-10
pubmed: 22820256
Nature. 2004 Nov 18;432(7015):338-41
pubmed: 15549096
Cell Rep. 2017 Mar 21;18(12):2907-2917
pubmed: 28329683
Nat Med. 2014 Sep;20(9):1035-42
pubmed: 25150496
Am J Cancer Res. 2017 Mar 01;7(3):473-483
pubmed: 28401005
Cancer Discov. 2014 Nov;4(11):1281-9
pubmed: 25107667
Dev Cell. 2019 Jan 28;48(2):167-183.e5
pubmed: 30554998
Nature. 2007 Aug 16;448(7155):811-5
pubmed: 17700700
Proc Natl Acad Sci U S A. 1983 May;80(10):2926-30
pubmed: 6574461
Nat Rev Clin Oncol. 2016 May;13(5):291-304
pubmed: 26598944
Sci Signal. 2017 Mar 14;10(470):
pubmed: 28292958
Cell Death Differ. 2014 Jun;21(6):956-66
pubmed: 24583641
Nat Commun. 2013;4:1398
pubmed: 23360989
Nature. 2012 Aug 2;488(7409):49-56
pubmed: 22832581
Sci Rep. 2018 Jun 18;8(1):9272
pubmed: 29915179

Auteurs

Zaili Luo (Z)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Dazhuan Xin (D)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Yunfei Liao (Y)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Kalen Berry (K)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Sean Ogurek (S)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Feng Zhang (F)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Liguo Zhang (L)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Chuntao Zhao (C)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Rohit Rao (R)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Xinran Dong (X)

Key Laboratory of Birth Defects, Children's Hospital, Fudan University and Institutes of Biomedical Sciences, Fudan University, Shanghai, 201102, China.

Hao Li (H)

Key Laboratory of Birth Defects, Children's Hospital, Fudan University and Institutes of Biomedical Sciences, Fudan University, Shanghai, 201102, China.

Jianzhong Yu (J)

Key Laboratory of Birth Defects, Children's Hospital, Fudan University and Institutes of Biomedical Sciences, Fudan University, Shanghai, 201102, China.

Yifeng Lin (Y)

Key Laboratory of Birth Defects, Children's Hospital, Fudan University and Institutes of Biomedical Sciences, Fudan University, Shanghai, 201102, China.

Guoying Huang (G)

Key Laboratory of Birth Defects, Children's Hospital, Fudan University and Institutes of Biomedical Sciences, Fudan University, Shanghai, 201102, China.

Lingli Xu (L)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Mei Xin (M)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Ryuichi Nishinakamura (R)

Institute of Molecular Embryology and Genetics, Kumamoto University, Kumamoto, Japan.

Jiyang Yu (J)

Department of Computational Biology, St. Jude Children's Research Hospital, Memphis, TN, 38105, USA.

Marcel Kool (M)

Hopp Children's Cancer Center Heidelberg (KiTZ); Division of Pediatric Neurooncology, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), 69120, Heidelberg, Germany.
Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands.

Stefan M Pfister (SM)

Hopp Children's Cancer Center Heidelberg (KiTZ); Division of Pediatric Neurooncology, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), 69120, Heidelberg, Germany.
Department of Pediatric Hematology and Oncology, Heidelberg University Hospital, 69120, Heidelberg, Germany.

Martine F Roussel (MF)

Department of Tumor Cell Biology, St. Jude Children's Research Hospital, Memphis, TN, 38105, USA.

Wenhao Zhou (W)

Key Laboratory of Birth Defects, Children's Hospital, Fudan University and Institutes of Biomedical Sciences, Fudan University, Shanghai, 201102, China. zhouwenhao@fudan.edu.cn.

William A Weiss (WA)

Department of Neurology, Pediatrics, and Surgery, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, 94143, USA.

Paul Andreassen (P)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.
Department of Pediatrics, University of Cincinnati, College of Medicine, Cincinnati, OH, 45229, USA.

Q Richard Lu (QR)

Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA. richard.lu@cchmc.org.
Department of Pediatrics, University of Cincinnati, College of Medicine, Cincinnati, OH, 45229, USA. richard.lu@cchmc.org.

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