Integrative network analysis reveals USP7 haploinsufficiency inhibits E-protein activity in pediatric T-lineage acute lymphoblastic leukemia (T-ALL)

USP7, which encodes a deubiquitylating enzyme, is among the most frequently mutated genes in pediatric T-ALL, with somatic heterozygous loss-of-function mutations (haploinsufficiency) predominantly affecting the subgroup that has aberrant TAL1 oncogene activation. Network analysis of > 200 T-ALL...

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Published inScientific reports Vol. 11; no. 1; pp. 5154 - 12
Main Authors Shaw, Timothy I., Dong, Li, Tian, Liqing, Qian, Chenxi, Liu, Yu, Ju, Bensheng, High, Anthony, Kavdia, Kanisha, Pagala, Vishwajeeth R., Shaner, Bridget, Pei, Deqing, Easton, John, Janke, Laura J., Porter, Shaina N., Ma, Xiaotu, Cheng, Cheng, Pruett-Miller, Shondra M., Choi, John, Yu, Jiyang, Peng, Junmin, Gu, Wei, Look, A. Thomas, Downing, James R., Zhang, Jinghui
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 04.03.2021
Nature Publishing Group
Nature Portfolio
Subjects
631/114
631/114/2114
631/67/1990/283/2125
Acute lymphoblastic leukemia
Cell Line, Tumor
Cell Lineage - genetics
Cell Proliferation - genetics
CRISPR
CRISPR-Cas Systems - genetics
Dosage
Drug development
Gene Expression Regulation, Leukemic - genetics
Gene regulation
Haploinsufficiency
Haploinsufficiency - genetics
Humanities and Social Sciences
Humans
Leukemia
Lymphatic leukemia
Lymphocytes T
Mass spectrometry
Mass spectroscopy
multidisciplinary
Oncogenes - genetics
Pediatrics
Precursor T-Cell Lymphoblastic Leukemia-Lymphoma - genetics
Precursor T-Cell Lymphoblastic Leukemia-Lymphoma - pathology
Proteins
Science
Science (multidisciplinary)
Synergistic effect
T-Cell Acute Lymphocytic Leukemia Protein 1 - genetics
Transcription
Transcriptional Activation - genetics
Tumor suppressor genes
Ubiquitin-Specific Peptidase 7 - genetics
Online AccessGet full text
ISSN2045-2322
2045-2322
DOI10.1038/s41598-021-84647-2

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Abstract USP7, which encodes a deubiquitylating enzyme, is among the most frequently mutated genes in pediatric T-ALL, with somatic heterozygous loss-of-function mutations (haploinsufficiency) predominantly affecting the subgroup that has aberrant TAL1 oncogene activation. Network analysis of > 200 T-ALL transcriptomes linked USP7 haploinsufficiency with decreased activities of E-proteins. E-proteins are also negatively regulated by TAL1, leading to concerted down-regulation of E-protein target genes involved in T-cell development. In T-ALL cell lines, we showed the physical interaction of USP7 with E-proteins and TAL1 by mass spectrometry and ChIP-seq. Haploinsufficient but not complete CRISPR knock-out of USP7 showed accelerated cell growth and validated transcriptional down-regulation of E-protein targets. Our study unveiled the synergistic effect of USP7 haploinsufficiency with aberrant TAL1 activation on T-ALL, implicating USP7 as a haploinsufficient tumor suppressor in T-ALL. Our findings caution against a universal oncogene designation for USP7 while emphasizing the dosage-dependent consequences of USP7 inhibitors currently under development as potential cancer therapeutics.
AbstractList USP7, which encodes a deubiquitylating enzyme, is among the most frequently mutated genes in pediatric T-ALL, with somatic heterozygous loss-of-function mutations (haploinsufficiency) predominantly affecting the subgroup that has aberrant TAL1 oncogene activation. Network analysis of > 200 T-ALL transcriptomes linked USP7 haploinsufficiency with decreased activities of E-proteins. E-proteins are also negatively regulated by TAL1, leading to concerted down-regulation of E-protein target genes involved in T-cell development. In T-ALL cell lines, we showed the physical interaction of USP7 with E-proteins and TAL1 by mass spectrometry and ChIP-seq. Haploinsufficient but not complete CRISPR knock-out of USP7 showed accelerated cell growth and validated transcriptional down-regulation of E-protein targets. Our study unveiled the synergistic effect of USP7 haploinsufficiency with aberrant TAL1 activation on T-ALL, implicating USP7 as a haploinsufficient tumor suppressor in T-ALL. Our findings caution against a universal oncogene designation for USP7 while emphasizing the dosage-dependent consequences of USP7 inhibitors currently under development as potential cancer therapeutics.
USP7, which encodes a deubiquitylating enzyme, is among the most frequently mutated genes in pediatric T-ALL, with somatic heterozygous loss-of-function mutations (haploinsufficiency) predominantly affecting the subgroup that has aberrant TAL1 oncogene activation. Network analysis of > 200 T-ALL transcriptomes linked USP7 haploinsufficiency with decreased activities of E-proteins. E-proteins are also negatively regulated by TAL1, leading to concerted down-regulation of E-protein target genes involved in T-cell development. In T-ALL cell lines, we showed the physical interaction of USP7 with E-proteins and TAL1 by mass spectrometry and ChIP-seq. Haploinsufficient but not complete CRISPR knock-out of USP7 showed accelerated cell growth and validated transcriptional down-regulation of E-protein targets. Our study unveiled the synergistic effect of USP7 haploinsufficiency with aberrant TAL1 activation on T-ALL, implicating USP7 as a haploinsufficient tumor suppressor in T-ALL. Our findings caution against a universal oncogene designation for USP7 while emphasizing the dosage-dependent consequences of USP7 inhibitors currently under development as potential cancer therapeutics.
USP7, which encodes a deubiquitylating enzyme, is among the most frequently mutated genes in pediatric T-ALL, with somatic heterozygous loss-of-function mutations (haploinsufficiency) predominantly affecting the subgroup that has aberrant TAL1 oncogene activation. Network analysis of > 200 T-ALL transcriptomes linked USP7 haploinsufficiency with decreased activities of E-proteins. E-proteins are also negatively regulated by TAL1, leading to concerted down-regulation of E-protein target genes involved in T-cell development. In T-ALL cell lines, we showed the physical interaction of USP7 with E-proteins and TAL1 by mass spectrometry and ChIP-seq. Haploinsufficient but not complete CRISPR knock-out of USP7 showed accelerated cell growth and validated transcriptional down-regulation of E-protein targets. Our study unveiled the synergistic effect of USP7 haploinsufficiency with aberrant TAL1 activation on T-ALL, implicating USP7 as a haploinsufficient tumor suppressor in T-ALL. Our findings caution against a universal oncogene designation for USP7 while emphasizing the dosage-dependent consequences of USP7 inhibitors currently under development as potential cancer therapeutics.
Abstract USP7, which encodes a deubiquitylating enzyme, is among the most frequently mutated genes in pediatric T-ALL, with somatic heterozygous loss-of-function mutations (haploinsufficiency) predominantly affecting the subgroup that has aberrant TAL1 oncogene activation. Network analysis of > 200 T-ALL transcriptomes linked USP7 haploinsufficiency with decreased activities of E-proteins. E-proteins are also negatively regulated by TAL1, leading to concerted down-regulation of E-protein target genes involved in T-cell development. In T-ALL cell lines, we showed the physical interaction of USP7 with E-proteins and TAL1 by mass spectrometry and ChIP-seq. Haploinsufficient but not complete CRISPR knock-out of USP7 showed accelerated cell growth and validated transcriptional down-regulation of E-protein targets. Our study unveiled the synergistic effect of USP7 haploinsufficiency with aberrant TAL1 activation on T-ALL, implicating USP7 as a haploinsufficient tumor suppressor in T-ALL. Our findings caution against a universal oncogene designation for USP7 while emphasizing the dosage-dependent consequences of USP7 inhibitors currently under development as potential cancer therapeutics.
USP7, which encodes a deubiquitylating enzyme, is among the most frequently mutated genes in pediatric T-ALL, with somatic heterozygous loss-of-function mutations (haploinsufficiency) predominantly affecting the subgroup that has aberrant TAL1 oncogene activation. Network analysis of > 200 T-ALL transcriptomes linked USP7 haploinsufficiency with decreased activities of E-proteins. E-proteins are also negatively regulated by TAL1, leading to concerted down-regulation of E-protein target genes involved in T-cell development. In T-ALL cell lines, we showed the physical interaction of USP7 with E-proteins and TAL1 by mass spectrometry and ChIP-seq. Haploinsufficient but not complete CRISPR knock-out of USP7 showed accelerated cell growth and validated transcriptional down-regulation of E-protein targets. Our study unveiled the synergistic effect of USP7 haploinsufficiency with aberrant TAL1 activation on T-ALL, implicating USP7 as a haploinsufficient tumor suppressor in T-ALL. Our findings caution against a universal oncogene designation for USP7 while emphasizing the dosage-dependent consequences of USP7 inhibitors currently under development as potential cancer therapeutics.USP7, which encodes a deubiquitylating enzyme, is among the most frequently mutated genes in pediatric T-ALL, with somatic heterozygous loss-of-function mutations (haploinsufficiency) predominantly affecting the subgroup that has aberrant TAL1 oncogene activation. Network analysis of > 200 T-ALL transcriptomes linked USP7 haploinsufficiency with decreased activities of E-proteins. E-proteins are also negatively regulated by TAL1, leading to concerted down-regulation of E-protein target genes involved in T-cell development. In T-ALL cell lines, we showed the physical interaction of USP7 with E-proteins and TAL1 by mass spectrometry and ChIP-seq. Haploinsufficient but not complete CRISPR knock-out of USP7 showed accelerated cell growth and validated transcriptional down-regulation of E-protein targets. Our study unveiled the synergistic effect of USP7 haploinsufficiency with aberrant TAL1 activation on T-ALL, implicating USP7 as a haploinsufficient tumor suppressor in T-ALL. Our findings caution against a universal oncogene designation for USP7 while emphasizing the dosage-dependent consequences of USP7 inhibitors currently under development as potential cancer therapeutics.
ArticleNumber 5154
Author Janke, Laura J.
Yu, Jiyang
Shaner, Bridget
Liu, Yu
Cheng, Cheng
Gu, Wei
Ma, Xiaotu
Pruett-Miller, Shondra M.
Downing, James R.
Shaw, Timothy I.
Peng, Junmin
Dong, Li
Qian, Chenxi
Easton, John
Porter, Shaina N.
Choi, John
Pei, Deqing
Zhang, Jinghui
High, Anthony
Kavdia, Kanisha
Ju, Bensheng
Look, A. Thomas
Pagala, Vishwajeeth R.
Tian, Liqing
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33664368$$D View this record in MEDLINE/PubMed
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Cites_doi 10.1093/nar/gkw937
10.1007/s12185-018-2518-z
10.1038/s41593-018-0328-5
10.1096/fj.201700473RR
10.1038/ng.3909
10.1016/j.ccr.2012.08.007
10.1038/ng.2287
10.1016/j.ccr.2012.06.007
10.1038/nbt.1508
10.1021/pr025556v
10.1016/j.celrep.2017.09.072
10.1073/pnas.91.8.3181
10.1093/bioinformatics/bty907
10.18632/oncotarget.16348
10.1002/pmic.201100523
10.1093/bioinformatics/btu638
10.1007/978-1-4939-2425-7_17
10.1038/nature07290
10.4049/jimmunol.178.9.5717
10.1158/1535-7163.MCT-09-0097
10.1038/ncomms4630
10.1111/febs.12843
10.1038/s41586-018-0177-0
10.1016/j.molcel.2015.07.033
10.1016/S1535-6108(02)00018-1
10.1021/cr3003533
10.1038/nature24006
10.1016/j.biocel.2016.08.025
10.1172/JCI61269
10.1038/nri2304
10.1093/emboj/16.7.1519
10.1038/nature08595
10.1056/NEJMra1400972
10.1038/nrd.2017.152
10.1126/science.1259037
10.1038/cddis.2013.400
10.1158/1078-0432.CCR-18-1740
10.1016/1044-0305(94)80016-2
10.1016/j.ccr.2004.05.023
10.1084/jem.20171066
10.1016/S1470-2045(08)70314-0
10.1038/nature25795
10.1038/nature737
10.1038/s41598-019-40896-w
10.1038/cr.2016.39
10.1038/nm.4180
10.1073/pnas.0506580102
10.1038/sj.onc.1204519
10.1016/j.exphem.2017.06.001
10.1073/pnas.1310249110
10.1016/S1097-2765(04)00157-1
10.1186/1471-2164-9-537
10.1093/nar/gkv007
10.1093/nar/gkw257
10.1074/jbc.271.49.31463
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References Nielsen, Norby, Pedersen, Jorgensen (CR26) 1996; 271
Pagala (CR28) 2015; 1278
Chauhan (CR17) 2012; 22
Sanda, Leong (CR55) 2017; 53
Mansour (CR3) 2014; 346
Colland (CR22) 2009; 8
Song (CR15) 2008; 455
Ritchie (CR38) 2015; 43
Hunger, Mullighan (CR2) 2015; 373
Fan (CR21) 2013; 4
Novellasdemunt (CR13) 2017; 21
Li, Brooks, Kon, Gu (CR54) 2004; 13
Huether (CR7) 2014; 5
Szklarczyk (CR37) 2017; 45
Everett (CR8) 1997; 16
Hao (CR10) 2015; 59
Ramirez (CR41) 2016; 44
Tan, Zhang, Sanda (CR47) 2019; 109
Dunham, Mullin, Gingras (CR29) 2012; 12
Sanda (CR46) 2012; 22
Coustan-Smith (CR33) 2009; 10
Jin (CR16) 2019; 25
Bhattacharya, Ghosh (CR12) 2014; 281
Zhang, Shin, Song, Lei, Liu (CR40) 2008; 9
Swatek, Komander (CR53) 2016; 26
Connelly, Pruett-Miller (CR27) 2019; 9
Khatamian, Paull, Califano, Yu (CR36) 2019; 35
Ma (CR49) 2018; 555
O'Neil, Billa, Oikemus, Kelliher (CR25) 2001; 20
Anders, Pyl, Huber (CR32) 2015; 31
Kharchenko, Tolstorukov, Park (CR39) 2008; 26
Aifantis, Raetz, Buonamici (CR1) 2008; 8
Subramanian (CR34) 2005; 102
Ferrando (CR6) 2002; 1
Zhang, Fonslow, Shan, Baek, Yates (CR30) 2013; 113
Du (CR35) 2018; 558
Liu (CR5) 2017; 49
Kategaya (CR23) 2017; 550
Harrigan, Jacq, Martin, Jackson (CR9) 2018; 17
Hsu, Wadman, Baer (CR24) 1994; 91
Wojciechowski, Lai, Kondo, Zhuang (CR50) 2007; 178
Van Vlierberghe, Ferrando (CR4) 2012; 122
Li (CR11) 2002; 416
Carra (CR18) 2017; 8
Downing (CR31) 2012; 44
O'Neil, Shank, Cusson, Murre, Kelliher (CR51) 2004; 5
Yang (CR42) 2019; 22
Peng, Elias, Thoreen, Licklider, Gygi (CR44) 2003; 2
Stolte (CR20) 2018; 215
Eng, McCormack, Yates (CR43) 1994; 5
Tavana (CR14) 2016; 22
Zhang (CR19) 2016; 79
Cai (CR48) 2018; 32
Pierce, Kleiger, Shan, Deshaies (CR52) 2009; 462
Bai (CR45) 2013; 110
X Du (84647_CR35) 2018; 558
D Szklarczyk (84647_CR37) 2017; 45
AA Ferrando (84647_CR6) 2002; 1
B Bai (84647_CR45) 2013; 110
WH Dunham (84647_CR29) 2012; 12
T Sanda (84647_CR55) 2017; 53
J Cai (84647_CR48) 2018; 32
M Li (84647_CR11) 2002; 416
SP Hunger (84647_CR2) 2015; 373
F Ramirez (84647_CR41) 2016; 44
KN Swatek (84647_CR53) 2016; 26
MS Song (84647_CR15) 2008; 455
M Li (84647_CR54) 2004; 13
J O'Neil (84647_CR25) 2001; 20
JR Downing (84647_CR31) 2012; 44
TK Tan (84647_CR47) 2019; 109
YH Hao (84647_CR10) 2015; 59
VR Pagala (84647_CR28) 2015; 1278
A Khatamian (84647_CR36) 2019; 35
L Novellasdemunt (84647_CR13) 2017; 21
JK Eng (84647_CR43) 1994; 5
R Huether (84647_CR7) 2014; 5
D Chauhan (84647_CR17) 2012; 22
L Kategaya (84647_CR23) 2017; 550
NW Pierce (84647_CR52) 2009; 462
YH Fan (84647_CR21) 2013; 4
C Zhang (84647_CR19) 2016; 79
PV Kharchenko (84647_CR39) 2008; 26
T Sanda (84647_CR46) 2012; 22
J Wojciechowski (84647_CR50) 2007; 178
S Bhattacharya (84647_CR12) 2014; 281
A Subramanian (84647_CR34) 2005; 102
HL Hsu (84647_CR24) 1994; 91
O Tavana (84647_CR14) 2016; 22
JA Harrigan (84647_CR9) 2018; 17
X Ma (84647_CR49) 2018; 555
G Carra (84647_CR18) 2017; 8
B Stolte (84647_CR20) 2018; 215
E Coustan-Smith (84647_CR33) 2009; 10
S Anders (84647_CR32) 2015; 31
J Peng (84647_CR44) 2003; 2
JP Connelly (84647_CR27) 2019; 9
X Yang (84647_CR42) 2019; 22
MR Mansour (84647_CR3) 2014; 346
RD Everett (84647_CR8) 1997; 16
F Colland (84647_CR22) 2009; 8
J O'Neil (84647_CR51) 2004; 5
I Aifantis (84647_CR1) 2008; 8
ME Ritchie (84647_CR38) 2015; 43
AL Nielsen (84647_CR26) 1996; 271
Y Zhang (84647_CR30) 2013; 113
Y Liu (84647_CR5) 2017; 49
P Van Vlierberghe (84647_CR4) 2012; 122
Y Zhang (84647_CR40) 2008; 9
Q Jin (84647_CR16) 2019; 25
References_xml – volume: 45
  start-page: D362
  year: 2017
  end-page: D368
  ident: CR37
  article-title: The STRING database in 2017: Quality-controlled protein–protein association networks, made broadly accessible
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkw937
– volume: 109
  start-page: 5
  year: 2019
  end-page: 17
  ident: CR47
  article-title: Oncogenic transcriptional program driven by TAL1 in T-cell acute lymphoblastic leukemia
  publication-title: Int. J. Hematol.
  doi: 10.1007/s12185-018-2518-z
– volume: 22
  start-page: 362
  year: 2019
  end-page: 373
  ident: CR42
  article-title: Differentiation of human pluripotent stem cells into neurons or cortical organoids requires transcriptional co-regulation by UTX and 53BP1
  publication-title: Nat. Neurosci.
  doi: 10.1038/s41593-018-0328-5
– volume: 32
  start-page: 5238
  year: 2018
  end-page: 5249
  ident: CR48
  article-title: USP7-TRIM27 axis negatively modulates antiviral type I IFN signaling
  publication-title: FASEB J.
  doi: 10.1096/fj.201700473RR
– volume: 49
  start-page: 1211
  year: 2017
  end-page: 1218
  ident: CR5
  article-title: The genomic landscape of pediatric and young adult T-lineage acute lymphoblastic leukemia
  publication-title: Nat. Genet.
  doi: 10.1038/ng.3909
– volume: 22
  start-page: 345
  year: 2012
  end-page: 358
  ident: CR17
  article-title: A small molecule inhibitor of ubiquitin-specific protease-7 induces apoptosis in multiple myeloma cells and overcomes bortezomib resistance
  publication-title: Cancer Cell
  doi: 10.1016/j.ccr.2012.08.007
– volume: 44
  start-page: 619
  year: 2012
  end-page: 622
  ident: CR31
  article-title: The Pediatric Cancer Genome Project
  publication-title: Nat. Genet.
  doi: 10.1038/ng.2287
– volume: 22
  start-page: 209
  year: 2012
  end-page: 221
  ident: CR46
  article-title: Core transcriptional regulatory circuit controlled by the TAL1 complex in human T cell acute lymphoblastic leukemia
  publication-title: Cancer Cell
  doi: 10.1016/j.ccr.2012.06.007
– volume: 26
  start-page: 1351
  year: 2008
  end-page: 1359
  ident: CR39
  article-title: Design and analysis of ChIP-seq experiments for DNA-binding proteins
  publication-title: Nat. Biotechnol.
  doi: 10.1038/nbt.1508
– volume: 2
  start-page: 43
  year: 2003
  end-page: 50
  ident: CR44
  article-title: Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC–MS/MS) for large-scale protein analysis: The yeast proteome
  publication-title: J. Proteome Res.
  doi: 10.1021/pr025556v
– volume: 21
  start-page: 612
  year: 2017
  end-page: 627
  ident: CR13
  article-title: USP7 is a tumor-specific WNT activator for APC-mutated colorectal cancer by mediating beta-catenin deubiquitination
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2017.09.072
– volume: 91
  start-page: 3181
  year: 1994
  end-page: 3185
  ident: CR24
  article-title: Formation of in vivo complexes between the TAL1 and E2A polypeptides of leukemic T cells
  publication-title: Proc. Natl. Acad. Sci U.S.A.
  doi: 10.1073/pnas.91.8.3181
– volume: 35
  start-page: 2165
  year: 2019
  end-page: 2166
  ident: CR36
  article-title: SJARACNe: A scalable software tool for gene network reverse engineering from big data
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/bty907
– volume: 8
  start-page: 35508
  year: 2017
  end-page: 35522
  ident: CR18
  article-title: Therapeutic inhibition of USP7-PTEN network in chronic lymphocytic leukemia: A strategy to overcome TP53 mutated/deleted clones
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.16348
– volume: 12
  start-page: 1576
  year: 2012
  end-page: 1590
  ident: CR29
  article-title: Affinity-purification coupled to mass spectrometry: Basic principles and strategies
  publication-title: Proteomics
  doi: 10.1002/pmic.201100523
– volume: 31
  start-page: 166
  year: 2015
  end-page: 169
  ident: CR32
  article-title: HTSeq–a Python framework to work with high-throughput sequencing data
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btu638
– volume: 1278
  start-page: 281
  year: 2015
  end-page: 305
  ident: CR28
  article-title: Quantitative protein analysis by mass spectrometry
  publication-title: Methods Mol. Biol.
  doi: 10.1007/978-1-4939-2425-7_17
– volume: 455
  start-page: 813
  year: 2008
  end-page: 817
  ident: CR15
  article-title: The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network
  publication-title: Nature
  doi: 10.1038/nature07290
– volume: 178
  start-page: 5717
  year: 2007
  end-page: 5726
  ident: CR50
  article-title: E2A and HEB are required to block thymocyte proliferation prior to pre-TCR expression
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.178.9.5717
– volume: 8
  start-page: 2286
  year: 2009
  end-page: 2295
  ident: CR22
  article-title: Small-molecule inhibitor of USP7/HAUSP ubiquitin protease stabilizes and activates p53 in cells
  publication-title: Mol. Cancer Ther.
  doi: 10.1158/1535-7163.MCT-09-0097
– volume: 5
  start-page: 3630
  year: 2014
  ident: CR7
  article-title: The landscape of somatic mutations in epigenetic regulators across 1,000 paediatric cancer genomes
  publication-title: Nat. Commun.
  doi: 10.1038/ncomms4630
– volume: 281
  start-page: 3061
  year: 2014
  end-page: 3078
  ident: CR12
  article-title: HAUSP, a novel deubiquitinase for Rb—MDM2 the critical regulator
  publication-title: FEBS J.
  doi: 10.1111/febs.12843
– volume: 558
  start-page: 141
  year: 2018
  end-page: 145
  ident: CR35
  article-title: Hippo/Mst signalling couples metabolic state and immune function of CD8alpha(+) dendritic cells
  publication-title: Nature
  doi: 10.1038/s41586-018-0177-0
– volume: 59
  start-page: 956
  year: 2015
  end-page: 969
  ident: CR10
  article-title: USP7 acts as a molecular rheostat to promote WASH-dependent endosomal protein recycling and is mutated in a human neurodevelopmental disorder
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2015.07.033
– volume: 1
  start-page: 75
  year: 2002
  end-page: 87
  ident: CR6
  article-title: Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia
  publication-title: Cancer Cell
  doi: 10.1016/S1535-6108(02)00018-1
– volume: 113
  start-page: 2343
  year: 2013
  end-page: 2394
  ident: CR30
  article-title: Protein analysis by shotgun/bottom-up proteomics
  publication-title: Chem. Rev.
  doi: 10.1021/cr3003533
– volume: 550
  start-page: 534
  year: 2017
  end-page: 538
  ident: CR23
  article-title: USP7 small-molecule inhibitors interfere with ubiquitin binding
  publication-title: Nature
  doi: 10.1038/nature24006
– volume: 79
  start-page: 209
  year: 2016
  end-page: 221
  ident: CR19
  article-title: USP7 promotes cell proliferation through the stabilization of Ki-67 protein in non-small cell lung cancer cells
  publication-title: Int. J. Biochem. Cell Biol.
  doi: 10.1016/j.biocel.2016.08.025
– volume: 122
  start-page: 3398
  year: 2012
  end-page: 3406
  ident: CR4
  article-title: The molecular basis of T cell acute lymphoblastic leukemia
  publication-title: J. Clin. Investig.
  doi: 10.1172/JCI61269
– volume: 8
  start-page: 380
  year: 2008
  end-page: 390
  ident: CR1
  article-title: Molecular pathogenesis of T-cell leukaemia and lymphoma
  publication-title: Nat. Rev. Immunol.
  doi: 10.1038/nri2304
– volume: 16
  start-page: 1519
  year: 1997
  end-page: 1530
  ident: CR8
  article-title: A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein
  publication-title: EMBO J.
  doi: 10.1093/emboj/16.7.1519
– volume: 462
  start-page: 615
  year: 2009
  end-page: 619
  ident: CR52
  article-title: Detection of sequential polyubiquitylation on a millisecond timescale
  publication-title: Nature
  doi: 10.1038/nature08595
– volume: 373
  start-page: 1541
  year: 2015
  end-page: 1552
  ident: CR2
  article-title: Acute lymphoblastic leukemia in children
  publication-title: N. Engl. J. Med.
  doi: 10.1056/NEJMra1400972
– volume: 17
  start-page: 57
  year: 2018
  end-page: 78
  ident: CR9
  article-title: Deubiquitylating enzymes and drug discovery: Emerging opportunities
  publication-title: Nat. Rev. Drug Discov.
  doi: 10.1038/nrd.2017.152
– volume: 346
  start-page: 1373
  year: 2014
  end-page: 1377
  ident: CR3
  article-title: Oncogene regulation. An oncogenic super-enhancer formed through somatic mutation of a noncoding intergenic element
  publication-title: Science
  doi: 10.1126/science.1259037
– volume: 4
  start-page: e867
  year: 2013
  ident: CR21
  article-title: USP7 inhibitor P22077 inhibits neuroblastoma growth via inducing p53-mediated apoptosis
  publication-title: Cell Death Dis.
  doi: 10.1038/cddis.2013.400
– volume: 25
  start-page: 222
  year: 2019
  end-page: 239
  ident: CR16
  article-title: USP7 Cooperates with NOTCH1 to drive the oncogenic transcriptional program in T-cell leukemia
  publication-title: Clin. Cancer Res.
  doi: 10.1158/1078-0432.CCR-18-1740
– volume: 5
  start-page: 976
  year: 1994
  end-page: 989
  ident: CR43
  article-title: An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database
  publication-title: J. Am. Soc. Mass Spectrom.
  doi: 10.1016/1044-0305(94)80016-2
– volume: 5
  start-page: 587
  year: 2004
  end-page: 596
  ident: CR51
  article-title: TAL1/SCL induces leukemia by inhibiting the transcriptional activity of E47/HEB
  publication-title: Cancer Cell
  doi: 10.1016/j.ccr.2004.05.023
– volume: 215
  start-page: 2137
  year: 2018
  end-page: 2155
  ident: CR20
  article-title: Genome-scale CRISPR-Cas9 screen identifies druggable dependencies in TP53 wild-type Ewing sarcoma
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20171066
– volume: 10
  start-page: 147
  year: 2009
  end-page: 156
  ident: CR33
  article-title: Early T-cell precursor leukaemia: A subtype of very high-risk acute lymphoblastic leukaemia
  publication-title: Lancet Oncol.
  doi: 10.1016/S1470-2045(08)70314-0
– volume: 555
  start-page: 371
  year: 2018
  end-page: 376
  ident: CR49
  article-title: Pan-cancer genome and transcriptome analyses of 1,699 paediatric leukaemias and solid tumours
  publication-title: Nature
  doi: 10.1038/nature25795
– volume: 416
  start-page: 648
  year: 2002
  end-page: 653
  ident: CR11
  article-title: Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization
  publication-title: Nature
  doi: 10.1038/nature737
– volume: 9
  start-page: 4194
  year: 2019
  ident: CR27
  article-title: CRISpy: A versatile and high-throughput analysis program for CRISPR-based genome editing
  publication-title: Sci. Rep.
  doi: 10.1038/s41598-019-40896-w
– volume: 26
  start-page: 399
  year: 2016
  end-page: 422
  ident: CR53
  article-title: Ubiquitin modifications
  publication-title: Cell Res.
  doi: 10.1038/cr.2016.39
– volume: 22
  start-page: 1180
  year: 2016
  end-page: 1186
  ident: CR14
  article-title: HAUSP deubiquitinates and stabilizes N-Myc in neuroblastoma
  publication-title: Nat. Med.
  doi: 10.1038/nm.4180
– volume: 102
  start-page: 15545
  year: 2005
  end-page: 15550
  ident: CR34
  article-title: Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.0506580102
– volume: 20
  start-page: 3897
  year: 2001
  end-page: 3905
  ident: CR25
  article-title: The DNA binding activity of TAL-1 is not required to induce leukemia/lymphoma in mice
  publication-title: Oncogene
  doi: 10.1038/sj.onc.1204519
– volume: 53
  start-page: 7
  year: 2017
  end-page: 15
  ident: CR55
  article-title: TAL1 as a master oncogenic transcription factor in T-cell acute lymphoblastic leukemia
  publication-title: Exp. Hematol.
  doi: 10.1016/j.exphem.2017.06.001
– volume: 110
  start-page: 16562
  year: 2013
  end-page: 16567
  ident: CR45
  article-title: U1 small nuclear ribonucleoprotein complex and RNA splicing alterations in Alzheimer's disease
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.1310249110
– volume: 13
  start-page: 879
  year: 2004
  end-page: 886
  ident: CR54
  article-title: A dynamic role of HAUSP in the p53-Mdm2 pathway
  publication-title: Mol. Cell
  doi: 10.1016/S1097-2765(04)00157-1
– volume: 9
  start-page: 537
  year: 2008
  ident: CR40
  article-title: Identifying positioned nucleosomes with epigenetic marks in human from ChIP-Seq
  publication-title: BMC Genomics
  doi: 10.1186/1471-2164-9-537
– volume: 43
  start-page: e47
  year: 2015
  ident: CR38
  article-title: limma powers differential expression analyses for RNA-sequencing and microarray studies
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkv007
– volume: 44
  start-page: W160
  year: 2016
  end-page: W165
  ident: CR41
  article-title: deepTools2: A next generation web server for deep-sequencing data analysis
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkw257
– volume: 271
  start-page: 31463
  year: 1996
  end-page: 31469
  ident: CR26
  article-title: E-box sequence and context-dependent TAL1/SCL modulation of basic helix–loop–helix protein-mediated transcriptional activation
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.271.49.31463
– volume: 122
  start-page: 3398
  year: 2012
  ident: 84647_CR4
  publication-title: J. Clin. Investig.
  doi: 10.1172/JCI61269
– volume: 31
  start-page: 166
  year: 2015
  ident: 84647_CR32
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btu638
– volume: 26
  start-page: 399
  year: 2016
  ident: 84647_CR53
  publication-title: Cell Res.
  doi: 10.1038/cr.2016.39
– volume: 22
  start-page: 209
  year: 2012
  ident: 84647_CR46
  publication-title: Cancer Cell
  doi: 10.1016/j.ccr.2012.06.007
– volume: 20
  start-page: 3897
  year: 2001
  ident: 84647_CR25
  publication-title: Oncogene
  doi: 10.1038/sj.onc.1204519
– volume: 35
  start-page: 2165
  year: 2019
  ident: 84647_CR36
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/bty907
– volume: 10
  start-page: 147
  year: 2009
  ident: 84647_CR33
  publication-title: Lancet Oncol.
  doi: 10.1016/S1470-2045(08)70314-0
– volume: 110
  start-page: 16562
  year: 2013
  ident: 84647_CR45
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.1310249110
– volume: 53
  start-page: 7
  year: 2017
  ident: 84647_CR55
  publication-title: Exp. Hematol.
  doi: 10.1016/j.exphem.2017.06.001
– volume: 1
  start-page: 75
  year: 2002
  ident: 84647_CR6
  publication-title: Cancer Cell
  doi: 10.1016/S1535-6108(02)00018-1
– volume: 109
  start-page: 5
  year: 2019
  ident: 84647_CR47
  publication-title: Int. J. Hematol.
  doi: 10.1007/s12185-018-2518-z
– volume: 8
  start-page: 380
  year: 2008
  ident: 84647_CR1
  publication-title: Nat. Rev. Immunol.
  doi: 10.1038/nri2304
– volume: 22
  start-page: 1180
  year: 2016
  ident: 84647_CR14
  publication-title: Nat. Med.
  doi: 10.1038/nm.4180
– volume: 1278
  start-page: 281
  year: 2015
  ident: 84647_CR28
  publication-title: Methods Mol. Biol.
  doi: 10.1007/978-1-4939-2425-7_17
– volume: 113
  start-page: 2343
  year: 2013
  ident: 84647_CR30
  publication-title: Chem. Rev.
  doi: 10.1021/cr3003533
– volume: 373
  start-page: 1541
  year: 2015
  ident: 84647_CR2
  publication-title: N. Engl. J. Med.
  doi: 10.1056/NEJMra1400972
– volume: 32
  start-page: 5238
  year: 2018
  ident: 84647_CR48
  publication-title: FASEB J.
  doi: 10.1096/fj.201700473RR
– volume: 8
  start-page: 2286
  year: 2009
  ident: 84647_CR22
  publication-title: Mol. Cancer Ther.
  doi: 10.1158/1535-7163.MCT-09-0097
– volume: 178
  start-page: 5717
  year: 2007
  ident: 84647_CR50
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.178.9.5717
– volume: 45
  start-page: D362
  year: 2017
  ident: 84647_CR37
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkw937
– volume: 22
  start-page: 362
  year: 2019
  ident: 84647_CR42
  publication-title: Nat. Neurosci.
  doi: 10.1038/s41593-018-0328-5
– volume: 462
  start-page: 615
  year: 2009
  ident: 84647_CR52
  publication-title: Nature
  doi: 10.1038/nature08595
– volume: 26
  start-page: 1351
  year: 2008
  ident: 84647_CR39
  publication-title: Nat. Biotechnol.
  doi: 10.1038/nbt.1508
– volume: 558
  start-page: 141
  year: 2018
  ident: 84647_CR35
  publication-title: Nature
  doi: 10.1038/s41586-018-0177-0
– volume: 21
  start-page: 612
  year: 2017
  ident: 84647_CR13
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2017.09.072
– volume: 13
  start-page: 879
  year: 2004
  ident: 84647_CR54
  publication-title: Mol. Cell
  doi: 10.1016/S1097-2765(04)00157-1
– volume: 16
  start-page: 1519
  year: 1997
  ident: 84647_CR8
  publication-title: EMBO J.
  doi: 10.1093/emboj/16.7.1519
– volume: 59
  start-page: 956
  year: 2015
  ident: 84647_CR10
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2015.07.033
– volume: 9
  start-page: 4194
  year: 2019
  ident: 84647_CR27
  publication-title: Sci. Rep.
  doi: 10.1038/s41598-019-40896-w
– volume: 44
  start-page: 619
  year: 2012
  ident: 84647_CR31
  publication-title: Nat. Genet.
  doi: 10.1038/ng.2287
– volume: 17
  start-page: 57
  year: 2018
  ident: 84647_CR9
  publication-title: Nat. Rev. Drug Discov.
  doi: 10.1038/nrd.2017.152
– volume: 416
  start-page: 648
  year: 2002
  ident: 84647_CR11
  publication-title: Nature
  doi: 10.1038/nature737
– volume: 25
  start-page: 222
  year: 2019
  ident: 84647_CR16
  publication-title: Clin. Cancer Res.
  doi: 10.1158/1078-0432.CCR-18-1740
– volume: 91
  start-page: 3181
  year: 1994
  ident: 84647_CR24
  publication-title: Proc. Natl. Acad. Sci U.S.A.
  doi: 10.1073/pnas.91.8.3181
– volume: 22
  start-page: 345
  year: 2012
  ident: 84647_CR17
  publication-title: Cancer Cell
  doi: 10.1016/j.ccr.2012.08.007
– volume: 43
  start-page: e47
  year: 2015
  ident: 84647_CR38
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkv007
– volume: 281
  start-page: 3061
  year: 2014
  ident: 84647_CR12
  publication-title: FEBS J.
  doi: 10.1111/febs.12843
– volume: 79
  start-page: 209
  year: 2016
  ident: 84647_CR19
  publication-title: Int. J. Biochem. Cell Biol.
  doi: 10.1016/j.biocel.2016.08.025
– volume: 5
  start-page: 976
  year: 1994
  ident: 84647_CR43
  publication-title: J. Am. Soc. Mass Spectrom.
  doi: 10.1016/1044-0305(94)80016-2
– volume: 550
  start-page: 534
  year: 2017
  ident: 84647_CR23
  publication-title: Nature
  doi: 10.1038/nature24006
– volume: 49
  start-page: 1211
  year: 2017
  ident: 84647_CR5
  publication-title: Nat. Genet.
  doi: 10.1038/ng.3909
– volume: 455
  start-page: 813
  year: 2008
  ident: 84647_CR15
  publication-title: Nature
  doi: 10.1038/nature07290
– volume: 4
  start-page: e867
  year: 2013
  ident: 84647_CR21
  publication-title: Cell Death Dis.
  doi: 10.1038/cddis.2013.400
– volume: 102
  start-page: 15545
  year: 2005
  ident: 84647_CR34
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.0506580102
– volume: 346
  start-page: 1373
  year: 2014
  ident: 84647_CR3
  publication-title: Science
  doi: 10.1126/science.1259037
– volume: 12
  start-page: 1576
  year: 2012
  ident: 84647_CR29
  publication-title: Proteomics
  doi: 10.1002/pmic.201100523
– volume: 9
  start-page: 537
  year: 2008
  ident: 84647_CR40
  publication-title: BMC Genomics
  doi: 10.1186/1471-2164-9-537
– volume: 5
  start-page: 3630
  year: 2014
  ident: 84647_CR7
  publication-title: Nat. Commun.
  doi: 10.1038/ncomms4630
– volume: 271
  start-page: 31463
  year: 1996
  ident: 84647_CR26
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.271.49.31463
– volume: 215
  start-page: 2137
  year: 2018
  ident: 84647_CR20
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20171066
– volume: 44
  start-page: W160
  year: 2016
  ident: 84647_CR41
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkw257
– volume: 2
  start-page: 43
  year: 2003
  ident: 84647_CR44
  publication-title: J. Proteome Res.
  doi: 10.1021/pr025556v
– volume: 5
  start-page: 587
  year: 2004
  ident: 84647_CR51
  publication-title: Cancer Cell
  doi: 10.1016/j.ccr.2004.05.023
– volume: 8
  start-page: 35508
  year: 2017
  ident: 84647_CR18
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.16348
– volume: 555
  start-page: 371
  year: 2018
  ident: 84647_CR49
  publication-title: Nature
  doi: 10.1038/nature25795
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Snippet USP7, which encodes a deubiquitylating enzyme, is among the most frequently mutated genes in pediatric T-ALL, with somatic heterozygous loss-of-function...
USP7, which encodes a deubiquitylating enzyme, is among the most frequently mutated genes in pediatric T-ALL, with somatic heterozygous loss-of-function...
Abstract USP7, which encodes a deubiquitylating enzyme, is among the most frequently mutated genes in pediatric T-ALL, with somatic heterozygous...
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StartPage 5154
SubjectTerms 631/114
631/114/2114
631/67/1990/283/2125
Acute lymphoblastic leukemia
Cell Line, Tumor
Cell Lineage - genetics
Cell Proliferation - genetics
CRISPR
CRISPR-Cas Systems - genetics
Dosage
Drug development
Gene Expression Regulation, Leukemic - genetics
Gene regulation
Haploinsufficiency
Haploinsufficiency - genetics
Humanities and Social Sciences
Humans
Leukemia
Lymphatic leukemia
Lymphocytes T
Mass spectrometry
Mass spectroscopy
multidisciplinary
Oncogenes - genetics
Pediatrics
Precursor T-Cell Lymphoblastic Leukemia-Lymphoma - genetics
Precursor T-Cell Lymphoblastic Leukemia-Lymphoma - pathology
Proteins
Science
Science (multidisciplinary)
Synergistic effect
T-Cell Acute Lymphocytic Leukemia Protein 1 - genetics
Transcription
Transcriptional Activation - genetics
Tumor suppressor genes
Ubiquitin-Specific Peptidase 7 - genetics
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Title Integrative network analysis reveals USP7 haploinsufficiency inhibits E-protein activity in pediatric T-lineage acute lymphoblastic leukemia (T-ALL)
URI https://link.springer.com/article/10.1038/s41598-021-84647-2
https://www.ncbi.nlm.nih.gov/pubmed/33664368
https://www.proquest.com/docview/2496262907
https://www.proquest.com/docview/2498488794
https://pubmed.ncbi.nlm.nih.gov/PMC7933146
https://doaj.org/article/cb7c285f227c42abb04cd250bb2d752a
Volume 11
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