USP7 controls Chk1 protein stability by direct deubiquitination.
Open accessAbstract
Chk1, an essential checkpoint kinase in the DNA damage response pathway (DDR), is tightly regulated by both ATR-dependent phosphorylation and proteasome-mediated degradation. Here we identify ubiquitin hydrolase USP7 as a novel regulator of Chk1 protein stability. USP7 was shown before to regulate other DDR proteins such as p53, Hdm2 and Claspin, an adaptor protein in the ATR-Chk1 pathway required for Chk1 activation. Depletion or inhibition of USP7 leads to lower Chk1 levels. The decreased Chk1 protein after USP7 knock down cannot be rescued by simultaneously elevating Claspin levels, demonstrating that the effect of USP7 on Chk1 is independent of its known effect on Claspin. Conversely, overexpression of USP7 wild type, but not a catalytic mutant version, elevates Chk1 levels and increases the half-life of Chk1 protein. Importantly, wild type, but not catalytic mutant USP7 can deubiquitinate Chk1 in vivo and in vitro, confirming that USP7 directly regulates Chk1 protein levels. Finally we show that USP7 catalytic mutant is (mono-)ubiquitinated, which suggests auto-deubiquitination by this ubiquitin hydrolase, possibly important for its regulation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
USP7 influences DSB repair by regulating checkpoint kinase 1 (Chk1).
“USP7 also influences DSB repair by regulating checkpoint kinase 1 (Chk1) (Faustrup et al., 2009; Alonso-de Vega et al., 2014; Zhang P. et al., 2014).”
From USP7 Is a Master Regulator of Genome Stability (2020) · cites this paper as Alonso-de Vega et al., 2014
USP7 controls Chk1 signaling by deubiquitinating and stabilizing both Chk1 and its activator protein Claspin.
“USP7 controls Chk1 signaling by deubiquitinating and stabilizing both Chk1 and its activator protein, Claspin (Faustrup et al., 2009; Alonso-de Vega et al., 2014; Zhang P. et al., 2014).”
From USP7 Is a Master Regulator of Genome Stability (2020) · cites this paper as Alonso-de Vega et al., 2014
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The ATM–Chk2 and ATR–Chk1 Pathways in DNA Damage Signaling and Cancer
Smith, J., Tho, L. M., Xu, N., & Gillespie, D. A. (2010) · Advances in cancer research · doi:10.1016/b978-0-12-380888-2.00003-0 · Cited by 1,279 · see citing works
Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization
Li, M., Chen, D., Shiloh, A., Luo, J., Nikolaev, A. Y., Qin, J., & Gu, W. J. (2002) · Nature · doi:10.1038/nature737 · Cited by 1,027 · see citing works
Regulation of monoubiquitinated PCNA by DUB autocleavage
Huang, T. T., Nijman, S. M. B., Mirchandani, K. D., Galardy, P. J., Cohn, M. A., Haas, W., Gygi, S. P., Ploegh, H. L., Bernards, R., & D’Andrea, A. D. (2006) · Nature Cell Biology · doi:10.1038/ncb1378 · Cited by 585 · see citing works
The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network
Song, M. S., Salmena, L., Carracedo, A., Egia, A., Lo-Coco, F., Teruya-Feldstein, J., & Pandolfi, P. P. (2008) · Nature · doi:10.1038/nature07290 · Cited by 548 · see citing works
DNA damage signalling guards against activated oncogenes and tumour progression
Bartek, J., Bartkova, J., & Lukas, J. (2007) · Oncogene · doi:10.1038/sj.onc.1210881 · Cited by 521 · see citing works
FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP
van der Horst, A., de Vries-Smits, A. M. M., Brenkman, A. B., van Triest, M. H., van den Broek, N. J. F., Colland, F., Maurice, M. M., & Burgering, B. M. T. (2006) · Nature Cell Biology · doi:10.1038/ncb1469 · Cited by 479 · see citing works
Activity-Based Chemical Proteomics Accelerates Inhibitor Development for Deubiquitylating Enzymes
Altun, M., Kramer, H., Willems, L. I., McDermott, J. L., Leach, C. A., Goldenberg, S. J., Kumar, S., Konietzny, R., Fischer, R., Kogan, E., et al. (2011) · Chemistry & Biology · doi:10.1016/j.chembiol.2011.08.018 · Cited by 401 · see citing works
Genotoxic Stress Targets Human Chk1 for Degradation by the Ubiquitin-Proteasome Pathway
Zhang, Y.-W., Otterness, D. M., Chiang, G. G., Xie, W., Liu, Y., Mercurio, F., & Abraham, R. T. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.07.019 · Cited by 283 · see citing works
Hussain, S., Zhang, Y., & Galardy, P. J. (2009) · Cell Cycle · doi:10.4161/cc.8.11.8739 · Cited by 257 · see citing works
Hu, M., Gu, L., Li, M., Jeffrey, P. D., Gu, W., & Shi, Y. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040027 · Cited by 251 · see citing works
The Multifaceted Roles of USP7: New Therapeutic Opportunities
Nicholson, B., & Kumar, S. (2011) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-011-9185-5 · Cited by 243 · see citing works
Polo-like Kinase-1 Controls Proteasome-Dependent Degradation of Claspin during Checkpoint Recovery
Mamely, I., van Vugt, M. A., Smits, V. A., Semple, J. I., Lemmens, B., Perrakis, A., Medema, R. H., & Freire, R. (2006) · Current Biology · doi:10.1016/j.cub.2006.08.026 · Cited by 227 · see citing works
Self-citationRapid PIKK-Dependent Release of Chk1 from Chromatin Promotes the DNA-Damage Checkpoint Response
Smits, V. A. J., Reaper, P. M., & Jackson, S. P. (2005) · Current Biology · doi:10.1016/j.cub.2005.11.066 · Cited by 199 · see citing works
Self-citationThe F Box Protein Fbx6 Regulates Chk1 Stability and Cellular Sensitivity to Replication Stress
Zhang, Y.-W., Brognard, J., Coughlin, C., You, Z., Dolled-Filhart, M. P., Aslanian, A., Manning, G., Abraham, R. T., & Hunter, T. R. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.06.030 · Cited by 186 · see citing works
Cell cycle-dependent and ATM-independent expression of human Chk1 kinase
Kaneko, Y., Watanabe, N., Morisaki, H., Akita, H., Fujimoto, A., Tominaga, K., Terasawa, M., Tachibana, A., Ikeda, K., & Nakanishi, M. (1999) · Oncogene · doi:10.1038/sj.onc.1202706 · Cited by 150 · see citing works
ATR, Claspin and the Rad9-Rad1-Hus1 Complex Regulate Chk1 and Cdc25A in the Absence of DNA Damage
Sørensen, C. S., Syljuåsen, R. G., Lukas, J., & Bártek, J. (2004) · Cell Cycle · doi:10.4161/cc.3.7.972 · Cited by 117 · see citing works
USP7 counteracts SCFβTrCP- but not APCCdh1-mediated proteolysis of Claspin
Faustrup, H., Bekker-Jensen, S., Bartek, J., Lukas, J., & Mailand, N. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200807137 · Cited by 113 · see citing works
Reversible Monoubiquitination Regulates the Parkinson Disease-associated Ubiquitin Hydrolase UCH-L1
Meray, R. K., & Lansbury, P. T. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m611153200 · Cited by 101 · see citing works
The USP19 Deubiquitinase Regulates the Stability of c-IAP1 and c-IAP2
Mei, Y., Alcivar, A., Hu, S., & Yang, X. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.282020 · Cited by 90 · see citing works
USP29 controls the stability of checkpoint adaptor Claspin by deubiquitination
Martín, Y., Cabrera, E., Amoedo, H., Hernández-Pérez, S., Domínguez-Kelly, R., & Freire, R. (2014) · Oncogene · doi:10.1038/onc.2014.38 · Cited by 77 · see citing works
Self-citationChk1 is required to maintain Claspin stability
Chini, C. C. S., Wood, J., & Chen, J. (2006) · Oncogene · doi:10.1038/sj.onc.1209447 · Cited by 62 · see citing works
Calcium/Calmodulin Regulates Ubiquitination of the Ubiquitin-specific Protease TRE17/USP6
Shen, C., Ye, Y., Robertson, S. E., Lau, A. W., Mak, D. D., & Chou, M. M. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m505220200 · Cited by 52 · see citing works
Lin, Y., Shih, H.-Y., Shang, Z., Matsunaga, S., & Chen, B. P. C. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku116 · Cited by 48 · see citing works
Mechanisms of ATR-mediated checkpoint signalling
Smits, V. A. J. (2010) · Frontiers in bioscience · doi:10.2741/3649 · Cited by 45 · see citing works
Self-citationCleavage and degradation of Claspin during apoptosis by caspases and the proteasome
Semple, J. I., Smits, V. A. J., Hernandez-Fernaud, J. R., Mamely, I., & Freire, R. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402134 · Cited by 45 · see citing works
Self-citationClaspin: Timing the Cell Cycle Arrest When the Genome is Damaged
Freire, R., van Vugt, M. A. T. M., Mamely, I., & Medema, R. H. (2006) · Cell Cycle · doi:10.4161/cc.5.24.3559 · Cited by 43 · see citing works
Spreading the Signal: Dissociation of Chk1 from Chromatin
Smits, V. A. J. (2006) · Cell Cycle · doi:10.4161/cc.5.10.2761 · Cited by 31 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Dewson, G., Eichhorn, P. J. A., & Komander, D. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00633-y · Cited by 337 · see citing works
USP7: Structure, substrate specificity, and inhibition
Pozhidaeva, A., & Bezsonova, I. (2019) · DNA Repair · doi:10.1016/j.dnarep.2019.02.005 · Cited by 178 · see citing works
Emerging insights into HAUSP (USP7) in physiology, cancer and other diseases.
Bhattacharya, S., Chakraborty, D., Basu, M., & Ghosh, M. K. (2018) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-018-0012-y · Cited by 162 · see citing works
USP7 is a SUMO deubiquitinase essential for DNA replication.
Lecona, E., Rodriguez-Acebes, S., Specks, J., Lopez-Contreras, A. J., Ruppen, I., Murga, M., Muñoz, J., Mendez, J., & Fernandez-Capetillo, O. (2016) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3185 · Cited by 148 · see citing works
USP7: Novel Drug Target in Cancer Therapy
Wang, Z., Kang, W.-T., You, Y., Pang, J., Ren, H., Suo, Z., Liu, H., & Zheng, Y. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00427 · Cited by 124 · see citing works
USP7 Is a Master Regulator of Genome Stability
Valles, G. J., Bezsonova, I., Woodgate, R., & Ashton, N. W. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00717 · Cited by 114 · see citing works
Ubiquitin-specific protease 7 sustains DNA damage response and promotes cervical carcinogenesis
Su, D., Ma, S., Shan, L., Wang, Y., Wang, Y., Cao, C., Liu, B., Yang, C., Wang, L., Tian, S., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci120518 · Cited by 114 · see citing works
DNA damage control: regulation and functions of checkpoint kinase 1
Smits, V. A. J., & Gillespie, D. A. (2015) · FEBS Journal · doi:10.1111/febs.13387 · Cited by 115 · see citing works
Self-citationPozhidaeva, A., Valles, G., Wang, F., Wu, J., Sterner, D. E., Nguyen, P., Weinstock, J., Kumar, K. G. S., Kanyo, J., Wright, D., et al. (2017) · Cell Chemical Biology · doi:10.1016/j.chembiol.2017.09.004 · Cited by 107 · see citing works
The emerging role of deubiquitinating enzymes in genomic integrity, diseases, and therapeutics
He, M., Zhou, Z., Shah, A. A., Zou, H., Tao, J., Chen, Q., & Wan, Y. (2016) · Cell & Bioscience · doi:10.1186/s13578-016-0127-1 · Cited by 106 · see citing works
USP7 - a crucial regulator of cancer hallmarks
Saha, G., Roy, S., Basu, M., & Ghosh, M. K. (2023) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2023.188903 · Cited by 106 · see citing works
DNA replication fork speed underlies cell fate changes and promotes reprogramming
Nakatani, T., Lin, J., Ji, F., Ettinger, A. W., Pontabry, J., Tokoro, M., Altamirano‐Pacheco, L., Fiorentino, J., Mahammadov, E., Hatano, Y., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01023-0 · Cited by 102 · see citing works
Ubiquitin-Specific Proteases: Players in Cancer Cellular Processes
Cruz, L. L., Soares, P., & Correia, M. (2021) · Pharmaceuticals · doi:10.3390/ph14090848 · Cited by 96 · see citing works
Li, X., Kong, L., Yang, Q., Duan, A., Ju, X., Cai, B., Chen, L., An, T., & Li, Y. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.011396 · Cited by 91 · see citing works
Wang, B., Zheng, J., Li, R., Tian, Y., Lin, J., Liang, Y., Sun, Q., Xu, A., Zheng, R., Liu, M., et al. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1996-0 · Cited by 80 · see citing works
Gao, H., Xi, Z., Dai, J., Xue, J., Guan, X., Zhao, L., Chen, Z., & Xing, F. (2024) · Molecular Cancer · doi:10.1186/s12943-024-02005-y · Cited by 79 · see citing works
Pinto-Fernández, A., & Kessler, B. M. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00133 · Cited by 73 · see citing works
The Hammer and the Dance of Cell Cycle Control
Παναγόπουλος, Α., & Altmeyer, M. (2020) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.11.002 · Cited by 70 · see citing works
Zhang, C., Lu, J., Zhang, Q.-W., Zhao, W., Guo, J.-H., Liu, S.-L., Wu, Y.-L., Jiang, B., & Gao, F.-H. (2016) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2016.08.025 · Cited by 67 · see citing works
Jiang, L., Xiong, J., Zhan, J., Yuan, F., Tang, M., Zhang, C., Cao, Z., Chen, Y., Lu, X., Li, Y., et al. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.780130 · Cited by 68 · see citing works
Hernández-Pérez, S., Cabrera, E., Salido, E., Lim, M., Reid, L., Lakhani, S. R., Khanna, K. K., Saunus, J. M., & Freire, R. (2017) · Oncogene · doi:10.1038/onc.2017.21 · Cited by 61 · see citing works
Dual-utility NLS drives RNF169-dependent DNA damage responses
An, L., Jiang, Y., Ng, H. H. W., Man, E. P. S., Chen, J., Khoo, U., Gong, Q., & Huen, M. S. Y. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616602114 · Cited by 60 · see citing works
Role of RAD51AP1 in homologous recombination DNA repair and carcinogenesis
Pires, E., Sung, P., & Wiese, C. (2017) · DNA repair · doi:10.1016/j.dnarep.2017.09.008 · Cited by 57 · see citing works
Kim, R. Q., van Dijk, W. J., & Sixma, T. K. (2016) · Journal of Structural Biology · doi:10.1016/j.jsb.2016.05.005 · Cited by 56 · see citing works
McGarry, E., Gaboriau, D. C. A., Rainey, M. D., Restuccia, U., Bachi, A., & Santocanale, C. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-2890 · Cited by 54 · see citing works
Periodontal Pathogens Promote Oral Squamous Cell Carcinoma by Regulating ATR and NLRP3 Inflammasome
Yao, Y., Shen, X., Zhou, M., & Tang, B. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.722797 · Cited by 54 · see citing works
Trip12 is an E3 ubiquitin ligase for USP 7/ HAUSP involved in the DNA damage response
Liu, X., Yang, X., Li, Y., Zhao, S., Li, C., Ma, P., & Mao, B. (2016) · FEBS Letters · doi:10.1002/1873-3468.12471 · Cited by 49 · see citing works
Ataxin-3 promotes genome integrity by stabilizing Chk1
Tu, Y., Liu, H., Zhu, X., Shen, H., Ma, X., Wang, F., Huang, M., Gong, J., Li, X., Wang, Y., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx095 · Cited by 53 · see citing works
Lu, H., Yuan, P., Ma, X., Jiang, X., Liu, S., Ma, C., Philipsen, S., Zhang, Q., Yang, J., Xu, F., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36409-z · Cited by 45 · see citing works
Wang, Y., Chen, H., Liu, W., Yan, H., Zhang, Y., Cheung, A. H. K., Zhang, J., Chen, B., Li, L., Zhou, Z., et al. (2022) · Theranostics · doi:10.7150/thno.75431 · Cited by 44 · see citing works
Deubiquitylation of deubiquitylases
Haq, S., & Ramakrishna, S. (2017) · Open Biology · doi:10.1098/rsob.170016 · Cited by 42 · see citing works
Basal CHK1 activity safeguards its stability to maintain intrinsic S-phase checkpoint functions
Michelena, J., Gatti, M., Teloni, F., Imhof, R., & Altmeyer, M. (2019) · The Journal of Cell Biology · doi:10.1083/jcb.201902085 · Cited by 41 · see citing works
Qiu, G., Sun, W., Jin, M., Lin, J., Lu, P., & Jin, W. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.12.003 · Cited by 39 · see citing works
Inhibition of ubiquitin-specific protease 7 sensitizes acute myeloid leukemia to chemotherapy
Cartel, M., Mouchel, P., Gotanègre, M., David, L., Bertoli, S., Mas, V. M., Besson, A., Sarry, J., Manenti, S., & Didier, C. (2020) · Leukemia · doi:10.1038/s41375-020-0878-x · Cited by 41 · see citing works
ATR inhibition rewires cellular signaling networks induced by replication stress
Wagner, S., Oehler, H., Voigt, A., Dalic, D., Freiwald, A., Serve, H. L., & Beli, P. (2015) · PROTEOMICS · doi:10.1002/pmic.201500172 · Cited by 38 · see citing works
Deubiquitylase USP7 regulates human terminal erythroid differentiation by stabilizing GATA1
Liang, L., Peng, Y., Zhang, J., Zhang, Y., Roy, M., Han, X., Xiao, X., Sun, S., Liu, H., Nie, L., et al. (2019) · Haematologica · doi:10.3324/haematol.2018.206227 · Cited by 37 · see citing works
Targeting ubiquitin specific protease 7 in cancer: A deubiquitinase with great prospects
Khusbu, F. Y., Chen, F., & Chen, H. (2018) · Cell Biochemistry and Function · doi:10.1002/cbf.3336 · Cited by 36 · see citing works
USP7 Regulates Cytokinesis through FBXO38 and KIF20B
Georges, A. A., Coyaud, É., Marcon, E., Greenblatt, J. F., Raught, B., & Frappier, L. (2019) · Scientific Reports · doi:10.1038/s41598-019-39368-y · Cited by 38 · see citing works
Roles of Ubiquitination and SUMOylation in DNA Damage Response
Su, S., Zhang, Y., & Liu, P. (2019) · Current Issues in Molecular Biology · doi:10.21775/cimb.035.059 · Cited by 34 · see citing works
USP7 manipulation by viral proteins
Bojagora, A., & Saridakis, V. (2020) · Virus Research · doi:10.1016/j.virusres.2020.198076 · Cited by 33 · see citing works
Ito, F., Yoshimoto, C., Yamada, Y., Sudo, T., & Kobayashi, H. (2018) · Oncotarget · doi:10.18632/oncotarget.24776 · Cited by 32 · see citing works
Ubiquitination of the DNA-damage checkpoint kinase CHK1 by TRAF4 is required for CHK1 activation
Yu, X., Li, W., Liu, H., Deng, Q., Wang, X., Hu, H., Xu-Monette, Z. Y., Xiong, W., Lu, Z., Young, K. H., et al. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00869-3 · Cited by 30 · see citing works
Termination of DNA replication forks: “Breaking up is hard to do”
Bailey, R., Moreno, S. P., & Gambus, A. (2015) · Nucleus · doi:10.1080/19491034.2015.1035843 · Cited by 26 · see citing works
Saha, S., Verma, R., Kumar, C., Kumar, B., Dey, A. K., Surjit, M., Mylavarapu, S. V. S., & Maiti, T. K. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-05003-4 · Cited by 22 · see citing works
Zhou, L., Ouyang, T., Li, M., Hong, T., Alriashy, M. H. S., Meng, W., & Zhang, N. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.784672 · Cited by 23 · see citing works
Liu, J., Zhou, T., Dong, X. D., Guo, Q., Zheng, L., Wang, X., Zhang, N., Li, D., Ren, L., Yi, F., et al. (2023) · Oncogene · doi:10.1038/s41388-023-02667-w · Cited by 23 · see citing works
ATXN3: a multifunctional protein involved in the polyglutamine disease spinocerebellar ataxia type 3
Hernández-Carralero, E., Quinet, G., & Freire, R. (2024) · Expert Reviews in Molecular Medicine · doi:10.1017/erm.2024.10 · Cited by 21 · see citing works
Stromberg, B. R., Singh, M. K., Torres, A. E., Burrows, A. C., Pal, D., Insinna, C., Rhee, Y., Dickson, A. S., Westlake, C. J., & Summers, M. K. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.101184 · Cited by 19 · see citing works
Activation of ATR-Chk1 pathway facilitates EBV-mediated transformation of primary tonsillar B-cells
Mordasini, V., Ueda, S., Aslandogmus, R., Berger, C., Gysin, C., Hühn, D., Sartori, A. A., Bernasconi, M., & Nadal, D. (2016) · Oncotarget · doi:10.18632/oncotarget.14120 · Cited by 19 · see citing works
DNA Polymerase ι Interacts with Both the TRAF-like and UBL1-2 Domains of USP7
Ashton, N. W., Valles, G. J., Jaiswal, N., Bezsonova, I., & Woodgate, R. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.166733 · Cited by 18 · see citing works
USP7/HAUSP: A SUMO deubiquitinase at the heart of DNA replication
Smits, V. A. J., & Freire, R. (2016) · BioEssays · doi:10.1002/bies.201600096 · Cited by 18 · see citing works
Self-citationA feedforward circuit shaped by ECT2 and USP7 contributes to breast carcinogenesis
Zhang, Q., Cao, C., Gong, W., Bao, K., Wang, Q., Wang, Y., Bi, L., Ma, S., Zhao, J., Liu, L., et al. (2020) · Theranostics · doi:10.7150/thno.46878 · Cited by 18 · see citing works
USP7 promotes temozolomide resistance by stabilizing MGMT in glioblastoma
Li, J., Feng, X., Liu, Z., Deng, Y., Sun, Z., Chen, B., Wu, L., Wang, X., Miao, L., Zeng, L., et al. (2025) · Cell Death and Disease · doi:10.1038/s41419-025-07969-3 · Cited by 17 · see citing works
Gagarina, V., Bojagora, A., Lacdao, I. K., Luthra, N., Pfoh, R., Mohseni, S., Chaharlangi, D., Tan, N., & Saridakis, V. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.12.026 · Cited by 17 · see citing works
Deubiquitinating Enzyme-Mediated Signaling Networks in Cancer Stem Cells
Kaushal, K., & Ramakrishna, S. (2020) · Cancers · doi:10.3390/cancers12113253 · Cited by 18 · see citing works
Status and role of the ubiquitin–proteasome system in renal fibrosis
Chen, Y., Dai, R., Cheng, M., Wang, W., Liu, C., Cao, Z., Ge, Y., Wang, Y., & Zhang, L. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.117210 · Cited by 16 · see citing works
Guo, L., Dong, Z., Zhang, X., Yang, Y., Hu, X., Ji, Y., Li, C., Wan, S., Xu, J., Liu, C., et al. (2023) · Phytomedicine · doi:10.1016/j.phymed.2023.154765 · Cited by 15 · see citing works
Yuan, Y., Miao, Y., Zeng, C.-H., Liu, J., Chen, X., Qian, L., Wang, X., Feng, Q., Yu, Z., Wang, J., et al. (2019) · Immunology · doi:10.1111/imm.13147 · Cited by 15 · see citing works
SCML2 contributes to tumor cell resistance to DNA damage through regulating p53 and CHK1 stability
Peng, Q., Shi, X., Li, D., Guo, J., Zhang, X., Zhang, X., & Chen, Q. (2023) · Cell Death and Differentiation · doi:10.1038/s41418-023-01184-3 · Cited by 13 · see citing works
Shi, S., Pan, X., Chen, M., Zhang, L., Zhang, S., Wang, X., Shi, S., Chen, Z., Lin, W., & Jiang, Y. (2023) · Hepatology Communications · doi:10.1097/hc9.0000000000000193 · Cited by 13 · see citing works
Shao, Y., Zhang, W., Du, D., Yu, Y., Li, Q., & Peng, X. (2022) · Aging · doi:10.18632/aging.204301 · Cited by 11 · see citing works
Dall’Osto, M., Pierini, L., Valery, N., Hoffmann, J., & Pillaire, M. (2021) · Molecular and Cellular Biology · doi:10.1128/mcb.00090-21 · Cited by 9 · see citing works
Zhu, Y., Zhang, Q., Yan, X., Liu, L., Zhai, C., Wang, Q., Chai, L., & Li, M. (2021) · Pulmonary Circulation · doi:10.1177/20458940211046131 · Cited by 9 · see citing works
USP35 dimer prevents its degradation by E3 ligase CHIP through auto-deubiquitinating activity
Park, J., Shin, S. C., Jin, K. S., Lim, M. J., Kim, Y., Kim, E. E., & Song, E. J. (2023) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-023-04740-9 · Cited by 8 · see citing works
Tu, Y., Li, X., Zhu, X., Liu, X., Guo, C., Jia, D., & Tang, T.-S. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.619911 · Cited by 7 · see citing works
TAOK1 promotes filament formation in HR repair through phosphorylating USP7
Zhu, T.-C., He, Z., Li, S.-T., Zheng, L., Zheng, X.-Y., Lan, X., Qu, C., Nie, R., Gu, C., Huang, L.-N., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2422262122 · Cited by 6 · see citing works
USP7 at the Crossroads of Ubiquitin Signaling, Cell Cycle, and Tumorigenesis
Lusardi, M., Rapetti, F., Spallarossa, A., Massone, M., Cichero, E., & Brullo, C. (2025) · Molecules · doi:10.3390/molecules30204038 · Cited by 6 · see citing works
Regulation of CHK1 by the Ubiquitin–Proteasome System
Cartel, M., & Didier, C. (2020) · FEBS Journal · doi:10.1111/febs.15173 · Cited by 5 · see citing works
Pawlak, A., Bajzert, J., Bugiel-Stabla, K., Suárez, B. H., Kutkowska, J., Rapak, A., Hildebrand, W., Obmińska‐Mrukowicz, B., Freire, R., & Smits, V. A. J. (2021) · Journal of Veterinary Internal Medicine · doi:10.1111/jvim.16082 · Cited by 6 · see citing works
Self-citationThe post translational modification of key regulators of ATR signaling in DNA replication
Chen, Y., & Yuan, J. (2021) · Genome Instability & Disease · doi:10.1007/s42764-021-00036-z · Cited by 6 · see citing works
Li, L., Wang, L., Liu, D., & Zhao, Y. (2023) · Cell Death Discovery · doi:10.1038/s41420-023-01611-x · Cited by 5 · see citing works
Hu, Y., Rosado, D., Norén, L., Micko, J., & Pedmale, U. V. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.15.524001 · Cited by 5 · see citing works
USP7 Deregulation Impairs S Phase Specific DNA Repair after Irradiation in Breast Cancer Cells
Vogt, M., Classen, S., Krause, A. K., Peter, N.-J., Petersen, C., Rothkamm, K., Borgmann, K., & Meyer, F. B. (2024) · Biomedicines · doi:10.3390/biomedicines12040762 · Cited by 4 · see citing works
Targeting the Ubiquitin Proteasome System in Cancer
Kumari, N., Lee, K. K., & Jha, S. (2018) · InTech eBooks · doi:10.5772/intechopen.76705 · Cited by 4 · see citing works
Ubiquitin-specific proteases as targets for anticancer drug therapies
Campos-Iglesias, D., López-Otı́n, C., & Freije, J. M. P. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-818168-3.00004-8 · Cited by 3 · see citing works
Huang, M. R., Yang, Z., Wang, S., Ge, Y., Lin, L., Alfajaro, M. M., Filler, R. B., Song, W., Kong, M., & Wei, J. (2026) · Advanced Science · doi:10.1002/advs.202518058 · Cited by 2 · see citing works
Recent Progress of Ubiquitin-Specific-Processing Protease 7 Inhibitors
Chi, L., Wang, H., Yu, F., Gao, C., Dai, H., Si, X., Liu, L., Wang, Z., Zheng, J.-H., Ke, Y., et al. (2023) · Russian Journal of Bioorganic Chemistry · doi:10.1134/s1068162023020073 · Cited by 2 · see citing works
Functional Relevance of Deubiquitinases in Life and Disease
Fraile, J. M., López-Otı́n, C., & Freije, J. M. P. (2017) · Springer eBooks · doi:10.1007/978-981-10-2513-6_16 · Cited by 1 · see citing works
Pal, D., & Summers, M. K. (2018) · InTech eBooks · doi:10.5772/intechopen.70482 · Cited by 1 · see citing works
Pozhidaeva, A. (2016) · OpenCommons at University of Connecticut (University of Connecticut)
USP9X controls DNA replication fork stability and the replication stress checkpoint through Claspin
McGarry, E. (2016) · Arrow@dit (Dublin Institute of Technology) · doi:10.13025/17576
The Role of Deubiquitinases in DNA Double-Strand Break Repair
Lu, J. L., Xi, Z., Huang, X., Xia, Q., & Long, X. (2018) · InTech eBooks · doi:10.5772/intechopen.73341
P22077 enhances the antitumor efficacy of Cisplatin and its mechanism
Qiu, J., Ren, Q., Wang, Y., Xie, Q.-L., Liu, Y., Yu, P., Wang, H., & Tian, J. (2022) · Journal of Pharmaceutical and Biopharmaceutical Research · doi:10.25082/jpbr.2021.02.002
Pandya, M. J., Augustyniak, W., Cliff, M. J., Lindner, I., Stinn, A., Kahmann, J. D., Temmerman, K., Dannatt, H. R. W., Waltho, J. P., & Watson, M. J. (2024) · Biomolecular NMR Assignments · doi:10.1007/s12104-024-10165-7
Usp7 contributes to the tail regeneration of planarians via Islet/Wnt1 axis
Liang, A., Liu, J., Zhang, Z., Xiao, J., Liu, D., Dong, Z., & Chen, G. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-06134-w
Reber, V., Keller, S., Loosli, S. A., Arima, Y., Kleele, T., Picotti, P., & Gstaiger, M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.06.687012
Fonctions et régulations de la kinase CHK1 dans l'hématopoïèse normale et leucémique
Cartel, M. (2019) · theses.fr (ABES) · doi:10.70675/7824b06fz5467z4c2cz89c1zf5bed2a53f34
PCNA-Polκ-Polδ/USP18 axes stabilize replication fork and restart to reduce cisplatin cytotoxicityPreprint
Subhadarsini, I., Sahu, J. K., Thakur, S., Dash, R., & Acharya, N. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.08.730955
Reber, V., Keller, S., Loosli, S. A., Arima, Y., Kleele, T., Picotti, P., & Gstaiger, M. (2026) · Molecular Systems Biology · doi:10.1038/s44320-026-00229-2
PCNA-Polκ-Polδ/USP18 axes stabilize replication fork and restart to reduce cisplatin cytotoxicityPreprint
Subhadarsini, I., Sahu, J. K., Thakur, S., Dash, R., & Acharya, N. (2026) · eLife · doi:10.7554/elife.112155.1
PCNA-Polκ-Polδ/USP18 axes stabilize replication fork and restart to reduce cisplatin cytotoxicityPreprint
Subhadarsini, I., Sahu, J. K., Thakur, S., Dash, R., & Acharya, N. (2026) · eLife · doi:10.7554/elife.112155
- Authors
- Alonso-de Vega, I., Martín, Y., & Smits, V. A.
- Affiliations
- Unidad de Investigación; Hospital Universitario de Canarias; Instituto de Tecnologías Biomédicas; Tenerife, Spain
- Hospital Universitario de Canarias (ES)
- Corresponding author
- Smits, Veronique Aj
- ORCID
- Smits, Veronique Aj
- Venue
- Cell Cycle
- Publisher
- Informa UK Limited
- Published
- 2014-12-15
- Volume
- 13
- Issue
- 24
- Pages
- 3921-3926
- ISSN
- 1538-4101 (ISSN-L)
- 1551-4005
- PMC
- PMC4614819
- OpenAlex
- W1977805567
- Cited by
- 92
- References
- 27
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 5 · 2023: 11 · 2022: 5 · 2021: 8 · 2020: 12 · 2019: 10 · 2018: 7 · 2017: 8 · 2016: 13 · 2015: 3
- FWCI
- 3.28
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cell Cycle (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Keywords
- USP7, Chk1, deubiquitination, protein stability, DNA damage response, ATR-Chk1 pathway, Claspin, ubiquitin hydrolase, proteasomal degradation, checkpoint kinase
- MeSH terms
- Checkpoint Kinase 1, Ubiquitin-Specific Peptidase 7, Humans, Protein Kinases, Tumor Suppressor Protein p53, Ubiquitin Thiolesterase, Cell Line, Tumor, Adaptor Proteins, Signal Transducing, Proto-Oncogene Proteins c-mdm2, Ubiquitination, Protein Stability, HEK293 Cells, Ataxia Telangiectasia Mutated Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
