A role for USP7 in DNA replication.
Open accessAbstract
The minichromosome maintenance (MCM) complex, which plays multiple important roles in DNA replication, is loaded onto chromatin following mitosis, remains on chromatin until the completion of DNA synthesis, and then is unloaded by a poorly defined mechanism that involves the MCM binding protein (MCM-BP). Here we show that MCM-BP directly interacts with the ubiquitin-specific protease USP7, that this interaction occurs predominantly on chromatin, and that MCM-BP can tether USP7 to MCM proteins. Detailed biochemical and structure analyses of the USP7-MCM-BP interaction showed that the (155)PSTS(158) MCM-BP sequence mediates critical interactions with the TRAF domain binding pocket of USP7. Analysis of the effects of USP7 knockout on DNA replication revealed that lack of USP7 results in slowed progression through late S phase without globally affecting the fork rate or origin usage. Lack of USP7 also resulted in increased levels of MCM proteins on chromatin, and investigation of the cause of this increase revealed a defect in the dissociation of MCM proteins from chromatin in mid- to late S phase. This role of USP7 mirrors the previously described role for MCM-BP in MCM complex unloading and suggests that USP7 works with MCM-BP to unload MCM complexes from chromatin at the end of S phase.
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USP7 TRAF-like domain substrates include p53, Mdm2, Mdm4, and MCM-BP.
“These substrates include the tumor suppressor p53 (Hu et al., 2006; Sheng et al., 2006), the Mdm2 E3 ubiquitin ligase (Hu et al., 2006; Sheng et al., 2006; Sarkari et al., 2010), the Mdm2 homolog Mdm4 (Sarkari et al., 2010) and mini-chromosome maintenance binding-protein MCM-BP (Jagannathan et al., 2014; Figure 1 and Table 1).”
From USP7 Is a Master Regulator of Genome Stability (2020) · cites this paper as Jagannathan et al., 2014
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[20] Processing of X-ray diffraction data collected in oscillation mode
Otwinowski, Z., & Minor, W. (1997) · Methods in Enzymology · doi:10.1016/s0076-6879(97)76066-x · Cited by 33,475 · see citing works
Systematic and Quantitative Assessment of the Ubiquitin-Modified Proteome
Kim, W., Bennett, E. J., Huttlin, E. L., Guo, A., Li, J., Possemato, A. P., Sowa, M. E., Rad, R., Rush, A. J., Comb, M. J., et al. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.08.025 · Cited by 1,582 · see citing works
Defining the Human Deubiquitinating Enzyme Interaction Landscape
Sowa, M. E., Bennett, E. J., Gygi, S. P., & Harper, J. W. (2009) · Cell · doi:10.1016/j.cell.2009.04.042 · Cited by 1,512 · see citing works
Version 1.2 of the Crystallography and NMR system
Brünger, A. T. (2007) · Nature Protocols · doi:10.1038/nprot.2007.406 · Cited by 1,335 · 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
Ubiquitination regulates PTEN nuclear import and tumor suppression
Trotman, L. C., Wang, X., Alimonti, A., Chen, Z., Teruya-Feldstein, J., Yang, H., Pavletich, N. P., Carver, B. S., Cordon-Cardo, C., Erdjument-Bromage, H., et al. (2007) · Cell · doi:10.1016/j.cell.2006.11.040 · Cited by 748 · see citing works
A dynamic role of HAUSP in the p53-Mdm2 pathway
Li, M., Brooks, C. L., Kon, N., & Gu, W. (2004) · Molecular Cell · doi:10.1016/s1097-2765(04)00157-1 · Cited by 679 · see citing works
Dormant origins licensed by excess Mcm2–7 are required for human cells to survive replicative stressPreprint
Ge, X. Q., Jackson, D. A., & Blow, J. J. (2007) · Genes & Development · doi:10.1101/gad.457807 · Cited by 605 · see citing works
Activation of the MCM2-7 Helicase by Association with Cdc45 and GINS proteins
Ilves, I., Petojevic, T., Pesavento, J. J., & Botchan, M. (2010) · Molecules and Cells · doi:10.1016/j.molcel.2009.12.030 · Cited by 593 · see citing works
Zegerman, P., & Diffley, J. (2007) · Nature · doi:10.1038/nature05432 · Cited by 555 · see citing works
A DNA Helicase Activity Is Associated with an MCM4, -6, and -7 Protein Complex
Ishimi, Y. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.39.24508 · Cited by 538 · see citing works
[10] Electron-density map interpretation
Jones, T. A., & Kjeldgaard, M. (1997) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(97)77012-5 · Cited by 507 · see citing works
Ibarra, A., Schwob, É., & Méndez, J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803978105 · Cited by 505 · see citing works
Cdc6p-dependent loading of Mcm proteins onto pre-replicative chromatin in budding yeast
Donovan, S., Harwood, J. C., Drury, L. S., & Diffley, J. F. X. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.11.5611 · Cited by 495 · see citing works
Everett, R. D., Meredith, M., Orr, A., Cross, A., Kathoria, M., & Parkinson, J. (1997) · The EMBO Journal · doi:10.1093/emboj/16.7.1519 · Cited by 491 · 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
Ivessa, A., Lenzmeier, B. A., Bessler, J. B., Goudsouzian, L. K., Schnakenberg, S. L., & Zakian, V. A. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00456-8 · Cited by 407 · see citing works
Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cellsPreprint
Arias, E. E., & Walter, J. C. (2007) · Genes & Development · doi:10.1101/gad.1508907 · Cited by 405 · see citing works
Disruption of HAUSP gene stabilizes p53.
Cummins, J. M., Rago, C., Kohli, M., Kinzler, K. W., Lengauer, C., & Vogelstein, B. (2004) · Nature · doi:10.1038/nature02501 · Cited by 379 · see citing works
Woodward, A. M., Göhler, T., Luciani, M. G., Oehlmann, M., Ge, X., Gartner, A., Jackson, D. A., & Blow, J. J. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200602108 · Cited by 369 · see citing works
Structure of the p53 Binding Domain of HAUSP/USP7 Bound to Epstein-Barr Nuclear Antigen 1
Saridakis, V., Sheng, Y., Sarkari, F., Holowaty, M. N., Shire, K., Nguyen, T., Zhang, R. G., Liao, J. C. C., Lee, W., Edwards, A. M., et al. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.02.029 · Cited by 362 · see citing works
Self-citationThe Mcm Complex: Unwinding the Mechanism of a Replicative Helicase
Bochman, M. L., & Schwacha, A. (2009) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00019-09 · Cited by 330 · see citing works
The Dbf4–Cdc7 kinase promotes S phase by alleviating an inhibitory activity in Mcm4
Sheu, Y.-J., & Stillman, B. (2010) · Nature · doi:10.1038/nature08647 · Cited by 324 · see citing works
The structural basis for MCM2–7 helicase activation by GINS and Cdc45
Costa, A., Ilves, I., Tamberg, N., Petojevic, T., Nogales, E., Botchan, M. R., & Berger, J. M. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2004 · Cited by 316 · see citing works
Molecular recognition of p53 and MDM2 by USP7/HAUSP.
Sheng, Y., Saridakis, V., Sarkari, F., Duan, S., Wu, T., Arrowsmith, C. H., & Frappier, L. (2006) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1067 · Cited by 315 · see citing works
Self-citationEdwards, M. C., Tutter, A. V., Cvetic, C., Gilbert, C. H., Prokhorova, T. A., & Walter, J. C. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204438200 · Cited by 269 · see citing works
Meulmeester, E., Maurice, M. M., Boutell, C., Teunisse, A. F. A. S., Ovaa, H., Abraham, T. E., Dirks, R. W., & Jochemsen, A. G. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.04.024 · Cited by 260 · see citing works
GMP Synthetase Stimulates Histone H2B Deubiquitylation by the Epigenetic Silencer USP7
van der Knaap, J. A., Kumar, B. R. P., Moshkin, Y. M., Langenberg, K. P. S., Krijgsveld, J., Heck, A. J. R., Karch, F., & Verrijzer, C. P. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.02.013 · Cited by 258 · see citing works
Faesen, A. C., Dirac, A. M. G., Shanmugham, A., Ovaa, H., Anastassis Perrakis, A., & Sixma, T. K. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.06.034 · Cited by 251 · 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
Interaction between the Origin Recognition Complex and the Replication Licensing Systemin Xenopus
Rowles, A., Chong, J. P. J., Brown, L., Howell, M., Evan, G. I., & Blow, J. J. (1996) · Cell · doi:10.1016/s0092-8674(00)81346-x · Cited by 248 · 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
Critical role for Daxx in regulating Mdm2
Tang, J., Qu, L., Zhang, J., Wang, W., Michaelson, J. S., Degenhardt, Y., El‐Deiry, W. S., & Yang, X. (2006) · Nature Cell Biology · doi:10.1038/ncb1442 · Cited by 239 · see citing works
Conti, C., Saccà, B., Herrick, J., Lalou, C., Pommier, Y. G., & Bensimon, A. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-08-0689 · Cited by 236 · see citing works
Holowaty, M. N., Zeghouf, M., Wu, H., Tellam, J., Athanasopoulos, V., Greenblatt, J., & Frappier, L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303977200 · Cited by 228 · see citing works
Self-citationProtein Interaction Domains of the Ubiquitin-specific Protease, USP7/HAUSP
Holowaty, M. N., Sheng, Y., Nguyen, T., Arrowsmith, C. H., & Frappier, L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m307200200 · Cited by 182 · see citing works
Self-citationRegulation of Replicon Size in Xenopus Egg Extracts
Walter, J. C., & Newport, J. W. (1997) · Science · doi:10.1126/science.275.5302.993 · Cited by 176 · see citing works
Lei, M., Kawasaki, Y., & Tye, B. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.9.5081 · Cited by 175 · see citing works
Cell Cycle Regulation of the Replication Licensing System: Involvement of a Cdk-dependent Inhibitor
Mahbubani, H. M., Chong, J. P. J., Chevalier, S., Thommes, P. A., & Blow, J. J. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.136.1.125 · Cited by 163 · see citing works
Interactions of human nuclear proteins P1Mcm3 and P1Cdc46.
Burkhart, R., Schulte, D., Hu, D., Musahl, C., Göhring, F., & Knippers, R. (1995) · PubMed · Cited by 132 · see citing works
A Role for H2B Ubiquitylation in DNA Replication
Trujillo, K. M., & Osley, M. A. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.09.019 · Cited by 128 · see citing works
Sarkari, F., Sanchez-Alcaraz, T., Wang, S., Holowaty, M. N., Sheng, Y., & Frappier, L. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000624 · Cited by 115 · see citing works
Self-citationSabouri, N., McDonald, K. R., Webb, C. J., Cristea, I., & Zakian, V. (2012) · Genes & Development · doi:10.1101/gad.184697.111 · Cited by 108 · see citing works
Interactions of Human Nuclear Proteins P1Mcm3 and P1Cdc46
Burkhart, R., Schulte, D., Hu, B., Musahl, C., Göhring, F., & Knippers, R. (1995) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1995.tb20281.x · Cited by 104 · see citing works
The DNA replication checkpoint aids survival of plants deficient in the novel replisome factor ETG1
Takahashi, N., Lammens, T., Boudolf, V., Maes, S., Yoshizumi, T., Jaeger, G. D., Witters, E., Inzé, D., & Veylder, L. D. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.107 · Cited by 94 · see citing works
Control of chromosomal DNA replication in the early Xenopus embryo
Blow, J. J. (2001) · The EMBO Journal · doi:10.1093/emboj/20.13.3293 · Cited by 86 · see citing works
Activation of the replicative DNA helicase: breaking up is hard to do
Boos, D., Frigola, J., & Diffley, J. F. X. (2012) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2012.01.011 · Cited by 85 · see citing works
Bilateral inhibition of HAUSP deubiquitinase by a viral interferon regulatory factor protein
Lee, H.-R., Choi, W., Lee, S., Hwang, J., Hwang, E., Guchhait, K., Haas, J., Tóth, Z., Jeon, Y. H., Oh, T.-K., et al. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2142 · Cited by 81 · see citing works
Salsman, J., Jagannathan, M., Paladino, P., Chan, P.-K., Dellaire, G., Raught, B., & Frappier, L. (2011) · Journal of Virology · doi:10.1128/jvi.05442-11 · Cited by 73 · see citing works
Self-citationTakahashi, N., Quimbaya, M., Schubert, V., Lammens, T., Vandepoele, K., Schubert, I. A., Matsui, M., Inzé, D., Berx, G., & Veylder, L. D. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000817 · Cited by 71 · see citing works
Defining replication origin efficiency using DNA fiber assays
Tuduri, S., Tourrière, H., & Pasero, P. (2009) · Chromosome Research · doi:10.1007/s10577-009-9098-y · Cited by 67 · see citing works
Sakwe, A. M., Nguyen, T., Athanasopoulos, V., Shire, K., & Frappier, L. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02384-06 · Cited by 67 · see citing works
Self-citationMCM-BP regulates unloading of the MCM2–7 helicase in late S phasePreprint
Nishiyama, A., Frappier, L., & Méchali, M. (2010) · Genes & Development · doi:10.1101/gad.614411 · Cited by 66 · see citing works
Self-citationJäger, W., Santag, S., Weidner-Glunde, M., Gellermann, E., Kati, S., Pietrek, M., Viejo‐Borbolla, A., & Schulz, T. F. (2012) · Journal of Virology · doi:10.1128/jvi.06840-11 · Cited by 65 · see citing works
Steinacher, R., Osman, F., Dalgaard, J. Z., Lorenz, A., & Whitby, M. C. (2012) · Genes & Development · doi:10.1101/gad.184663.111 · Cited by 65 · see citing works
The MCM complex: (just) a replicative helicase?
Costa, A., & Onesti, S. (2008) · Biochemical Society Transactions · doi:10.1042/bst0360136 · Cited by 62 · see citing works
Bochman, M. L., & Schwacha, A. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq422 · Cited by 61 · see citing works
Sarkari, F., Wang, X., Nguyen, T., & Frappier, L. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016598 · Cited by 59 · see citing works
Self-citationSarkari, F., La Delfa, A., Arrowsmith, C. H., Frappier, L., Sheng, Y., & Saridakis, V. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2010.08.017 · Cited by 54 · see citing works
Self-citationRegulation of mammalian replication origin usage in Xenopus egg extract
Dimitrova, D. S., & Gilbert, D. M. (1998) · Journal of Cell Science · doi:10.1242/jcs.111.19.2989 · Cited by 49 · see citing works
Ubiquitin-specific Protease 7 Is a Regulator of Ubiquitin-conjugating Enzyme UbE2E1
Sarkari, F., Wheaton, K., Delfa, A. L., Mohamed, M., Shaikh, F., Khatun, R., Arrowsmith, C. H., Frappier, L., Saridakis, V., & Sheng, Y. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.469262 · Cited by 47 · see citing works
Self-citationChing, W., Koyuncu, E., Singh, S. K., Arbelo-Roman, C., Härtl, B., Kremmer, E., Speiseder, T., Meier, C., & Dobner, T. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003273 · Cited by 47 · see citing works
RMI1 Promotes DNA Replication Fork Progression and Recovery from Replication Fork Stress
Yang, J., O’Donnell, L., Durocher, D., & Brown, G. W. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.00255-12 · Cited by 32 · see citing works
Self-citationThe MCM-associated protein MCM-BP is important for human nuclear morphology
Jagannathan, M., Sakwe, A. M., Nguyen, T., & Frappier, L. (2012) · Journal of Cell Science · doi:10.1242/jcs.089938 · Cited by 24 · see citing works
Self-citationDing, L., & Forsburg, S. L. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.282541 · Cited by 23 · see citing works
Santosa, V., Martha, S. A., Hirose, N., & Tanaka, K. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.432393 · Cited by 19 · see citing works
Interactions of the Human MCM-BP Protein with MCM Complex Components and Dbf4
Nguyen, T., Jagannathan, M., Shire, K., & Frappier, L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035931 · Cited by 16 · see citing works
Self-citationAntrobus, R., & Boutell, C. (2008) · Virus Research · doi:10.1016/j.virusres.2008.05.017 · Cited by 15 · see citing works
Unscheduled DNA replication origin activation at inserted HPV 18 sequences in a HPV‐18/MYC amplicon
Conti, C., Herrick, J., & Bensimon, A. (2007) · Genes Chromosomes and Cancer · doi:10.1002/gcc.20448 · Cited by 12 · see citing works
Purification and functional inactivation of the fission yeast MCMMCM-BPcomplex
Li, J., Schnick, J., Hayles, J., & MacNeill, S. A. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.10.033 · Cited by 12 · see citing works
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Cheng, A. Z., Yockteng-Melgar, J., Jarvis, M. C., Malik-Soni, N., Borozan, I., Carpenter, M. A., McCann, J. L., Ebrahimi, D., Shaban, N. M., Marcon, E., et al. (2018) · Nature Microbiology · doi:10.1038/s41564-018-0284-6 · Cited by 132 · see citing works
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Pozhidaeva, 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
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Pozhidaeva, A., Mohni, K. N., Dhe‐Paganon, S., Arrowsmith, C. H., Weller, S. K., Korzhnev, D. M., & Bezsonova, I. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.664805 · Cited by 40 · see citing works
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Galarreta, A., Valledor, P., Ubieto‐Capella, P., Lafarga, V., Zarzuela, E., Muñoz, J., Malumbres, M., Lecona, E., & Fernández-Capetillo, Ó. (2021) · The EMBO Journal · doi:10.15252/embj.201899692 · Cited by 37 · 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
Self-citationCurrent and future directions of USP7 interactome in cancer study
Park, H., & Baek, K. (2023) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2023.188992 · Cited by 35 · 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
Self-citationInsight in the multilevel regulation of NER
Dijk, M., Typas, D., Mullenders, L. H. F., & Pines, A. (2014) · Experimental Cell Research · doi:10.1016/j.yexcr.2014.08.010 · Cited by 32 · see citing works
Targeting Deubiquitinating Enzymes in Glioblastoma Multiforme: Expectations and Challenges
Jin, W., Mao, X., & Qiu, G. (2016) · Medicinal Research Reviews · doi:10.1002/med.21421 · Cited by 32 · see citing works
Tamberg, N., Tahk, S., Koit, S., Kristjuhan, K., Kasvandik, S., Kristjuhan, A., & Ilves, I. (2018) · Scientific Reports · doi:10.1038/s41598-018-30562-y · Cited by 32 · see citing works
Bimodal regulation of the PRC2 complex by USP7 underlies tumorigenesis
Su, D., Wang, W., Hou, Y., Wang, L., Yi, X., Cao, C., Wang, Y., Gao, H. F., Wang, Y., Yang, C., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab209 · Cited by 29 · 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
Czech‐Sioli, M., Siebels, S., Radau, S., Zahedi, R. P., Schmidt, C., Dobner, T., Grundhoff, A. T., & Fischer, N. (2019) · Journal of Virology · doi:10.1128/jvi.01638-19 · 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
LRR1-mediated replisome disassembly promotes DNA replication by recycling replisome components
Fan, Y., Köberlin, M. S., Ratnayeke, N., Liu, C., Deshpande, M., Gerhardt, J., & Meyer, T. (2021) · Journal of Cell Biology · doi:10.1083/jcb.202009147 · Cited by 23 · see citing works
Independent functions of DNMT1 and USP7 at replication foci
Yarychkivska, O., Tavana, O., Gu, W. J., & Bestor, T. H. (2018) · Epigenetics & Chromatin · doi:10.1186/s13072-018-0179-z · Cited by 22 · see citing works
Termination of Eukaryotic Replication Forks
Gambus, A. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-6955-0_8 · Cited by 21 · 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
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
Self-citationThe termination of UHRF1-dependent PAF15 ubiquitin signaling is regulated by USP7 and ATAD5
Miyashita, R., Nishiyama, A., Qin, W., Chiba, Y., Kori, S., Kato, N., Konishi, C., Kumamoto, S., Kozuka‐Hata, H., Oyama, M., et al. (2023) · eLife · doi:10.7554/elife.79013 · Cited by 15 · see citing works
Zhang, M.-J., Chen, D.-S., Li, H., Liu, W., Han, G., & Han, Y. (2019) · Europe PMC (PubMed Central) · Cited by 15 · see citing works
A SUMO and ubiquitin code coordinates protein traffic at replication factories
Lecona, E., & Fernández-Capetillo, Ó. (2016) · BioEssays · doi:10.1002/bies.201600129 · Cited by 16 · see citing works
Adhami, H. A., Vallet, J., Schaal, C., Schumacher, P., Bardet, A. F., Dumas, M., Chicher, J., Hammann, P., Daujat, S., & Weber, M. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad071 · Cited by 15 · see citing works
Epstein-Barr Virus BGLF2 commandeers RISC to interfere with cellular miRNA function
Campbell, A. M., de la Cruz-Herrera, C. F., Marcon, E., Greenblatt, J. F., & Frappier, L. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010235 · Cited by 15 · see citing works
Self-citationThe MCM2-7 Complex: Roles beyond DNA Unwinding
Rankin, B. D., & Rankin, S. (2024) · Biology · doi:10.3390/biology13040258 · Cited by 14 · see citing works
G 1 /S Cell Cycle Induction by Epstein-Barr Virus BORF2 Is Mediated by P53 and APOBEC3B
Yockteng-Melgar, J., Shire, K., Cheng, A. Z., Malik-Soni, N., Harris, R. S., & Frappier, L. (2022) · Journal of Virology · doi:10.1128/jvi.00660-22 · Cited by 13 · see citing works
Self-citationUSP7 Inhibitors Destabilize EBNA1 and Suppress Epstein‐Barr Virus Tumorigenesis
Chen, C., Addepalli, K., Soldan, S. S., Castro-Muñoz, L. J., Preston‐Alp, S., Patel, R. J., Albitz, C. J., Tang, H., Tempera, I., & Lieberman, P. M. (2025) · Journal of Medical Virology · doi:10.1002/jmv.70168 · Cited by 13 · see citing works
Coordinating DNA Replication and Mitosis through Ubiquitin/SUMO and CDK1
Galarreta, A., Valledor, P., Fernández-Capetillo, Ó., & Lecona, E. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22168796 · Cited by 10 · see citing works
The role of USP7 in the Shoc2-ERK1/2 signaling axis and Noonan-like syndrome with loose anagen hair
Wilson, P. G., Abdelmoti, L. G., Norcross, R. G., Jang, E. R., Palayam, M., & Galperin, E. (2021) · Journal of Cell Science · doi:10.1242/jcs.258922 · Cited by 9 · see citing works
Nucleosomes specify co-factor access to p53
Chakraborty, D., Sandate, C. R., Isbel, L., Kempf, G., Weiss, J., Cavadini, S., Kater, L., Seebacher, J., Kozicka, Z., Stoos, L., et al. (2025) · Molecular Cell · doi:10.1016/j.molcel.2025.06.027 · 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
Wang, S., Tian, X., Zhong, Y., Xie, X., Gao, M., Zhang, C., Cheng, X., Qi, Y., Zhong, B., Feng, P., et al. (2025) · PLoS Pathogens · doi:10.1371/journal.ppat.1013052 · Cited by 5 · see citing works
Korchak, E. J., Sharafi, M., Maisonet, I. J., Salazar‐Chaparro, A. F., Semenova, I. V., Khan, H., O’Neil, A., Caro, P., Schaaf, C. P., Buhrlage, S. J., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2510252122 · 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
USP7 couples DNA replication termination to mitotic entryPreprint
Galarreta, A., Lecona, E., Valledor, P., Ubieto‐Capella, P., Lafarga, V., Specks, J., & Fernández-Capetillo, Ó. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/305318 · Cited by 4 · see citing works
Targeting the USP7-CDK1 axis suppresses estrogen receptor-positive breast cancer progression
Lin, J., Lin, Y., Hsu, K., Liu, Y.-E., Chen, Y.-C., Yeh, Y.-L., Huang, H.-Y., Hsieh, C., Chen, D., & Wu, H. (2025) · Cancer Cell International · doi:10.1186/s12935-025-03693-2 · Cited by 3 · see citing works
Research progress of DUB enzyme in breast cancer
Tang, W., Li, N., & Lai, J. (2025) · Clinical and Experimental Medicine · doi:10.1007/s10238-025-01878-7 · Cited by 3 · 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
Shen, X., Wang, R., Su, F., Guo, J., Zhao, D. L., Yuan, F., Zhang, T., & Hou, X. (2026) · PeerJ · doi:10.7717/peerj.20702 · Cited by 1 · see citing works
Lim, D., Park, J.-W., Shin, H.-C., Kim, S. J., & Ku, B. (2026) · The Journal of Microbiology · doi:10.71150/jm.2511009 · Cited by 1 · see citing works
Chen, S., Wang, M., Zeng, Y., Li, X., Zhong, H., Liu, Y., Tao, Y., Yang, X., Luo, C., Chen, S., et al. (2026) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2026.118857 · Cited by 2 · see citing works
TRIP12 governs DNA Polymerase β involvement in DNA damage response and repairPreprint
Inanç, B., Fang, Q., Andrews, J., Zeng, X., Clark, J., Li, J., Dey, N. B., Ibrahim, M., Sykora, P., Yu, Z., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.08.588474 · Cited by 1 · see citing works
Korchak, E. J., Soriano, G., Semenova, I., Hao, B., Štepihar, D., Bayat, T., Tacer, K. F., & Bezsonova, I. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.24.720667 · Cited by 1 · see citing works
Pozhidaeva, A. (2016) · OpenCommons at University of Connecticut (University of Connecticut)
Asthana, S., Srivast, M., & Mathur, R. (2023) · Research Square · doi:10.21203/rs.3.rs-2801152/v1
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
Ashurov, L. (2014) · YorkSpace (York University)
Fonctions et régulations de la kinase CHK1 dans l'hématopoïèse normale et leucémique
Cartel, M. (2019) · theses.fr (ABES) · doi:10.70675/7824b06fz5467z4c2cz89c1zf5bed2a53f34
Host Ubiquitin-Specific Proteases Regulate All Stages of Herpesvirus Infection
Maarouf, M., Peterson, C. S., & Mohni, K. N. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27219631
- Authors
- Jagannathan, M., Nguyen, T., Gallo, D., Luthra, N., Brown, G. W., Saridakis, V., & Frappier, L.
- Affiliations
- University of Toronto (CA)
- York University (CA)
- Venue
- Molecular and Cellular Biology
- Publisher
- Informa UK Limited
- Published
- 2014-01-01
- Volume
- 34
- Issue
- 1
- Pages
- 132-145
- ISSN
- 0270-7306 (ISSN-L)
- 1098-5549
- PMC
- PMC3911275
- OpenAlex
- W2135682361
- Cited by
- 71
- References
- 70
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 3 · 2023: 5 · 2022: 4 · 2021: 7 · 2020: 4 · 2019: 7 · 2018: 8 · 2017: 4 · 2016: 7 · 2015: 4 · 2014: 6
- FWCI
- 2.54
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular and Cellular Biology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research (MOP79368, 106583, 84306)
- 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 › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- USP7, MCM complex, DNA replication, chromatin, TRAF domain, protein-protein interaction, late S phase, ubiquitin-specific protease
- MeSH terms
- Ubiquitin-Specific Peptidase 7, Animals, Cells, Cultured, Chromatin, DNA Replication, Flow Cytometry, HeLa Cells, Humans, Models, Molecular, Nuclear Proteins, Protein Binding, Blotting, Western, G1 Phase, S Phase, Protein Structure, Tertiary, Crystallography, X-Ray, Cell Cycle Proteins, RNA Interference, Ubiquitin Thiolesterase, HCT116 Cells, Adaptor Proteins, Signal Transducing, HEK293 Cells, Minichromosome Maintenance Complex Component 7
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