RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair

The DNA-damage response in human biology and disease

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The DNA Damage Response: Making It Safe to Play with Knives

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ATM and ATR Substrate Analysis Reveals Extensive Protein Networks Responsive to DNA Damage

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Sensing DNA Damage Through ATRIP Recognition of RPA-ssDNA Complexes

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53BP1 Inhibits Homologous Recombination in Brca1-Deficient Cells by Blocking Resection of DNA Breaks

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SUMO

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Human CtIP promotes DNA end resection

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RNF8 Ubiquitylates Histones at DNA Double-Strand Breaks and Promotes Assembly of Repair Proteins

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MDC1 Directly Binds Phosphorylated Histone H2AX to Regulate Cellular Responses to DNA Double-Strand Breaks

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Double-strand break repair: 53BP1 comes into focus

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Sumoylation: A Regulatory Protein Modification in Health and Disease

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The increasing complexity of the ubiquitin code

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Function and regulation of SUMO proteases

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Targeting DNA Repair in Cancer: Beyond PARP Inhibitors

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Regulation of DNA Damage Responses by Ubiquitin and SUMO

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Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis

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A comprehensive compilation of SUMO proteomics

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Protein Group Modification and Synergy in the SUMO Pathway as Exemplified in DNA Repair

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RPA-coated single-stranded DNA as a platform for post-translational modifications in the DNA damage response

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Protein posttranslational modifications in health and diseases: Functions, regulatory mechanisms, and therapeutic implications

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SUMO and the robustness of cancer

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Shieldin complex promotes DNA end-joining and counters homologous recombination in BRCA1-null cells

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Signalling mechanisms and cellular functions of SUMO

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Regulation of DNA double-strand break repair by ubiquitin and ubiquitin-like modifiers

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The post-translational modification, SUMOylation, and cancer (Review)

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Ionizing-radiation induced DNA double-strand breaks: A direct and indirect lighting up

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The same, only different – DNA damage checkpoints and their reversal throughout the cell cycle

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Heterochromatic breaks move to the nuclear periphery to continue recombinational repair

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Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress

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SUMO-targeted ubiquitin ligases

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Control of Nuclear Activities by Substrate-Selective and Protein-Group SUMOylation

Jentsch, S., & Psakhye, I. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133453 · Cited by 232

Oxidative stress–induced assembly of PML nuclear bodies controls sumoylation of partner proteins

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Spatiotemporal regulation of posttranslational modifications in the DNA damage response

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RNF4-Dependent Hybrid SUMO-Ubiquitin Chains Are Signals for RAP80 and Thereby Mediate the Recruitment of BRCA1 to Sites of DNA Damage

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RFWD3-Mediated Ubiquitination Promotes Timely Removal of Both RPA and RAD51 from DNA Damage Sites to Facilitate Homologous Recombination

Inano, S., Sato, K., Katsuki, Y., Kobayashi, W., Tanaka, H., Nakajima, K., Nakada, S., Miyoshi, H., Knies, K., Takaori‐Kondo, A., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.04.022 · Cited by 172

Push back to respond better: regulatory inhibition of the DNA double-strand break response

Panier, S., & Durocher, D. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3659 · Cited by 177

RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response

Poulsen, S. L., Hansen, R. K., Wagner, S., van Cuijk, L., van Belle, G. J., Streicher, W. W., Wikström, M., Choudhary, C., Houtsmuller, A. B., Marteijn, J. A. F., et al. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201212075 · Cited by 175

The proteasomal de‐ubiquitinating enzyme POH1 promotes the double‐strand DNA break response

Butler, L. R., Densham, R. M., Jia, J., Garvin, A. J., Stone, H. R., Shah, V., Weekes, D. B., Festy, F., Beesley, J. F. J., & Morris, J. R. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.232 · Cited by 168

PARP1-dependent recruitment of KDM4D histone demethylase to DNA damage sites promotes double-strand break repair

Khoury-Haddad, H., Guttmann‐Raviv, N., Ipenberg, I., Huggins, D. J., Jeyasekharan, A. D. D., & Ayoub, N. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1317585111 · Cited by 148

A conserved SUMO pathway repairs topoisomerase DNA-protein cross-links by engaging ubiquitin-mediated proteasomal degradation

Sun, Y., Jenkins, L. M. M., Su, Y. P., Nitiss, K. C., Nitiss, J. L., & Pommier, Y. G. (2020) · Science Advances · doi:10.1126/sciadv.aba6290 · Cited by 148

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

Systematic characterization of deubiquitylating enzymes for roles in maintaining genome integrity

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Ubiquitylation, neddylation and the DNA damage response

Brown, J. S., & Jackson, S. P. (2015) · Open Biology · doi:10.1098/rsob.150018 · Cited by 155

Molecular Mechanisms of Arsenic-Induced Disruption of DNA Repair

Tam, L. M., Price, N. E., & Wang, Y. (2020) · Chemical Research in Toxicology · doi:10.1021/acs.chemrestox.9b00464 · Cited by 157

SUMO-2 Orchestrates Chromatin Modifiers in Response to DNA Damage

Hendriks, I. A., Treffers, L. W., Vries, M. V., Olsen, J. V., & Vertegaal, A. C. O. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.033 · Cited by 136

Neddylation Promotes Ubiquitylation and Release of Ku from DNA-Damage Sites

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JMJD1C demethylates MDC1 to regulate the RNF8 and BRCA1–mediated chromatin response to DNA breaks

Watanabe, S., Watanabe, K., Akimov, V., Bártková, J., Blagoev, B., Lukas, J., & Bártek, J. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2702 · Cited by 139

The Nuclear SUMO-Targeted Ubiquitin Quality Control Network Regulates the Dynamics of Cytoplasmic Stress Granules

Keiten‐Schmitz, J., Wagner, K., Piller, T., Kaulich, M., Alberti, S., & Müller, S. P. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.05.017 · Cited by 130

The Chromatin Response to DNA Breaks: Leaving a Mark on Genome Integrity

Smeenk, G., & van Attikum, H. (2013) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-061809-174504 · Cited by 135

Regulation of recombination at yeast nuclear pores controls repair and triplet repeat stabilityPreprint

Su, X. A., Dion, V., Gasser, S. M., & Freudenreich, C. H. (2015) · Genes & Development · doi:10.1101/gad.256404.114 · Cited by 133

Decoding the SUMO signal

Hay, R. T. (2013) · Biochemical Society Transactions · doi:10.1042/bst20130015 · Cited by 125

Systematic E2 screening reveals a UBE2D–RNF138–CtIP axis promoting DNA repair

Schmidt, C. K., Galanty, Y., Sczaniecka-Clift, M., Coates, J., Jhujh, S. S., Demir, M., Cornwell, M., Beli, P., & Jackson, S. P. (2015) · Nature Cell Biology · doi:10.1038/ncb3260 · Cited by 123

Ubiquitin-SUMO Circuitry Controls Activated Fanconi Anemia ID Complex Dosage in Response to DNA Damage

Gibbs‐Seymour, I., Oka, Y., Rajendra, E., Weinert, B. T., Passmore, L. A., Patel, K. J., Olsen, J. V., Choudhary, C., Bekker‐Jensen, S., & Mailand, N. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.12.001 · Cited by 116

SUMO and ubiquitin-dependent XPC exchange drives nucleotide excision repair

van Cuijk, L., van Belle, G. J., der Velden, Y. T.-V., Poulsen, S. L., Janssens, R. C., Theil, A. F., Sabatella, M., Lans, H., Mailand, N., Houtsmuller, A. B., et al. (2015) · Nature Communications · doi:10.1038/ncomms8499 · Cited by 113

Structural basis for the RING-catalyzed synthesis of K63-linked ubiquitin chains

Branigan, E., Plechanovová, A., Jaffray, E., Naismith, J. H., & Hay, R. T. (2015) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3052 · Cited by 118

RNF4 is required for DNA double-strand break repair in vivo

Vyas, R., Kumar, R., Clermont, F. F., Helfricht, A., Kalev, P., Sotiropoulou, P., Hendriks, I. A., Radaelli, E., Hochepied, T., Blanpain, C., et al. (2012) · Cell Death and Differentiation · doi:10.1038/cdd.2012.145 · Cited by 120

RNF4 and PLK1 are required for replication fork collapse in ATR-deficient cellsPreprint

Ragland, R. L., Patel, S., Rivard, R. S., Smith, K. D., Peters, A. A., Bielinsky, A., & Brown, E. J. (2013) · Genes & Development · doi:10.1101/gad.223180.113 · Cited by 120

A phosphorylation–deubiquitination cascade regulates the BRCA2–RAD51 axis in homologous recombinationPreprint

Luo, K., Li, L., Li, Y., Wu, C., Yin, Y., Chen, Y., Deng, M., Nowsheen, S., Yuan, J., & Lou, Z. (2016) · Genes & Development · doi:10.1101/gad.289439.116 · Cited by 116

WWP2 ubiquitylates RNA polymerase II for DNA-PK-dependent transcription arrest and repair at DNA breaksPreprint

Caron, P., Pankotai, T., Wiegant, W. W., Tollenaere, M. A. X., Furst, A., Bonhomme, C., Helfricht, A., de Groot, A., Pastink, A., Vertegaal, A. C. O., et al. (2019) · Genes & Development · doi:10.1101/gad.321943.118 · Cited by 110

Arkadia, a Novel SUMO-Targeted Ubiquitin Ligase Involved in PML Degradation

Erker, Y., Neyret‐Kahn, H., Seeler, J.-S., Dejean, A., Atfi, A., & Lévy, L. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01019-12 · Cited by 112

The STUbL RNF4 regulates protein group SUMOylation by targeting the SUMO conjugation machinery

Kumar, R., González‐Prieto, R., Xiao, Z., Vries, M. V., & Vertegaal, A. C. O. (2017) · Nature Communications · doi:10.1038/s41467-017-01900-x · Cited by 113

A new vertebrate SUMO enzyme family reveals insights into SUMO-chain assembly

Eisenhardt, N., Chaugule, V. K., Koidl, S., Droescher, M., Doğan, E., Rettich, J., Sutinen, P., Imanishi, S. Y., Hofmann, K., Palvimo, J. J., et al. (2015) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3114 · Cited by 109

The Heterochromatic Barrier to DNA Double Strand Break Repair: How to Get the Entry Visa

Goodarzi, A. A., & Jeggo, P. A. (2012) · International Journal of Molecular Sciences · doi:10.3390/ijms130911844 · Cited by 113

Dynamic elements of replication protein A at the crossroads of DNA replication, recombination, and repair

Caldwell, C. C., & Spies, M. (2020) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2020.1813070 · Cited by 106

Ube2W conjugates ubiquitin to α-amino groups of protein N-termini

Tatham, M. H., Plechanovová, A., Jaffray, E., Salmen, H., & Hay, R. T. (2013) · Biochemical Journal · doi:10.1042/bj20130244 · Cited by 103

Cell cycle-dependent control of homologous recombination

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The ubiquitin codes in cellular stress responses

Sheng, X., Xia, Z., Yang, H., & Hu, R. (2023) · Protein & Cell · doi:10.1093/procel/pwad045 · Cited by 117

FAM35A associates with REV7 and modulates DNA damage responses of normal and BRCA1‐defective cells

Tomida, J., Takata, K., Bhetawal, S., Person, M. D., Chao, H., Tang, D. G., & Wood, R. D. (2018) · The EMBO Journal · doi:10.15252/embj.201899543 · Cited by 106

Growing sphere of influence: Cdc48/p97 orchestrates ubiquitin-dependent extraction from chromatin

Dantuma, N. P., & Hoppe, T. (2012) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.06.003 · Cited by 101

Ubiquitin-dependent and independent roles of SUMO in proteostasis

Liebelt, F., & Vertegaal, A. C. O. (2016) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00091.2016 · Cited by 101

A Chain of Events: Regulating Target Proteins by SUMO Polymers

Jansen, N. S., & Vertegaal, A. C. O. (2020) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.09.002 · Cited by 99

DNA Repair Pathway Gene Expression Score Correlates with Repair Proficiency and Tumor Sensitivity to Chemotherapy

Pitroda, S. P., Pashtan, I. M., Logan, H. L., Budke, B., Darga, T. E., Weichselbaum, R. R., & Connell, P. P. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3008291 · Cited by 98

SUMO-SIM interactions: From structure to biological functions

Lascorz, J., Codina-Fabra, J., Reverter, D., & Torres‐Rosell, J. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.11.007 · Cited by 100

SUMO-Dependent Relocalization of Eroded Telomeres to Nuclear Pore Complexes Controls Telomere Recombination

Churikov, D., Charifi, F., Eckert‐Boulet, N., Silva, S. D. R., Simon, M., Lisby, M., & Géli, V. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.008 · Cited by 94

Role of p97/VCP (Cdc48) in genome stability

Vaz, B., Halder, S., & Ramadan, K. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00060 · Cited by 95

Deubiquitylating Enzymes and DNA Damage Response Pathways

Jacq, X., Kemp, M. I., Martin, N. M. B., & Jackson, S. P. (2013) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-013-9635-3 · Cited by 90

Nuclear Dynamics of Heterochromatin Repair

Amaral, N., Ryu, T., Li, X., & Chiolo, I. (2017) · Trends in Genetics · doi:10.1016/j.tig.2016.12.004 · Cited by 95

A fine-scale dissection of the DNA double-strand break repair machinery and its implications for breast cancer therapy

Liu, C., Srihari, S., Cao, K. L., Chenevix‐Trench, G., Simpson, P. T., Ragan, M. A., & Khanna, K. K. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku284 · Cited by 91

Insights in Post-Translational Modifications: Ubiquitin and SUMO

Salas‐Lloret, D., & González‐Prieto, R. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23063281 · Cited by 97

SUMO Chain-Induced Dimerization Activates RNF4

Rojas‐Fernández, A., Plechanovová, A., Hattersley, N., Jaffray, E., Tatham, M. H., & Hay, R. T. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.02.031 · Cited by 90

Functions of Ubiquitin and SUMO in DNA Replication and Replication Stress

García‐Rodríguez, N., Wong, R. P. C., & Ulrich, H. D. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00087 · Cited by 90

Debulking of topoisomerase DNA-protein crosslinks (TOP-DPC) by the proteasome, non-proteasomal and non-proteolytic pathways

Sun, Y., Saha, L. K., Saha, S. T., Jo, U., & Pommier, Y. G. (2020) · DNA repair · doi:10.1016/j.dnarep.2020.102926 · Cited by 87

Building up and breaking down: mechanisms controlling recombination during replication

Branzei, D., & Szakál, B. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2017.1304355 · Cited by 84

DNA-damage-induced degradation of EXO1 exonuclease limits DNA end resection to ensure accurate DNA repair

Tomimatsu, N., Mukherjee, B., Harris, J. L., Boffo, F. L., Hardebeck, M. C., Potts, P. R., Khanna, K. K., & Burma, S. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.772475 · Cited by 85

Noncovalent Interactions with SUMO and Ubiquitin Orchestrate Distinct Functions of the SLX4 Complex in Genome Maintenance

Ouyang, J., Garner, E., Hallet, A., Nguyen, H. D., Rickman, K. A., Gill, G., Smogorzewska, A., & Zou, L. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.11.015 · Cited by 84

Mechanism and disease association of E2-conjugating enzymes: lessons from UBE2T and UBE2L3

Alpi, A. F., Chaugule, V. K., & Walden, H. (2016) · Biochemical Journal · doi:10.1042/bcj20160028 · Cited by 81

System-wide Analysis of SUMOylation Dynamics in Response to Replication Stress Reveals Novel Small Ubiquitin-like Modified Target Proteins and Acceptor Lysines Relevant for Genome Stability

Xiao, Z., Chang, J.-G., Hendriks, I. A., Sigurðsson, J. O., Olsen, J. V., & Vertegaal, A. C. O. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.o114.044792 · Cited by 81

Role of Deubiquitinating Enzymes in DNA Repair

Kee, Y., & Huang, T. T. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.00847-15 · Cited by 81

Ataxin‐3 consolidates the MDC1‐dependent DNA double‐strand break response by counteracting the SUMO‐targeted ubiquitin ligase RNF4

Pfeiffer, A., Luijsterburg, M. S., Ács, K., Wiegant, W. W., Helfricht, A., Herzog, L. K., Minoia, M., Böttcher, C., Salomons, F. A., van Attikum, H., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201695151 · Cited by 80

Distinct SUMO Ligases Cooperate with Esc2 and Slx5 to Suppress Duplication-Mediated Genome Rearrangements

de Albuquerque, C. P., Wang, G., Lee, N. S., Kolodner, R. D., Putnam, C. D., & Zhou, H. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003670 · Cited by 83

Crosstalk between ubiquitin and other post-translational modifications on chromatin during double-strand break repair

Zhao, Y. J., Brickner, J. R., Majid, M. C., & Mosammaparast, N. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.01.005 · Cited by 79

The SUMO system: a master organizer of nuclear protein assemblies

Raman, N., Nayak, A., & Muller, S. (2013) · Chromosoma · doi:10.1007/s00412-013-0429-6 · Cited by 77

SUMO, a small, but powerful, regulator of double-strand break repair

Garvin, A. J., & Morris, J. R. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0281 · Cited by 73

Relocation of Collapsed Forks to the Nuclear Pore Complex Depends on Sumoylation of DNA Repair Proteins and Permits Rad51 Association

Whalen, J. M., Dhingra, N., Wei, L., Zhao, X., & Freudenreich, C. H. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107635 · Cited by 75

CHD chromatin remodelling enzymes and the DNA damage response

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A modular toolbox to generate complex polymeric ubiquitin architectures using orthogonal sortase enzymes

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