Regulation of DNA repair by ubiquitylation (original) (raw)

• Sancar, A., Lindsey-Boltz, L. A., Unsal-Kacmaz, K. & Linn, S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73, 39–85 (2004).
  CAS PubMed Google Scholar
• Hoeijmakers, J. H. Genome maintenance mechanisms for preventing cancer. Nature 411, 366–374 (2001). An excellent overview of mammalian DNA-repair pathways.
  CAS PubMed Google Scholar
• Kennedy, R. D. & D'Andrea, A. D. The Fanconi Anemia/BRCA pathway: new faces in the crowd. Genes Dev. 19, 2925–2940 (2005).
  CAS PubMed Google Scholar
• Rothfuss, A. & Grompe, M. Repair kinetics of genomic interstrand DNA cross-links: evidence for DNA double-strand break-dependent activation of the Fanconi anemia/BRCA pathway. Mol. Cell. Biol. 24, 123–134 (2004).
  CAS PubMed PubMed Central Google Scholar
• Niedzwiedz, W. et al. The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol. Cell 15, 607–620 (2004).
  CAS PubMed Google Scholar
• D'Andrea, A. D. The Fanconi road to cancer. Genes Dev. 17, 1933–1936 (2003).
  CAS PubMed Google Scholar
• D'Andrea, A. D. & Grompe, M. The Fanconi anaemia/BRCA pathway. Nature Rev. Cancer 3, 23–34 (2003).
  CAS Google Scholar
• Niedernhofer, L. J., Lalai, A. S. & Hoeijmakers, J. H. Fanconi anemia (cross)linked to DNA repair. Cell 123, 1191–1198 (2005).
  CAS PubMed Google Scholar
• Garcia-Higuera, I. et al. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 7, 249–262 (2001). Provides the first evidence that FA proteins are involved in a common pathway to monoubiquitylate FANCD2.
  CAS PubMed Google Scholar
• Howlett, N. G. et al. Biallelic inactivation of BRCA2 in Fanconi anemia. Science 297, 606–609 (2002).
  CAS PubMed Google Scholar
• Wang, X., Andreassen, P. R. & D'Andrea, A. D. Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol. Cell. Biol. 24, 5850–5862 (2004).
  CAS PubMed PubMed Central Google Scholar
• Meetei, A. R. et al. A novel ubiquitin ligase is deficient in Fanconi anemia. Nature Genet. 35, 165–170 (2003). Reports the identification of a ubiquitin-ligase catalytic subunit in the FA core complex.
  CAS PubMed Google Scholar
• Matsushita, N. et al. A FancD2-monoubiquitin fusion reveals hidden functions of Fanconi anemia core complex in DNA repair. Mol. Cell 9, 841–847 (2005).
  Google Scholar
• Meetei, A. R. et al. A human ortholog of archael DNA repair protein HEF is defective in Fanconi anemia complementation group M. Nature Genet. 37, 958–963 (2005).
  CAS PubMed Google Scholar
• Mosedale, G. et al. The vertebrate Hef orthologue is a component of the Fanconi anemia tumour suppressor pathway. Nature Struct. Mol. Biol. 12, 963–971 (2005).
  Google Scholar
• Andreassen, P. R., D'Andrea, A. D. & Taniguchi, T. ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev. 18, 1958–1963 (2004).
  CAS PubMed PubMed Central Google Scholar
• Hussain, S. et al. Direct interaction of FANCD2 with BRCA2 in DNA damage response pathways. Hum. Mol. Genet. 13, 1241–1248 (2004).
  CAS PubMed Google Scholar
• Lomonosov, M., Anand, S., Sangrithi, M., Davies, R. & Venkitaraman, A. R. Stabilization of stalled DNA replication forks by the BRCA2 breast cancer susceptibility protein. Genes Dev. 17, 3017–3022 (2003).
  CAS PubMed PubMed Central Google Scholar
• Montes de Oca, R. et al. Regulated interaction of the Fanconi anemia protein, FANCD2, with chromatin. Blood 105, 1003–1009 (2005).
  PubMed Google Scholar
• Taniguchi, T. et al. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 100, 2414–2420 (2002).
  CAS PubMed Google Scholar
• Nijman, S. M. et al. The deubiquitinating enzyme USP1 regulates the Fanconi Anemia pathway. Mol. Cell 17, 331–339 (2005). Reports the results of a DUB-gene family RNAi library screen to identify negative regulators of the FA pathway.
  CAS PubMed Google Scholar
• Vandenberg, C. J. et al. BRCA1-independent ubiquitination of FANCD2. Mol. Cell 12, 247–254 (2003).
  CAS PubMed Google Scholar
• Mallery, D. L., Vandenberg, C. J. & Hiom, K. Activation of the E3 ligase function of the BRCA1/BARD1 complex by polyubiquitin chains. EMBO J. 21, 6755–6762 (2002).
  CAS PubMed PubMed Central Google Scholar
• Chiba, N. & Parvin, J. D. The BRCA1 and BARD1 association with the RNA polymerase II holoenzyme. Cancer Res. 62, 4222–4228 (2002).
  CAS PubMed Google Scholar
• Ratner, J. N., Balasubramanian, B., Corden, J., Warren, S. L. & Bregman, D. B. Ultraviolet radiation-induced ubiquitination and proteasomal degradation of the large subunit of RNA polymerase II. Implications for transcription-coupled DNA repair. J. Biol. Chem. 273, 5184–5189 (1998).
  CAS PubMed Google Scholar
• Hashizume, R. et al. The ring heterodimer brca1–bard1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J. Biol. Chem. 276, 14537–14540 (2001).
  CAS PubMed Google Scholar
• Dong, Y. et al. Regulation of BRCC, a holoenzyme complex containing BRCA1 and BRCA2, by a signalosome-like subunit and its role in DNA repair. Mol. Cell 12, 1087–1099 (2003).
  CAS PubMed Google Scholar
• Jensen, D. E. et al. BAP1: a novel ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene 16, 1097–1112 (1998).
  CAS PubMed Google Scholar
• Cope, G. A. et al. Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science 298, 608–611 (2002). Discovery of a novel metalloprotease domain in CSN complex that is responsible for deubiquitylation and/or deneddylation activities.
  CAS PubMed Google Scholar
• Hoege, C., Pfander, B., Moldovan, G. L., Pyrowolakis, G. & Jentsch, S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419, 135–141 (2002). Shows that PCNA in yeast can be modified by SUMO, monoubiquitin or polyubiquitin to promote RAD6-dependent error-prone or error-free post-replication repair.
  CAS PubMed Google Scholar
• Ulrich, H. D. & Jentsch, S. Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J. 19, 3388–3397 (2000).
  CAS PubMed PubMed Central Google Scholar
• Stelter, P. & Ulrich, H. D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425, 188–191 (2003).
  CAS PubMed Google Scholar
• Haracska, L., Torres-Ramos, C. A., Johnson, R. E., Prakash, S. & Prakash, L. Opposing effects of ubiquitin conjugation and SUMO modification of PCNA on replicational bypass of DNA lesions in Saccharomyces cerevisiae. Mol. Cell. Biol. 24, 4267–4274 (2004).
  CAS PubMed PubMed Central Google Scholar
• Spence, J., Sadis, S., Haas, A. L. & Finley, D. A ubiquitin mutant with specific defects in DNA repair and multiubiquitination. Mol. Cell. Biol. 15, 1265–1273 (1995).
  CAS PubMed PubMed Central Google Scholar
• Hofmann, R. M. & Pickart, C. M. Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96, 645–653 (1999).
  CAS PubMed Google Scholar
• Pfander, B., Moldovan, G. L., Sacher, M., Hoege, C. & Jentsch, S. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436, 428–433 (2005).
  CAS PubMed Google Scholar
• Papouli, E. et al. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19, 123–133 (2005).
  CAS PubMed Google Scholar
• Kannouche, P. L., Wing, J. & Lehmann, A. R. Interaction of human DNA polymerase ε with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14, 491–500 (2004). First to show that mammalian PCNA is monoubiquitylated in order to functionally interact with a Y-family TLS polymerase.
  CAS PubMed Google Scholar
• Watanabe, K. et al. Rad18 guides polε to replication stalling sites through physical interaction and PCNA monoubiquitination. EMBO J. 23, 3886–3896 (2004).
  CAS PubMed PubMed Central Google Scholar
• Masutani, C. et al. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase ε. Nature 399, 700–704 (1999).
  CAS PubMed Google Scholar
• Kannouche, P. et al. Domain structure, localization, and function of DNA polymerase ε, defective in xeroderma pigmentosum variant cells. Genes Dev. 15, 158–172 (2001).
  CAS PubMed PubMed Central Google Scholar
• Friedberg, E. C., Wagner, R. & Radman, M. Specialized DNA polymerases, cellular survival, and the genesis of mutations. Science 296, 1627–1630 (2002).
  CAS PubMed Google Scholar
• Murakumo, Y. et al. Interactions in the error-prone postreplication repair proteins hREV1, hREV3, and hREV7. J. Biol. Chem. 276, 35644–35651 (2001).
  CAS PubMed Google Scholar
• Ohashi, E. et al. Interaction of hREV1 with three human Y-family DNA polymerases. Genes Cells 9, 523–531 (2004).
  CAS PubMed Google Scholar
• Guo, C. et al. Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J. 22, 6621–6630 (2003).
  CAS PubMed PubMed Central Google Scholar
• Tissier, A. et al. Co-localization in replication foci and interaction of human Y-family members, DNA polymerase pol ε and REVl protein. DNA Repair (Amst.) 3, 1503–1514 (2004).
  CAS Google Scholar
• Garg, P. & Burgers, P. M. Ubiquitinated proliferating cell nuclear antigen activates translesion DNA polymerases ε and REV1. Proc. Natl Acad. Sci. USA 102, 18361–18366 (2005).
  CAS PubMed PubMed Central Google Scholar
• Bienko, M. et al. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 310, 1821–1824 (2005). Describes two novel ubiquitin binding domains, UBM and UBZ, that allow Y-family TLS polymerases to interact with monoubiquitylated PCNA.
  CAS PubMed Google Scholar
• Kannouche, P. L. & Lehmann, A. R. Ubiquitination of PCNA and the polymerase switch in human cells. Cell Cycle 3, 1011–1013 (2004).
  CAS PubMed Google Scholar
• Miyase, S. et al. Differential regulation of Rad18 through Rad6-dependent mono- and polyubiquitination. J. Biol. Chem. 280, 515–524 (2005).
  CAS PubMed Google Scholar
• McCulloch, S. D. et al. Preferential cis–syn thymine dimer bypass by DNA polymerase ε occurs with biased fidelity. Nature 428, 97–100 (2004).
  CAS PubMed Google Scholar
• Li, Z., Xiao, W., McCormick, J. J. & Maher, V. M. Identification of a protein essential for a major pathway used by human cells to avoid UV- induced DNA damage. Proc. Natl Acad. Sci. USA 99, 4459–4464 (2002).
  CAS PubMed PubMed Central Google Scholar
• Leach, C. A. & Michael, W. M. Ubiquitin/SUMO modification of PCNA promotes replication fork progression in Xenopus laevis egg extracts. J. Cell Biol. 171, 947–954 (2005).
  CAS PubMed PubMed Central Google Scholar
• Wood, R. D. et al. DNA damage recognition and nucleotide excision repair in mammalian cells. Cold Spring Harb. Symp. Quant. Biol. 65, 173–182 (2000).
  CAS PubMed Google Scholar
• Friedberg, E. C. How nucleotide excision repair protects against cancer. Nature Rev. Cancer 1, 22–33 (2001).
  CAS Google Scholar
• Svejstrup, J. Q. Mechanisms of transcription-coupled DNA repair. Nature Rev. Mol. Cell Biol. 3, 21–29 (2002).
  CAS Google Scholar
• Fitch, M. E., Nakajima, S., Yasui, A. & Ford, J. M. In vivo recruitment of XPC to UV-induced cyclobutane pyrimidine dimers by the DDB2 gene product. J. Biol. Chem. 278, 46906–46910 (2003).
  CAS PubMed Google Scholar
• Moser, J. et al. The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions. DNA Repair (Amst.) 4, 571–582 (2005).
  CAS Google Scholar
• Cleaver, J. E. Cancer in xeroderma pigmentosum and related disorders of DNA repair. Nature Rev. Cancer 5, 564–573 (2005).
  CAS Google Scholar
• Groisman, R. et al. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113, 357–367 (2003). Provides evidence for ubiquitin ligase activity that is linked to two NER protein complexes and that is negatively regulated by the CSN.
  CAS PubMed Google Scholar
• Cope, G. A. & Deshaies, R. J. COP9 signalosome: a multifunctional regulator of SCF and other cullin-based ubiquitin ligases. Cell 114, 663–671 (2003).
  CAS PubMed Google Scholar
• Sugasawa, K. et al. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 121, 387–400 (2005). Shows that XPC is polyubiquitylated in response to UV damage.
  CAS PubMed Google Scholar
• Masutani, C. et al. Purification and cloning of a nucleotide excision repair complex involving the xeroderma pigmentosum group C protein and a human homologue of yeast RAD23. EMBO J. 13, 1831–1843 (1994).
  CAS PubMed PubMed Central Google Scholar
• Shivji, M. K., Eker, A. P. & Wood, R. D. DNA repair defect in xeroderma pigmentosum group C and complementing factor from HeLa cells. J. Biol. Chem. 269, 22749–22757 (1994).
  CAS PubMed Google Scholar
• Sugasawa, K., Shimizu, Y., Iwai, S. & Hanaoka, F. A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex. DNA Repair (Amst.) 1, 95–107 (2002).
  CAS Google Scholar
• Wakasugi, M. et al. DDB accumulates at DNA damage sites immediately after UV irradiation and directly stimulates nucleotide excision repair. J. Biol. Chem. 277, 1637–1640 (2002).
  CAS PubMed Google Scholar
• Ng, J. M. et al. A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev. 17, 1630–1645 (2003).
  CAS PubMed PubMed Central Google Scholar
• Okuda, Y. et al. Relative levels of the two mammalian Rad23 homologs determine composition and stability of the xeroderma pigmentosum group C protein complex. DNA Repair (Amst.) 3, 1285–1295 (2004).
  CAS Google Scholar
• Russell, S. J., Reed, S. H., Huang, W., Friedberg, E. C. & Johnston, S. A. The 19S regulatory complex of the proteasome functions independently of proteolysis in nucleotide excision repair. Mol. Cell 3, 687–695 (1999).
  CAS PubMed Google Scholar
• Ortolan, T. G., Chen, L., Tongaonkar, P. & Madura, K. Rad23 stabilizes Rad4 from degradation by the Ub–proteasome pathway. Nucleic Acids Res. 32, 6490–6500 (2004).
  CAS PubMed PubMed Central Google Scholar
• Heessen, S., Masucci, M. G. & Dantuma, N. P. The UBA2 domain functions as an intrinsic stabilization signal that protects Rad23 from proteasomal degradation. Mol. Cell 18, 225–235 (2005).
  CAS PubMed Google Scholar
• Bregman, D. B. et al. UV-induced ubiquitination of RNA polymerase II: a novel modification deficient in Cockayne syndrome cells. Proc. Natl Acad. Sci. USA 93, 11586–11590 (1996).
  CAS PubMed PubMed Central Google Scholar
• Kleiman, F. E. et al. BRCA1/BARD1 inhibition of mRNA 3′ processing involves targeted degradation of RNA polymerase II. Genes Dev. 19, 1227–1237 (2005).
  CAS PubMed PubMed Central Google Scholar
• Woudstra, E. C. et al. A Rad26–Def1 complex coordinates repair and RNA pol II proteolysis in response to DNA damage. Nature 415, 929–933 (2002).
  CAS PubMed Google Scholar
• Svejstrup, J. Q. Rescue of arrested RNA polymerase II complexes. J. Cell Sci. 116, 447–451 (2003).
  CAS PubMed Google Scholar
• Hardeland, U. et al. Thymine DNA glycosylase. Prog. Nucleic Acid Res. Mol. Biol. 68, 235–253 (2001).
  CAS PubMed Google Scholar
• Scharer, O. D. & Jiricny, J. Recent progress in the biology, chemistry and structural biology of DNA glycosylases. Bioessays 23, 270–281 (2001).
  CAS PubMed Google Scholar
• Hardeland, U., Steinacher, R., Jiricny, J. & Schar, P. Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 21, 1456–1464 (2002). Provides evidence that TDG is modified by SUMO, which is important in facilitating BER.
  CAS PubMed PubMed Central Google Scholar
• Steinacher, R. & Schar, P. Functionality of human thymine DNA glycosylase requires SUMO-regulated changes in protein conformation. Curr. Biol. 15, 616–623 (2005).
  CAS PubMed Google Scholar
• Huang, T. T., Wuerzberger-Davis, S. M., Wu, Z. H. & Miyamoto, S. Sequential modification of NEMO/IKKγ by SUMO-1 and ubiquitin mediates NF-κB activation by genotoxic stress. Cell 115, 565–576 (2003).
  CAS PubMed Google Scholar
• Gocke, C. B., Yu, H. & Kang, J. Systematic identification and analysis of mammalian small ubiquitin-like modifier substrates. J. Biol. Chem. 280, 5004–5012 (2005).
  CAS PubMed Google Scholar
• Pickart, C. M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503–533 (2001).
  CAS PubMed Google Scholar
• Pickart, C. M. Ubiquitin in chains. Trends Biochem. Sci. 25, 544–548 (2000).
  CAS PubMed Google Scholar
• Johnson, E. S. Ubiquitin branches out. Nature Cell Biol. 4, E295–E298 (2002).
  CAS PubMed Google Scholar
• Hicke, L., Schubert, H. L. & Hill, C. P. Ubiquitin-binding domains. Nature Rev. Mol. Cell Biol. 6, 610–621 (2005).
  CAS Google Scholar
• Sun, L. & Chen, Z. J. The novel functions of ubiquitination in signaling. Curr. Opin. Cell Biol. 16, 119–126 (2004).
  CAS PubMed Google Scholar
• Chen, Z. J. Ubiquitin signalling in the NF-κB pathway. Nature Cell Biol. 7, 758–765 (2005).
  CAS PubMed Google Scholar
• Amerik, A. Y. & Hochstrasser, M. Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 1695, 189–207 (2004).
  CAS PubMed Google Scholar
• Wilkinson, K. D. Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J. 11, 1245–1256 (1997).
  CAS PubMed Google Scholar
• Di Fiore, P. P., Polo, S. & Hofmann, K. When ubiquitin meets ubiquitin receptors: a signalling connection. Nature Rev. Mol. Cell Biol. 4, 491–497 (2003).
  CAS Google Scholar
• Welchman, R. L., Gordon, C. & Mayer, R. J. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nature Rev. Mol. Cell Biol. 6, 599–609 (2005).
  CAS Google Scholar
• Gill, G. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev. 18, 2046–2059 (2004).
  CAS PubMed Google Scholar
• Desterro, J. M., Rodriguez, M. S., Kemp, G. D. & Hay, R. T. Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J. Biol. Chem. 274, 10618–10624 (1999).
  CAS PubMed Google Scholar
• Hay, R. T. Protein modification by SUMO. Trends Biochem. Sci. 26, 332–333 (2001).
  CAS PubMed Google Scholar
• Johnson, E. S. Protein modification by SUMO. Annu. Rev. Biochem. 73, 355–382 (2004).
  CAS PubMed Google Scholar
• Hori, T. et al. Covalent modification of all members of human cullin family proteins by NEDD8. Oncogene 18, 6829–6834 (1999).
  CAS PubMed Google Scholar
• Liu, J., Furukawa, M., Matsumoto, T. & Xiong, Y. NEDD8 modification of CUL1 dissociates p120(CAND1), an inhibitor of CUL1–SKP1 binding and SCF ligases. Mol. Cell 10, 1511–1518 (2002).
  CAS PubMed Google Scholar
• Hanna, J., Leggett, D. S. & Finley, D. Ubiquitin depletion as a key mediator of toxicity by translational inhibitors. Mol. Cell. Biol. 23, 9251–9261 (2003).
  CAS PubMed PubMed Central Google Scholar
• Park, W. H. et al. Direct DNA binding activity of the fanconi anemia d2 protein. J. Biol. Chem. 280, 23593–23598 (2005).
  CAS PubMed Google Scholar
• Guterman, A. & Glickman, M. H. Deubiquitinating enzymes are IN(trinsic to proteasome function). Curr. Protein Pept. Sci. 5, 201–211 (2004).
  CAS PubMed Google Scholar
• Mimnaugh, E. G., Chen, H. Y., Davie, J. R., Celis, J. E. & Neckers, L. Rapid deubiquitination of nucleosomal histones in human tumor cells caused by proteasome inhibitors and stress response inducers: effects on replication, transcription, translation, and the cellular stress response. Biochemistry 36, 14418–14429 (1997).
  CAS PubMed Google Scholar
• Voorhees, P. M. & Orlowski, R. Z. The proteasome and proteasome inhibitors in cancer therapy. Annu. Rev. Pharmacol. Toxicol. 46, 189–213 (2006).
  CAS PubMed Google Scholar
• Mimnaugh, E. G. et al. Prevention of cisplatin-DNA adduct repair and potentiation of cisplatin-induced apoptosis in ovarian carcinoma cells by proteasome inhibitors. Biochem. Pharmacol. 60, 1343–1354 (2000).
  CAS PubMed Google Scholar
• Huang, T. T. et al. Regulation of monoubiquitinated PCNA by DUB autocleavage. Nature Cell Biol. 8, 339–347 (2006).
  CAS PubMed Google Scholar