Two-way communications between ubiquitin-like modifiers and DNA (original) (raw)

• Flotho, A. & Melchior, F. SUMOylation: a regulatory protein modification in health and disease. Annu. Rev. Biochem. 82, 357–385 (2013).
  Article CAS PubMed Google Scholar
• Jackson, S.P. & Durocher, D. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 49, 795–807 (2013).
  Article CAS PubMed Google Scholar
• Kerscher, O., Felberbaum, R. & Hochstrasser, M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22, 159–180 (2006).
  Article CAS PubMed Google Scholar
• Ulrich, H.D. & Walden, H. Ubiquitin signalling in DNA replication and repair. Nat. Rev. Mol. Cell Biol. 11, 479–489 (2010).
  Article CAS PubMed Google Scholar
• Geng, F., Wenzel, S. & Tansey, W.P. Ubiquitin and proteasomes in transcription. Annu. Rev. Biochem. 81, 177–201 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Gill, G. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev. 18, 2046–2059 (2004).
  Article CAS PubMed Google Scholar
• Müller, S., Ledl, A. & Schmidt, D. SUMO: a regulator of gene expression and genome integrity. Oncogene 23, 1998–2008 (2004).
  Article PubMed CAS Google Scholar
• Bergink, S. & Jentsch, S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 458, 461–467 (2009).
  Article CAS PubMed Google Scholar
• Aravind, L. & Koonin, E.V. SAP: a putative DNA-binding motif involved in chromosomal organization. Trends Biochem. Sci. 25, 112–114 (2000).
  Article CAS PubMed Google Scholar
• Palvimo, J.J. PIAS proteins as regulators of small ubiquitin-related modifier (SUMO) modifications and transcription. Biochem. Soc. Trans. 35, 1405–1408 (2007).
  Article CAS PubMed Google Scholar
• Suzuki, R. et al. Solution structures and DNA binding properties of the N-terminal SAP domains of SUMO E3 ligases from Saccharomyces cerevisiae and Oryza sativa. Proteins 75, 336–347 (2009).
  Article 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).
  Article CAS PubMed Google Scholar
• Huttner, D. & Ulrich, H.D. Cooperation of replication protein A with the ubiquitin ligase Rad18 in DNA damage bypass. Cell Cycle 7, 3629–3633 (2008).
  Article CAS PubMed Google Scholar
• Nakajima, S. et al. Replication-dependent and -independent responses of RAD18 to DNA damage in human cells. J. Biol. Chem. 281, 34687–34695 (2006).
  Article CAS PubMed Google Scholar
• Notenboom, V. et al. Functional characterization of Rad18 domains for Rad6, ubiquitin, DNA binding and PCNA modification. Nucleic Acids Res. 35, 5819–5830 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Tsuji, Y. et al. Recognition of forked and single-stranded DNA structures by human RAD18 complexed with RAD6B protein triggers its recruitment to stalled replication forks. Genes Cells 13, 343–354 (2008).
  Article CAS PubMed Google Scholar
• Hopfner, K.P., Gerhold, C.B., Lakomek, K. & Wollmann, P. Swi2/Snf2 remodelers: hybrid views on hybrid molecular machines. Curr. Opin. Struct. Biol. 22, 225–233 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Eisen, J.A., Sweder, K.S. & Hanawalt, P.C. Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. Nucleic Acids Res. 23, 2715–2723 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Lawrence, C. The RAD6 DNA repair pathway in Saccharomyces cerevisiae: what does it do, and how does it do it? BioEssays 16, 253–258 (1994).
  Article CAS PubMed Google Scholar
• Parker, J.L. & Ulrich, H.D. Mechanistic analysis of PCNA poly-ubiquitylation by the ubiquitin protein ligases Rad18 and Rad5. EMBO J. 28, 3657–3666 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Garg, P. & Burgers, P.M. Ubiquitinated proliferating cell nuclear antigen activates translesion DNA polymerases η and REV1. Proc. Natl. Acad. Sci. USA 102, 18361–18366 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Iyer, L.M., Babu, M.M. & Aravind, L. The HIRAN domain and recruitment of chromatin remodeling and repair activities to damaged DNA. Cell Cycle 5, 775–782 (2006).
  Article CAS PubMed Google Scholar
• Blastyák, A., Hajdu, I., Unk, I. & Haracska, L. Role of double-stranded DNA translocase activity of human HLTF in replication of damaged DNA. Mol. Cell. Biol. 30, 684–693 (2010).
  Article PubMed CAS Google Scholar
• Blastyák, A. et al. Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol. Cell 28, 167–175 (2007).
  Article PubMed PubMed Central CAS Google Scholar
• Sriramachandran, A.M. & Dohmen, R.J. SUMO-targeted ubiquitin ligases. Biochim. Biophys. Acta 1843, 75–85 (2014).
  Article CAS PubMed Google Scholar
• Uzunova, K. et al. Ubiquitin-dependent proteolytic control of SUMO conjugates. J. Biol. Chem. 282, 34167–34175 (2007).
  Article CAS PubMed Google Scholar
• Lescasse, R., Pobiega, S., Callebaut, I. & Marcand, S. End-joining inhibition at telomeres requires the translocase and polySUMO-dependent ubiquitin ligase Uls1. EMBO J. 32, 805–815 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Häkli, M., Karvonen, U., Janne, O.A. & Palvimo, J.J. The RING finger protein SNURF is a bifunctional protein possessing DNA binding activity. J. Biol. Chem. 276, 23653–23660 (2001).
  Article PubMed Google Scholar
• Vidal, M. Role of polycomb proteins Ring1A and Ring1B in the epigenetic regulation of gene expression. Int. J. Dev. Biol. 53, 355–370 (2009).
  Article CAS PubMed Google Scholar
• Bentley, M.L. et al. Recognition of UbcH5c and the nucleosome by the Bmi1/Ring1b ubiquitin ligase complex. EMBO J. 30, 3285–3297 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Scrima, A. et al. Detecting UV-lesions in the genome: the modular CRL4 ubiquitin ligase does it best!. FEBS Lett. 585, 2818–2825 (2011).
  Article CAS PubMed Google Scholar
• Sugasawa, K. Regulation of damage recognition in mammalian global genomic nucleotide excision repair. Mutat. Res. 685, 29–37 (2010).
  Article CAS PubMed Google Scholar
• Fischer, E.S. et al. The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell 147, 1024–1039 (2011).
  Article CAS PubMed Google Scholar
• Yeh, J.I. et al. Damaged DNA induced UV-damaged DNA-binding protein (UV-DDB) dimerization and its roles in chromatinized DNA repair. Proc. Natl. Acad. Sci. USA 109, E2737–E2746 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Kegel, A. & Sjogren, C. The Smc5/6 complex: more than repair? Cold Spring Harb. Symp. Quant. Biol. 75, 179–187 (2010).
  Article CAS PubMed Google Scholar
• Wu, N. & Yu, H. The Smc complexes in DNA damage response. Cell Biosci. 2, 5 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Andrews, E.A. et al. Nse2, a component of the Smc5–6 complex, is a SUMO ligase required for the response to DNA damage. Mol. Cell. Biol. 25, 185–196 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Duan, X. et al. Structural and functional insights into the roles of the Mms21 subunit of the Smc5/6 complex. Mol. Cell 35, 657–668 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Potts, P.R. & Yu, H. Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol. Cell. Biol. 25, 7021–7032 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Zhao, X. & Blobel, G. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl. Acad. Sci. USA 102, 4777–4782 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Doyle, J.M., Gao, J., Wang, J., Yang, M. & Potts, P.R. MAGE-RING protein complexes comprise a family of E3 ubiquitin ligases. Mol. Cell 39, 963–974 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Kim, H. & D'Andrea, A.D. Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev. 26, 1393–1408 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Kottemann, M.C. & Smogorzewska, A. Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 493, 356–363 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Coulthard, R. et al. Architecture and DNA recognition elements of the Fanconi anemia FANCM-FAAP24 complex. Structure 21, 1648–1658 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Tao, Y. et al. The structure of the FANCM–MHF complex reveals physical features for functional assembly. Nat. Commun. 3, 782 (2012).
  Article PubMed CAS Google Scholar
• Morohashi, H., Maculins, T. & Labib, K. The amino-terminal TPR domain of Dia2 tethers SCFDia2 to the replisome progression complex. Curr. Biol. 19, 1943–1949 (2009).
  Article CAS PubMed Google Scholar
• Mimura, S., Komata, M., Kishi, T., Shirahige, K. & Kamura, T. SCFDia2 regulates DNA replication forks during S-phase in budding yeast. EMBO J. 28, 3693–3705 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Andress, E.J., Holic, R., Edelmann, M.J., Kessler, B.M. & Yu, V.P. Dia2 controls transcription by mediating assembly of the RSC complex. PLoS ONE 6, e21172 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Kim, J. & Roeder, R.G. Direct Bre1-Paf1 complex interactions and RING finger-independent Bre1-Rad6 interactions mediate histone H2B ubiquitylation in yeast. J. Biol. Chem. 284, 20582–20592 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Davies, A.A., Huttner, D., Daigaku, Y., Chen, S. & Ulrich, H.D. Activation of ubiquitin-dependent DNA damage bypass is mediated by Replication Protein A. Mol. Cell 29, 625–636 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Niimi, A. et al. Regulation of proliferating cell nuclear antigen ubiquitination in mammalian cells. Proc. Natl. Acad. Sci. USA 105, 16125–16130 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Al-Hakim, A. et al. The ubiquitous role of ubiquitin in the DNA damage response. DNA Repair (Amst.) 9, 1229–1240 (2010).
  Article CAS Google Scholar
• Bekker-Jensen, S. & Mailand, N. The ubiquitin- and SUMO-dependent signaling response to DNA double-strand breaks. FEBS Lett. 585, 2914–2919 (2011).
  Article CAS PubMed Google Scholar
• Ulrich, H.D. Ubiquitin and SUMO in DNA repair at a glance. J. Cell Sci. 125, 249–254 (2012).
  Article CAS PubMed Google Scholar
• Mermershtain, I. & Glover, J.N. Structural mechanisms underlying signaling in the cellular response to DNA double strand breaks. Mutat. Res. 750, 15–22 (2013).
  Article CAS PubMed Google Scholar
• Lou, Z. et al. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell 21, 187–200 (2006).
  Article CAS PubMed Google Scholar
• Stewart, G.S., Wang, B., Bignell, C.R., Taylor, A.M. & Elledge, S.J. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421, 961–966 (2003).
  Article CAS PubMed Google Scholar
• Stucki, M. et al. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123, 1213–1226 (2005).
  Article CAS PubMed Google Scholar
• Huen, M.S. et al. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131, 901–914 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Kolas, N.K. et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318, 1637–1640 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Mailand, N. et al. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131, 887–900 (2007).
  Article CAS PubMed Google Scholar
• Bekker-Jensen, S. et al. HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nat. Cell Biol. 12, 80–86 (2010).
  Article CAS PubMed Google Scholar
• Doil, C. et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136, 435–446 (2009).
  Article CAS PubMed Google Scholar
• Stewart, G.S. et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136, 420–434 (2009).
  Article CAS PubMed Google Scholar
• Mattiroli, F. et al. RNF168 ubiquitinates K13–15 on H2A/H2AX to drive DNA damage signaling. Cell 150, 1182–1195 (2012).
  Article CAS PubMed Google Scholar
• Panier, S. et al. Tandem protein interaction modules organize the ubiquitin-dependent response to DNA double-strand breaks. Mol. Cell 47, 383–395 (2012).
  Article CAS PubMed Google Scholar
• Kim, H., Chen, J. & Yu, X. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316, 1202–1205 (2007).
  Article CAS PubMed Google Scholar
• Liu, Z., Wu, J. & Yu, X. CCDC98 targets BRCA1 to DNA damage sites. Nat. Struct. Mol. Biol. 14, 716–720 (2007).
  Article CAS PubMed Google Scholar
• Sobhian, B. et al. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316, 1198–1202 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Wang, B. et al. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316, 1194–1198 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Paull, T.T., Cortez, D., Bowers, B., Elledge, S.J. & Gellert, M. Direct DNA binding by Brca1. Proc. Natl. Acad. Sci. USA 98, 6086–6091 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Yamane, K., Katayama, E. & Tsuruo, T. The BRCT regions of tumor suppressor BRCA1 and of XRCC1 show DNA end binding activity with a multimerizing feature. Biochem. Biophys. Res. Commun. 279, 678–684 (2000).
  Article CAS PubMed Google Scholar
• Huang, J. et al. RAD18 transmits DNA damage signalling to elicit homologous recombination repair. Nat. Cell Biol. 11, 592–603 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Vyas, R. et al. RNF4 is required for DNA double-strand break repair in vivo. Cell Death Differ. 20, 490–502 (2013).
  Article CAS PubMed Google Scholar
• Yin, Y. et al. SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev. 26, 1196–1208 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Galanty, Y., Belotserkovskaya, R., Coates, J. & Jackson, S.P. RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev. 26, 1179–1195 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Parker, J.L. & Ulrich, H.D. A SUMO-interacting motif activates budding yeast ubiquitin ligase Rad18 towards SUMO-modified PCNA. Nucleic Acids Res. 40, 11380–11388 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Havens, C.G. & Walter, J.C. Mechanism of CRL4Cdt2, a PCNA-dependent E3 ubiquitin ligase. Genes Dev. 25, 1568–1582 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Arias, E.E. & Walter, J.C. Replication-dependent destruction of Cdt1 limits DNA replication to a single round per cell cycle in Xenopus egg extracts. Genes Dev. 19, 114–126 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Hu, J., McCall, C.M., Ohta, T. & Xiong, Y. Targeted ubiquitination of CDT1 by the DDB1–CUL4A–ROC1 ligase in response to DNA damage. Nat. Cell Biol. 6, 1003–1009 (2004).
  Article CAS PubMed Google Scholar
• Kondo, T. et al. Rapid degradation of Cdt1 upon UV-induced DNA damage is mediated by SCFSkp2 complex. J. Biol. Chem. 279, 27315–27319 (2004).
  Article CAS PubMed Google Scholar
• Arias, E.E. & Walter, J.C. PCNA functions as a molecular platform to trigger Cdt1 destruction and prevent re-replication. Nat. Cell Biol. 8, 84–90 (2006).
  Article CAS PubMed Google Scholar
• Hu, J. & Xiong, Y. An evolutionarily conserved function of proliferating cell nuclear antigen for Cdt1 degradation by the Cul4-Ddb1 ubiquitin ligase in response to DNA damage. J. Biol. Chem. 281, 3753–3756 (2006).
  Article CAS PubMed Google Scholar
• Jin, J., Arias, E.E., Chen, J., Harper, J.W. & Walter, J.C. A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 23, 709–721 (2006).
  Article CAS PubMed Google Scholar
• Senga, T. et al. PCNA is a cofactor for Cdt1 degradation by CUL4/DDB1-mediated N-terminal ubiquitination. J. Biol. Chem. 281, 6246–6252 (2006).
  Article CAS PubMed Google Scholar
• Havens, C.G. & Walter, J.C. Docking of a specialized PIP Box onto chromatin-bound PCNA creates a degron for the ubiquitin ligase CRL4Cdt2. Mol. Cell 35, 93–104 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Havens, C.G. et al. Direct role for proliferating cell nuclear antigen in substrate recognition by the E3 ubiquitin ligase CRL4Cdt2. J. Biol. Chem. 287, 11410–11421 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Kim, Y., Starostina, N.G. & Kipreos, E.T. The CRL4Cdt2 ubiquitin ligase targets the degradation of p21Cip1 to control replication licensing. Genes Dev. 22, 2507–2519 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Nishitani, H. et al. CDK inhibitor p21 is degraded by a proliferating cell nuclear antigen-coupled Cul4–DDB1Cdt2 pathway during S phase and after UV irradiation. J. Biol. Chem. 283, 29045–29052 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Abbas, T. et al. PCNA-dependent regulation of p21 ubiquitylation and degradation via the CRL4Cdt2 ubiquitin ligase complex. Genes Dev. 22, 2496–2506 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Centore, R.C. et al. CRL4Cdt2-mediated destruction of the histone methyltransferase Set8 prevents premature chromatin compaction in S phase. Mol. Cell 40, 22–33 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Liu, C. et al. Cop9/signalosome subunits and Pcu4 regulate ribonucleotide reductase by both checkpoint-dependent and -independent mechanisms. Genes Dev. 17, 1130–1140 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Bacquin, A. et al. The helicase FBH1 is tightly regulated by PCNA via CRL4Cdt2-mediated proteolysis in human cells. Nucleic Acids Res. 41, 6501–6513 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Shibutani, S.T. et al. Intrinsic negative cell cycle regulation provided by PIP box- and Cul4Cdt2-mediated destruction of E2f1 during S phase. Dev. Cell 15, 890–900 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Kim, S.H. & Michael, W.M. Regulated proteolysis of DNA polymerase eta during the DNA-damage response in C. elegans. Mol. Cell 32, 757–766 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Mortensen, U.H., Bendixen, C., Sunjevaric, I. & Rothstein, R. DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl. Acad. Sci. USA 93, 10729–10734 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Shinohara, A., Shinohara, M., Ohta, T., Matsuda, S. & Ogawa, T. Rad52 forms ring structures and co-operates with RPA in single-strand DNA annealing. Genes Cells 3, 145–156 (1998).
  Article CAS PubMed Google Scholar
• Sacher, M., Pfander, B., Hoege, C. & Jentsch, S. Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat. Cell Biol. 8, 1284–1290 (2006).
  Article CAS PubMed Google Scholar
• Torres-Rosell, J. et al. The Smc5–Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 9, 923–931 (2007).
  Article CAS PubMed Google Scholar
• Altmannova, V. et al. Rad52 SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Res. 38, 4708–4721 (2010).
  Article CAS PubMed PubMed Central 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).
  Article 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).
  Article CAS PubMed Google Scholar
• Parker, J.L. et al. SUMO modification of PCNA is controlled by DNA. EMBO J. 27, 2422–2431 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Windecker, H. & Ulrich, H.D. Architecture and assembly of poly-SUMO chains on PCNA in Saccharomyces cerevisiae. J. Mol. Biol. 376, 221–231 (2008).
  Article CAS PubMed Google Scholar
• Eilebrecht, S., Smet-Nocca, C., Wieruszeski, J.M. & Benecke, A. SUMO-1 possesses DNA binding activity. BMC Res. Notes 3, 146 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Zilio, N. et al. DNA-dependent SUMO modification of PARP-1. DNA Repair (Amst.) 12, 761–773 (2013).
  Article CAS Google Scholar
• Woodhouse, B.C. & Dianov, G.L. Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair (Amst.) 7, 1077–1086 (2008).
  Article CAS Google Scholar
• Martin, N. et al. PARP-1 transcriptional activity is regulated by SUMOylation upon heat shock. EMBO J. 28, 3534–3548 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Messner, S. et al. SUMOylation of poly(ADP-ribose) polymerase 1 inhibits its acetylation and restrains transcriptional coactivator function. FASEB J. 23, 3978–3989 (2009).
  Article CAS PubMed Google Scholar
• Wilson, M.D., Harreman, M. & Svejstrup, J.Q. Ubiquitylation and degradation of elongating RNA polymerase II: the last resort. Biochim. Biophys. Acta 1829, 151–157 (2013).
  Article CAS PubMed Google Scholar
• Harreman, M. et al. Distinct ubiquitin ligases act sequentially for RNA polymerase II polyubiquitylation. Proc. Natl. Acad. Sci. USA 106, 20705–20710 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Somesh, B.P. et al. Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest. Cell 121, 913–923 (2005).
  Article CAS PubMed Google Scholar
• Somesh, B.P. et al. Communication between distant sites in RNA polymerase II through ubiquitylation factors and the polymerase CTD. Cell 129, 57–68 (2007).
  Article CAS PubMed Google Scholar
• Wilson, M.D. et al. Proteasome-mediated processing of Def1, a critical step in the cellular response to transcription stress. Cell 154, 983–995 (2013).
  Article 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).
  Article CAS PubMed Google Scholar
• Nakagawa, K. & Yokosawa, H. Degradation of transcription factor IRF-1 by the ubiquitin-proteasome pathway: the C-terminal region governs the protein stability. Eur. J. Biochem. 267, 1680–1686 (2000).
  Article CAS PubMed Google Scholar
• Landré, V., Pion, E., Narayan, V., Xirodimas, D.P. & Ball, K.L. DNA-binding regulates site-specific ubiquitination of IRF-1. Biochem. J. 449, 707–717 (2013).
  Article PubMed CAS Google Scholar
• Cortázar, D., Kunz, C., Saito, Y., Steinacher, R. & Schar, P. The enigmatic thymine DNA glycosylase. DNA Repair (Amst.) 6, 489–504 (2007).
  Article CAS Google Scholar
• Hardeland, U., Steinacher, R., Jiricny, J. & Schär, P. Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 21, 1456–1464 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Fitzgerald, M.E. & Drohat, A.C. Coordinating the initial steps of base excision repair: apurinic/apyrimidinic endonuclease 1 actively stimulates thymine DNA glycosylase by disrupting the product complex. J. Biol. Chem. 283, 32680–32690 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Baba, D. et al. Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 435, 979–982 (2005).
  Article CAS PubMed 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).
  Article CAS PubMed Google Scholar
• Kapetanaki, M.G. et al. The DDB1–CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc. Natl. Acad. Sci. USA 103, 2588–2593 (2006).
  Article CAS PubMed Google Scholar
• Wang, H. et al. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell 22, 383–394 (2006).
  Article PubMed CAS Google Scholar
• Lan, L. et al. Monoubiquitinated histone H2A destabilizes photolesion-containing nucleosomes with concomitant release of UV-damaged DNA-binding protein E3 ligase. J. Biol. Chem. 287, 12036–12049 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Shilatifard, A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu. Rev. Biochem. 75, 243–269 (2006).
  Article CAS PubMed Google Scholar
• Sato, K., Toda, K., Ishiai, M., Takata, M. & Kurumizaka, H. DNA robustly stimulates FANCD2 monoubiquitylation in the complex with FANCI. Nucleic Acids Res. 40, 4553–4561 (2012).
  Article CAS PubMed PubMed Central Google Scholar