Cooperativity of the SUMO and ubiquitin pathways in genome stability

Biomolecules

Volumn 6, Issue 1, 2016, Pages

  Nie, Minghua ^a   Boddy, Michael N ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

DNA damage; STUbL; SUMO; Ubiquitin

Indexed keywords

FANCONI ANEMIA GROUP D2 PROTEIN; PEPTIDES AND PROTEINS; PROTEIN NSE1; PROTEIN ZNF451; RAD18 PROTEIN; RAD51 PROTEIN; RAD52 PROTEIN; RAP1 PROTEIN; RECQ HELICASE; SUMO 2 PROTEIN; SUMO PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP C PROTEIN; SUMO 1 PROTEIN;

DNA REPAIR; DNA REPLICATION; ENZYME ACTIVITY; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SUMOYLATION; UBIQUITINATION; DNA DAMAGE; METABOLISM;

DNA DAMAGE; DNA REPAIR; GENOMIC INSTABILITY; SIGNAL TRANSDUCTION; SUMO-1 PROTEIN; UBIQUITIN;

EID: 85012040214     PISSN: None     EISSN: 2218273X     Source Type: Journal    
DOI: 10.3390/biom6010014     Document Type: Review

References (94)

1. Friedberg E.C.; Walker G.C.; Siede W.; Wood R.D.; Schultz R.A.; Ellenburger T. DNA Repair and Mutagenesis; American Society for Microbiology Press: Washington, DC, USA, 2006; p. 1118.
2. Polo, S.E.; Jackson, S.P. Dynamics of DNA damage response proteins at DNA breaks: A focus on protein modifications. Genes Dev. 2011, 25, 409–433.
3. Kerscher, O.; Felberbaum, R.; Hochstrasser, M. Modification of Proteins by Ubiquitin and Ubiquitin-Like Proteins. Annu. Rev. Cell Dev. Biol. 2006, 22, 159–180.
4. Dantuma, N.P.; van Attikum, H. Spatiotemporal regulation of posttranslational modifications in the DNA damage response. EMBO J. 2016, 35, 6–23.
5. Sarangi, P.; Zhao X. SUMO-mediated regulation of DNA damage repair and responses. Trends Biochem. Sci.2015, 40, 233–242.
6. Jackson, S.P.; Durocher, D. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 2013, 49,795–807.
7. Bologna, S.; Ferrari, S. It takes two to tango: Ubiquitin and SUMO in the DNA damage response. Front. Genet. 2013, 4, 106.
8. Pinder, J.B.; Attwood, K.M.; Dellaire, G. Reading, writing, and repair: The role of ubiquitin and the ubiquitin-like proteins in DNA damage signaling and repair. Front. Genet. 2013, 4, 45.
9. Zhao Y.; Brickner J.R.; Majid M.C.; Mosammaparast N. Crosstalk between ubiquitin and other post-translational modifications on chromatin during double-strand break repair. Trends Cell. Biol. 2014, 24, 426–434.
10. Ulrich, H.D. Two-way communications between ubiquitin-like modifiers and DNA. Nat. Struct. Mol. Biol.2014, 21, 317–324.
11. Ulrich, H.D. Ubiquitin and SUMO in DNA repair at a glance. J. Cell Sci. 2012, 125, 249–254.
12. Ulrich, H.D. Mutual interactions between the SUMO and ubiquitin systems: A plea of no contest. Trends Cell. Biol.2005, 15, 525–532.
13. Heideker, J.; Perry, J.J.; Boddy, M.N. Genome stability roles of SUMO-targeted ubiquitin ligases. DNA Repair 2009, 8, 517–524.
14. Perry, J.J.; Tainer J.A.; Boddy, M.N. A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem. Sci. 2008, 33, 201–208.
15. Sriramachandran, A.M.; Dohmen, R.J. SUMO-targeted ubiquitin ligases. Biochim. Biophys. Acta 2014, 1843,75–85.
16. Geoffroy, M.C.; Hay, R.T. An additional role for SUMO in ubiquitin-mediated proteolysis. Nat. Rev. Mol. Cell Biol. 2009, 10, 564–568.
17. Hunter, T.; Sun, H. Crosstalk between the SUMO and ubiquitin pathways. Ernst Scher. Found. Symp. Proc. 2008, 2008, 1–16.
18. Chung, I.; Zhao X. DNA break-induced sumoylation is enabled by collaboration between a SUMO ligase and the ssDNA-binding complex RPA. Genes Dev. 2015, 29, 1593–1598.
19. Andrews, E.A.; Palecek, J.; Sergeant, J.; Taylor, E.; Lehmann, A.R.; Watts, F.Z. Nse2, a component of the Smc5–6 complex, is a SUMO ligase required for the response to DNA damage. Mol. Cell. Biol. 2005, 25, 185–196.
20. McDonald, W.H.; Pavlova, Y.; Yates, J.R., 3rd; Boddy, M.N. Novel essential DNA repair proteins Nse1 and Nse2 are subunits of the fission yeast Smc5-Smc6 complex. J. Biol. Chem. 2003, 278, 45460–45467.
21. Potts, P.R.; Yu, H. Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol. Cell. Biol. 2005, 25, 7021–7032.
22. 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 2005, 102, 4777–4782.
23. Pebernard, S.; Schaffer, L.; Campbell, D.; Head, S.R.; Boddy, M.N. Localization of Smc5/6 to centromeres and telomeres requires heterochromatin and SUMO, respectively. EMBO J. 2008, 27, 3011–3023.
24. Pebernard, S.; Perry, J.J.; Tainer J.A.; Boddy, M.N. Nse1 RING-like domain supports functions of the Smc5-Smc6 holocomplex in genome stability. Mol. Biol. Cell 2008, 19, 4099–4109.
25. Tapia-Alveal, C.; O’Connell, M.J. Nse1-dependent recruitment of Smc5/6 to lesion-containing loci contributes to the repair defects of mutant complexes. Mol. Biol. Cell 2011, 22, 4669–4682.
26. 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 2010, 39, 963–974.
27. Raschle, M.; Smeenk, G.; Hansen, R.K.; Temu, T.; Oka, Y.; Hein, M.Y.; Nagaraj, N.; Long, D.T.; Walter, J.C.; Hofmann, K.; et al. Proteomics reveals dynamic assembly of repair complexes during bypass of DNAcross-links. Science 2015, 348.
28. Wu, C.S.; Ouyang, J.; Mori, E.; Nguyen, H.D.; Marechal, A.; Hallet, A.; Chen, D.J.; Zou, L. SUMOylation of ATRIP potentiates DNA damage signaling by boosting multiple protein interactions in the ATR pathway. Genes Dev. 2014, 28, 1472–1484.
29. Watts, F.Z.; Skilton, A.; Ho, J.C.; Boyd, L.K.; Trickey, M.A.; Gardner, L.; Ogi, F.; Outwin, E.A. The role of Schizosaccharomyces pombe SUMO ligases in genome stability. Biochem. Soc. Trans. 2007, 35, 1379–1384.
30. Johnson, E.S.; Gupta, A.A. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 2001, 106, 735–744.
31. Galanty, Y.; Belotserkovskaya, R.; Coates, J.; Polo, S.; Miller, K.M.; Jackson, S.P. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 2009, 462, 935–939.
32. Wu, C.S.; Zou, L. The SUMO (Small Ubiquitin-likeModifier) Ligase PIAS3 Primes ATR for Checkpoint Activation. J. Biol. Chem. 2016, 291, 279–290.
33. Morris, J.R.; Boutell, C.; Keppler, M.; Densham, R.; Weekes, D.; Alamshah, A.; Butler, L.; Galanty, Y.; Pangon, L.; Kiuchi, T.; et al. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 2009, 462, 886–890.
34. Ryu, T.; Spatola, B.; Delabaere, L.; Bowlin, K.; Hopp, H.; Kunitake, R.; Karpen, G.H.; Chiolo, I. Heterochromatic breaks move to the nuclear periphery to continue recombinational repair. Nat. Cell Biol. 2015, 17, 1401–1411.
35. Dou, H.; Huang, C.; Singh, M.; Carpenter, P.B.; Yeh, E.T. Regulation of DNA repair through deSUMOylation and SUMOylation of replication protein A complex. Mol. Cell 2010, 39, 333–345.
36. Merrill, J.C.; Melhuish, T.A.; Kagey, M.H.; Yang, S.H.; Sharrocks, A.D.; Wotton, D. A role for non-covalentSUMO interaction motifs in Pc2/CBX4 E3 activity. PLoS ONE 2010, 5, e8794.
37. Yang, S.H.; Sharrocks, A.D. The SUMO E3 ligase activity of Pc2 is coordinated through a SUMO interactionmotif. Mol. Cell. Biol. 2010, 30, 2193–2205.
38. Balakirev, M.Y.; Mullally, J.E.; Favier, A.; Assard, N.; Sulpice, E.; Lindsey, D.F.; Rulina, A.V.; Gidrol, X.; Wilkinson, K.D. Wss1 metalloprotease partners with Cdc48/Doa1 in processing genotoxic SUMO conjugates. Elife 2015, 4.
39. Guervilly, J.H.; Takedachi, A.; Naim, V.; Scaglione, S.; Chawhan, C.; Lovera, Y.; Despras, E.; Kuraoka, I.; Kannouche, P.; Rosselli, F.; et al. The SLX4 complex is a SUMO E3 ligase that impacts on replication stress outcome and genome stability. Mol. Cell 2015, 57, 123–137.
40. Cappadocia, L.; Pichler, A.; Lima, C.D. Structural basis for catalytic activation by the human ZNF451 SUMO E3 ligase. Nat. Struct. Mol. Biol. 2015, 22, 968–975
41. Eisenhardt, N.; Chaugule, V.K.; Koidl, S.; Droescher, M.; Dogan, E.; Rettich, J.; Sutinen, P.; Imanishi, S.Y.; Hofmann, K.; Palvimo, J.J.; et al. A new vertebrate SUMO enzyme family reveals insights into SUMO-chain assembly. Nat. Struct. Mol. Biol. 2015, 22, 959–967.
42. Ouyang, J.; Garner, E.; Hallet, A.; Nguyen, H.D.; Rickman, K.A.; Gill, G.; Smogorzewska, A.; Zou, L. Noncovalent interactions with SUMO and ubiquitin orchestrate distinct functions of the SLX4 complex in genome maintenance. Mol. Cell 2015, 57, 108–122.
43. Gonzalez-Prieto, R.; Cuijpers, S.A.; Luijsterburg, M.S.; van Attikum, H.; Vertegaal, A.C. SUMOylation and PARylation cooperate to recruit and stabilize SLX4 at DNA damage sites. EMBO Rep. 2015, 16, 512–519.
44. O’Neill, B.M.; Hanway, D.; Winzeler, E.A.; Romesberg, F.E. Coordinated functions of WSS1, PSY2 and TOF1 in the DNA damage response. Nucleic Acids Res. 2004, 32, 6519–6530.
45. Stingele, J.; Schwarz, M.S.; Bloemeke, N.; Wolf, P.G.; Jentsch, S. A DNA-dependent protease involved in DNA-protein crosslink repair. Cell 2014, 158, 327–338.
46. Nie, M.; Aslanian, A.; Prudden, J.; Heideker, J.; Vashisht, A.A.; Wohlschlegel, J.A.; Yates, J.R., III; Boddy, M.N. Dual Recruitment of Cdc48 (p97)-Ufd1-Npl4 Ubiquitin-selective Segregase by Small Ubiquitin-like Modifier Protein (SUMO) and Ubiquitin in SUMO-targeted Ubiquitin Ligase-mediated Genome Stability Functions. J. Biol. Chem. 2012, 287, 29610–29619.
47. Parker, J.L.; Ulrich, H.D. SIM-dependent enhancement of substrate-specific SUMOylation by a ubiquitin ligase in vitro. Biochem. J. 2014, 457, 435–440.
48. Boddy, M.N.; Shanahan, P.; McDonald, W.H.; Lopez-Girona, A.; Noguchi, E.; Yates, J.R., III; Russell, P. Replication checkpoint kinase Cds1 regulates recombinational repair protein Rad60. Mol. Cell. Biol. 2003, 23, 5939–5946.
49. Morishita, T.; Tsutsui, Y.; Iwasaki, H.; Shinagawa, H. The Schizosaccharomyces pombe rad60 Gene Is Essential for Repairing Double-Strand DNA Breaks Spontaneously Occurring during Replication and Induced by DNA-Damaging Agents. Mol. Cell. Biol. 2002, 22, 3537–3548.
50. Prudden, J.; Perry, J.J.; Arvai, A.S.; Tainer J.A.; Boddy, M.N. Molecular mimicry of SUMO promotes DNA repair. Nat. Struct. Mol. Biol. 2009, 16, 509–516.
51. Prudden, J.; Perry, J.J.; Nie, M.; Vashisht, A.A.; Arvai, A.S.; Hitomi, C.; Guenther, G.; Wohlschlegel, J.A.; Tainer J.A.; Boddy, M.N. DNA repair and global sumoylation are regulated by distinct Ubc9 noncovalent complexes. Mol. Cell. Biol. 2011, 31, 2299–2310.
52. Sekiyama, N.; Arita, K.; Ikeda, Y.; Hashiguchi, K.; Ariyoshi, M.; Tochio, H.; Saitoh, H.; Shirakawa, M. Structural basis for regulation of poly-SUMO chain by a SUMO-like domain of Nip45. Proteins 2010, 78, 1491–1502.
53. Prudden, J.; Pebernard, S.; Raffa, G.; Slavin, D.A.; Perry, J.J.; Tainer J.A.; McGowan, C.H.; Boddy, M.N. SUMO-targeted ubiquitin ligases in genome stability. EMBO J. 2007, 26, 4089–4101.
54. Albuquerque, C.P.; Wang, G.; Lee, N.S.; Kolodner, R.D.; Putnam, C.D.; Zhou, H. Distinct SUMO ligases cooperate with Esc2 and Slx5 to suppress duplication-mediated genome rearrangements. PLoS Genet. 2013, 9, e1003670.
55. Heideker, J.; Prudden, J.; Perry, J.J.; Tainer J.A.; Boddy, M.N. SUMO-Targeted Ubiquitin Ligase, Rad60, and Nse2 SUMO Ligase Suppress Spontaneous Top1-Mediated DNA Damage and Genome Instability. PLoS Genet. 2011, 7, e1001320.
56. Simpson-Lavy, K.J.; Johnston, M. SUMOylation regulates the SNF1 protein kinase. Proc. Natl. Acad. Sci. USA 2013, 110, 17432–17437.
57. Urulangodi, M.; Sebesta, M.; Menolfi, D.; Szakal, B.; Sollier, J.; Sisakova, A.; Krejci, L.; Branzei, D. Local regulation of the Srs2 helicase by the SUMO-like domain protein Esc2 promotes recombination at sites of stalled replication. Genes Dev. 2015, 29, 2067–2080.
58. Choi, K.; Szakal, B.; Chen, Y.H.; Branzei, D.; Zhao X. The Smc5/6 complex and Esc2 influence multiple replication-associated recombination processes in Saccharomyces cerevisiae. Mol. Biol. Cell 2010, 21, 2306–2314.
59. Sollier, J.; Driscoll, R.; Castellucci, F.; Foiani, M.; Jackson, S.P.; Branzei, D. The Saccharomyces cerevisiae Esc2 and Smc5–6 proteins promote sister chromatid junction-mediated intra-S repair. Mol. Biol. Cell 2009, 20, 1671–1682.
60. Xie, Y.; Rubenstein, E.M.; Matt, T.; Hochstrasser, M. SUMO-independent in vivo activity of a SUMO-targeted ubiquitin ligase toward a short-lived transcription factor. Genes Dev. 2010, 24, 893–903.
61. Hickey, C.M.; Hochstrasser, M. STUbL-mediated degradation of the transcription factor MATalpha2 requires degradation elements that coincide with corepressor binding sites. Mol. Biol. Cell 2015, 26, 3401–3412.
62. Nie, M.; Vashisht, A.A.; Wohlschlegel, J.A.; Boddy, M.N. High Confidence Fission Yeast SUMO Conjugates Identified by Tandem Denaturing Affinity Purification. Sci. Rep. 2015, 5, 14389.
63. Nagai, S.; Dubrana, K.; Tsai-Pflugfelder, M.; Davidson, M.B.; Roberts, T.M.; Brown, G.W.; Varela, E.; Hediger, F.; Gasser, S.M.; Krogan, N.J. Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 2008, 322, 597–602.
64. Su, X.A.; Dion, V.; Gasser, S.M.; Freudenreich, C.H. Regulation of recombination at yeast nuclear pores controls repair and triplet repeat stability. Genes Dev. 2015, 29, 1006–1017.
65. Torres-Rosell, J.; Sunjevaric, I.; De Piccoli, G.; Sacher, M.; Eckert-Boulet, N.; Reid, R.; Jentsch, S.; Rothstein, R.; Aragón, L.; Lisby, M. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 2007, 9, 923–931.
66. Yang, K.; Moldovan, G.L.; Vinciguerra, P.; Murai, J.; Takeda, S.; D’Andrea, A.D. Regulation of the Fanconi anemia pathway by a SUMO-like delivery network. Genes Dev. 2011, 25, 1847–1858.
67. Groocock, L.M.; Nie, M.; Prudden, J.; Moiani, D.; Wang, T.; Cheltsov, A.; Rambo, R.P.; Arvai, A.S.; Hitomi, C.; Tainer J.A.; et al. RNF4 interacts with both SUMO and nucleosomes to promote the DNA damage response. EMBO Rep. 2014, 15, 601–608.
68. Hakli, 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. 2001, 276, 23653–23660.
69. Lescasse, R.; Pobiega, S.; Callebaut, I.; Marcand, S. End-joining inhibition at telomeres requires the translocase and polySUMO-dependent ubiquitin ligase Uls1. EMBO J. 2013, 32, 805–815.
70. Galanty, Y.; Belotserkovskaya, R.; Coates, J.; Jackson, S.P. RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev. 2012, 26, 1179–1195.
71. Yin, Y.; Seifert, A.; Chua, J.S.; Maure, J.F.; Golebiowski, F.; Hay, R.T. SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev. 2012, 26, 1196–1208.
72. Luo, K.; Zhang, H.; Wang, L.; Yuan, J.; Lou, Z. Sumoylation ofMDC1 is important for proper DNA damage response. EMBO J. 2012, 31, 3008–3019.
73. Mullen, J.R.; Brill, S.J. Activation of the Slx5-Slx8 ubiquitin ligase by poly-small ubiquitin-likemodifier conjugates.J. Biol. Chem. 2008, 283, 19912–19921.
74. Guzzo, C.M.; Berndsen, C.E.; Zhu, J.; Gupta, V.; Datta, A.; Greenberg, R.A.; Wolberger, C.; Matunis, M.J. RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage. Sci Signal. 2012, 5, ra88.
75. Kohler, J.B.; Jorgensen, M.L.; Beinoraite, G.; Thorsen, M.; Thon, G. Concerted action of the ubiquitin-fusion degradation protein 1 (Ufd1) and Sumo-targeted ubiquitin ligases (STUbLs) in the DNA-damage response. PLoS ONE 2013, 8, e80442.
76. Nie, M.; Boddy, M.N. Pli1PIAS1 SUMO Ligase Protected by the Nuclear Pore-associated SUMO Protease Ulp1SENP1/2. J. Biol. Chem. 2015, 290, 22678–22685.
77. Kohler, J.B.; Tammsalu, T.; Jorgensen, M.M.; Steen, N.; Hay, R.T.; Thon, G. Targeting of SUMO substrates to a Cdc48-Ufd1-Npl4 segregase and STUbL pathway in fission yeast. Nat. Commun. 2015, 6, 8827.
78. 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. Ubiquitin-SUMO circuitry controls activated fanconi anemia ID complex dosage in response to DNA damage. Mol. Cell 2015, 57, 150–164.
79. Golebiowski, F.; Matic, I.; Tatham, M.H.; Cole, C.; Yin, Y.; Nakamura, A.; Cox, J.; Barton, G.J.; Mann, M.; Hay, R.T. System-wide changes to SUMO modifications in response to heat shock. Sci. Signal. 2009, 2, ra24.
80. Tatham, M.H.; Matic, I.; Mann, M.; Hay, R.T. Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci. Signal. 2011, 4, rs4.
81. Sacher, M.; Pfander, B.; Hoege, C.; Jentsch, S. Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat. Cell Biol. 2006, 8, 1284–1290.
82. Altmannova, V.; Eckert-Boulet, N.; Arneric, M.; Kolesar, P.; Chaloupkova, R.; Damborsky, J.; Sung, P.; Zhao X.; Lisby, M.; Krejci, L. Rad52 SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Res. 2010, 38, 4708–4721.
83. Bergink, S.; Ammon, T.; Kern, M.; Schermelleh, L.; Leonhardt, H.; Jentsch, S. Role of Cdc48/p97 as a SUMO-targeted segregase curbing Rad51-Rad52 interaction. Nat. Cell Biol. 2013, 15, 526–532.
84. Psakhye, I.; Jentsch, S. Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 2012, 151, 807–820.
85. Sugasawa, K.; Okuda, Y.; Saijo, M.; Nishi, R.; Matsuda, N.; Chu, G.; Mori, T.; Iwai, S.; Tanaka, K.; Tanaka, K.; et al. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 2005, 121, 387–400.
86. Puumalainen, M.R.; Lessel, D.; Ruthemann, P.; Kaczmarek, N.; Bachmann, K.; Ramadan, K.; Naegeli, H. Chromatin retention of DNA damage sensors DDB2 and XPC through loss of p97 segregase causes genotoxicity. Nat. Commun. 2014, 5.
87. Akita, M.; Tak, Y.S.; Shimura, T.; Matsumoto, S.; Okuda-Shimizu, Y.; Shimizu, Y.; Nishi, R.; Saitoh, H.; Iwai, S.; Mori, T.; et al. SUMOylation of xeroderma pigmentosum group C protein regulates DNA damage recognition during nucleotide excision repair. Sci. Rep. 2015, 5, 10984.
88. Poulsen, S.L.; Hansen, R.K.; Wagner, S.A.; van Cuijk, L.; van Belle, G.J.; Streicher, W.; Wikström, M.; Choudhary, C.; Houtsmuller, A.B.; Marteijn, J.A.; et al. RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response. J. Cell Biol. 2013, 201, 797–807.
89. van Cuijk, L.; van Belle, G.J.; Turkyilmaz, Y.; Poulsen, S.L.; Janssens, R.C.; Theil, A.F.; Sabatella, M.; Lans, H.; Mailand, N.; Houtsmuller, A.B.; et al. SUMO and ubiquitin-dependent XPC exchange drives nucleotide excision repair. Nat. Commun. 2015, 6, 7499.
90. Cybulski, K.E.; Howlett, N.G. FANCP/SLX4: A Swiss army knife of DNA interstrand crosslink repair. Cell Cycle 2011, 10, 1757–1763.
91. Garner, E.; Kim, Y.; Lach, F.P.; Kottemann, M.C.; Smogorzewska, A. Human GEN1 and the SLX4-associated nucleases MUS81 and SLX1 are essential for the resolution of replication-induced Holliday junctions. Cell Rep. 2013, 5, 207–215.
92. Wechsler, T.; Newman, S.; West, S.C. Aberrant chromosome morphology in human cells defective for Holliday junction resolution. Nature 2011, 471, 642–646.
93. Fekairi, S.; Scaglione, S.; Chahwan, C.; Taylor, E.R.; Tissier, A.; Coulon, S.; Dong, M.; Ruse, C.; Yates, J.R., III; Russell, P.; et al. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 2009, 138, 78–89.
94. Svendsen, J.M.; Smogorzewska, A.; Sowa, M.E.; O’Connell, B.C.; Gygi, S.P.; Elledge, S.J.; Harper, J.W. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 2009, 138, 63–77.