Lysine-targeting specificity in ubiquitin and ubiquitin-like modification pathways

Nature Structural and Molecular Biology

Volumn 21, Issue 4, 2014, Pages 308-316

  Mattiroli, Francesca ^a,b   Sixma, Titia K ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CULLIN; LYSINE; POLYUBIQUITIN; PROTEIN; UBIQUITIN;

CELL CYCLE REGULATION; CONSENSUS SEQUENCE; DNA DAMAGE; DYNAMICS; ENZYMATIC DEGRADATION; ENZYME ACTIVE SITE; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; HUMAN; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TARGETING; REVIEW; RING FINGER MOTIF; SUMOYLATION; UBIQUITIN LIKE MODIFICATION; UBIQUITINATION;

HUMANS; LYSINE; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUBSTRATE SPECIFICITY; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84898734084     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2792     Document Type: Review

References (132)

1. Hochstrasser, M. Origin and function of ubiquitin-like proteins. Nature 458, 422-429 (2009
2. 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
3. Mattiroli, F. et al. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150, 1182-1195 (2012
4. Wang, H. et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature 431, 873-878 (2004
5. Sun, Z.W. & Allis, C.D. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418, 104-108 (2002
6. Dorsman, J.C. et al. Identification of the Fanconi anemia complementation group I gene, FANCI. Cell. Oncol. 29, 211-218 (2007
7. Sims, A.E. et al. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat. Struct. Mol. Biol. 14, 564-567 (2007
8. Smogorzewska, A. et al. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 129, 289-301 (2007
9. Hunt, L.T. & Dayhoff, M.O. Amino-Terminal sequence identity of ubiquitin and the nonhistone component of nuclear protein A24. Biochem. Biophys. Res. Commun. 74, 650-655 (1977
10. Tatham, M.H., Matic, I., Mann, M. & Hay, R.T. Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci. Signal. 4, rs4 (2011
11. Wagner, S.A. et al. A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol. Cell. Proteomics 10, M111 013284 (2011
12. Kessler, B.M. Ubiquitin-omics reveals novel networks and associations with human disease. Curr. Opin. Chem. Biol. 17, 59-65 (2013
13. Danielsen, J.M. et al. Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol. Cell. Proteomics 10, M110 003590 (2011
14. Behrends, C. & Harper, J.W. Constructing and decoding unconventional ubiquitin chains. Nat. Struct. Mol. Biol. 18, 520-528 (2011
15. Xu, G., Paige, J.S. & Jaffrey, S.R. Global analysis of lysine ubiquitination by ubiquitin remnant immunoaffinity profiling. Nat. Biotechnol. 28, 868-873 (2010
16. Sarraf, S.A. et al. Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature 496, 372-376 (2013
17. Deshaies, R.J. & Joazeiro, C.A. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434 (2009
18. Kamadurai, H.B. et al. Mechanism of ubiquitin ligation and lysine prioritization by a HECT E3. eLife 2, e00828 (2013
19. Varshavsky, A. Naming a targeting signal. Cell 64, 13-15 (1991
20. Winston, J.T. et al. The SCFβ-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in I?Ba and β-catenin and stimulates I?Ba ubiquitination in vitro. Genes Dev. 13, 270-283 (1999
21. Orlicky, S., Tang, X., Willems, A., Tyers, M. & Sicheri, F. Structural basis for phosphodependent substrate selection and orientation by the SCFCdc4 ubiquitin ligase. Cell 112, 243-256 (2003
22. Jin, J. et al. SCFβ-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes Dev. 17, 3062-3074 (2003
23. Bentley, M.L. et al. Recognition of UbcH5c and the nucleosome by the Bmi1/Ring1b ubiquitin ligase complex. EMBO J. 30, 3285-3297 (2011
24. Buchwald, G. et al. Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b. EMBO J. 25, 2465-2474 (2006
25. Petroski, M.D. & Deshaies, R.J. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6, 9-20 (2005
26. Zheng, N. et al. Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416, 703-709 (2002
27. Smit, J.J. & Sixma, T.K. RBR E3-ligases at work. EMBO Rep. 15, 142-154 (2014
28. Duda, D.M. et al. Structural regulation of cullin-RING ubiquitin ligase complexes. Curr. Opin. Struct. Biol. 21, 257-264 (2011
29. Fischer, E.S. et al. The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell 147, 1024-1039 (2011
30. Petroski, M.D. & Deshaies, R.J. Context of multiubiquitin chain attachment influences the rate of Sic1 degradation. Mol. Cell 11, 1435-1444 (2003
31. Tang, X. et al. Suprafacial orientation of the SCFCdc4 dimer accommodates multiple geometries for substrate ubiquitination. Cell 129, 1165-1176 (2007
32. King, R.W., Deshaies, R.J., Peters, J.M. & Kirschner, M.W. How proteolysis drives the cell cycle. Science 274, 1652-1659 (1996
33. Skaar, J.R. & Pagano, M. Control of cell growth by the SCF and APC/C ubiquitin ligases. Curr. Opin. Cell Biol. 21, 816-824 (2009
34. Min, M., Mayor, U. & Lindon, C. Ubiquitination site preferences in anaphase promoting complex/cyclosome (APC/C) substrates. Open Bio. 3, 130097 (2013
35. Skowyra, D., Craig, K.L., Tyers, M., Elledge, S.J. & Harper, J.W. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91, 209-219 (1997
36. Sadowski, M., Suryadinata, R., Lai, X., Heierhorst, J. & Sarcevic, B. Molecular basis for lysine specificity in the yeast ubiquitin-conjugating enzyme Cdc34. Mol. Cell. Biol. 30, 2316-2329 (2010
37. Latres, E., Chiaur, D.S. & Pagano, M. The human F box protein β-Trcp associates with the Cul1/Skp1 complex and regulates the stability of β-catenin. Oncogene 18, 849-854 (1999
38. Wu, G. et al. Structure of a β-TrCP1-Skp1-β-catenin complex: Destruction motif binding and lysine specificity of the SCFβ-TrCP1 ubiquitin ligase. Mol. Cell 11, 1445-1456 (2003
39. Baldi, L., Brown, K., Franzoso, G. & Siebenlist, U. Critical role for lysines 21 and 22 in signal-induced, ubiquitin-mediated proteolysis of I?Ba. J. Biol. Chem. 271, 376-379 (1996
40. Vuillard, L., Nicholson, J. & Hay, R.T. A complex containing (TrCP recruits Cdc34 to catalyse ubiquitination of I?Ba. FEBS Lett. 455, 311-314 (1999
41. Kaiser, P., Flick, K., Wittenberg, C. & Reed, S.I. Regulation of transcription by ubiquitination without proteolysis: Cdc34/SCF(Met30)-mediated inactivation of the transcription factor Met4. Cell 102, 303-314 (2000
42. Menant, A., Baudouin-Cornu, P., Peyraud, C., Tyers, M. & Thomas, D. Determinants of the ubiquitin-mediated degradation of the Met4 transcription factor. J. Biol. Chem. 281, 11744-11754 (2006
43. Flick, K., Raasi, S., Zhang, H., Yen, J.L. & Kaiser, P. A ubiquitin-interacting motif protects polyubiquitinated Met4 from degradation by the 26S proteasome. Nat. Cell Biol. 8, 509-515 (2006
44. Chen, J. & Chen, Z.J. Regulation of NF-?B by ubiquitination. Curr. Opin. Immunol. 25, 4-12 (2013
45. Dou, H., Buetow, L., Sibbet, G.J., Cameron, K. & Huang, D.T. Essentiality of a non-RING element in priming donor ubiquitin for catalysis by a monomeric E3. Nat. Struct. Mol. Biol. 20, 982-986 (2013
46. Haglund, K. et al. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5, 461-466 (2003
47. Lee, J.T. & Gu, W. The multiple levels of regulation by p53 ubiquitination. Cell Death Differ. 17, 86-92 (2010
48. Rodriguez, M.S., Desterro, J.M., Lain, S., Lane, D.P. & Hay, R.T. Multiple C-Terminal lysine residues target p53 for ubiquitin-proteasome-mediated degradation. Mol. Cell. Biol. 20, 8458-8467 (2000
49. Shiloh, Y., Shema, E., Moyal, L. & Oren, M. RNF20-RNF40: A ubiquitin-driven link between gene expression and the DNA damage response. FEBS Lett. 585, 2795-2802 (2011
50. Dupont, S. et al. FAM/USP9x, a deubiquitinating enzyme essential for TGFβ signaling, controls Smad4 monoubiquitination. Cell 136, 123-135 (2009
51. Garner, E. & Smogorzewska, A. Ubiquitylation and the Fanconi anemia pathway. FEBS Lett. 585, 2853-2860 (2011
52. Cole, A.R., Lewis, L.P. & Walden, H. The structure of the catalytic subunit FANCL of the Fanconi anemia core complex. Nat. Struct. Mol. Biol. 17, 294-298 (2010
53. Alpi, A.F., Pace, P.E., Babu, M.M. & Patel, K.J. Mechanistic insight into site-restricted monoubiquitination of FANCD2 by Ube2t, FANCL, and FANCI. Mol. Cell 32, 767-777 (2008
54. Moldovan, G.L., Pfander, B. & Jentsch, S. PCNA, the maestro of the replication fork. Cell 129, 665-679 (2007
55. 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
56. Langerak, P., Nygren, A.O., Krijger, P.H., van Den Berk, P.C. & Jacobs, H. A/T mutagenesis in hypermutated immunoglobulin genes strongly depends on PCNAK164 modification. J. Exp. Med. 204, 1989-1998 (2007
57. Hibbert, R.G., Huang, A., Boelens, R. & Sixma, T.K. E3 ligase Rad18 promotes monoubiquitination rather than ubiquitin chain formation by E2 enzyme Rad6. Proc. Natl. Acad. Sci. USA 108, 5590-5595 (2011
58. Hibbert, R.G. & Sixma, T.K. Intrinsic flexibility of ubiquitin on proliferating cell nuclear antigen (PCNA) in translesion synthesis. J. Biol. Chem. 287, 39216-39223 (2012
59. Cao, R., Tsukada, Y. & Zhang, Y. Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol. Cell 20, 845-854 (2005
60. De Napoles, M. et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell 7, 663-676 (2004
61. Gatti, M. et al. A novel ubiquitin mark at the N-Terminal tail of histone H2As targeted by RNF168 ubiquitin ligase. Cell Cycle 11, 2538-2544 (2012
62. Fradet-Turcotte, A. et al. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 499, 50-54 (2013
63. Mattiroli, F., Uckelmann, M., Sahtoe, D.D., Van Dijk, W.J. & Sixma, T.K. The nucleosome acidic patch plays a critical role in RNF168-dependent ubiquitination of histone H2A. Nat. Commun. 5, 3291 (2014
64. Marchese, A. & Trejo, J. Ubiquitin-dependent regulation of G protein-coupled receptor trafficking and signaling. Cell. Signal. 25, 707-716 (2013
65. Stawiecka-Mirota, M. et al. Targeting of Sna3p to the endosomal pathway depends on its interaction with Rsp5p and multivesicular body sorting on its ubiquitylation. Traffic 8, 1280-1296 (2007
66. Duda, D.M. et al. Structure of HHARI, a RING-IBR-RING ubiquitin ligase: Autoinhibition of an Ariadne-family E3 and insights into ligation mechanism. Structure 21, 1030-1041 (2013
67. Spratt, D.E., Mercier, P. & Shaw, G.S. Structure of the HHARI catalytic domain shows glimpses of a HECT E3 ligase. PLoS ONE 8, e74047 (2013
68. Wauer, T. & Komander, D. Structure of the human Parkin ligase domain in an autoinhibited state. EMBO J. 32, 2099-2112 (2013
69. Trempe, J.F. et al. Structure of parkin reveals mechanisms for ubiquitin ligase activation. Science 340, 1451-1455 (2013
70. Stieglitz, B. et al. Structural basis for ligase-specific conjugation of linear ubiquitin chains by HOIP. Nature 503, 422-426 (2013
71. Kelsall, I.R. et al. TRIAD1 and HHARI bind to and are activated by distinct neddylated Cullin-RING ligase complexes. EMBO J. 32, 2848-2860 (2013
72. Smit, J.J. et al. Target specificity of the E3 ligase LUBAC for ubiquitin and NEMO relies on different minimal requirements. J. Biol. Chem. 288, 31728-31737 (2013
73. Wenzel, D.M. & Klevit, R.E. Following Ariadne's thread: A new perspective on RBR ubiquitin ligases. BMC Biol. 10, 24 (2012
74. Chen, Z. & Pickart, C.M. A 25-kilodalton ubiquitin carrier protein (E2) catalyzes multi-ubiquitin chain synthesis via lysine 48 of ubiquitin. J. Biol. Chem. 265, 21835-21842 (1990
75. 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
76. Eddins, M.J., Carlile, C.M., Gomez, K.M., Pickart, C.M. & Wolberger, C. Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation. Nat. Struct. Mol. Biol. 13, 915-920 (2006
77. Williamson, A. et al. Identification of a physiological E2 module for the human anaphase-promoting complex. Proc. Natl. Acad. Sci. USA 106, 18213-18218 (2009
78. Wickliffe, K.E., Lorenz, S., Wemmer, D.E., Kuriyan, J. & Rape, M. The mechanism of linkage-specific ubiquitin chain elongation by a single-subunit E2. Cell 144, 769-781 (2011
79. Plechanovová, A., Jaffray, E.G., Tatham, M.H., Naismith, J.H. & Hay, R.T. Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis. Nature 489, 115-120 (2012
80. Pruneda, J.N. et al. Structure of an E3:E2~Ub complex reveals an allosteric mechanism shared among RING/U-box ligases. Mol. Cell 47, 933-942 (2012
81. Dou, H., Buetow, L., Sibbet, G.J., Cameron, K. & Huang, D.T. BIRC7-E2 ubiquitin conjugate structure reveals the mechanism of ubiquitin transfer by a RING dimer. Nat. Struct. Mol. Biol. 19, 876-883 (2012
82. Scaglione, K.M. et al. The ubiquitin-conjugating enzyme (E2) Ube2w ubiquitinates the N terminus of substrates. J. Biol. Chem. 288, 18784-18788 (2013
83. Tatham, M.H., Plechanovova, A., Jaffray, E.G., Salmen, H. & Hay, R.T. Ube2W conjugates ubiquitin to a-Amino groups of protein N-Termini. Biochem. J. 453, 137-145 (2013
84. Kim, H.C. & Huibregtse, J.M. Polyubiquitination by HECT E3s and the determinants of chain type specificity. Mol. Cell. Biol. 29, 3307-3318 (2009
85. Maspero, E. et al. Structure of a ubiquitin-loaded HECT ligase reveals the molecular basis for catalytic priming. Nat. Struct. Mol. Biol. 20, 696-701 (2013
86. Stieglitz, B., Morris-Davies, A.C., Koliopoulos, M.G., Christodoulou, E. & Rittinger, K. LUBAC synthesizes linear ubiquitin chains via a thioester intermediate. EMBO Rep. 13, 840-846 (2012
87. Smit, J.J. et al. The E3 ligase HOIP specifies linear ubiquitin chain assembly through its RING-IBR-RING domain and the unique LDD extension. EMBO J. 31, 3833-3844 (2012
88. Bernier-Villamor, V., Sampson, D.A., Matunis, M.J. & Lima, C.D. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108, 345-356 (2002
89. Sampson, D.A., Wang, M. & Matunis, M.J. The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J. Biol. Chem. 276, 21664-21669 (2001
90. Desterro, J.M., Rodriguez, M.S. & Hay, R.T. SUMO-1 modification of I?B? inhibits NF-?B activation. Mol. Cell 2, 233-239 (1998
91. Mohideen, F. et al. A molecular basis for phosphorylation-dependent SUMO conjugation by the E2 UBC9. Nat. Struct. Mol. Biol. 16, 945-952 (2009
92. Hietakangas, V. et al. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc. Natl. Acad. Sci. USA 103, 45-50 (2006
93. Yang, X.J. & Gregoire, S. A recurrent phospho-sumoyl switch in transcriptional repression and beyond. Mol. Cell 23, 779-786 (2006
94. Mahajan, R., Gerace, L. & Melchior, F. Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association. J. Cell Biol. 140, 259-270 (1998
95. Pichler, A., Knipscheer, P., Saitoh, H., Sixma, T.K. & Melchior, F. The RanBP2 SUMO E3 ligase is neither HECT-nor RING-Type. Nat. Struct. Mol. Biol. 11, 984-991 (2004
96. Reverter, D. & Lima, C.D. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 435, 687-692 (2005
97. Werner, A., Flotho, A. & Melchior, F. The RanBP2/RanGAP1. *SUMO1/Ubc9 complex is a multisubunit SUMO E3 ligase. Mol. Cell 46, 287-298 (2012
98. 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
99. Yunus, A.A. & Lima, C.D. Structure of the Siz/PIAS SUMO E3 ligase Siz1 and determinants required for SUMO modification of PCNA. Mol. Cell 35, 669-682 (2009
100. Pichler, A. et al. SUMO modification of the ubiquitin-conjugating enzyme E2-25K. Nat. Struct. Mol. Biol. 12, 264-269 (2005
101. Psakhye, I. & Jentsch, S. Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151, 807-820 (2012
102. Reindle, A. et al. Multiple domains in Siz SUMO ligases contribute to substrate selectivity. J. Cell Sci. 119, 4749-4757 (2006
103. Scott, D.C. et al. A dual E3 mechanism for Rub1 ligation to Cdc53. Mol. Cell 39, 784-796 (2010
104. Kurz, T. et al. Dcn1 functions as a scaffold-Type E3 ligase for cullin neddylation. Mol. Cell 29, 23-35 (2008
105. Sims, J.J. & Cohen, R.E. Linkage-specific avidity defines the lysine 63-linked polyubiquitin-binding preference of rap80. Mol. Cell 33, 775-783 (2009
106. Komander, D. & Rape, M. The ubiquitin code. Annu. Rev. Biochem. 81, 203-229 (2012
107. Dikic, I., Wakatsuki, S. & Walters, K.J. Ubiquitin-binding domains: From structures to functions. Nat. Rev. Mol. Cell Biol. 10, 659-671 (2009
108. Polo, S. et al. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416, 451-455 (2002
109. Bienko, M. et al. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 310, 1821-1824 (2005
110. MacKay, C. et al. Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 142, 65-76 (2010
111. Kratz, K. et al. Deficiency of FANCD2-Associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142, 77-88 (2010
112. Smogorzewska, A. et al. A genetic screen identifies FAN1, a Fanconi anemia-Associated nuclease necessary for DNA interstrand crosslink repair. Mol. Cell 39, 36-47 (2010
113. Liu, T., Ghosal, G., Yuan, J., Chen, J. & Huang, J. FAN1 acts with FANCI-FANCD2 to promote DNA interstrand cross-link repair. Science 329, 693-696 (2010
114. Huang, M. & D'Andrea, A.D. A new nuclease member of the FAN club. Nat. Struct. Mol. Biol. 17, 926-928 (2010
115. Richly, H. et al. Transcriptional activation of polycomb-repressed genes by ZRF1. Nature 468, 1124-1128 (2010
116. Yuan, J., Ghosal, G. & Chen, J. The HARP-like domain-containing protein AH2/ZRANB3 binds to PCNA and participates in cellular response to replication stress. Mol. Cell 47, 410-421 (2012
117. Weston, R., Peeters, H. & Ahel, D. ZRANB3 is a structure-specific ATP-dependent endonuclease involved in replication stress response. Genes Dev. 26, 1558-1572 (2012
118. Ciccia, A. et al. Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress. Mol. Cell 47, 396-409 (2012
119. Hecker, C.M., Rabiller, M., Haglund, K., Bayer, P. & Dikic, I. Specification of SUMO1-And SUMO2-interacting motifs. J. Biol. Chem. 281, 16117-16127 (2006
120. 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
121. Armstrong, A.A., Mohideen, F. & Lima, C.D. Recognition of SUMO-modified PCNA requires tandem receptor motifs in Srs2. Nature 483, 59-63 (2012
122. Moldovan, G.L. et al. Inhibition of homologous recombination by the PCNA-interacting protein PARI. Mol. Cell 45, 75-86 (2012
123. Pilla, E. et al. A novel SUMO1-specific interacting motif in dipeptidyl peptidase 9 (DPP9) that is important for enzymatic regulation. J. Biol. Chem. 287, 44320-44329 (2012
124. Keusekotten, K. et al. OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell 153, 1312-1326 (2013
125. Nijman, S.M. et al. A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786 (2005
126. Cooper, E.M. et al. K63-specific deubiquitination by two JAMM/MPN+ complexes: BRISC-Associated Brcc36 and proteasomal Poh1. EMBO J. 28, 621-631 (2009
127. Mevissen, T.E. et al. OTU deubiquitinases reveal mechanisms of linkage specificity and enable ubiquitin chain restriction analysis. Cell 154, 169-184 (2013
128. Bremm, A., Freund, S.M. & Komander, D. Lys11-linked ubiquitin chains adopt compact conformations and are preferentially hydrolyzed by the deubiquitinase Cezanne. Nat. Struct. Mol. Biol. 17, 939-947 (2010
129. Faesen, A.C. et al. The differential modulation of USP activity by internal regulatory domains, interactors and eight ubiquitin chain types. Chem. Biol. 18, 1550-1561 (2011
130. Schulz, S. et al. Ubiquitin-specific protease-like 1 (USPL1) is a SUMO isopeptidase with essential, non-catalytic functions. EMBO Rep. 13, 930-938 (2012
131. Hickey, C.M., Wilson, N.R. & Hochstrasser, M. Function and regulation of SUMO proteases. Nat. Rev. Mol. Cell Biol. 13, 755-766 (2012
132. Wei, N., Serino, G. & Deng, X.W. The COP9 signalosome: More than a protease. Trends Biochem. Sci. 33, 592-600 (2008.