The deubiquitylase USP15 stabilizes newly synthesized REST and rescues its expression at mitotic exit

Cell Cycle

Volumn 12, Issue 12, 2013, Pages 1964-1977

  Faronato, Monica ^a   Patel, Vruti ^a   Darling, Sarah ^a   Dearden, Laura ^a   Clague, Michael J ^a   Urbé, Sylvie ^a   Coulson, Judy M ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Cell cycle; Co translational; Deubiquitination; G1; NRSF; Post translational modification; Protein degradation; Ubiquitin specific peptidase 15

Indexed keywords

CYCLOHEXIMIDE; EPOXOMICIN; PROTEIN USP 15; RE1 SILENCING TRANSCRIPTION FACTOR; REGULATOR PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE PROGRESSION; CELL FRACTIONATION; CELL SYNCHRONIZATION; CONTROLLED STUDY; CYTOLYSIS; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MITOSIS; NERVE CELL DIFFERENTIATION; POLYSOME; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA INTERFERENCE; RNA PROCESSING; UBIQUITINATION;

EID: 84879386934     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.25035     Document Type: Article

References (79)

1. Hammond-Martel I, Yu H, Affar B. Roles of ubiquitin signaling in transcription regulation. Cell Signal 2012; 24:410-21; PMID:22033037; http://dx.doi.org/10.1016/j.cellsig.2011.10.009
2. Clague MJ, Coulson JM, Urbé S. Cellular functions of the DUBs. J Cell Sci 2012; 125:277-86; PMID:22357969; http://dx.doi.org/10.1242/jcs.090985
3. Grabbe C, Husnjak K, Dikic I. The spatial and temporal organization of ubiquitin networks. Nat Rev Mol Cell Biol 2011; 12:295-307; PMID:21448225; http://dx.doi.org/10.1038/nrm3099
4. Komander D, Clague MJ, Urbé S. Breaking the chains: Structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 2009; 10:550-63; PMID:19626045; http://dx.doi.org/10.1038/nrm2731
5. Sacco JJ, Coulson JM, Clague MJ, Urbé S. Emerging roles of deubiquitinases in cancer-associated pathways. IUBMB Life 2010; 62:140-57; PMID:20073038
6. Luise C, Capra M, Donzelli M, Mazzarol G, Jodice MG, Nuciforo P, et al. An atlas of altered expression of deubiquitinating enzymes in human cancer. PLoS One 2011; 6:e15891; PMID:21283576; http://dx.doi.org/10.1371/journal.pone. 0015891
7. Fulda S, Rajalingam K, Dikic I. Ubiquitylation in immune disorders and cancer: From molecular mechanisms to therapeutic implications. EMBO Mol Med 2012; 4:545-56; PMID:22730341; http://dx.doi.org/10.1002/emmm.201100707
8. Hussain S, Zhang Y, Galardy PJ. DUBs and cancer: The role of deubiquitinating enzymes as oncogenes, non-oncogenes and tumor suppressors. Cell Cycle 2009; 8:1688-97; PMID:19448430; http://dx.doi.org/10.4161/cc.8.11.8739
9. Clague MJ, Urbé S. Ubiquitin: Same molecule, different degradation pathways. Cell 2010; 143:682-5; PMID:21111229; http://dx.doi.org/10.1016/j. cell.2010.11.012
10. Smith MH, Ploegh HL, Weissman JS. Road to ruin: Targeting proteins for degradation in the endoplasmic reticulum. Science 2011; 334:1086-90; PMID:22116878; http://dx.doi.org/10.1126/science. 1209235
11. Schubert U, Antón LC, Gibbs J, Norbury CC, Yewdell JW, Bennink Jr. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000; 404:770-4; PMID:10783891; http://dx.doi.org/10.1038/ 35008096 (Pubitemid 30212405)
12. Kim W, Bennett EJ, Huttlin EL, Guo A, Li J, Possemato A, et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 2011; 44:325-40; PMID:21906983; http://dx.doi.org/10.1016/j.molcel.2011.08. 025
13. Chong JA, Tapia-Ramírez J, Kim S, Toledo-Aral JJ, Zheng Y, Boutros MC, et al. REST: A mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 1995; 80:949-57; PMID:7697725; http://dx.doi.org/10.1016/0092-8674(95)90298-8
14. Schoenherr CJ, Anderson DJ. The neuron-restrictive silencer factor (NRSF): A coordinate repressor of multiple neuron-specific genes. Science 1995; 267:1360-3; PMID:7871435; http://dx.doi.org/10.1126/science. 7871435
15. Guan H, Ricciardi RP. Transformation by E1A oncoprotein involves ubiquitin-mediated proteolysis of the neuronal and tumor repressor REST in the nucleus. J Virol 2012; 86:5594-602; PMID:22419809; http://dx.doi.org/10.1128/ JVI.06811-11
16. Guardavaccaro D, Frescas D, Dorrello NV, Peschiaroli A, Multani AS, Cardozo T, et al. Control of chromosome stability by the beta-TrCP-REST-Mad2 axis. Nature 2008; 452:365-9; PMID:18354482; http://dx.doi.org/10.1038/ nature06641 (Pubitemid 351430786)
17. Westbrook TF, Hu G, Ang XL, Mulligan P, Pavlova NN, Liang A, et al. SCFbeta-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature 2008; 452:370-4; PMID:18354483; http://dx.doi.org/10.1038/nature06780 (Pubitemid 351430796)
18. Otto SJ, McCorkle SR, Hover J, Conaco C, Han JJ, Impey S, et al. A new binding motif for the transcriptional repressor REST uncovers large gene networks devoted to neuronal functions. J Neurosci 2007; 27:6729-39; PMID:17581960; http://dx.doi.org/10.1523/JNEUROSCI.0091-07.2007 (Pubitemid 46983428)
19. Johnson DS, Mortazavi A, Myers RM, Wold B. Genome-wide mapping of in vivo protein-DNA interactions. Science 2007; 316:1497-502; PMID:17540862; http://dx.doi.org/10.1126/science.1141319 (Pubitemid 46906620)
20. Gopalakrishnan V. REST and the RESTless: In stem cells and beyond. Future Neurol 2009; 4:317-29; PMID:19885378; http://dx.doi.org/10.2217/fnl.09.1
21. Bithell A. REST: Transcriptional and epigenetic regulator. Epigenomics 2011; 3:47-58; PMID:22126152; http://dx.doi.org/10.2217/epi.10.76
22. Gao Z, Ding P, Hsieh J. Profiling of REST-Dependent microRNAs Reveals Dynamic Modes of Expression. Front Neurosci 2012; 6:67; PMID:22590451; http://dx.doi.org/10.3389/fnins.2012.00067
23. Coulson JM. Transcriptional regulation: Cancer, neurons and the REST. Curr Biol 2005; 15:R665-8; PMID:16139198; http://dx.doi.org/10.1016/j.cub.2005. 08.032 (Pubitemid 41219582)
24. Faronato M, Coulson JM. REST (RE1 silencing transcription factor). Atlas Genet Cytogenet Oncol Haematol 2011; 15:208-13
25. Majumder S. REST in good times and bad: Roles in tumor suppressor and oncogenic activities. Cell Cycle 2006; 5:1929-35; PMID:16929174; http://dx.doi.org/10.4161/cc.5.17.2982 (Pubitemid 44435297)
26. Coulson JM, Edgson JL, Woll PJ, Quinn JP. A splice variant of the neuron-restrictive silencer factor repressor is expressed in small cell lung cancer: A potential role in derepression of neuroendocrine genes and a useful clinical marker. Cancer Res 2000; 60:1840-4; PMID:10766169 (Pubitemid 30207641)
27. Gurrola-Diaz C, Lacroix J, Dihlmann S, Becker CM, von Knebel Doeberitz M. Reduced expression of the neuron restrictive silencer factor permits transcription of glycine receptor alpha1 subunit in smallcell lung cancer cells. Oncogene 2003; 22:5636-45; PMID:12944912; http://dx.doi.org/10.1038/sj.onc. 1206790 (Pubitemid 37102700)
28. Coulson JM, Fiskerstrand CE, Woll PJ, Quinn JP. Arginine vasopressin promoter regulation is mediated by a neuron-restrictive silencer element in small cell lung cancer. Cancer Res 1999; 59:5123-7; PMID:10537286 (Pubitemid 29503971)
29. Westbrook TF, Martin ES, Schlabach MR, Leng Y, Liang AC, Feng B, et al. A genetic screen for candidate tumor suppressors identifies REST. Cell 2005; 121:837-48; PMID:15960972; http://dx.doi.org/10.1016/j.cell.2005.03.033
30. Lawinger P, Venugopal R, Guo ZS, Immaneni A, Sengupta D, Lu W, et al. The neuronal repressor REST/NRSF is an essential regulator in medulloblastoma cells. Nat Med 2000; 6:826-31; PMID:10888935; http://dx.doi.org/10.1038/77565 (Pubitemid 30469435)
31. Su X, Kameoka S, Lentz S, Majumder S. Activation of REST/NRSF target genes in neural stem cells is sufficient to cause neuronal differentiation. Mol Cell Biol 2004; 24:8018-25; PMID:15340064; http://dx.doi.org/10.1128/MCB.24.18. 8018-8025.2004 (Pubitemid 39167452)
32. Fuller GN, Su X, Price RE, Cohen ZR, Lang FF, Sawaya R, et al. Many human medulloblastoma tumors overexpress repressor element-1 silencing transcription (REST)/neuron-restrictive silencer factor, which can be functionally countered by REST-VP16. Mol Cancer Ther 2005; 4:343-9; PMID:15767543 (Pubitemid 40443919)
33. Ballas N, Grunseich C, Lu DD, Speh JC, Mandel G. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 2005; 121:645-57; PMID:15907476; http://dx.doi.org/10.1016/j. cell.2005.03.013 (Pubitemid 40720016)
34. Moss AC, Jacobson GM, Walker LE, Blake NW, Marshall E, Coulson JM. SCG3 transcript in peripheral blood is a prognostic biomarker for RESTdeficient small cell lung cancer. Clin Cancer Res 2009; 15:274-83; PMID:19118055; http://dx.doi.org/10.1158/1078-0432.CCR-08-1163
35. Kreisler A, Strissel PL, Strick R, Neumann SB, Schumacher U, Becker CM. Regulation of the NRSF/REST gene by methylation and CREB affects the cellular phenotype of small-cell lung cancer. Oncogene 2010; 29:5828-38; PMID:20697351; http://dx.doi.org/10.1038/onc.2010.321
36. Pance A, Livesey FJ, Jackson AP. A role for the transcriptional repressor REST in maintaining the phenotype of neurosecretory-deficient PC12 cells. J Neurochem 2006; 99:1435-44; PMID:17064356; http://dx.doi.org/10.1111/j.1471- 4159.2006.04190.x (Pubitemid 44730097)
37. Lee JH, Shimojo M, Chai YG, Hersh LB. Studies on the interaction of REST4 with the cholinergic repressor element-1/neuron restrictive silencer element. Brain Res Mol Brain Res 2000; 80:88-98; PMID:11039732; http://dx.doi.org/10. 1016/S0169-328X(00)00129-7 (Pubitemid 30612440)
38. Ye Y, Scheel H, Hofmann K, Komander D. Dissection of USP catalytic domains reveals five common insertion points. Mol Biosyst 2009; 5:1797-808; PMID:19734957; http://dx.doi.org/10.1039/b907669g
39. Urbé S, Liu H, Hayes SD, Heride C, Rigden DJ, Clague MJ. Systematic survey of deubiquitinase localization identifies USP21 as a regulator of centrosomeand microtubule-associated functions. Mol Biol Cell 2012; 23:1095-103; PMID:22298430; http://dx.doi.org/10.1091/mbc.E11-08-0668
40. Faronato M, Urbé S, Coulson JM. USP15 (ubiquitin specific peptidase 15). Atlas Genet Cytogenet Oncol Haematol 2011; 15:645-51
41. Sowa ME, Bennett EJ, Gygi SP, Harper JW. Defining the human deubiquitinating enzyme interaction landscape. Cell 2009; 138:389-403; PMID:19615732; http://dx.doi.org/10.1016/j.cell.2009.04.042
42. Song EJ, Werner SL, Neubauer J, Stegmeier F, Aspden J, Rio D, et al. The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev 2010; 24:1434-47; PMID:20595234; http://dx.doi.org/10.1101/gad.1925010
43. Hayes SD, Liu H, MacDonald E, Sanderson CM, Coulson JM, Clague MJ, et al. Direct and indirect control of mitogen-activated protein kinase pathwayassociated components, BRAP/IMP E3 ubiquitin ligase and CRAF/RAF1 kinase, by the deubiquitylating enzyme USP15. J Biol Chem 2012; 287:43007-18; PMID:23105109; http://dx.doi.org/10.1074/jbc. M112.386938
44. Huang Z, Wu Q, Guryanova OA, Cheng L, Shou W, Rich JN, et al. Deubiquitylase HAUSP stabilizes REST and promotes maintenance of neural progenitor cells. Nat Cell Biol 2011; 13:142-52; PMID:21258371; http://dx.doi.org/10.1038/ncb2153
45. Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, et al. Global quantification of mammalian gene expression control. Nature 2011; 473:337-42; PMID:21593866; http://dx.doi.org/10.1038/nature10098
46. Huang Z, Zhou W, Bao S. Role of deubiquitylase HAUSP in stem cell maintenance. Cell Cycle 2011; 10:1182-3; PMID:21490432; http://dx.doi.org/10. 4161/cc.10.8.15260
47. Rubenstein EM, Hochstrasser M. Redundancy and variation in the ubiquitin-mediated proteolytic targeting of a transcription factor. Cell Cycle 2010; 9:4282-5; PMID:20980825; http://dx.doi.org/10.4161/cc.9.21.13741
48. Tsuchiya Y, Morita T, Kim M, Iemura S, Natsume T, Yamamoto M, et al. Dual regulation of the transcriptional activity of Nrf1 by ß-TrCP-and Hrd1-dependent degradation mechanisms. Mol Cell Biol 2011; 31:4500-12; PMID:21911472; http://dx.doi.org/10.1128/MCB.05663-11
49. Yamasaki S, Yagishita N, Sasaki T, Nakazawa M, Kato Y, Yamadera T, et al. Cytoplasmic destruction of p53 by the endoplasmic reticulum-resident ubiquitin ligase 'Synoviolin'. EMBO J 2007; 26:113-22; PMID:17170702; http://dx.doi.org/ 10.1038/sj.emboj.7601490 (Pubitemid 46094704)
50. Ravid T, Kreft SG, Hochstrasser M. Membrane and soluble substrates of the Doa10 ubiquitin ligase are degraded by distinct pathways. EMBO J 2006; 25:533-43; PMID:16437165; http://dx.doi.org/10.1038/sj.emboj.7600946 (Pubitemid 43237660)
51. Brandman O, Stewart-Ornstein J, Wong D, Larson A, Williams CC, Li GW, et al. A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell 2012; 151:1042-54; PMID:23178123; http://dx.doi.org/10.1016/j.cell.2012.10.044
52. Cayli S, Klug J, Chapiro J, Fröhlich S, Krasteva G, Orel L, et al. COP9 signalosome interacts ATP-dependently with p97/valosin-containing protein (VCP) and controls the ubiquitination status of proteins bound to p97/VCP. J Biol Chem 2009; 284:34944-53; PMID:19826004; http://dx.doi.org/10.1074/jbc. M109.037952
53. Huang X, Langelotz C, Hetfeld-Pechoc BK, Schwenk W, Dubiel W. The COP9 signalosome mediates betacatenin degradation by deneddylation and blocks adenomatous polyposis coli destruction via USP15. J Mol Biol 2009; 391:691-702; PMID:19576224; http://dx.doi.org/10.1016/j.jmb.2009.06.066
54. Hetfeld BK, Helfrich A, Kapelari B, Scheel H, Hofmann K, Guterman A, et al. The zinc finger of the CSN-associated deubiquitinating enzyme USP15 is essential to rescue the E3 ligase Rbx1. Curr Biol 2005; 15:1217-21; PMID:16005295; http://dx.doi.org/10.1016/j.cub.2005.05.059 (Pubitemid 40950520)
55. Eletr ZM, Wilkinson KD. An emerging model for BAP1's role in regulating cell cycle progression. Cell Biochem Biophys 2011; 60:3-11; PMID:21484256; http://dx.doi.org/10.1007/s12013-011-9184-6
56. Gomez-Ferreria MA, Bashkurov M, Mullin M, Gingras AC, Pelletier L. CEP192 interacts physically and functionally with the K63-deubiquitinase CYLD to promote mitotic spindle assembly. Cell Cycle 2012; 11:3555-8; PMID:22895009; http://dx.doi.org/10.4161/cc.21574
57. Kim J, Kim WJ, Liu Z, Loda M, Freeman MR. The ubiquitin-specific protease USP2a enhances tumor progression by targeting cyclin A1 in bladder cancer. Cell Cycle 2012; 11:1123-30; PMID:22370483; http://dx.doi.org/10.4161/cc.11.6.19550
58. Giovinazzi S, Morozov VM, Summers MK, Reinhold WC, Ishov AM. USP7 and Daxx regulate mitosis progression and taxane sensitivity by affecting stability of Aurora-A kinase. Cell Death Differ 2013; 20:721-31; PMID:23348568; http://dx.doi.org/10.1038/cdd.2012.169
59. Meijer IM, van Leeuwen JE. ERBB2 is a target for USP8-mediated deubiquitination. Cell Signal 2011; 23:458-67; PMID:21044682; http://dx.doi.org/10.1016/j.cellsig.2010.10.023
60. Zhang Y, Foreman O, Wigle DA, Kosari F, Vasmatzis G, Salisbury JL, et al. USP44 regulates centrosome positioning to prevent aneuploidy and suppress tumorigenesis. J Clin Invest 2012; 122:4362-74; PMID:23187126; http://dx.doi.org/10.1172/JCI63084
61. Stegmeier F, Rape M, Draviam VM, Nalepa G, Sowa ME, Ang XL, et al. Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature 2007; 446:876-81; PMID:17443180; http://dx.doi.org/10.1038/nature05694
62. Aressy B, Jullien D, Cazales M, Marcellin M, Bugler B, Burlet-Schiltz O, et al. A screen for deubiquitinating enzymes involved in the G2/M checkpoint identifies USP50 as a regulator of HSP90-dependent Wee1 stability. Cell Cycle 2010; 9:3815-22; PMID:20930503; http://dx.doi.org/10.4161/cc.9.18.13133
63. Shibazaki M, Maesawa C, Akasaka K, Kasai S, Yasuhira S, Kanno K, et al. Transcriptional and post-transcriptional regulation of ßIII-tubulin protein expression in relation with cell cycle-dependent regulation of tumor cells. Int J Oncol 2012; 40:695-702; PMID:22159867
64. Martínez-Balbás MA, Dey A, Rabindran SK, Ozato K, Wu C. Displacement of sequence-specific transcription factors from mitotic chromatin. Cell 1995; 83:29-38; PMID:7553870; http://dx.doi.org/10.1016/0092-8674(95)90231- 7
65. Prasanth KV, Sacco-Bubulya PA, Prasanth SG, Spector DL. Sequential entry of components of the gene expression machinery into daughter nuclei. Mol Biol Cell 2003; 14:1043-57; PMID:12631722; http://dx.doi.org/10.1091/mbc.E02-10-0669 (Pubitemid 36337451)
66. Zaidi SK, Young DW, Montecino M, Lian JB, Stein JL, van Wijnen AJ, et al. Architectural epigenetics: Mitotic retention of mammalian transcriptional regulatory information. Mol Cell Biol 2010; 30:4758-66; PMID:20696837; http://dx.doi.org/10.1128/MCB.00646-10
67. Bruce AW, López-Contreras AJ, Flicek P, Down TA, Dhami P, Dillon SC, et al. Functional diversity for REST (NRSF) is defined by in vivo binding affinity hierarchies at the DNA sequence level. Genome Res 2009; 19:994-1005; PMID:19401398; http://dx.doi.org/10.1101/gr.089086.108
68. Baker RT, Wang XW, Woollatt E, White JA, Sutherland GR. Identification, functional characterization, and chromosomal localization of USP15, a novel human ubiquitin-specific protease related to the UNP oncoprotein, and a systematic nomenclature for human ubiquitin-specific proteases. Genomics 1999; 59:264-74; PMID:10444327; http://dx.doi.org/10.1006/geno.1999.5879 (Pubitemid 29406907)
69. Eichhorn PJ, Rodón L, Gonzàlez-Juncà A, Dirac A, Gili M, Martínez-Sáez E, et al. USP15 stabilizes TGF-ß receptor I and promotes oncogenesis through the activation of TGF-ß signaling in glioblastoma. Nat Med 2012; 18:429-35; PMID:22344298; http://dx.doi.org/10.1038/nm.2619
70. Kamal MM, Sathyan P, Singh SK, Zinn PO, Marisetty AL, Liang S, et al. REST regulates oncogenic properties of glioblastoma stem cells. Stem Cells 2012; 30:405-14; PMID:22228704; http://dx.doi.org/10.1002/stem.1020
71. Blom T, Tynninen O, Puputti M, Halonen M, Paetau A, Haapasalo H, et al. Molecular genetic analysis of the REST/NRSF gene in nervous system tumors. Acta Neuropathol 2006; 112:483-90; PMID:16823502; http://dx.doi.org/10.1007/s00401- 006-0102-8 (Pubitemid 44469168)
72. Vos RM, Altreuter J, White EA, Howley PM. The ubiquitin-specific peptidase USP15 regulates human papillomavirus type 16 E6 protein stability. J Virol 2009; 83:8885-92; PMID:19553310; http://dx.doi.org/10.1128/JVI.00605-09
73. Schweitzer K, Bozko PM, Dubiel W, Naumann M. CSN controls NFkappaB by deubiquitinylation of IkappaBalpha. EMBO J 2007; 26:1532-41; PMID:17318178; http://dx.doi.org/10.1038/sj.emboj.7601600 (Pubitemid 46480929)
74. Xu M, Takanashi M, Oikawa K, Tanaka M, Nishi H, Isaka K, et al. USP15 plays an essential role for caspase-3 activation during Paclitaxel-induced apoptosis. Biochem Biophys Res Commun 2009; 388:366-71; PMID:19665996; http://dx.doi.org/10.1016/j.bbrc.2009.08.015
75. Inui M, Manfrin A, Mamidi A, Martello G, Morsut L, Soligo S, et al. USP15 is a deubiquitylating enzyme for receptor-activated SMADs. Nat Cell Biol 2011; 13:1368-75; PMID:21947082; http://dx.doi.org/10.1038/ncb2346
76. Duttler S, Pechmann S, Frydman J. Principles of cotranslational ubiquitination and quality control at the ribosome. Mol Cell 2013; 50:379-93; PMID:23583075; http://dx.doi.org/10.1016/j.molcel. 2013.03.010
77. Wang F, Durfee LA, Huibregtse JM. A cotranslational ubiquitination pathway for quality control of misfolded proteins. Mol Cell 2013; 50:368-78; PMID:23583076; http://dx.doi.org/10.1016/j.molcel.2013.03.009
78. Feldman M, van der Goot FG. Novel ubiquitin-dependent quality control in the endoplasmic reticulum. Trends Cell Biol 2009; 19:357-63; PMID:19631546; http://dx.doi.org/10.1016/j.tcb.2009.05.005
79. Durfee LA, Huibregtse JM. The ISG15 conjugation system. Methods Mol Biol 2012; 832:141-9; PMID:22350882; http://dx.doi.org/10.1007/978-1-61779-474-2-9