Ubiquitin-like modifications in the DNA damage response

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 803-805, Issue , 2017, Pages 56-75

  Wang, Zhifeng ^a   Zhu, Wei Guo ^a   Xu, Xingzhi ^a,b  

^a Shenzhen University School of Medicine   (China)

^b CAPITAL NORMAL UNIVERSITY   (China)

Author keywords

DNA damage response; FATylation; ISGylation; NEDDylation; SUMOylation; Ubiquitin like modifiers (UBLs); UFMylation

Indexed keywords

CULLIN; DNA; DOUBLE STRANDED DNA; NEDD8 PROTEIN; PROTEIN FAT10; PROTEIN ISG15; PROTEIN UFM1; SUMO PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; ATG12 PROTEIN, HUMAN; AUTOPHAGY RELATED PROTEIN; AUTOPHAGY RELATED PROTEIN 12; CYTOKINE; ISG15 PROTEIN, HUMAN; NEDD8 PROTEIN, HUMAN; PROTEIN; SUMO 1 PROTEIN; UBD PROTEIN, HUMAN; UFM1 PROTEIN, HUMAN; URM1 PROTEIN, HUMAN;

CELL STRESS; DNA CROSS LINKING; DNA DAMAGE RESPONSE; DNA MODIFICATION; DNA STRAND BREAKAGE; ENZYME ACTIVITY; EXCISION REPAIR; FATYLATION; HUMAN; ISGYLATION; MALIGNANT NEOPLASM; MOLECULAR HYBRIDIZATION; NEDDYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SUMOYLATION; UBIQUITINATION; UFMYLATION; DNA DAMAGE; DOWN REGULATION; DRUG DEVELOPMENT; GENETICS; METABOLISM; NEOPLASMS;

AUTOPHAGY-RELATED PROTEIN 12; AUTOPHAGY-RELATED PROTEINS; CYTOKINES; DNA DAMAGE; DOWN-REGULATION; DRUG DISCOVERY; HUMANS; NEOPLASMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; SUMO-1 PROTEIN; UBIQUITINATION; UBIQUITINS;

EID: 85024923297     PISSN: 00275107     EISSN: 18792871     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2017.07.001     Document Type: Review

References (394)

1. Ciccia, A., Elledge, S.J., The DNA damage response: making it safe to play with knives. Mol. Cell 40 (2010), 179–204.
2. Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation. Cell 144 (2011), 646–674.
3. Hoeijmakers, J.H., Genome maintenance mechanisms for preventing cancer. Nature 411 (2001), 366–374.
4. Abraham, R.T., Phosphatidylinositol 3-kinase related kinases. Curr. Opin. Immunol. 8 (1996), 412–418.
5. Glickman, M.H., Ciechanover, A., The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82 (2002), 373–428.
6. Schulman, B.A., Harper, J.W., Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat. Rev. Mol. Cell Biol. 10 (2009), 319–331.
7. Hochstrasser, M., Origin and function of ubiquitin-like proteins. Nature 458 (2009), 422–429.
8. Flotho, A., Melchior, F., Sumoylation: a regulatory protein modification in health and disease. Annu. Rev. Biochem 82 (2013), 357–385.
9. Wilkinson, K.A., Nakamura, Y., Henley, J.M., Targets and consequences of protein SUMOylation in neurons. Brain Res. Rev. 64 (2010), 195–212.
10. Gareau, J.R., Lima, C.D., The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat. Rev. Mol. Cell Biol. 11 (2010), 861–871.
11. 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 (2002), 345–356.
12. Rytinki, M.M., Kaikkonen, S., Pehkonen, P., Jaaskelainen, T., Palvimo, J.J., PIAS proteins: pleiotropic interactors associated with SUMO. Cell. Mol. Life Sci. 66 (2009), 3029–3041.
13. Shin, E.J., Shin, H.M., Nam, E., Kim, W.S., Kim, J.H., Oh, B.H., Yun, Y., DeSUMOylating isopeptidase: a second class of SUMO protease. EMBO Rep. 13 (2012), 339–346.
14. Schulz, S., Chachami, G., Kozaczkiewicz, L., Winter, U., Stankovic-Valentin, N., Haas, P., Hofmann, K., Urlaub, H., Ovaa, H., Wittbrodt, J., Meulmeester, E., Melchior, F., Ubiquitin-specific protease-like 1 (USPL1) is a SUMO isopeptidase with essential, non-catalytic functions. EMBO Rep. 13 (2012), 930–938.
15. Guo, C., Henley, J.M., Wrestling with stress: roles of protein SUMOylation and deSUMOylation in cell stress response. IUBMB Life 66 (2014), 71–77.
16. Hickey, C.M., Wilson, N.R., Hochstrasser, M., Function and regulation of SUMO proteases. Nat. Rev. Mol. Cell Biol. 13 (2012), 755–766.
17. Kolli, N., Mikolajczyk, J., Drag, M., Mukhopadhyay, D., Moffatt, N., Dasso, M., Salvesen, G., Wilkinson, K.D., Distribution and paralogue specificity of mammalian deSUMOylating enzymes. Biochem. J 430 (2010), 335–344.
18. Alegre, K.O., Reverter, D., Swapping small ubiquitin-like modifier (SUMO) isoform specificity of SUMO proteases SENP6 and SENP7. J. Biol. Chem. 286 (2011), 36142–36151.
19. Shen, L.N., Geoffroy, M.C., Jaffray, E.G., Hay, R.T., Characterization of SENP7, a SUMO-2/3-specific isopeptidase. Biochem. J 421 (2009), 223–230.
20. Goeres, J., Chan, P.K., Mukhopadhyay, D., Zhang, H., Raught, B., Matunis, M.J., The SUMO-specific isopeptidase SENP2 associates dynamically with nuclear pore complexes through interactions with karyopherins and the Nup 107–160 nucleoporin subcomplex. Mol. Biol. Cell 22 (2011), 4868–4882.
21. 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., 2, 2009, ra24.
22. Guo, C., Hildick, K.L., Luo, J., Dearden, L., Wilkinson, K.A., Henley, J.M., SENP3-mediated deSUMOylation of dynamin-related protein 1 promotes cell death following ischaemia. EMBO J. 32 (2013), 1514–1528.
23. Lee, Y.J., Miyake, S., Wakita, H., McMullen, D.C., Azuma, Y., Auh, S., Hallenbeck, J.M., Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells. J. Cereb. Blood Flow Metab. 27 (2007), 950–962.
24. Xu, Y., Zuo, Y., Zhang, H., Kang, X., Yue, F., Yi, Z., Liu, M., Yeh, E.T., Chen, G., Cheng, J., Induction of SENP1 in endothelial cells contributes to hypoxia-driven VEGF expression and angiogenesis. J. Biol. Chem. 285 (2010), 36682–36688.
25. Zhou, D., Udpa, N., Ronen, R., Stobdan, T., Liang, J., Appenzeller, O., Zhao, H.W., Yin, Y., Du, Y., Guo, L., Cao, R., Wang, Y., Jin, X., Huang, C., Jia, W., Cao, D., Guo, G., Gamboa, J.L., Villafuerte, F., Callacondo, D., Xue, J., Liu, S., Frazer, K.A., Li, Y., Bafna, V., Haddad, G.G., Whole-genome sequencing uncovers the genetic basis of chronic mountain sickness in Andean highlanders. Am. J. Hum. Genet. 93 (2013), 452–462.
26. Cimarosti, H., Ashikaga, E., Jaafari, N., Dearden, L., Rubin, P., Wilkinson, K.A., Henley, J.M., Enhanced SUMOylation and SENP-1 protein levels following oxygen and glucose deprivation in neurones. J. Cereb. Blood Flow Metab., 2012, 17–22.
27. Lee, M.H., Mabb, A.M., Gill, G.B., Yeh, E.T., Miyamoto, S., NF-kappaB induction of the SUMO protease SENP2: A negative feedback loop to attenuate cell survival response to genotoxic stress. Mol. Cell 43 (2011), 180–191.
28. Olsen, J.V., Vermeulen, M., Santamaria, A., Kumar, C., Miller, M.L., Jensen, L.J., Gnad, F., Cox, J., Jensen, T.S., Nigg, E.A., Brunak, S., Mann, M., Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal., 3, 2010, ra3.
29. Kuo, M.L., W. den besten, M.C. thomas C.J. sherr, arf-induced turnover of the nucleolar nucleophosmin-associated SUMO-2/3 protease senp3. ABBV Cell Cycle 7 (2008), 3378–3387.
30. Yan, S., Sun, X., Xiang, B., Cang, H., Kang, X., Chen, Y., Li, H., Shi, G., Yeh, E.T., Wang, B., Wang, X., Yi, J., Redox regulation of the stability of the SUMO protease SENP3 via interactions with CHIP and Hsp90. EMBO J. 29 (2010), 3773–3786.
31. Bailey, D., O'Hare, P., Characterization of the localization and proteolytic activity of the SUMO-specific protease, SENP1. J. Biol. Chem. 279 (2004), 692–703.
32. Sharma, P., Yamada, S., Lualdi, M., Dasso, M., Kuehn, M.R., Senp1 is essential for desumoylating Sumo1-modified proteins but dispensable for Sumo2 and Sumo3 deconjugation in the mouse embryo. Cell Rep. 3 (2013), 1640–1650.
33. Lee, Y.J., Castri, P., Bembry, J., Maric, D., Auh, S., Hallenbeck, J.M., SUMOylation participates in induction of ischemic tolerance. J. Neurochem. 109 (2009), 257–267.
34. Lee, Y.J., Mou, Y., Maric, D., Klimanis, D., Auh, S., Hallenbeck, J.M., Elevated global SUMOylation in Ubc9 transgenic mice protects their brains against focal cerebral ischemic damage. PLoS One, 6, 2011, e25852.
35. Truong, K., Lee, T.D., Chen, Y., Small ubiquitin-like modifier (SUMO) modification of E1 Cys domain inhibits E1 Cys domain enzymatic activity. J. Biol. Chem. 287 (2012), 15154–15163.
36. Leitao, B.B., Jones, M.C., Brosens, J.J., The SUMO E3-ligase PIAS1 couples reactive oxygen species-dependent JNK activation to oxidative cell death. FASEB J. 25 (2011), 3416–3425.
37. Bossis, G., Melchior, F., Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Mol. Cell 21 (2006), 349–357.
38. Xu, Z., Lam, L.S., Lam, L.H., Chau, S.F., Ng, T.B., Au, S.W., Molecular basis of the redox regulation of SUMO proteases: a protective mechanism of intermolecular disulfide linkage against irreversible sulfhydryl oxidation. FASEB J. 22 (2008), 127–137.
39. Feligioni, M., Brambilla, E., Camassa, A., Sclip, A., Arnaboldi, A., Morelli, F., Antoniou, X., Borsello, T., Crosstalk between JNK and SUMO signaling pathways: deSUMOylation is protective against H2O2-induced cell injury. PLoS One, 6, 2011, e28185.
40. Wang, R.T., Zhi, X.Y., Zhang, Y., Zhang, J., Inhibition of SENP1 induces radiosensitization in lung cancer cells. Exp. Ther. Med. 6 (2013), 1054–1058.
41. Jin, Z.L., Pei, H., Xu, Y.H., Yu, J., Deng, T., The SUMO-specific protease SENP5 controls DNA damage response and promotes tumorigenesis in hepatocellular carcinoma. Eur. Rev. Med. Pharmacol. Sci. 20 (2016), 3566–3573.
42. 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. 28 (2014), 1472–1484.
43. 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 (2002), 135–141.
44. Stelter, P., Ulrich, H.D., Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425 (2003), 188–191.
45. Pfander, B., Moldovan, G.L., Sacher, M., Hoege, C., Jentsch, S., SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436 (2005), 428–433.
46. Parker, J.L., Bucceri, A., Davies, A.A., Heidrich, K., Windecker, H., Ulrich, H.D., SUMO modification of PCNA is controlled by DNA. EMBO J. 27 (2008), 2422–2431.
47. Despras, E., Sittewelle, M., Pouvelle, C., Delrieu, N., Cordonnier, A.M., Kannouche, P.L., Rad18-dependent SUMOylation of human specialized DNA polymerase eta is required to prevent under-replicated DNA. Nat. Commun., 7, 2016, 13326.
48. Shim, H.S., Wei, M., Brandhorst, S., Longo, V.D., Starvation promotes REV1 SUMOylation and p53-dependent sensitization of melanoma and breast cancer cells. Cancer Res. 75 (2015), 1056–1067.
49. Akita, M., Tak, Y.S., Shimura, T., Matsumoto, S., Okuda-Shimizu, Y., Shimizu, Y., Nishi, R., Saitoh, H., Iwai, S., Mori, T., Ikura, T., Sakai, W., Hanaoka, F., Sugasawa, K., SUMOylation of xeroderma pigmentosum group C protein regulates DNA damage recognition during nucleotide excision repair. Sci. Rep., 5, 2015, 10984.
50. Poulsen, S.L., Hansen, R.K., Wagner, S.A., van Cuijk, L., van Belle, G.J., Streicher, W., Wikstrom, M., Choudhary, C., Houtsmuller, A.B., Marteijn, J.A., Bekker-Jensen, S., Mailand, N., RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response. J. Cell Biol. 201 (2013), 797–807.
51. Wang, Q.E., Zhu, Q., Wani, G., El-Mahdy, M.A., Li, J., Wani, A.A., DNA repair factor XPC is modified by SUMO-1 and ubiquitin following UV irradiation. Nucleic Acids Res. 33 (2005), 4023–4034.
52. Hang, L.E., Lopez, C.R., Liu, X., Williams, J.M., Chung, I., Wei, L., Bertuch, A.A., Zhao, X., Regulation of Ku-DNA association by Yku70 C-terminal tail and SUMO modification. J. Biol. Chem. 289 (2014), 10308–10317.
53. Moriyama, T., Fujimitsu, Y., Yoshikai, Y., Sasano, T., Yamada, K., Murakami, M., Urano, T., Sugasawa, K., Saitoh, H., SUMO-modification and elimination of the active DNA demethylation enzyme TDG in cultured human cells. Biochem. Biophys. Res. Commun. 447 (2014), 419–424.
54. Sarangi, P., Bartosova, Z., Altmannova, V., Holland, C., Chavdarova, M., Lee, S.E., Krejci, L., Zhao, X., Sumoylation of the Rad1 nuclease promotes DNA repair and regulates its DNA association. Nucleic Acids Res. 42 (2014), 6393–6404.
55. Sinigalia, E., Alvisi, G., Segre, C.V., Mercorelli, B., Muratore, G., Winkler, M., Hsiao, H.H., Urlaub, H., Ripalti, A., Chiocca, S., Palu, G., Loregian, A., The human cytomegalovirus DNA polymerase processivity factor UL44 is modified by SUMO in a DNA-dependent manner. PLoS One, 7, 2012, e49630.
56. 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 57 (2015), 150–164.
57. Sacher, M., Pfander, B., Hoege, C., Jentsch, S., Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat. Cell Biol. 8 (2006), 1284–1290.
58. Ohuchi, T., Seki, M., Branzei, D., Maeda, D., Ui, A., Ogiwara, H., Tada, S., Enomoto, T., Rad52 sumoylation and its involvement in the efficient induction of homologous recombination. DNA Repair (Amst.) 7 (2008), 879–889.
59. Altmannova, V., Eckert-Boulet, N., Arneric, M., Kolesar, P., Chaloupkova, R., Damborsky, J., Sung, P., Zhao, X., Lisby, M., Krejci Rad52, L., SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Res. 38 (2010), 4708–4721.
60. 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. 15 (2013), 526–532.
61. Wu, S.Y., Chiang, C.M., Crosstalk between sumoylation and acetylation regulates p53-dependent chromatin transcription and DNA binding. EMBO J. 28 (2009), 1246–1259.
62. Sarangi, P., Steinacher, R., Altmannova, V., Fu, Q., Paull, T.T., Krejci, L., Whitby, M.C., Zhao, X., Sumoylation influences DNA break repair partly by increasing the solubility of a conserved end resection protein. PLoS Genet., 11, 2015, e1004899.
63. Vigasova, D., Sarangi, P., Kolesar, P., Vlasakova, D., Slezakova, Z., Altmannova, V., Nikulenkov, F., Anrather, D., Gith, R., Zhao, X., Chovanec, M., Krejci Lif1, L., SUMOylation and its role in non-homologous end-joining. Nucleic Acids Res. 41 (2013), 5341–5353.
64. Sridharan, V., Park, H., Ryu, H., Azuma, Y., SUMOylation regulates polo-like kinase 1-interacting checkpoint helicase (PICH) during mitosis. J. Biol. Chem. 290 (2015), 3269–3276.
65. Ryu, H., Al-Ani, G., Deckert, K., Kirkpatrick, D., Gygi, S.P., Dasso, M., Azuma, Y., PIASy mediates SUMO-2/3 conjugation of poly(ADP-ribose) polymerase 1 (PARP1) on mitotic chromosomes. J. Biol. Chem. 285 (2010), 14415–14423.
66. Luo, K., Zhang, H., Wang, L., Yuan, J., Lou, Z., Sumoylation of MDC1 is important for proper DNA damage response. EMBO J. 31 (2012), 3008–3019.
67. Morris, J.R., Boutell, C., Keppler, M., Densham, R., Weekes, D., Alamshah, A., Butler, L., Galanty, Y., Pangon, L., Kiuchi, T., Ng, T., Solomon, E., The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462 (2009), 886–890.
68. Danielsen, J.R., Povlsen, L.K., Villumsen, B.H., Streicher, W., Nilsson, J., Wikstrom, M., Bekker-Jensen, S., Mailand, N., DNA damage-inducible SUMOylation of HERC2 promotes RNF8 binding via a novel SUMO-binding Zinc finger. J. Cell Biol. 197 (2012), 179–187.
69. Ismail, I.H., Gagne, J.P., Caron, M.C., McDonald, D., Xu, Z., Masson, J.Y., Poirier, G.G., Hendzel, M.J., CBX4-mediated SUMO modification regulates BMI1 recruitment at sites of DNA damage. Nucleic Acids Res. 40 (2012), 5497–5510.
70. Pfeiffer, A., Luijsterburg, M.S., Acs, K., Wiegant, W.W., Helfricht, A., Herzog, L.K., Minoia, M., Bottcher, C., Salomons, F.A., van Attikum, H., Dantuma, N.P., Ataxin-3 consolidates the MD-dependent DNA double-strand break response by counteracting the SUMO-targeted ubiquitin ligase RNF4. EMBO J., 2017, C1.
71. Paget, M., Dubuissez, V., Dehennaut, J., Nassour, B.T., Harmon, N., Spruyt, I., Loison, C., Abbadie, B.R., Rood, D., HIC1 (hypermethylated in cancer 1) SUMOylation is dispensable for DNA repair but is essential for the apoptotic DNA damage response (DDR) to irreparable DNA double-strand breaks (DSBs). Oncotarget 8 (2017), 2916–2935.
72. Johnson, E.S., Gupta, A.A., An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106 (2001), 735–744.
73. Veaute, X., Jeusset, J., Soustelle, C., Kowalczykowski, S.C., Le Cam, E., Fabre, F., The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423 (2003), 309–312.
74. Krejci, L., Van Komen, S., Li, Y., Villemain, J., Reddy, M.S., Klein, H., Ellenberger, T., Sung, P., DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423 (2003), 305–309.
75. Papouli, E., Chen, S., Davies, A.A., Huttner, D., Krejci, L., Sung, P., Ulrich, H.D., Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19 (2005), 123–133.
76. Burkovics, P., Sebesta, M., Sisakova, A., Plault, N., Szukacsov, V., Robert, T., Pinter, L., Marini, V., Kolesar, P., Haracska, L., Gangloff, S., Krejci, L., Srs2 mediates PCNA-SUMO-dependent inhibition of DNA repair synthesis. EMBO J. 32 (2013), 742–755.
77. Moldovan, G.L., Dejsuphong, D., Petalcorin, M.I., Hofmann, K., Takeda, S., Boulton, S.J., D'Andrea, A.D., Inhibition of homologous recombination by the PCNA-interacting protein PARI. Mol. Cell 45 (2012), 75–86.
78. Fugger, K., Mistrik, M., Danielsen, J.R., Dinant, C., Falck, J., Bartek, J., Lukas, J., Mailand, N., Human Fbh1 helicase contributes to genome maintenance via pro- and anti-recombinase activities. J. Cell Biol. 186 (2009), 655–663.
79. Bacquin, A., Pouvelle, C., Siaud, N., Perderiset, M., Salome-Desnoulez, S., Tellier-Lebegue, C., Lopez, B., Charbonnier, J.B., Kannouche, P.L., The helicase FBH1 is tightly regulated by PCNA via CRL4(Cdt2)-mediated proteolysis in human cells. Nucleic Acids Res. 41 (2013), 6501–6513.
80. Kim, S.H., Michael, W.M., Regulated proteolysis of DNA polymerase eta during the DNA-damage response in C. elegans. Mol. Cell 32 (2008), 757–766.
81. 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 (2002), 1456–1464.
82. Kim, H., D'Andrea, A.D., Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev. 26 (2012), 1393–1408.
83. Hodskinson, M.R., Silhan, J., Crossan, G.P., Garaycoechea, J.I., Mukherjee, S., Johnson, C.M., Scharer, O.D., Patel, K.J., Mouse SLX4 is a tumor suppressor that stimulates the activity of the nuclease XPF-ERCC1 in DNA crosslink repair. Mol. Cell 54 (2014), 472–484.
84. Klein Douwel, D., Boonen, R.A., Long, D.T., Szypowska, A.A., Raschle, M., Walter, J.C., Knipscheer, P., XPF-ERCC1 acts in Unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/SLX4. Mol. Cell 54 (2014), 460–471.
85. Lengsfeld, B.M., Rattray, A.J., Bhaskara, V., Ghirlando, R., Paull, T.T., Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell 28 (2007), 638–651.
86. Clerici, M., Mantiero, D., Lucchini, G., Longhese, M.P., The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J. Biol. Chem. 280 (2005), 38631–38638.
87. Nicolette, M.L., Lee, K., Guo, Z., Rani, M., Chow, J.M., Lee, S.E., Paull, T.T., Mre11-Rad50-Xrs2 and Sae2 promote 5’ strand resection of DNA double-strand breaks. Nat. Struct. Mol. Biol. 17 (2010), 1478–1485.
88. Cannavo, E., Cejka, P., Sae2 promotes dsDNA endonuclease activity within Mre11-Rad50-Xrs2 to resect DNA breaks. Nature 514 (2014), 122–125.
89. Bi, B., Rybalchenko, N., Golub, E.I., Radding, C.M., Human and yeast Rad52 proteins promote DNA strand exchange. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 9568–9572.
90. Davis, A.P., Symington, L.S., The Rad52-Rad59 complex interacts with Rad51 and replication protein A. DNA Repair (Amst.) 2 (2003), 1127–1134.
91. 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., 5, 2012, ra88.
92. Hu, X., Paul, A., Wang, B., Rap80 protein recruitment to DNA double-strand breaks requires binding to both small ubiquitin-like modifier (SUMO) and ubiquitin conjugates. J. Biol. Chem. 287 (2012), 25510–25519.
93. Huen, M.S., Grant, R., Manke, I., Minn, K., Yu, X., Yaffe, M.B., Chen, J., RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131 (2007), 901–914.
94. Kolas, N.K., Chapman, J.R., Nakada, S., Ylanko, J., Chahwan, R., Sweeney, F.D., Panier, S., Mendez, M., Wildenhain, J., Thomson, T.M., Pelletier, L., Jackson, S.P., Durocher, D., Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318 (2007), 1637–1640.
95. Mailand, N., Bekker-Jensen, S., Faustrup, H., Melander, F., Bartek, J., Lukas, C., Lukas, J., RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131 (2007), 887–900.
96. Wang, B., Elledge, S.J., Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 20759–20763.
97. Doil, C., Mailand, N., Bekker-Jensen, S., Menard, P., Larsen, D.H., Pepperkok, R., Ellenberg, J., Panier, S., Durocher, D., Bartek, J., Lukas, J., Lukas, C., RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136 (2009), 435–446.
98. Bekker-Jensen, S., Rendtlew Danielsen, J., Fugger, K., Gromova, I., Nerstedt, A., Lukas, C., Bartek, J., Lukas, J., Mailand, N., HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nat. Cell Biol., 12, 2010 (80-86, supp 81-12).
99. Dehennaut, V., Loison, I., Dubuissez, M., Nassour, J., Abbadie, C., Leprince, D., DNA double-strand breaks lead to activation of hypermethylated in cancer 1 (HIC1) by SUMOylation to regulate DNA repair. J. Biol. Chem. 288 (2013), 10254–10264.
100. Stankovic-Valentin, N., Deltour, S., Seeler, J., Pinte, S., Vergoten, G., Guerardel, C., Dejean, A., Leprince, D., An acetylation/deacetylation-SUMOylation switch through a phylogenetically conserved psiKXEP motif in the tumor suppressor HIC1 regulates transcriptional repression activity. Mol. Cell. Biol. 27 (2007), 2661–2675.
101. Van Rechem, C., Boulay, G., Pinte, S., Stankovic-Valentin, N., Guerardel, C., Leprince, D., Differential regulation of HIC1 target genes by CtBP and NuRD, via an acetylation/SUMOylation switch, in quiescent versus proliferating cells. Mol. Cell. Biol. 30 (2010), 4045–4059.
102. Kumar, S., Tomooka, Y., Noda, M., Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochem. Biophys. Res. Commun. 185 (1992), 1155–1161.
103. Kamitani, T., Kito, K., Nguyen, H.P., Yeh, E.T., Characterization of NEDD8, a developmentally down-regulated ubiquitin-like protein. J. Biol. Chem. 272 (1997), 28557–28562.
104. Whitby, F.G., Xia, G., Pickart, C.M., Hill, C.P., Crystal structure of the human ubiquitin-like protein NEDD8 and interactions with ubiquitin pathway enzymes. J. Biol. Chem. 273 (1998), 34983–34991.
105. Liakopoulos, D., Doenges, G., Matuschewski, K., Jentsch, S., A novel protein modification pathway related to the ubiquitin system. EMBO J. 17 (1998), 2208–2214.
106. Lammer, D., Mathias, N., Laplaza, J.M., Jiang, W., Liu, Y., Callis, J., Goebl, M., Estelle, M., Modification of yeast Cdc53p by the ubiquitin-related protein rub1p affects function of the SCFCdc4 complex. Genes Dev. 12 (1998), 914–926.
107. Mendoza, H.M., Shen, L.N., Botting, C., Lewis, A., Chen, J., Ink, B., Hay, R.T., NEDP1, a highly conserved cysteine protease that deNEDDylates Cullins. J. Biol. Chem. 278 (2003), 25637–25643.
108. Wada, H., Kito, K., Caskey, L.S., Yeh, E.T., Kamitani, T., Cleavage of the C-terminus of NEDD8 by UCH-L3. Biochem. Biophys. Res. Commun. 251 (1998), 688–692.
109. Pan, Z.Q., Kentsis, A., Dias, D.C., Yamoah, K., Wu, K., Nedd8 on cullin: building an expressway to protein destruction. Oncogene 23 (2004), 1985–1997.
110. Gong, L., Yeh, E.T., Identification of the activating and conjugating enzymes of the NEDD8 conjugation pathway. J. Biol. Chem. 274 (1999), 12036–12042.
111. Osaka, F., Kawasaki, H., Aida, N., Saeki, M., Chiba, T., Kawashima, S., Tanaka, K., Kato, S., A new NEDD8-ligating system for cullin-4A. Genes Dev. 12 (1998), 2263–2268.
112. Huang, D.T., Ayrault, O., Hunt, H.W., Taherbhoy, A.M., Duda, D.M., Scott, D.C., Borg, L.A., Neale, G., Murray, P.J., Roussel, M.F., Schulman E2-RING, B.A., expansion of the NEDD8 cascade confers specificity to cullin modification. Mol. Cell 33 (2009), 483–495.
113. Abida, W.M., Nikolaev, A., Zhao, W., Zhang, W., Gu, W., FBXO11 promotes the Neddylation of p53 and inhibits its transcriptional activity. J. Biol. Chem. 282 (2007), 1797–1804.
114. Kamura, T., Conrad, M.N., Yan, Q., Conaway, R.C., Conaway, J.W., The Rbx1 subunit of SCF and VHL E3 ubiquitin ligase activates Rub1 modification of cullins Cdc53 and Cul2. Genes Dev. 13 (1999), 2928–2933.
115. Oved, S., Mosesson, Y., Zwang, Y., Santonico, E., Shtiegman, K., Marmor, M.D., Kochupurakkal, B.S., Katz, M., Lavi, S., Cesareni, G., Yarden, Y., Conjugation to Nedd8 instigates ubiquitylation and down-regulation of activated receptor tyrosine kinases. J. Biol. Chem. 281 (2006), 21640–21651.
116. Xirodimas, D.P., Saville, M.K., Bourdon, J.C., Hay, R.T., Lane, D.P., Mdm2-mediated NEDD8 conjugation of p53 inhibits its transcriptional activity. Cell 118 (2004), 83–97.
117. Abidi, N., Xirodimas, D.P., Regulation of cancer-related pathways by protein NEDDylation and strategies for the use of NEDD8 inhibitors in the clinic. Endocr. Relat. Cancer 22 (2015), T55–70.
118. Kurz, T., Ozlu, N., Rudolf, F., O'Rourke, S.M., Luke, B., Hofmann, K., Hyman, A.A., Bowerman, B., Peter, M., The conserved protein DCN-1/Dcn1p is required for cullin neddylation in C. elegans and S. cerevisiae. Nature 435 (2005), 1257–1261.
119. Kurz, T., Chou, Y.C., Willems, A.R., Meyer-Schaller, N., Hecht, M.L., Tyers, M., Peter, M., Sicheri, F., Dcn1 functions as a scaffold-type E3 ligase for cullin neddylation. Mol. Cell 29 (2008), 23–35.
120. Scott, D.C., Monda, J.K., Grace, C.R., Duda, D.M., Kriwacki, R.W., Kurz, T., Schulman, B.A., A dual E3 mechanism for Rub1 ligation to Cdc53. Mol. Cell 39 (2010), 784–796.
121. Kim, A.Y., Bommelje, C.C., Lee, B.E., Yonekawa, Y., Choi, L., Morris, L.G., Huang, G., Kaufman, A., Ryan, R.J., Hao, B., Ramanathan, Y., Singh, B., SCCRO (DCUN1D1) is an essential component of the E3 complex for neddylation. J. Biol. Chem. 283 (2008), 33211–33220.
122. Meyer-Schaller, N., Chou, Y.C., Sumara, I., Martin, D.D., Kurz, T., Katheder, N., Hofmann, K., Berthiaume, L.G., Sicheri, F., Peter, M., The human Dcn1-like protein DCNL3 promotes Cul3 neddylation at membranes. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 12365–12370.
123. Monda, J.K., Scott, D.C., Miller, D.J., Lydeard, J., King, D., Harper, J.W., Bennett, E.J., Schulman, B.A., Structural conservation of distinctive N-terminal acetylation-dependent interactions across a family of mammalian NEDD8 ligation enzymes. Structure 21 (2013), 42–53.
124. Watson, I.R., Irwin, M.S., Ohh, M., NEDD8 pathways in cancer, sine quibus non. Cancer Cell 19 (2011), 168–176.
125. Cope, G.A., Suh, G.S., Aravind, L., Schwarz, S.E., Zipursky, S.L., Koonin, E.V., Deshaies, R.J., Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science 298 (2002), 608–611.
126. Lingaraju, G.M., Bunker, R.D., Cavadini, S., Hess, D., Hassiepen, U., Renatus, M., Fischer, E.S., Thoma, N.H., Crystal structure of the human COP9 signalosome. Nature 512 (2014), 161–165.
127. Sharon, M., Mao, H., Boeri Erba, E., Stephens, E., Zheng, N., Robinson, C.V., Symmetrical modularity of the COP9 signalosome complex suggests its multifunctionality. Structure 17 (2009), 31–40.
128. Kito, E.T., Yeh, T., NUB1, a NEDD8-interacting protein, is induced by interferon and down-regulates the NEDD8 expression. J. Biol. Chem. 276 (2001), 20603–20609.
129. Kamitani, T., Kito, K., Fukuda-Kamitani, T., Yeh, E.T., Targeting of NEDD8 and its conjugates for proteasomal degradation by NUB1. J. Biol. Chem. 276 (2001), 46655–46660.
130. Liu, S., Yang, H., Zhao, J., Zhang, Y.H., Song, A.X., Hu, H.Y., NEDD8 ultimate buster-1 long (NUB1L) protein promotes transfer of NEDD8 to proteasome for degradation through the P97UFD1/NPL4 complex. J. Biol. Chem. 288 (2013), 31339–31349.
131. Liu, S., Fu, Q.S., Zhao, J., Hu, H.Y., Structural and mechanistic insights into the arginine/lysine-rich peptide motifs that interact with P97/VCP. Biochim. Biophys. Acta 1834 (2013), 2672–2678.
132. Mo, Z., Zhang, Q., Liu, Z., Lauer, J., Shi, Y., Sun, L., Griffin, P.R., Yang, X.L., Neddylation requires glycyl-tRNA synthetase to protect activated E2. Nat. Struct. Mol. Biol. 23 (2016), 730–737.
133. Zheng, J., Yang, X., Harrell, J.M., Ryzhikov, S., Shim, E.H., Lykke-Andersen, K., Wei, N., Sun, H., Kobayashi, R., Zhang, H., CAND1 binds to unneddylated CUL1 and regulates the formation of SCF ubiquitin E3 ligase complex. Mol. Cell 10 (2002), 1519–1526.
134. 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 (2002), 1511–1518.
135. Duda, D.M., Borg, L.A., Scott, D.C., Hunt, H.W., Hammel, M., Schulman, B.A., Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 134 (2008), 995–1006.
136. Emberley, E.D., Mosadeghi, R., Deshaies, R.J., Deconjugation of Nedd8 from Cul1 is directly regulated by Skp1-F-box and substrate, and the COP9 signalosome inhibits deneddylated SCF by a noncatalytic mechanism. J. Biol. Chem. 287 (2012), 29679–29689.
137. Enchev, R.I., Scott, D.C., da Fonseca, P.C., Schreiber, A., Monda, J.K., Schulman, B.A., Peter, M., Morris, E.P., Structural basis for a reciprocal regulation between SCF and CSN. Cell Rep. 2 (2012), 616–627.
138. Schmidt, M.W., McQuary, P.R., Wee, S., Hofmann, K., Wolf, D.A., F-box-directed CRL complex assembly and regulation by the CSN and CAND1. Mol. Cell 35 (2009), 586–597.
139. Zemla, A., Thomas, Y., Kedziora, S., Knebel, A., Wood, N.T., Rabut, G., Kurz, T., CSN- and CAND1-dependent remodelling of the budding yeast SCF complex. Nat. Commun., 4, 2013, 1641.
140. Pierce, N.W., Lee, J.E., Liu, X., Sweredoski, M.J., Graham, R.L., Larimore, E.A., Rome, M., Zheng, N., Clurman, B.E., Hess, S., Shan, S.O., Deshaies, R.J., Cand1 promotes assembly of new SCF complexes through dynamic exchange of F box proteins. Cell 153 (2013), 206–215.
141. Wu, S., Zhu, W., Nhan, T., Toth, J.I., Petroski, M.D., Wolf, D.A., CAND1 controls in vivo dynamics of the cullin 1-RING ubiquitin ligase repertoire. Nat. Commun., 4, 2013, 1642.
142. Duda, D.M., Scott, D.C., Calabrese, M.F., Zimmerman, E.S., Zheng, N., Schulman, B.A., Structural regulation of cullin-RING ubiquitin ligase complexes. Curr. Opin. Struct. Biol. 21 (2011), 257–264.
143. Chew, E.H., Hagen, T., Substrate-mediated regulation of cullin neddylation. J. Biol. Chem. 282 (2007), 17032–17040.
144. Chairatvit, K., Ngamkitidechakul, C., Control of cell proliferation via elevated NEDD8 conjugation in oral squamous cell carcinoma. Mol. Cell. Biochem. 306 (2007), 163–169.
145. Melchor, L., Saucedo-Cuevas, L.P., Munoz-Repeto, I., Rodriguez-Pinilla, S.M., Honrado, E., Campoverde, A., Palacios, J., Nathanson, K.L., Garcia, M.J., Benitez, J., Comprehensive characterization of the DNA amplification at 13q34 in human breast cancer reveals TFDP1 and CUL4A as likely candidate target genes. Breast Cancer Res., 11, 2009, R86.
146. Zhao, Y., Morgan, M.A., Sun, Y., Targeting Neddylation pathways to inactivate cullin-RING ligases for anticancer therapy. Antioxid. Redox Signal. 21 (2014), 2383–2400.
147. Swords, R.T., Pevonedistat, (MLN4924), a First-in-Class NEDD8-activating enzyme inhibitor, in patients with acute myeloid leukaemia and myelodysplastic syndromes: a phase 1 study (vol 169, pg 534, 2015). Br. J. Haematol., 171, 2015, 294.
148. Ratcliffe, W.G., Kaelin, P.J. Jr., Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30 (2008), 393–402.
149. Stickle, N.H., Chung, J., Klco, J.M., Hill, R.P., Kaelin, W.G. Jr., Ohh, M., pVHL modification by NEDD8 is required for fibronectin matrix assembly and suppression of tumor development. Mol. Cell. Biol. 24 (2004), 3251–3261.
150. Russell, R.C., Ohh, M., NEDD8 acts as a ‘molecular switch’ defining the functional selectivity of VHL. EMBO Rep. 9 (2008), 486–491.
151. Watson, I.R., Li, B.K., Roche, O., Blanch, A., Ohh, M., Irwin, M.S., Chemotherapy induces NEDP1-mediated destabilization of MDM2. Oncogene 29 (2010), 297–304.
152. Liu, G., Xirodimas, D.P., NUB1 promotes cytoplasmic localization of p53 through cooperation of the NEDD8 and ubiquitin pathways. Oncogene 29 (2010), 2252–2261.
153. Dohmesen, C., Koeppel, M., Dobbelstein, M., Specific inhibition of Mdm2-mediated neddylation by Tip60. ABBV Cell Cycle 7 (2008), 222–231.
154. S. Carter, K.H. Vousden, p53-Ubl fusions as models of ubiquitination, sumoylation and neddylation of p53, Cell Cycle, 7 (2008) 2519–2528.
155. Xirodimas, D.P., Sundqvist, A., Nakamura, A., Shen, L., Botting, C., Hay, R.T., Ribosomal proteins are targets for the NEDD8 pathway. EMBO Rep. 9 (2008), 280–286.
156. Sundqvist, A., Liu, G., Mirsaliotis, A., Xirodimas, D.P., Regulation of nucleolar signalling to p53 through NEDDylation of L11. EMBO Rep. 10 (2009), 1132–1139.
157. Sun, X.X., Wang, Y.G., Xirodimas, D.P., Dai, M.S., Perturbation of 60 S ribosomal biogenesis results in ribosomal protein L5- and L11-dependent p53 activation. J. Biol. Chem. 285 (2010), 25812–25821.
158. Gao, F., Cheng, J., Shi, T., Yeh, E.T., Neddylation of a breast cancer-associated protein recruits a class III histone deacetylase that represses NFkappaB-dependent transcription. Nat. Cell Biol. 8 (2006), 1171–1177.
159. Garcia, K., Blank, J.L., Bouck, D.C., Liu, X.J., Sappal, D.S., Hather, G., Cosmopoulos, K., Thomas, M.P., Kuranda, M., Pickard, M.D., Liu, R., Bandi, S., Smith, P.G., Lightcap, E.S., Nedd8-activating enzyme inhibitor MLN4924 provides synergy with mitomycin C through interactions with ATR, BRCA1/BRCA2, and chromatin dynamics pathways. Mol. Cancer Ther. 13 (2014), 1625–1635.
160. Guihard, S., Ramolu, L., Macabre, C., Wasylyk, B., Noel, G., Abecassis, J., Jung, A.C., The NEDD8 conjugation pathway regulates p53 transcriptional activity and head and neck cancer cell sensitivity to ionizing radiation. Int. J. Oncol. 41 (2012), 1531–1540.
161. Jazaeri, A.A., Shibata, E., Park, J., Bryant, J.L., Conaway, M.R., Modesitt, S.C., Smith, P.G., Milhollen, M.A., Berger, A.J., Dutta, A., Overcoming platinum resistance in preclinical models of ovarian cancer using the neddylation inhibitor MLN4924. Mol. Cancer Ther. 12 (2013), 1958–1967.
162. Kee, Y., Huang, M., Chang, S., Moreau, L.A., Park, E., Smith, P.G., D'Andrea, A.D., Inhibition of the Nedd8 system sensitizes cells to DNA interstrand cross-linking agents. Mol. Cancer Res. 10 (2012), 369–377.
163. Nawrocki, S.T., Kelly, K.R., Smith, P.G., Espitia, C.M., Possemato, A., Beausoleil, S.A., Milhollen, M., Blakemore, S., Thomas, M., Berger, A., Carew, J.S., Disrupting protein NEDDylation with MLN4924 is a novel strategy to target cisplatin resistance in ovarian cancer. Clin. Cancer Res. 19 (2013), 3577–3590.
164. Pan, W.W., Zhou, J.J., Yu, C., Xu, Y., Guo, L.J., Zhang, H.Y., Zhou, D., Song, F.Z., Fan, H.Y., Ubiquitin E3 ligase CRL4(CDT2/DCAF2) as a potential chemotherapeutic target for ovarian surface epithelial cancer. J. Biol. Chem. 288 (2013), 29680–29691.
165. Wei, D., Li, H., Yu, J., Sebolt, J.T., Zhao, L., Lawrence, T.S., Smith, P.G., Morgan, M.A., Sun, Y., Radiosensitization of human pancreatic cancer cells by MLN4924, an investigational NEDD8-activating enzyme inhibitor. Cancer Res. 72 (2012), 282–293.
166. Yang, D., Tan, M., Wang, G., The p21-dependent radiosensitization of human breast cancer cells by MLN4924, an investigational inhibitor of NEDD8 activating enzyme. PLoS One, 7, 2012, e34079.
167. Soucy, T.A., Smith, P.G., Milhollen, M.A., Berger, A.J., Gavin, J.M., Adhikari, S., Brownell, J.E., Burke, K.E., Cardin, D.P., Critchley, S., Cullis, C.A., Doucette, A., Garnsey, J.J., Gaulin, J.L., Gershman, R.E., Lublinsky, A.R., McDonald, A., Mizutani, H., Narayanan, U., Olhava, E.J., Peluso, S., Rezaei, M., Sintchak, M.D., Talreja, T., Thomas, M.P., Traore, T., Vyskocil, S., Weatherhead, G.S., Yu, J., Zhang, J., Dick, L.R., Claiborne, C.F., Rolfe, M., Bolen, J.B., Langston, S.P., An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 458 (2009), 732–736.
168. Brownell, J.E., Sintchak, M.D., Gavin, J.M., Liao, H., Bruzzese, F.J., Bump, N.J., Soucy, T.A., Milhollen, M.A., Yang, X., Burkhardt, A.L., Ma, J., Loke, H.K., Lingaraj, T., Wu, D., Hamman, K.B., Spelman, J.J., Cullis, C.A., Langston, S.P., Vyskocil, S., Sells, T.B., Mallender, W.D., Visiers, I., Li, P., Claiborne, C.F., Rolfe, M., Bolen, J.B., Dick, L.R., Substrate-assisted inhibition of ubiquitin-like protein-activating enzymes: the NEDD8 E1 inhibitor MLN4924 forms a NEDD8-AMP mimetic in situ. Mol. Cell 37 (2010), 102–111.
169. Lin, J.J., Milhollen, M.A., Smith, P.G., Narayanan, U., Dutta, A., NEDD8-targeting drug MLN4924 elicits DNA rereplication by stabilizing Cdt1 in S phase, triggering checkpoint activation, apoptosis, and senescence in cancer cells. Cancer Res. 70 (2010), 10310–10320.
170. Rizzardi, L.F., Cook, J.G., Flipping the switch from g1 to s phase with e3 ubiquitin ligases. Genes Cancer 3 (2012), 634–648.
171. Swords, R.T., Kelly, K.R., Smith, P.G., Garnsey, J.J., Mahalingam, D., Medina, E., Oberheu, K., Padmanabhan, S., O'Dwyer, M., Nawrocki, S.T., Giles, F.J., Carew, J.S., Inhibition of NEDD8-activating enzyme: a novel approach for the treatment of acute myeloid leukemia. Blood 115 (2010), 3796–3800.
172. Guo, Z.P., Hu, Y.C., Xie, Y., Jin, F., Song, Z.Q., Liu, X.D., Ma, T., Zhou, P.K., MLN4924 suppresses the BRCA1 complex and synergizes with PARP inhibition in NSCLC cells. Biochem. Biophys. Res. Commun. 483 (2017), 223–229.
173. Rulina, A.V., Mittler, F., Obeid, P., Gerbaud, S., Guyon, L., Sulpice, E., Kermarrec, F., Assard, N., Dolega, M.E., Gidrol, X., Balakirev, M.Y., Distinct outcomes of CRL-Nedd8 pathway inhibition reveal cancer cell plasticity. Cell. Death. Dis., 7, 2016, e2505.
174. Malhab, L.J., Descamps, S., Delaval, B., Xirodimas, D.P., The use of the NEDD8 inhibitor MLN4924 (Pevonedistat) in a cyclotherapy approach to protect wild-type p53 cells from MLN4924 induced toxicity. Sci. Rep., 6, 2016, 37775.
175. Schlierf, A., Altmann, E., Quancard, J., Jefferson, A.B., Assenberg, R., Renatus, M., Jones, M., Hassiepen, U., Schaefer, M., Kiffe, M., Weiss, A., Wiesmann, C., Sedrani, R., Eder, J., Martoglio, B., Targeted inhibition of the COP9 signalosome for treatment of cancer. Nat. Commun., 7, 2016, 13166.
176. Altmann, E., Erbel, P., Renatus, M., Schaefer, M., Schlierf, A., Druet, A., Kieffer, L., Sorge, M., Pfister, K., Hassiepen, U., Jones, M., Ruedisser, S., Ostermeier, D., Martoglio, B., Jefferson, A.B., Quancard, J., Azaindoles as zinc-Binding small-Molecule inhibitors of the JAMM protease CSN5. Angew. Chem. Int. Ed. Engl. 56 (2017), 1294–1297.
177. Jones, J., Wu, K., Yang, Y., Guerrero, C., Nillegoda, N., Pan, Z.Q., Huang, L., A targeted proteomic analysis of the ubiquitin-like modifier nedd8 and associated proteins. J. Proteome Res. 7 (2008), 1274–1287.
178. Merbl, Y., Refour, P., Patel, H., Springer, M., Kirschner, M.W., Profiling of ubiquitin-like modifications reveals features of mitotic control. Cell 152 (2013), 1160–1172.
179. Milhollen, M.A., Narayanan, U., Soucy, T.A., Veiby, P.O., Smith, P.G., Amidon, B., Inhibition of NEDD8-activating enzyme induces rereplication and apoptosis in human tumor cells consistent with deregulating CDT1 turnover. Cancer Res. 71 (2011), 3042–3051.
180. Jia, L., Li, H., Sun, Y., Induction of p21-dependent senescence by an NAE inhibitor MLN4924, as a mechanism of growth suppression. Neoplasia 13 (2011), 561–569.
181. Moreno, S.P., Bailey, R., Campion, N., Herron, S., Gambus, A., Polyubiquitylation drives replisome disassembly at the termination of DNA replication. Science 346 (2014), 477–481.
182. Maric, M., Maculins, T., De Piccoli, G., Labib, K., Cdc48 and a ubiquitin ligase drive disassembly of the CMG helicase at the end of DNA replication. Science, 346, 2014, 1253596.
183. Brown, J.S., Lukashchuk, N., Sczaniecka-Clift, M., Britton, S., le Sage, C., Calsou, P., Beli, P., Galanty, Y., Jackson, S.P., Neddylation promotes ubiquitylation and release of Ku from DNA-damage sites. Cell Rep. 11 (2015), 704–714.
184. Postow, L., Funabiki, H., An SCF complex containing fbxl12 mediates DNA damage-induced ku80 ubiquitylation. ABBV Cell Cycle 12 (2013), 587–595.
185. Postow, L., Ghenoiu, C., Woo, E.M., Krutchinsky, A.N., Chait, B.T., Funabiki, H., Ku80 removal from DNA through double strand break-induced ubiquitylation. J. Cell Biol. 182 (2008), 467–479.
186. Postow, L., Destroying the ring: freeing DNA from Ku with ubiquitin. FEBS Lett. 585 (2011), 2876–2882.
187. Ma, T., Chen, Y., Zhang, F., Yang, C.Y., Wang, S., Yu, X., RNF111-dependent neddylation activates DNA damage-induced ubiquitination. Mol. Cell 49 (2013), 897–907.
188. Li, T., Guan, J., Huang, Z., Hu, X., Zheng, X., RNF168-mediated H2A neddylation antagonizes ubiquitylation of H2A and regulates DNA damage repair. J. Cell Sci. 127 (2014), 2238–2248.
189. Jimeno, S., Fernandez-Avila, M.J., Cruz-Garcia, A., Cepeda-Garcia, C., Gomez-Cabello, D., Huertas, P., Neddylation inhibits CtIP-mediated resection and regulates DNA double strand break repair pathway choice. Nucleic Acids Res. 43 (2015), 987–999.
190. Koinuma, D., Shinozaki, M., Komuro, A., Goto, K., Saitoh, M., Hanyu, A., Ebina, M., Nukiwa, T., Miyazawa, K., Imamura, T., Miyazono, K., Arkadia amplifies TGF-beta superfamily signalling through degradation of Smad7. EMBO J. 22 (2003), 6458–6470.
191. Erker, H., Neyret-Kahn, J.S., Seeler, A., Dejean, A., Atfi, L., Arkadia, a novel SUMO-targeted ubiquitin ligase involved in PML degradation. Mol. Cell. Biol. 33 (2013), 2163–2177.
192. Fousteri, M., Mullenders, L.H., Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects. Cell Res. 18 (2008), 73–84.
193. Groisman, R., Polanowska, J., Kuraoka, I., Sawada, J., Saijo, M., Drapkin, R., Kisselev, A.F., Tanaka, K., Nakatani, Y., The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113 (2003), 357–367.
194. Fischer, E.S., Scrima, A., Bohm, K., Matsumoto, S., Lingaraju, G.M., Faty, M., Yasuda, T., Cavadini, S., Wakasugi, M., Hanaoka, F., Iwai, S., Gut, H., Sugasawa, K., Thoma, N.H., The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell 147 (2011), 1024–1039.
195. Tornaletti, S., DNA repair in mammalian cells: transcription-coupled DNA repair: directing your effort where it's most needed. Cell. Mol. Life Sci. 66 (2009), 1010–1020.
196. Cavadini, S., Fischer, E.S., Bunker, R.D., Potenza, A., Lingaraju, G.M., Goldie, K.N., Mohamed, W.I., Faty, M., Petzold, G., Beckwith, R.E., Tichkule, R.B., Hassiepen, U., Abdulrahman, W., Pantelic, R.S., Matsumoto, S., Sugasawa, K., Stahlberg, H., Thoma, N.H., Cullin-RING ubiquitin E3 ligase regulation by the COP9 signalosome. Nature 531 (2016), 598–603.
197. Wang, H., Zhai, L., Xu, J., Joo, H.Y., Jackson, S., H. Erdjument-Bromage, P., Tempst, Y., Xiong, Y., Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell 22 (2006), 383–394.
198. Havens, C.G., Walter, J.C., Mechanism of CRL4(Cdt2), a PCNA-dependent E3 ubiquitin ligase. Genes Dev. 25 (2011), 1568–1582.
199. 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 (2004), 39–85.
200. Xirodimas, D.P., Novel substrates and functions for the ubiquitin-like molecule NEDD8. Biochem. Soc. Trans. 36 (2008), 802–806.
201. Kim, L.S., Kim, J.H., Heat shock protein as molecular targets for breast cancer therapeutics. J Breast Cancer 14 (2011), 167–174.
202. Leidecker, O., Matic, I., Mahata, B., Pion, E., Xirodimas, D.P., The ubiquitin E1 enzyme Ube1 mediates NEDD8 activation under diverse stress conditions. ABBV Cell Cycle 11 (2012), 1142–1150.
203. Hjerpe, R., Thomas, Y., Chen, J., Zemla, A., Curran, S., Shpiro, N., Dick, L.R., Kurz, T., Changes in the ratio of free NEDD8 to ubiquitin triggers NEDDylation by ubiquitin enzymes. Biochem. J 441 (2012), 927–936.
204. Singh, R.K., Zerath, S., Kleifeld, O., Scheffner, M., Glickman, M.H., Fushman, D., Recognition and cleavage of related to ubiquitin 1 (Rub1) and Rub1-ubiquitin chains by components of the ubiquitin-proteasome system. Mol. Cell. Proteomics 11 (2012), 1595–1611.
205. Korant, B.D., Blomstrom, D.C., Jonak, G.J., Knight, E. Jr., Interferon-induced proteins. Purification and characterization of a 15,000-dalton protein from human and bovine cells induced by interferon. J. Biol. Chem. 259 (1984), 14835–14839.
206. Haas, A.L., Ahrens, P., Bright, P.M., Ankel, H., Interferon induces a 15 k Da protein exhibiting marked homology to ubiquitin. J. Biol. Chem. 262 (1987), 11315–11323.
207. Blomstrom, D.C., Fahey, D., Kutny, R., Korant, B.D., Knight, E. Jr., Molecular characterization of the interferon-induced 15-kDa protein. Molecular cloning and nucleotide and amino acid sequence. J. Biol. Chem. 261 (1986), 8811–8816.
208. Dao, C.T., Zhang, D.E., ISG15: a ubiquitin-like enigma. Front. Biosci. 10 (2005), 2701–2722.
209. Narasimhan, J., Wang, M., Fu, Z., Klein, J.M., Haas, A.L., Kim, J.J., Crystal structure of the interferon-induced ubiquitin-like protein ISG15. J. Biol. Chem. 280 (2005), 27356–27365.
210. Potter, J.L., Narasimhan, J., Mende-Mueller, L., Haas, A.L., Precursor processing of pro-ISG15/UCRP, an interferon-beta-induced ubiquitin-like protein. J. Biol. Chem. 274 (1999), 25061–25068.
211. Yuan, R.M., Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 20 (2001), 362–371.
212. Krug, R.M., Zhao, C., Beaudenon, S., Properties of the ISG15 E1 enzyme UbE1L. Methods Enzymol. 398 (2005), 32–40.
213. Kim, K.I., Yan, M., Malakhova, O., Luo, J.K., Shen, M.F., Zou, W., de la Torre, J.C., L, Ube1, ISGylation are not essential for alpha/beta interferon signaling. Mol. Cell. Biol. 26 (2006), 472–479.
214. de Veer, M.J., Holko, M., Frevel, M., Walker, E., Der, S., Paranjape, J.M., Silverman, R.H., Williams, B.R., Functional classification of interferon-stimulated genes identified using microarrays. J. Leukoc. Biol. 69 (2001), 912–920.
215. Kim, K.I., Malakhova, O.A., Hoebe, K., Yan, M., Beutler, B., Zhang, D.E., Enhanced antibacterial potential in UBP43-deficient mice against Salmonella typhimurium infection by up-regulating type I IFN signaling. J. Immunol. 175 (2005), 847–854.
216. Kim, K.I., Giannakopoulos, N.V., Virgin, H.W., Zhang, D.E., Interferon-inducible ubiquitin E2 Ubc8, is a conjugating enzyme for protein ISGylation. Mol. Cell. Biol. 24 (2004), 9592–9600.
217. Zhao, C., Beaudenon, S.L., Kelley, M.L., Waddell, M.B., Yuan, W., Schulman, B.A., Huibregtse, J.M., Krug, R.M., The UbcH8 ubiquitin E2 enzyme is also the E2 enzyme for ISG15, an IFN-alpha/beta-induced ubiquitin-like protein. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 7578–7582.
218. Durfee, L.A., Kelley, M.L., Huibregtse, J.M., The basis for selective E1-E2 interactions in the ISG15 conjugation system. J. Biol. Chem. 283 (2008), 23895–23902.
219. Morales, D.J., Lenschow, D.J., The antiviral activities of ISG15. J. Mol. Biol. 425 (2013), 4995–5008.
220. Zou, W., Zhang, D.E., The interferon-inducible ubiquitin-protein isopeptide ligase (E3) EFP also functions as an ISG15 E3 ligase. J. Biol. Chem. 281 (2006), 3989–3994.
221. Dastur, S., Beaudenon, M., Kelley, R.M., Krug, J.M., Herc5, an interferon-induced HECT E3 enzyme, is required for conjugation of ISG15 in human cells. J. Biol. Chem. 281 (2006), 4334–4338.
222. Wong, J.J., Pung, Y.F., Sze, N.S., Chin, K.C., HERC5 is an IFN-induced HECT-type E3 protein ligase that mediates type I IFN-induced ISGylation of protein targets. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 10735–10740.
223. Okumura, F., Zou, W., Zhang, D.E., ISG15 modification of the eIF4E cognate 4EHP enhances cap structure-binding activity of 4EHP. Genes Dev. 21 (2007), 255–260.
224. Ketscher, L., Basters, A., Prinz, M., Knobeloch, K.P., mHERC6 is the essential ISG15 E3 ligase in the murine system. Biochem. Biophys. Res. Commun. 417 (2012), 135–140.
225. Oudshoorn, D., van Boheemen, S., Sanchez-Aparicio, M.T., Rajsbaum, R., Garcia-Sastre, A., Versteeg, G.A., HERC6 is the main E3 ligase for global ISG15 conjugation in mouse cells. PLoS One, 7, 2012, e29870.
226. Versteeg, G.A., Hale, B.G., van Boheemen, S., Wolff, T., Lenschow, D.J., Garcia-Sastre, A., Species-specific antagonism of host ISGylation by the influenza B virus NS1 protein. J. Virol. 84 (2010), 5423–5430.
227. Park, J.M., Yang, S.W., Yu, K.R., Ka, S.H., Lee, S.W., Seol, J.H., Jeon, Y.J., Chung, C.H., Modification of PCNA by ISG15 plays a crucial role in termination of error-prone translesion DNA synthesis. Mol. Cell 54 (2014), 626–638.
228. Malakhov, M.P., Malakhova, O.A., Kim, K.I., Ritchie, K.J., Zhang, D.E., UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J. Biol. Chem. 277 (2002), 9976–9981.
229. Malakhova, O.A., Kim, K.I., Luo, J.K., Zou, W., Kumar, K.G., Fuchs, S.Y., Shuai, K., Zhang, D.E., UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. EMBO J. 25 (2006), 2358–2367.
230. Ritchie, K.J., Malakhov, M.P., Hetherington, C.J., Zhou, L., Little, M.T., Malakhova, O.A., Sipe, J.C., Orkin, S.H., Zhang, D.E., Dysregulation of protein modification by ISG15 results in brain cell injury. Genes Dev. 16 (2002), 2207–2212.
231. Malakhova, O., Malakhov, M., Hetherington, C., Zhang, D.E., Lipopolysaccharide activates the expression of ISG15-specific protease UBP43 via interferon regulatory factor 3. J. Biol. Chem. 277 (2002), 14703–14711.
232. Ritchie, K.J., Hahn, C.S., Kim, K.I., Yan, M., Rosario, D., Li, L., de la Torre, J.C., Zhang, D.E., Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat. Med. 10 (2004), 1374–1378.
233. Malakhova, O.A., Yan, M., Malakhov, M.P., Yuan, Y., Ritchie, K.J., Kim, K.I., Peterson, L.F., Shuai, K., Zhang, D.E., Protein ISGylation modulates the JAK-STAT signaling pathway. Genes Dev. 17 (2003), 455–460.
234. Knobeloch, K.P., Utermohlen, O., Kisser, A., Prinz, M., Horak, I., Reexamination of the role of ubiquitin-like modifier ISG15 in the phenotype of UBP43-deficient mice. Mol. Cell. Biol. 25 (2005), 11030–11034.
235. Catic, A., Fiebiger, E., Korbel, G.A., Blom, D., Galardy, P.J., Ploegh, H.L., Screen for ISG15-crossreactive deubiquitinases. PLoS One, 2, 2007, e679.
236. Reyes-Turcu, F.E., Ventii, K.H., Wilkinson, K.D., Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem 78 (2009), 363–397.
237. Giannakopoulos, N.V., Luo, J.K., Papov, V., Zou, W., Lenschow, D.J., Jacobs, B.S., Borden, E.C., Li, J., Virgin, H.W., Zhang, D.E., Proteomic identification of proteins conjugated to ISG15 in mouse and human cells. Biochem. Biophys. Res. Commun. 336 (2005), 496–506.
238. Zhao, C., Denison, C., Huibregtse, J.M., Gygi, S., Krug, R.M., Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 10200–10205.
239. Lenschow, D.J., Giannakopoulos, N.V., Gunn, L.J., Johnston, C., O'Guin, A.K., Schmidt, R.E., Levine, B., Virgin, H.W.t., Identification of interferon-stimulated gene 15 as an antiviral molecule during Sindbis virus infection in vivo. J. Virol. 79 (2005), 13974–13983.
240. Hsiang, T.Y., Zhao, C., Krug, R.M., Interferon-induced ISG15 conjugation inhibits influenza A virus gene expression and replication in human cells. J. Virol. 83 (2009), 5971–5977.
241. Okumura, A., Lu, G., Pitha-Rowe, I., Pitha, P.M., Innate antiviral response targets HIV-1 release by the induction of ubiquitin-like protein ISG15. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 1440–1445.
242. Okumura, A., Pitha, P.M., Harty, R.N., ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 3974–3979.
243. Lenschow, D.J., Lai, C., N. Frias-Staheli, N.V., Giannakopoulos, A., Lutz, T., Wolff, A., Osiak, B., Levine, R.E., Schmidt, A. Garcia-Sastre, Leib, D.A., Pekosz, A., Knobeloch, K.P., Horak, I., IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 1371–1376.
244. Tang, Y., Zhong, G., Zhu, L., Liu, X., Shan, Y., Feng, H., Bu, Z., Chen, H., Wang, C., Herc5 attenuates influenza A virus by catalyzing ISGylation of viral NS1 protein. J. Immunol. 184 (2010), 5777–5790.
245. Guerra, S., Caceres, A., Knobeloch, K.P., Horak, I., Esteban, M., Vaccinia virus E3 protein prevents the antiviral action of ISG15. PLoS Pathog., 4, 2008, e1000096.
246. Osiak, O., Utermohlen, S., Niendorf, I., Horak, K.P., ISG15, an interferon-stimulated ubiquitin-like protein, is not essential for STAT1 signaling and responses against vesicular stomatitis and lymphocytic choriomeningitis virus. Mol. Cell. Biol. 25 (2005), 6338–6345.
247. Shi, H.X., Yang, K., Liu, X., Liu, X.Y., Wei, B., Shan, Y.F., Zhu, L.H., Wang, C., Positive regulation of interferon regulatory factor 3 activation by Herc5 via ISG15 modification. Mol. Cell. Biol. 30 (2010), 2424–2436.
248. Bogunovic, D., Byun, M., Durfee, L.A., Abhyankar, A., Sanal, O., Mansouri, D., Salem, S., Radovanovic, I., Grant, A.V., Adimi, P., Mansouri, N., Okada, S., Bryant, V.L., Kong, X.F., Kreins, A., Velez, M.M., Boisson, B., Khalilzadeh, S., Ozcelik, U., Darazam, I.A., Schoggins, J.W., Rice, C.M., Al-Muhsen, S., Behr, M., Vogt, G., Puel, A., Bustamante, J., Gros, P., Huibregtse, J.M., Abel, L., Boisson-Dupuis, S., Casanova, J.L., Mycobacterial disease and impaired IFN-gamma immunity in humans with inherited ISG15 deficiency. Science 337 (2012), 1684–1688.
249. Hsiao, N.W., Chen, J.W., Yang, T.C., Orloff, G.M., Wu, Y.Y., Lai, C.H., Lan, Y.C., Lin, C.W., ISG15 over-expression inhibits replication of the Japanese encephalitis virus in human medulloblastoma cells. Antiviral Res. 85 (2010), 504–511.
250. Pincetic, A., Kuang, Z., Seo, E.J., Leis, J., The interferon-induced gene ISG15 blocks retrovirus release from cells late in the budding process. J. Virol. 84 (2010), 4725–4736.
251. Kuang, Z., Seo, E.J., Leis, J., Mechanism of inhibition of retrovirus release from cells by interferon-induced gene ISG15. J. Virol. 85 (2011), 7153–7161.
252. Durfee, L.A., Lyon, N., Seo, K., Huibregtse, J.M., The ISG15 conjugation system broadly targets newly synthesized proteins: implications for the antiviral function of ISG15. Mol. Cell 38 (2010), 722–732.
253. Woods, M.W., Kelly, J.N., Hattlmann, C.J., Tong, J.G., Xu, L.S., Coleman, M.D., Quest, G.R., Smiley, J.R., Barr, S.D., Human HERC5 restricts an early stage of HIV-1 assembly by a mechanism correlating with the ISGylation of Gag. Retrovirology, 8, 2011, 95.
254. Pincetic, A., Leis, J., The mechanism of budding of retroviruses from cell membranes. Adv Virol 2009 (2009), 6239691–6239699.
255. Malakhova, O.A., Zhang, D.E., ISG15 inhibits Nedd4 ubiquitin E3 activity and enhances the innate antiviral response. J. Biol. Chem. 283 (2008), 8783–8787.
256. Dai, J., Pan, W., Wang, P., ISG15 facilitates cellular antiviral response to dengue and west nile virus infection in vitro. Virol. J., 8, 2011, 468.
257. Zhao, C., Hsiang, T.Y., Kuo, R.L., Krug, R.M., ISG15 conjugation system targets the viral NS1 protein in influenza A virus-infected cells. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 2253–2258.
258. Lu, G., Reinert, J.T., Pitha-Rowe, I., Okumura, A., Kellum, M., Knobeloch, K.P., Hassel, B., Pitha, P.M., ISG15 enhances the innate antiviral response by inhibition of IRF-3 degradation. Cell Mol Biol (Noisy-le-grand) 52 (2006), 29–41.
259. Kim, M.J., Hwang, S.Y., Imaizumi, T., Yoo, J.Y., Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation. J. Virol. 82 (2008), 1474–1483.
260. Werneke, S.W., Schilte, C., Rohatgi, A., Monte, K.J., Michault, A., Arenzana-Seisdedos, F., Vanlandingham, D.L., Higgs, S., Fontanet, A., Albert, M.L., Lenschow, D.J., ISG15 is critical in the control of Chikungunya virus infection independent of UbE1L mediated conjugation. PLoS Pathog., 7, 2011, e1002322.
261. Jeon, Y.J., Choi, J.S., Lee, J.Y., Yu, K.R., Kim, S.M., Ka, S.H., Oh, K.H., Kim, K.I., Zhang, D.E., Bang, O.S., Chung, C.H., ISG15 modification of filamin B negatively regulates the type I interferon-induced JNK signalling pathway. EMBO Rep. 10 (2009), 374–380.
262. Im, E., Yoo, L., Hyun, M., Shin, W.H., Chung, K.C., Covalent ISG15 conjugation positively regulates the ubiquitin E3 ligase activity of parkin. Open Biol, 6, 2016.
263. Villarroya-Beltri, C., Baixauli, F., Mittelbrunn, M., Fernandez-Delgado, I., Torralba, D., Moreno-Gonzalo, O., Baldanta, S., Enrich, C., Guerra, S., Sanchez-Madrid, F., ISGylation controls exosome secretion by promoting lysosomal degradation of MVB proteins. Nat. Commun., 7, 2016, 13588.
264. Park, J.H., Yang, S.W., Park, J.M., Ka, S.H., Kim, J.H., Kong, Y.Y., Jeon, Y.J., Seol, J.H., Chung, C.H., Positive feedback regulation of p53 transactivity by DNA damage-induced ISG15 modification. Nat. Commun., 7, 2016, 12513.
265. Jeon, Y.J., Jo, M.G., Yoo, H.M., Hong, S.H., Park, J.M., Ka, S.H., Oh, K.H., Seol, J.H., Jung, Y.K., Chung, C.H., Chemosensitivity is controlled by p63 modification with ubiquitin-like protein ISG15. J. Clin. Invest. 122 (2012), 2622–2636.
266. Mustachio, L.M., Kawakami, M., Lu, Y., Rodriguez-Canales, J., Mino, B., Behrens, C., Wistuba, I., Bota-Rabassedas, N., Yu, J., Lee, J.J., Roszik, J., Zheng, L., Liu, X., Freemantle, S.J., Dmitrovsky, E., The ISG15-specific protease USP18 regulates stability of PTEN. Oncotarget 8 (2017), 3–14.
267. Jeon, Y.J., Park, J.H., Chung, C.H., Interferon-Stimulated gene 15 in the control of cellular responses to genotoxic stress. Mol. Cells 40 (2017), 83–89.
268. Andersen, J.B., Aaboe, M., Borden, E.C., Goloubeva, O.G., Hassel, B.A., Orntoft, T.F., Stage-associated overexpression of the ubiquitin-like protein ISG15, in bladder cancer. Br. J. Cancer 94 (2006), 1465–1471.
269. Bektas, N., Noetzel, E., Veeck, J., Press, M.F., Kristiansen, G., Naami, A., Hartmann, A., Dimmler, A., Beckmann, M.W., Knuchel, R., Fasching, P.A., Dahl, E., The ubiquitin-like molecule interferon-stimulated gene 15 (ISG15) is a potential prognostic marker in human breast cancer. Breast Cancer Res., 10, 2008, R58.
270. Chi, L.M., Lee, C.W., Chang, K.P., Hao, S.P., Lee, H.M., Liang, Y., Hsueh, C., Yu, C.J., Lee, I.N., Chang, Y.J., Lee, S.Y., Yeh, Y.M., Chang, Y.S., Chien, K.Y., Yu, J.S., Enhanced interferon signaling pathway in oral cancer revealed by quantitative proteome analysis of microdissected specimens using 16O/18O labeling and integrated two-dimensional LC-ESI-MALDI tandem MS. Mol. Cell. Proteomics 8 (2009), 1453–1474.
271. Satake, H., Tamura, K., Furihata, M., Anchi, T., Sakoda, H., Kawada, C., Iiyama, T., Ashida, S., Shuin, T., The ubiquitin-like molecule interferon-stimulated gene 15 is overexpressed in human prostate cancer. Oncol. Rep. 23 (2010), 11–16.
272. Desai, S.D., Haas, A.L., Wood, L.M., Tsai, Y.C., Pestka, S., Rubin, E.H., Saleem, A., Nur, E.K.A., Liu, L.F., Elevated expression of ISG15 in tumor cells interferes with the ubiquitin/26S proteasome pathway. Cancer Res. 66 (2006), 921–928.
273. Zuo, C., Sheng, X., Ma, M., Xia, M., Ouyang, L., ISG15 in the tumorigenesis and treatment of cancer: an emerging role in malignancies of the digestive system. Oncotarget 7 (2016), 74393–74409.
274. Padovan, E., Terracciano, L., Certa, U., Jacobs, B., Reschner, A., Bolli, M., Spagnoli, G.C., Borden, E.C., Heberer, M., Interferon stimulated gene 15 constitutively produced by melanoma cells induces e-cadherin expression on human dendritic cells. Cancer Res. 62 (2002), 3453–3458.
275. Laljee, R.P., Muddaiah, S., Salagundi, B., Cariappa, P.M., Indra, A.S., Sanjay, V., Ramanathan, A., Interferon stimulated gene-ISG15 is a potential diagnostic biomarker in oral squamous cell carcinomas. Asian Pac. J. Cancer Prev. 14 (2013), 1147–1150.
276. Chen, M.F., Lee, K.D., Lu, M.S., Chen, C.C., Hsieh, M.J., Liu, Y.H., Lin, P.Y., Chen, W.C., The predictive role of E2-EPF ubiquitin carrier protein in esophageal squamous cell carcinoma. J Mol Med (Berl) 87 (2009), 307–320.
277. Yan, W., Shih, J.H., Rodriguez-Canales, J., Tangrea, M.A., Ylaya, K., Hipp, J., Player, A., Hu, N., Goldstein, A.M., Taylor, P.R., Emmert-Buck, M.R., Erickson, H.S., Identification of unique expression signatures and therapeutic targets in esophageal squamous cell carcinoma. BMC Res Notes, 5, 2012, 73.
278. Tao, J., Hua, P., Wen, J., Hu, Y., Yang, H., Xie, X., Prognostic value of ISG15 mRNA level in drinkers with esophageal squamous cell cancers. Int J Clin Exp Pathol 8 (2015), 10975–10984.
279. Jinawath, N., Furukawa, Y., Hasegawa, S., Li, M., Tsunoda, T., Satoh, S., Yamaguchi, T., Imamura, H., Inoue, M., Shiozaki, H., Nakamura, Y., Comparison of gene-expression profiles between diffuse- and intestinal-type gastric cancers using a genome-wide cDNA microarray. Oncogene 23 (2004), 6830–6844.
280. Shen, J., Wei, J., Wang, H., Yue, G., Yu, L., Yang, Y., Xie, L., Zou, Z., Qian, X., Ding, Y., Guan, W., Liu, B., A three-gene signature as potential predictive biomarker for irinotecan sensitivity in gastric cancer. J. Transl. Med., 11, 2013, 73.
281. Lee, J., Li, L., Gretz, N., Gebert, J., Dihlmann, S., Absent in Melanoma 2 (AIM2) is an important mediator of interferon-dependent and -independent HLA-DRA and HLA-DRB gene expression in colorectal cancers. Oncogene 31 (2012), 1242–1253.
282. Ina, S., Hirono, S., Noda, T., Yamaue, H., Identifying molecular markers for chemosensitivity to gemcitabine in pancreatic cancer: increased expression of interferon-stimulated gene 15 kd is associated with intrinsic chemoresistance. Pancreas 39 (2010), 473–485.
283. McLaughlin, P.M., Helfrich, W., Kok, K., Mulder, M., Hu, S.W., Brinker, M.G., Ruiters, M.H., de Leij, L.F., Buys, C.H., The ubiquitin-activating enzyme E1-like protein in lung cancer cell lines. Int. J. Cancer 85 (2000), 871–876.
284. Desai, S.D., Wood, L.M., Tsai, Y.C., Hsieh, T.S., Marks, J.R., Scott, G.L., Giovanella, B.C., Liu, L.F., ISG15 as a novel tumor biomarker for drug sensitivity. Mol. Cancer Ther. 7 (2008), 1430–1439.
285. Desai, S.D., Reed, R.E., Burks, J., Wood, L.M., Pullikuth, A.K., Haas, A.L., Liu, L.F., Breslin, J.W., Meiners, S., Sankar, S., ISG15 disrupts cytoskeletal architecture and promotes motility in human breast cancer cells. Exp Biol Med (Maywood) 237 (2012), 38–49.
286. Matsumura, Y., Yashiro, M., Ohira, M., Tabuchi, H., Hirakawa, K., 5-Fluorouracil up-regulates interferon pathway gene expression in esophageal cancer cells. Anticancer Res. 25 (2005), 3271–3278.
287. Kiessling, A., Hogrefe, C., Erb, S., Bobach, C., Fuessel, S., Wessjohann, L., Seliger, B., Expression, regulation and function of the ISGylation system in prostate cancer. Oncogene 28 (2009), 2606–2620.
288. Kok, K., Hofstra, R., Pilz, A., van den Berg, A., Terpstra, P., Buys, C.H., Carritt, B., A gene in the chromosomal region 3p21 with greatly reduced expression in lung cancer is similar to the gene for ubiquitin-activating enzyme. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 6071–6075.
289. Katsoulidis, E., Sassano, A., Majchrzak-Kita, B., Carayol, N., Yoon, P., Jordan, A., Druker, B.J., Fish, E.N., Platanias, L.C., Suppression of interferon (IFN)-inducible genes and IFN-mediated functional responses in BCR-ABL-expressing cells. J. Biol. Chem. 283 (2008), 10793–10803.
290. Yan, M., Luo, J.K., Ritchie, K.J., Sakai, I., Takeuchi, K., Ren, R., Zhang, D.E., Ubp43 regulates BCR-ABL leukemogenesis via the type 1 interferon receptor signaling. Blood 110 (2007), 305–312.
291. Feng, Q., Sekula, D., Guo, Y., Liu, X., Black, C.C., Galimberti, F., Shah, S.J., Sempere, L.F., Memoli, V., Andersen, J.B., Hassel, B.A., Dragnev, K., Dmitrovsky, E., UBE1L causes lung cancer growth suppression by targeting cyclin D1. Mol. Cancer Ther. 7 (2008), 3780–3788.
292. Fan, W., Cai, W., Parimoo, S., Schwarz, D.C., Lennon, G.G., Weissman, S.M., Identification of seven new human MHC class I region genes around the HLA-F locus. Immunogenetics 44 (1996), 97–103.
293. Buchsbaum, S., Bercovich, B., Ciechanover, A., FAT10 is a proteasomal degradation signal that is itself regulated by ubiquitination. Mol. Biol. Cell 23 (2012), 225–232.
294. Groettrup, M., Pelzer, C., Schmidtke, G., Hofmann, K., Activating the ubiquitin family: UBA6 challenges the field. Trends Biochem. Sci. 33 (2008), 230–237.
295. Theng, S.S., Wang, W., Mah, W.C., Chan, C., Zhuo, J., Gao, Y., Qin, H., Lim, L., Chong, S.S., Song, J., Lee, C.G., Disruption of FAT10-MAD2 binding inhibits tumor progression. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), E5282–5291.
296. Raasi, S., Schmidtke, G., Groettrup, M., The ubiquitin-like protein FAT10 forms covalent conjugates and induces apoptosis. J. Biol. Chem. 276 (2001), 35334–35343.
297. Schmidtke, G., Aichem, A., Groettrup, M., FAT10ylation as a signal for proteasomal degradation. Biochim. Biophys. Acta 1843 (2014), 97–102.
298. Liu, Y.C., Pan, J., Zhang, C., Fan, W., Collinge, M., Bender, J.R., Weissman, S.M., A MHC-encoded ubiquitin-like protein (FAT10) binds noncovalently to the spindle assembly checkpoint protein MAD2. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 4313–4318.
299. Chiu, Y.H., Sun, Q., Chen, Z.J., E1-L2 activates both ubiquitin and FAT10. Mol. Cell 27 (2007), 1014–1023.
300. Lukasiak, S., Schiller, C., Oehlschlaeger, P., Schmidtke, G., Krause, P., Legler, D.F., Autschbach, F., Schirmacher, P., Breuhahn, K., Groettrup, M., Proinflammatory cytokines cause FAT10 upregulation in cancers of liver and colon. Oncogene 27 (2008), 6068–6074.
301. Dokmanovic, M., Chang, B.D., Fang, J., Roninson, I.B., Retinoid-induced growth arrest of breast carcinoma cells involves co-activation of multiple growth-inhibitory genes. Cancer Biol. Ther. 1 (2002), 24–27.
302. Ross, M.J., Wosnitzer, M.S., Ross, M.D., Granelli, B., Gusella, G.L., Husain, M., Kaufman, L., Vasievich, M., D'Agati, V.D., Wilson, P.D., Klotman, M.E., Klotman, P.E., Role of ubiquitin-like protein FAT10 in epithelial apoptosis in renal disease. J. Am. Soc. Nephrol. 17 (2006), 996–1004.
303. Gruen, J.R., Nalabolu, S.R., Chu, T.W., Bowlus, C., Fan, W.F., Goei, V.L., Wei, H., Sivakamasundari, R., Liu, Y.C., Xu, H.X., Parimoo, S., Nallur, G., Ajioka, R., Shukla, H., BrayWard, P., Pan, J., Weissman, S.M., A transcription map of the major histocompatibility complex (MHC) class I region. Genomics 36 (1996), 70–85.
304. Choi, Y., Kim, J.K., Yoo, J.Y., NFkappaB and STAT3 synergistically activate the expression of FAT10, a gene counteracting the tumor suppressor p53. Mol. Oncol. 8 (2014), 642–655.
305. Aichem, A., Groettrup, M., The ubiquitin-like modifier FAT10 in cancer development. Int. J. Biochem. Cell Biol. 79 (2016), 451–461.
306. Hipp, B., Kalveram, S., Raasi, M., Groettrup, G., FAT10, a ubiquitin-independent signal for proteasomal degradation. Mol. Cell. Biol. 25 (2005), 3483–3491.
307. Zhang, D.W., Jeang, K.T., p53 negatively regulates the expression of FAT10, a gene upregulated in various cancers. Oncogene 25 (2006), 2318–2327.
308. Hipp, M.S., Raasi, S., Groettrup, M., Schmidtke, G., NEDD8 ultimate buster-1L interacts with the ubiquitin-like protein FAT10 and accelerates its degradation. J. Biol. Chem. 279 (2004), 16503–16510.
309. Lim, C.B., Zhang, D., Lee, C.G., FAT10, a gene up-regulated in various cancers, is cell-cycle regulated. Cell Div, 1, 2006, 20.
310. Pelzer, I., Kassner, K., Matentzoglu, R.K., Singh, H.P., Wollscheid, M., Scheffner, G., Schmidtke, M., UBE1L2, a novel E1 enzyme specific for ubiquitin. J. Biol. Chem. 282 (2007), 23010–23014.
311. Jin, J., Li, X., Gygi, S.P., Harper, J.W., Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 447 (2007), 1135–1138.
312. Gavin, J.M., Chen, J.J., Liao, H., Rollins, N., Yang, X., Xu, Q., Ma, J., Loke, H.K., Lingaraj, T., Brownell, J.E., Mallender, W.D., Gould, A.E., Amidon, B.S., Dick, L.R., Mechanistic studies on activation of ubiquitin and di-ubiquitin-like protein FAT10, by ubiquitin-like modifier activating enzyme 6, Uba6. J. Biol. Chem. 287 (2012), 15512–15522.
313. A, Aichem, A., Pelzer, S., Lukasiak, B., Kalveram, P.W., Sheppard, N., Rani, G., Schmidtke, Groettrup, M., USE1 is a bispecific conjugating enzyme for ubiquitin and FAT10, which FAT10ylates itself in cis. Nat. Commun., 1, 2010, 13.
314. Gu, X., Zhao, F., Zheng, M., Fei, X., Chen, X., Huang, S., Xie, Y., Mao, Y., Cloning and characterization of a gene encoding the human putative ubiquitin conjugating enzyme E2Z (UBE2Z). Mol. Biol. Rep. 34 (2007), 183–188.
315. Aichem, A., Catone, N., Groettrup, M., Investigations into the auto-FAT10ylation of the bispecific E2 conjugating enzyme UBA6-specific E2 enzyme 1. FEBS J. 281 (2014), 1848–1859.
316. Bialas, J., Groettrup, M., Aichem, A., Conjugation of the ubiquitin activating enzyme UBE1 with the ubiquitin-like modifier FAT10 targets it for proteasomal degradation. PLoS One, 10, 2015, e0120329.
317. Wu, C., Liu, Y., Gu, X., Zhu, T., Yang, S., Sun, W., LMO2 blocks the UBA6-USE1 interaction and downstream FAT10ylation by targeting the ubiquitin fold domain of UBA6. Biochem. Biophys. Res. Commun. 478 (2016), 1442–1448.
318. Aichem, A., Kalveram, B., Spinnenhirn, V., Kluge, K., Catone, N., Johansen, T., Groettrup, M., The proteomic analysis of endogenous FAT10 substrates identifies p62/SQSTM1 as a substrate of FAT10ylation. J. Cell Sci. 125 (2012), 4576–4585.
319. Leng, L., Xu, C., Wei, C., Zhang, J., Liu, B., Ma, J., Li, N., Qin, W., Zhang, W., Zhang, C., Xing, X., Zhai, L., Yang, F., Li, M., Jin, C., Yuan, Y., Xu, P., Qin, J., Xie, H., He, F., Wang, J., A proteomics strategy for the identification of FAT10-modified sites by mass spectrometry. J. Proteome Res. 13 (2014), 268–276.
320. Schliehe, C., Bitzer, A., van den Broek, M., Groettrup, M., Stable antigen is most effective for eliciting CD8+ T-cell responses after DNA vaccination and infection with recombinant vaccinia virus in vivo. J. Virol. 86 (2012), 9782–9793.
321. Schmidtke, G., Kalveram, B., Weber, E., Bochtler, P., Lukasiak, S., Hipp, M.S., Groettrup, M., The UBA domains of NUB1L are required for binding but not for accelerated degradation of the ubiquitin-like modifier FAT10. J. Biol. Chem. 281 (2006), 20045–20054.
322. Lee, C.G., Ren, J., Cheong, I.S., Ban, K.H., Ooi, L.L., Yong Tan, S., Kan, A., Nuchprayoon, I., Jin, R., Lee, K.H., Choti, M., Lee, L.A., Expression of the FAT10 gene is highly upregulated in hepatocellular carcinoma and other gastrointestinal and gynecological cancers. Oncogene 22 (2003), 2592–2603.
323. Canaan, A., Yu, X., Booth, C.J., Lian, J., Lazar, I., Gamfi, S.L., Castille, K., Kohya, N., Nakayama, Y., Liu, Y.C., Eynon, E., Flavell, R., Weissman, S.M., FAT10/diubiquitin-like protein-deficient mice exhibit minimal phenotypic differences. Mol. Cell. Biol. 26 (2006), 5180–5189.
324. Raasi, S., Schmidtke, G., de Giuli, R., Groettrup, M., A ubiquitin-like protein which is synergistically inducible by interferon-gamma and tumor necrosis factor-alpha. Eur. J. Immunol. 29 (1999), 4030–4036.
325. Spinnenhirn, V., Farhan, H., Basler, M., Aichem, A., Canaan, A., Groettrup, M., The ubiquitin-like modifier FAT10 decorates autophagy-targeted Salmonella and contributes to Salmonella resistance in mice. J. Cell Sci. 127 (2014), 4883–4893.
326. Nguyen, N.T., Now, H., Kim, W.J., Kim, N., Yoo, J.Y., Ubiquitin-like modifier FAT10 attenuates RIG-I mediated antiviral signaling by segregating activated RIG-I from its signaling platform. Sci. Rep., 6, 2016, 23377.
327. Liu, L., Dong, Z., Liang, J., Cao, C., Sun, J., Ding, Y., Wu, D., As an independent prognostic factor, FAT10 promotes hepatitis B virus-related hepatocellular carcinoma progression via Akt/GSK3beta pathway. Oncogene 33 (2014), 909–920.
328. Han, T., Liu, Z., Li, H., Xie, W., Zhang, R., Zhu, L., Guo, F., Han, Y., Sheng, Y., Xie, X., High expression of UBD correlates with epirubicin resistance and indicates poor prognosis in triple-negative breast cancer. Onco Targets Ther 8 (2015), 1643–1649.
329. Dong, D., Jiang, W., Lei, J., Chen, L., Liu, X., Ge, J., Che, B., Xi, X., Shao, J., Ubiquitin-like protein FAT10 promotes bladder cancer progression by stabilizing survivin. Oncotarget 7 (2016), 81463–81473.
330. Ji, F., Jin, X., Jiao, C.H., Xu, Q.W., Wang, Z.W., Chen, Y.L., FAT10 level in human gastric cancer and its relation with mutant p53 level, lymph node metastasis and TNM staging. World J. Gastroenterol. 15 (2009), 2228–2233.
331. Dai, B., Zhang, Y., Zhang, P., Pan, C., Xu, C., Wan, W., Wu, Z., Zhang, J., Zhang, L., Upregulation of p-Smad2 contributes to FAT10-induced oncogenic activities in glioma. Tumour Biol. 37 (2016), 8621–8631.
332. Yuan, J., Tu, Y., Mao, X., He, S., Wang, L., Fu, G., Zong, J., Zhang, Y., Increased expression of FAT10 is correlated with progression and prognosis of human glioma. Pathol. Oncol. Res. 18 (2012), 833–839.
333. Sun, G.H., Liu, Y.D., Yu, G., Li, N., Sun, X., Yang, J., Increased FAT10 expression is related to poor prognosis in pancreatic ductal adenocarcinoma. Tumour Biol. 35 (2014), 5167–5171.
334. Ma, C., Zhang, Z., Cui, Y., Yuan, H., Wang, F., Silencing FAT10 inhibits metastasis of osteosarcoma. Int. J. Oncol. 49 (2016), 666–674.
335. Ren, J., Kan, A., Leong, S.H., Ooi, L.L., Jeang, K.T., Chong, S.S., Kon, O.L., Lee, C.G., FAT10 plays a role in the regulation of chromosomal stability. J. Biol. Chem. 281 (2006), 11413–11421.
336. Ren, J., Wang, Y., Gao, Y., Mehta, S.B., Lee, C.G., FAT10 mediates the effect of TNF-alpha in inducing chromosomal instability. J. Cell Sci. 124 (2011), 3665–3675.
337. Gao, Y., Theng, S.S., Mah, W.C., Lee, C.G., Silibinin down-regulates FAT10 and modulate TNF-alpha/IFN-gamma-induced chromosomal instability and apoptosis sensitivity. Biol Open 4 (2015), 961–969.
338. Yuan, R., Wang, K., Hu, J., Yan, C., Li, M., Yu, X., Liu, X., Lei, J., Guo, W., Wu, L., Hong, K., Shao, J., Ubiquitin-like protein FAT10 promotes the invasion and metastasis of hepatocellular carcinoma by modifying beta-catenin degradation. Cancer Res. 74 (2014), 5287–5300.
339. Liu, X., Chen, L., Ge, J., Yan, C., Huang, Z., Hu, J., Wen, C., Li, M., Huang, D., Qiu, Y., Hao, H., Yuan, R., Lei, J., Yu, X., Shao, J., The ubiquitin-like protein FAT10 stabilizes eEF1A1 expression to promote tumor proliferation in a complex manner. Cancer Res. 76 (2016), 4897–4907.
340. Gao, Y., Theng, S.S., Zhuo, J., Teo, W.B., Ren, J., Lee, C.G., FAT10, an ubiquitin-like protein, confers malignant properties in non-tumorigenic and tumorigenic cells. Carcinogenesis 35 (2014), 923–934.
341. Chen, J., Yang, L., Chen, H., Yuan, T., Liu, M., Chen, P., Recombinant adenovirus encoding FAT10 small interfering RNA inhibits HCC growth in vitro and in vivo. Exp. Mol. Pathol. 96 (2014), 207–211.
342. Zhao, S., Jiang, T., Tang, H., Cui, F., Liu, C., Guo, F., Lu, H., Xue, Y., Jiang, W., Peng, Z., Yan, D., Ubiquitin, D is an independent prognostic marker for survival in stage IIB-IIC colon cancer patients treated with 5-fluoruracil-based adjuvant chemotherapy. J. Gastroenterol. Hepatol. 30 (2015), 680–688.
343. Peng, X., Shao, J., Shen, Y., Zhou, Y., Cao, Q., Hu, J., He, W., Yu, X., Liu, X., Marian, A.J., Hong, K., FAT10 protects cardiac myocytes against apoptosis. J. Mol. Cell. Cardiol. 59 (2013), 1–10.
344. Buchsbaum, S., Bercovich, B., Ziv, T., Ciechanover, A., Modification of the inflammatory mediator LRRFIP2 by the ubiquitin-like protein FAT10 inhibits its activity during cellular response to LPS. Biochem. Biophys. Res. Commun. 428 (2012), 11–16.
345. Xue, F., Zhu, L., Meng, Q.W., Wang, L., Chen, X.S., Zhao, Y.B., Xing, Y., Wang, X.Y., Cai, L., FAT10 is associated with the malignancy and drug resistance of non-small-cell lung cancer. Onco Targets Ther 9 (2016), 4397–4409.
346. Li, T., Santockyte, R., Yu, S., Shen, R.F., Tekle, E., Lee, C.G., Yang, D.C., Chock, P.B., FAT10 modifies p53 and upregulates its transcriptional activity. Arch. Biochem. Biophys. 509 (2011), 164–169.
347. Komatsu, M., Chiba, T., Tatsumi, K., Iemura, S., Tanida, I., Okazaki, N., Ueno, T., Kominami, E., Natsume, T., Tanaka, K., A novel protein-conjugating system for Ufm1, a ubiquitin-fold modifier. EMBO J. 23 (2004), 1977–1986.
348. Kang, S.H., Kim, G.R., Seong, M., Baek, S.H., Seol, J.H., Bang, O.S., Ovaa, H., Tatsumi, K., Komatsu, M., Tanaka, K., Chung, C.H., Two novel ubiquitin-fold modifier 1 (Ufm1)-specific proteases, UfSP1 and UfSP2. J. Biol. Chem. 282 (2007), 5256–5262.
349. Daniel, J., Liebau, E., The ufm1 cascade. Cells 3 (2014), 627–638.
350. Watson, C.M., Crinnion, L.A., Gleghorn, L., Newman, W.G., Ramesar, R., Beighton, P., Wallis, G.A., Identification of a mutation in the ubiquitin-fold modifier 1-specific peptidase 2 gene UFSP2, in an extended South African family with Beukes hip dysplasia. S. Afr. Med. J. 105 (2015), 558–563.
351. Dou, T., Gu, S., Liu, J., Chen, F., Zeng, L., Guo, L., Xie, Y., Mao, Y., Isolation and characterization of ubiquitin-activating enzyme E1-domain containing 1, UBE1DC1. Mol. Biol. Rep. 32 (2005), 265–271.
352. Bacik, J.P., Walker, J.R., Ali, M., Schimmer, A.D., Dhe-Paganon, S., Crystal structure of the human ubiquitin-activating enzyme 5 (UBA5) bound to ATP: mechanistic insights into a minimalistic E1 enzyme. J. Biol. Chem. 285 (2010), 20273–20280.
353. Zheng, M., Gu, X., Zheng, D., Yang, Z., Li, F., Zhao, J., Xie, Y., Ji, C., Mao, Y., UBE1DC1, an ubiquitin-activating enzyme, activates two different ubiquitin-like proteins. J. Cell. Biochem. 104 (2008), 2324–2334.
354. Tatsumi, K., Yamamoto-Mukai, H., Shimizu, R., Waguri, S., Sou, Y.S., Sakamoto, A., Taya, C., Shitara, H., Hara, T., Chung, C.H., Tanaka, K., Yamamoto, M., Komatsu, M., The Ufm1-activating enzyme Uba5 is indispensable for erythroid differentiation in mice. Nat. Commun., 2, 2011, 181.
355. Wei, X., UFMylation: a unique & fashionable modification for life. Genomics Proteomics Bioinformatics 14 (2016), 140–146.
356. Mizushima, T., Tatsumi, K., Ozaki, Y., Kawakami, T., Suzuki, A., Ogasahara, K., Komatsu, M., Kominami, E., Tanaka, K., Yamane, T., Crystal structure of Ufc1, the Ufm1-conjugating enzyme. Biochem. Biophys. Res. Commun. 362 (2007), 1079–1084.
357. Tatsumi, K., Sou, Y.S., Tada, N., Nakamura, E., Iemura, S., Natsume, T., Kang, S.H., Chung, C.H., Kasahara, M., Kominami, E., Yamamoto, M., Tanaka, K., Komatsu, M., A novel type of E3 ligase for the Ufm1 conjugation system. J. Biol. Chem. 285 (2010), 5417–5427.
358. Yoo, H.M., Kang, S.H., Kim, J.Y., Lee, J.E., Seong, M.W., Lee, S.W., Ka, S.H., Sou, Y.S., Komatsu, M., Tanaka, K., Lee, S.T., Noh, D.Y., Baek, S.H., Jeon, Y.J., Chung, C.H., Modification of ASC1 by UFM1 is crucial for ERalpha transactivation and breast cancer development. Mol. Cell 56 (2014), 261–274.
359. Pick, E., Hofmann, K., Glickman, M.H., PCI complexes: beyond the proteasome, CSN, and eIF3 Troika. Mol. Cell 35 (2009), 260–264.
360. Cai, Y., Pi, W., Sivaprakasam, S., Zhu, X., Zhang, M., Chen, J., Makala, L., Lu, C., Wu, J., Teng, Y., Pace, B., Tuan, D., Singh, N., Li, H., UFBP1, a key component of the ufm1 conjugation system, is essential for ufmylation-Mediated regulation of erythroid development. PLoS Genet., 11, 2015, e1005643.
361. Wu, J., Lei, G., Mei, M., Tang, Y., Li, H., A novel C53/LZAP-interacting protein regulates stability of C53/LZAP and DDRGK domain-containing Protein 1 (DDRGK1) and modulates NF-kappaB signaling. J. Biol. Chem. 285 (2010), 15126–15136.
362. Xu, J., Wu, R.C., O'Malley, B.W., Normal and cancer-related functions of the p160 steroid receptor co-activator (SRC) family. Nat. Rev. Cancer 9 (2009), 615–630.
363. Yoo, H.M., Park, J.H., Jeon, Y.J., Chung, C.H., Ubiquitin-fold modifier 1 acts as a positive regulator of breast cancer. Front Endocrinol (Lausanne), 6, 2015, 36.
364. Azfer, A., Niu, J., Rogers, L.M., Adamski, F.M., Kolattukudy, P.E., Activation of endoplasmic reticulum stress response during the development of ischemic heart disease. Am. J. Physiol. Heart Circ. Physiol. 291 (2006), H1411–1420.
365. Zhang, Y., Zhang, M., Wu, J., Lei, G., Li, H., Transcriptional regulation of the Ufm1 conjugation system in response to disturbance of the endoplasmic reticulum homeostasis and inhibition of vesicle trafficking. PLoS One, 7, 2012, e48587.
366. Zhang, M., Zhu, X., Zhang, Y., Cai, Y., Chen, J., Sivaprakasam, S., Gurav, A., Pi, W., Makala, L., Wu, J., Pace, B., Lo, Tuan-, Ganapathy, V., Singh, N., Li, H., RCAD/Ufl1, a Ufm1 E3 ligase, is essential for hematopoietic stem cell function and murine hematopoiesis. Cell Death Differ. 22 (2015), 1922–1934.
367. Gannavaram, S., Connelly, P.S., Daniels, M.P., Duncan, R., Salotra, P., Nakhasi, H.L., Deletion of mitochondrial associated ubiquitin fold modifier protein Ufm1 in Leishmania donovani results in loss of beta-oxidation of fatty acids and blocks cell division in the amastigote stage. Mol. Microbiol. 86 (2012), 187–198.
368. Chen, C., Itakura, E., Weber, K.P., Hegde, R.S., de Bono, M., An ER complex of ODR-4 and ODR-8/Ufm1 specific protease 2 promotes GPCR maturation by a Ufm1-independent mechanism. PLoS Genet., 10, 2014, e1004082.
369. Homrich, M., Wobst, H., Laurini, C., Sabrowski, J., Schmitz, B., Diestel, S., Cytoplasmic domain of NCAM140 interacts with ubiquitin-fold modifier-conjugating enzyme-1 (Ufc1). Exp. Cell Res. 324 (2014), 192–199.
370. Colin, E., Daniel, J., Ziegler, A., Wakim, J., Scrivo, A., Haack, T.B., Khiati, S., Denomme, A.S., Amati-Bonneau, P., Charif, M., Procaccio, V., Reynier, P., Aleck, K.A., Botto, L.D., Herper, C.L., Kaiser, C.S., Nabbout, R., N'Guyen, S., Mora-Lorca, J.A., Assmann, B., Christ, S., Meitinger, T., Strom, T.M., Prokisch, H., Miranda-Vizuete, A., Hoffmann, G.F., Lenaers, G., Bomont, P., Liebau, E., Bonneau, D., Biallelic variants in UBA5 reveal that disruption of the UFM1 cascade can result in early-Onset encephalopathy. Am. J. Hum. Genet. 99 (2016), 695–703.
371. Hu, X., Pang, Q., Shen, Q., Liu, H., He, J., Wang, J., Xiong, J., Zhang, H., Chen, F., Ubiquitin-fold modifier 1 inhibits apoptosis by suppressing the endoplasmic reticulum stress response in Raw264.7 cells. Int. J. Mol. Med. 33 (2014), 1539–1546.
372. Rubio, M.D., Wood, K., Haroutunian, V., Meador-Woodruff, J.H., Dysfunction of the ubiquitin proteasome and ubiquitin-like systems in schizophrenia. Neuropsychopharmacology 38 (2013), 1910–1920.
373. Schroder, M., Kaufman, R.J., The mammalian unfolded protein response. Annu. Rev. Biochem 74 (2005), 739–789.
374. Lemaire, K., Moura, R.F., Granvik, M., Igoillo-Esteve, M., Hohmeier, H.E., Hendrickx, N., Newgard, C.B., Waelkens, E., Cnop, M., Schuit, F., Ubiquitin fold modifier 1 (UFM1) and its target UFBP1 protect pancreatic beta cells from ER stress-induced apoptosis. PLoS One, 6, 2011, e18517.
375. Liu, J., Wang, Y., Song, L., Zeng, L., Yi, W., Liu, T., Chen, H., Wang, M., Ju, Z., Cong, Y.S., A critical role of DDRGK1 in endoplasmic reticulum homoeostasis via regulation of IRE1alpha stability. Nat. Commun., 8, 2017, 14186.
376. Hertel, P., Daniel, J., Stegehake, D., Vaupel, H., Kailayangiri, S., Gruel, C., Woltersdorf, C., Liebau, E., The ubiquitin-fold modifier 1 (Ufm1) cascade of Caenorhabditis elegans. J. Biol. Chem. 288 (2013), 10661–10671.
377. Liu, H., Li, J., Tillman, B., French, B.A., French, S.W., Ufmylation and FATylation pathways are downregulated in human alcoholic and nonalcoholic steatohepatitis, and mice fed DDC, where Mallory-Denk bodies (MDBs) form. Exp. Mol. Pathol. 97 (2014), 81–88.
378. Xi, P., Ding, D., Zhou, J., Wang, M., Cong, Y.S., DDRGK1 regulates NF-kappaB activity by modulating IkappaBalpha stability. PLoS One, 8, 2013, e64231.
379. Gavin, J.M., Hoar, K., Xu, Q., Ma, J., Lin, Y., Chen, J., Chen, W., Bruzzese, F.J., Harrison, S., Mallender, W.D., Bump, N.J., Sintchak, M.D., Bence, N.F., Li, P., Dick, L.R., Gould, A.E., Chen, J.J., Mechanistic study of Uba5 enzyme and the Ufm1 conjugation pathway. J. Biol. Chem. 289 (2014), 22648–22658.
380. da Silva, S.R., Paiva, S.L., Bancerz, M., Geletu, M., Lewis, A.M., Chen, J., Cai, Y., Lukkarila, J.L., Li, H., Gunning, P.T., A selective inhibitor of the UFM1-activating enzyme, UBA5. Bioorg. Med. Chem. Lett. 26 (2016), 4542–4547.
381. Pirone, L., Xolalpa, W., Sigurethsson, J.O., Ramirez, J., Perez, C., Gonzalez, M., de Sabando, A.R., Elortza, F., Rodriguez, M.S., Mayor, U., Olsen, J.V., Barrio, R., Sutherland, J.D., A comprehensive platform for the analysis of ubiquitin-like protein modifications using in vivo biotinylation. Sci. Rep., 7, 2017, 40756.
382. Tatham, M.H., Geoffroy, M.C., Shen, L., Plechanovova, A., Hattersley, N., Jaffray, E.G., Palvimo, J.J., Hay, R.T., RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10 (2008), 538–546.
383. Galanty, R., Belotserkovskaya, J., Coates, S.P., RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev. 26 (2012), 1179–1195.
384. Vyas, R., Kumar, R., Clermont, F., Helfricht, A., Kalev, P., Sotiropoulou, P., Hendriks, I.A., Radaelli, E., Hochepied, T., Blanpain, C., Sablina, A., van Attikum, H., Olsen, J.V., Jochemsen, A.G., Vertegaal, A.C., Marine, J.C., RNF4 is required for DNA double-strand break repair in vivo. Cell Death Differ. 20 (2013), 490–502.
385. 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. 26 (2012), 1196–1208.
386. Takeuchi, T., Yokosawa, H., ISG15 modification of Ubc13 suppresses its ubiquitin-conjugating activity. Biochem. Biophys. Res. Commun. 336 (2005), 9–13.
387. Zou, W., Papov, V., Malakhova, O., Kim, K.I., Dao, C., Li, J., ISG15 modification of ubiquitin E2 Ubc13 disrupts its ability to form thioester bond with ubiquitin. Biochem. Biophys. Res. Commun. 336 (2005), 61–68.
388. Takeuchi, S., Iwahara, Y., Saeki, H., Sasajima, H., Link between the ubiquitin conjugation system and the ISG15 conjugation system: ISG15 conjugation to the UbcH6 ubiquitin E2 enzyme. J. Biochem. 138 (2005), 711–719.
389. Liu, H., Stone, S.L., Cytoplasmic degradation of the Arabidopsis transcription factor abscisic acid insensitive 5 is mediated by the RING-type E3 ligase KEEP ON GOING. J. Biol. Chem. 288 (2013), 20267–20279.
390. Lachaud, D., Castor, K., Hain, I., Munoz, J., Wilson, T.J., MacArtney, D., Distinct functional roles for the two SLX4 ubiquitin-binding UBZ domains mutated in Fanconi anemia. J. Cell Sci. 127 (2014), 2811–2817.
391. Guervilly, A., Takedachi, V., Naim, S., Scaglione, C., Chawhan, Y., Lovera, E., Despras, I., Kuraoka, P., Kannouche, F., The SLX4 complex is a SUMO E3 ligase that impacts on replication stress outcome and genome stability. Mol. Cell 57 (2015), 123–137.
392. 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 57 (2015), 108–122.
393. Fan, J.B., Arimoto, K., Motamedchaboki, K., Yan, M., Wolf, D.A., Zhang, D.E., Identification and characterization of a novel ISG15-ubiquitin mixed chain and its role in regulating protein homeostasis. Sci. Rep., 5, 2015, 12704.
394. Cajee, R., Hull, M., Modification by ubiquitin-like proteins: significance in apoptosis and autophagy pathways. Int. J. Mol. Sci. 13 (2012), 11804–11831.