315
Views
5
CrossRef citations to date
0
Altmetric
Review Article

The role of ubiquitin-binding domains in human pathophysiology

, , &
Pages 280-290 | Received 17 Jan 2014, Accepted 11 Apr 2014, Published online: 05 Jun 2014

References

  • Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998;67:425–79
  • Varshavsky A. Regulated protein degradation. Trends Biochem Sci 2005;30:283–6
  • Mukhopadhyay D, Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007;315:201–5
  • Hirsch C, Gauss R, Horn SC, et al. The ubiquitylation machinery of the endoplasmic reticulum. Nature 2009;458:453–60
  • Vucic D, Dixit VM, Wertz IE. Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat Rev Mol Cell Biol 2011;12:439–52
  • Kirkin V, McEwan DG, Novak I, Dikic I. A role for ubiquitin in selective autophagy. Mol Cell 2009;34:259–69
  • Elsasser S, Finley D. Delivery of ubiquitinated substrates to protein-unfolding machines. Nat Cell Biol 2005;7:742–9
  • Staub O, Rotin D. Role of ubiquitylation in cellular membrane transport. Physiol Rev 2006;86:669–707
  • Huang TT, D’Andrea AD. Regulation of DNA repair by ubiquitylation. Nat Rev Mol Cell Biol 2006;7:323–34
  • Raiborg C, Bache KG, Gillooly DJ, et al. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol 2002;4:394–8
  • Hurley JH, Lee S, Prag G. Ubiquitin-binding domains. Biochem J 2006;399:361–72
  • Hicke L, Schubert HL, Hill CP. Ubiquitin-binding domains. Nat Rev Mol Cell Biol 2005;6:610–21
  • Dikic I, Wakatsuki S, Walters KJ. Ubiquitin-binding domains – from structures to functions. Nat Rev Mol Cell Biol 2009;10:659–71
  • Komander D, Rape M. The ubiquitin code. Annu Rev Biochem 2012;81:203–29
  • Ciechanover A, Ben-Saadon R. N-terminal ubiquitination: more protein substrates join in. Trends Cell Biol 2004;14:103–6
  • Ravid T, Hochstrasser M. Autoregulation of an E2 enzyme by ubiquitin-chain assembly on its catalytic residue. Nat Cell Biol 2007;9:422–7
  • Wang XL, Herr RA, Chua WJ, et al. Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J Cell Biol 2007;177:613–24
  • Pickart CM. Mechanisms underlying ubiquitination. Annu Rev Biochem 2001;70:503–33
  • Chau V, Tobias JW, Bachmair A, et al. A multiubiquitin chain is confined to specific lysise in a targeted short-lived protein. Science 1989;243:1576–83
  • Cook WJ, Jeffrey LC, Carson M, et al. Structure of a diubiquitin conjugate and a model for interaction with ubiquitin conjugating enzyme (E2). J Biol Chem 1992;267:16467–71
  • Sun LJ, Chen ZJ. The novel functions of ubiquitination in signaling. Curr Opin Cell Biol 2004;16:119–26
  • Hicke L, Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 2003;19:141–72
  • Spence J, Gali RR, Dittmar G, et al. Cell cycle-regulated modification of the ribosome by a variant multiubiquitin chain. Cell 2000;102:67–76
  • Komander D. The emerging complexity of protein ubiquitination. Biochem Soc Trans 2009;37:937–53
  • Wu-Baer F, Lagrazon K, Yuan W, Baer R. The BRCA1/BARD1 heterodimer assembles polyubiquitin chains through an unconventional linkage involving lysine residue K6 of ubiquitin. J Biol Chem 2003;278:34743–6
  • Morris JR, Solomon E. BRCA1: BARD1 induces the formation of conjugated ubiquitin structures, dependent on K6 of ubiquitin, in cells during DNA replication and repair. Hum Mol Genet 2004;13:807–17
  • Kirisako T, Kamei K, Murata S, et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J 2006;25:4877–87
  • Iwai K, Tokunaga F. Linear polyubiquitination: a new regulator of NF-kappaB activation. EMBO Rep 2009;10:706–13
  • Tokunaga F, Sakata S, Saeki Y, et al. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat Cell Biol 2009;11:123–32
  • Rahighi S, Ikeda F, Kawasaki M, et al. Specific recognition of linear ubiquitin chains by NEMO is important for NF-κB activation. Cell 2009;136:1098–109
  • Nakasone Mark A, Livnat-Levanon N, Glickman Michael H, et al. Mixed-linkage ubiquitin chains send mixed messages. Structure (London, England: 1993) 2013;21:727–40
  • Ikeda F, Dikic I. Atypical ubiquitin chains: new molecular signals – ‘protein modifications: beyond the usual suspects’ review series. EMBO Rep 2008;9:536–42
  • Husnjak K, Dikic I. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu Rev Biochem 2012;81:291–322
  • Kulathu Y, Komander D. Atypical ubiquitylation – the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat Rev Mol Cell Biol 2012;13:508–23
  • Massey LK, Mah AL, Ford DL, et al. Overexpression of ubiquilin decreases ubiquitination and degradation of presenilin proteins. J Alzheimers Dis 2004;6:79–92
  • Raasi S, Pickart CM. Rad23 ubiquitin-associated domains (UBA) inhibit 26 S proteasome-catalyzed proteolysis by sequestering lysine 48-linked polyubiquitin chains. J Biol Chem 2003;278:8951–9
  • Brignone C, Bradley KE, Kisselev AF, Grossman SR. A post-ubiquitination role for MDM2 and hHR23A in the p53 degradation pathway. Oncogene 2004;23:4121–9
  • Walters KJ, Lech PJ, Goh AM, et al. DNA-repair protein hHR23a alters its protein structure upon binding proteasomal subunit S5a. Proc Natl Acad Sci USA 2003;100:12694–9
  • Deveraux Q, Ustrell V, Pickart C, Rechsteiner M. A 26-S protease subunit that binds ubiquitin conjugates. J Biol Chem 1994;269:7059–61
  • Fisher RD, Wang B, Alam SL, et al. Structure and ubiquitin binding of the ubiquitin-interacting motif. J Biol Chem 2003;278:28976–84
  • Lee S, Tsai YC, Mattera R, et al. Structural basis for ubiquitin recognition and autoubiquitination by Rabex-5. Nat Struct Mol Biol 2006;13:264–71
  • Hirano S, Kawasaki M, Ura H, et al. Double-sided ubiquitin binding of Hrs-UIM in endosomal protein sorting. Nat Struct Mol Biol 2006;13:272–7
  • Haririnia A, Verma R, Purohit N, et al. Mutations in the hydrophobic core of ubiquitin differentially affect its recognition by receptor proteins. J Mol Biol 2008;375:979–96
  • Penengo L, Mapelli M, Murachelli AG, et al. Crystal structure of the ubiquitin binding domains of rabex-5 reveals two modes of interaction with ubiquitin. Cell 2006;124:1183–95
  • VanDemark AP, Hofmann RM, Tsui C, et al. Molecular insights into polyubiquitin chain assembly: crystal structure of the Mms2/Ubc13 heterodimer. Cell 2001;105:711–20
  • Wu T, Merbl Y, Huo Y, et al. UBE2S drives elongation of K11-linked ubiquitin chains by the anaphase-promoting complex. Proc Natl Acad Sci USA 2010;107:1355–60
  • Chen Z, Pickart CM. A 25-kilodalton ubiquitin carrier protein (E2) catalyzes multi-ubiquitin chain synthesis via lysine 48 of ubiquitin. J Biol Chem 1990;265:21835–42
  • Wilson RC, Edmondson SP, Flatt JW, et al. The E2-25K ubiquitin-associated (UBA) domain aids in polyubiquitin chain synthesis and linkage specificity. Biochem Biophys Res Commun 2011;405:662–6
  • Song S, Kim S-Y, Hong Y-M, et al. Essential role of E2-25K/Hip-2 in mediating amyloid-β neurotoxicity. Mol Cell 2003;12:553–63
  • Barnham KJ, Cappai R, Beyreuther K, et al. Delineating common molecular mechanisms in Alzheimer’s and prion diseases. Trends Biochem Sci 2006;31:465–72
  • van Leeuwen FW, de Kleijn DP, van den Hurk HH, et al. Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer’s and Down patients. Science 1998;279:242–7
  • De Vrij FM, Sluijs JA, Gregori L, et al. Mutant ubiquitin expressed in Alzheimer’s disease causes neuronal death. FASEB J 2001;15:2680–8
  • Lindsten K, de Vrij FMS, Verhoef LGGC, et al. Mutant ubiquitin found in neurodegenerative disorders is a ubiquitin fusion degradation substrate that blocks proteasomal degradation. J Cell Biol 2002;157:417–27
  • Ko S, Kang GB, Song SM, et al. Structural basis of E2-25K/UBB + 1 interaction leading to proteasome inhibition and neurotoxicity. J Biol Chem 2010;285:36070–80
  • de Pril R, Fischer DF, Roos RA, van Leeuwen FW. Ubiquitin-conjugating enzyme E2-25K increases aggregate formation and cell death in polyglutamine diseases. Mol Cell Neurosci 2007;34:10–19
  • Reyes-Turcu FE, Horton JR, Mullally JE, et al. The ubiquitin binding domain ZnFUBP recognizes the C-terminal diglycine motif of unanchored ubiquitin. Cell 2006;124:1197–208
  • Sokratous K, Roach LV, Channing D, et al. Probing affinity and ubiquitin linkage selectivity of ubiquitin-binding domains using mass spectrometry. J Am Chem Soc 2012;134:6416–24
  • Raasi S, Orlov I, Fleming KG, Pickart CM. Binding of polyubiquitin chains to ubiquitin-associated (UBA) domains of HHR23A. J Mol Biol 2004;341:1367–79
  • Raasi S, Varadan R, Fushman D, Pickart CM. Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat Struct Mol Biol 2005;12:708–14
  • Varadan R, Assfalg M, Raasi S, et al. Structural determinants for selective recognition of a lys48-linked polyubiquitin chain by a UBA domain. Mol Cell 2005;18:687–98
  • Castaneda CA, Kashyap TR, Nakasone MA, et al. Unique structural, dynamical, and functional properties of k11-linked polyubiquitin chains. Structure 2013;21:1168–81
  • Zhang D, Raasi S, Fushman D. Affinity makes the difference: nonselective interaction of the UBA domain of ubiquilin-1 with monomeric ubiquitin and polyubiquitin chains. J Mol Biol 2008;377:162–80
  • Hacker H, Karin M. Regulation and function of IKK and IKK-related kinases. Sci STKE 2006;2006:re13
  • Wu CJ, Conze DB, Li T, et al. Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation [corrected]. Nat Cell Biol 2006;8:398–406
  • Ea CK, Deng L, Xia ZP, et al. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell 2006;22:245–57
  • Bloor S, Ryzhakov G, Wagner S, et al. Signal processing by its coil zipper domain activates IKK gamma. Proc Natl Acad Sci USA 2008;105:1279–84
  • Wagner S, Carpentier I, Rogov V, et al. Ubiquitin binding mediates the NF-kappaB inhibitory potential of ABIN proteins. Oncogene 2008;27:3739–45
  • Lo YC, Lin SC, Rospigliosi CC, et al. Structural basis for recognition of diubiquitins by NEMO. Mol Cell 2009;33:602–15
  • Doffinger R, Smahi A, Bessia C, et al. X-linked anhidrotic ectodermal dysplasia with immunodeficiency is caused by impaired NF-kappaB signaling. Nat Genet 2001;27:277–85
  • Filipe-Santos O, Bustamante J, Haverkamp MH, et al. X-linked susceptibility to mycobacteria is caused by mutations in NEMO impairing CD40-dependent IL-12 production. J Exp Med 2006;203:1745–59
  • Song HY, Rothe M, Goeddel DV. The tumor necrosis factor-inducible zinc finger protein A20 interacts with TRAF1/TRAF2 and inhibits NF-kappaB activation. Proc Natl Acad Sci USA 1996;93:6721–5
  • Wang YY, Li L, Han KJ, et al. A20 is a potent inhibitor of TLR3- and Sendai virus-induced activation of NF-kappaB and ISRE and IFN-beta promoter. FEBS Lett 2004;576:86–90
  • Sarma V, Lin Z, Clark L, et al. Activation of the B-cell surface receptor CD40 induces A20, a novel zinc finger protein that inhibits apoptosis. J Biol Chem 1995;270:12343–6
  • Fries KL, Miller WE, Raab-Traub N. The A20 protein interacts with the Epstein–Barr virus latent membrane protein 1 (LMP1) and alters the LMP1/TRAF1/TRADD complex. Virology 1999;264:159–66
  • Graham RR, Cotsapas C, Davies L, et al. Genetic variants near TNFAIP3 on 6q23 are associated with systemic lupus erythematosus. Nat Genet 2008;40:1059–61
  • Musone SL, Taylor KE, Lu TT, et al. Multiple polymorphisms in the TNFAIP3 region are independently associated with systemic lupus erythematosus. Nat Genet 2008;40:1062–4
  • Hammer GE, Turer EE, Taylor KE, et al. Expression of A20 by dendritic cells preserves immune homeostasis and prevents colitis and spondyloarthritis. Nat Immunol 2011;12:1184–93
  • Vereecke L, Sze M, Mc Guire C, et al. Enterocyte-specific A20 deficiency sensitizes to tumor necrosis factor-induced toxicity and experimental colitis. J Exp Med 2010;207:1513–23
  • Matmati M, Jacques P, Maelfait J, et al. A20 (TNFAIP3) deficiency in myeloid cells triggers erosive polyarthritis resembling rheumatoid arthritis. Nat Genet 2011;43:908–12
  • Kool M, van Loo G, Waelput W, et al. The ubiquitin-editing protein A20 prevents dendritic cell activation, recognition of apoptotic cells, and systemic autoimmunity. Immunity 2011;35:82–96
  • Tavares RM, Turer EE, Liu CL, et al. The ubiquitin modifying enzyme A20 restricts B cell survival and prevents autoimmunity. Immunity 2010;33:181–91
  • Shembade N, Ma A, Harhaj EW. Inhibition of NF-kappaB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 2010;327:1135–9
  • Wertz IE, O’Rourke KM, Zhou H, et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004;430:694–9
  • Skaug B, Chen J, Du F, et al. Direct, noncatalytic mechanism of IKK inhibition by A20. Mol Cell 2011;44:559–71
  • Verhelst K, Carpentier I, Kreike M, et al. A20 inhibits LUBAC-mediated NF-κB activation by binding linear polyubiquitin chains via its zinc finger 7. EMBO J 2012;31:3845–55
  • Kato M, Sanada M, Kato I, et al. Frequent inactivation of A20 in B-cell lymphomas. Nature 2009;459:712–16
  • Schmitz R, Hansmann ML, Bohle V, et al. TNFAIP3 (A20) is a tumor suppressor gene in Hodgkin lymphoma and primary mediastinal B cell lymphoma. J Exp Med 2009;206:981–9
  • Hunter AM, LaCasse EC, Korneluk RG. The inhibitors of apoptosis (IAPs) as cancer targets. Apoptosis 2007;12:1543–68
  • Gyrd-Hansen M, Darding M, Miasari M, et al. IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-kappaB as well as cell survival and oncogenesis. Nat Cell Biol 2008;10:1309–17
  • Layfield R, Ciani B, Ralston SH, et al. Structural and functional studies of mutations affecting the UBA domain of SQSTM1 (p62) which cause Paget's disease of bone. Biochem Soc Trans 2004;32:728–30
  • Cavey JR, Ralston SH, Sheppard PW, et al. Loss of ubiquitin binding is a unifying mechanism by which mutations of SQSTM1 cause Paget's disease of bone. Calcif Tissue Int 2006;78:271–7
  • Visconti MR, Langston AL, Alonso N, et al. Mutations of SQSTM1 are associated with severity and clinical outcome in paget disease of bone. J Bone Miner Res 2010;25:2368–73
  • Michou L, Collet C, Laplanche JL, et al. Genetics of Paget’s disease of bone. Joint Bone Spine 2006;73:243–8
  • Garner TP, Long J, Layfield R, Searle MS. Impact of p62/SQSTM1 UBA domain mutations linked to Paget’s disease of bone on ubiquitin recognition. Biochemistry 2011;50:4665–74
  • Goode A, Layfield R. Recent advances in understanding the molecular basis of Paget disease of bone. J Clin Pathol 2010;63:199–203
  • Rea SL, Walsh JP, Layfield R, et al. New insights into the role of sequestosome 1/p62 mutant proteins in the pathogenesis of Paget's disease of bone. Endocr Rev 2013;34:501–24
  • Hoege C, Pfander B, Moldovan GL, et al. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 2002;419:135–41
  • Tomida J, Masuda Y, Hiroaki H, et al. DNA damage-induced ubiquitylation of RFC2 subunit of replication factor C complex. J Biol Chem 2008;283:9071–9
  • Bergink S, Salomons FA, Hoogstraten D, et al. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev 2006;20:1343–52
  • Smogorzewska A, Matsuoka S, Vinciguerra P, et al. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 2007;129:289–301
  • Hofmann K. Ubiquitin-binding domains and their role in the DNA damage response. DNA Repair (Amst) 2009;8:544–56
  • Kim H, Chen J, Yu X. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 2007;316:1202–5
  • Kolas NK, Chapman JR, Nakada S, et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 2007;318:1637–40
  • Mailand N, Bekker-Jensen S, Faustrup H, et al. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 2007;131:887–900
  • Huen MS, Grant R, Manke I, et al. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 2007;131:901–14
  • Doil C, Mailand N, Bekker-Jensen S, et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 2009;136:435–46
  • Pinato S, Scandiuzzi C, Arnaudo N, et al. RNF168, a new RING finger, MIU-containing protein that modifies chromatin by ubiquitination of histones H2A and H2AX. BMC Mol Biol 2009;10:55
  • Pinato S, Gatti M, Scandiuzzi C, et al. UMI, a novel RNF168 ubiquitin binding domain involved in the DNA damage signaling pathway. Mol Cell Biol 2011;31:118–26
  • Cao J, Yan Q. Histone ubiquitination and deubiquitination in transcription, DNA damage response, and cancer. Front Oncol 2012;2:26
  • Lehmann AR. DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie 2003;85:1101–11
  • Licht CL, Stevnsner T, Bohr VA. Cockayne syndrome group B cellular and biochemical functions. Am J Hum Genet 2003;73:1217–39
  • Hanawalt PC, Spivak G. Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol 2008;9:958–70
  • Anindya R, Mari P-O, Kristensen U, et al. A ubiquitin-binding domain in Cockayne syndrome B required for transcription-coupled nucleotide excision repair. Mol Cell 2010;38:637–48
  • Taniguchi T, D’Andrea AD. Molecular pathogenesis of Fanconi anemia: recent progress. Blood 2006;107:4223–33
  • Moldovan G-L, D’Andrea AD. How the Fanconi anemia pathway guards the genome. Annu Rev Genet 2009;43:223–49
  • Auerbach AD, Wolman SR. Susceptibility of Fanconi's anaemia fibroblasts to chromosome damage by carcinogens. Nature 1976;261:494–6
  • Garcia-Higuera I, Taniguchi T, Ganesan S, et al. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 2001;7:249–62
  • Sims AE, Spiteri E, Sims RJ, et al. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat Struct Mol Biol 2007;14:564–7
  • Taniguchi T, Garcia-Higuera I, Andreassen PR, et al. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 2002;100:2414–20
  • Wang X, Andreassen PR, D’Andrea AD. Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol Cell Biol 2004;24:5850–62
  • Cybulski KE, Howlett NG. FANCP/SLX4: a Swiss army knife of DNA interstrand crosslink repair. Cell Cycle 2011;10:1757–63
  • Kim Y, Lach FP, Desetty R, et al. Mutations of the SLX4 gene in Fanconi anemia. Nat Genet 2011;43:142–6
  • Kratz K, Schopf B, Kaden S, et al. Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 2010;142:77–88
  • MacKay C, Declais AC, Lundin C, et al. Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 2010;142:65–76
  • Smogorzewska A, Desetty R, Saito TT, et al. A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol Cell 2010;39:36–47
  • Stoepker C, Hain K, Schuster B, et al. SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat Genet 2011;43:138–41
  • Rego MA, Kolling FW, Vuono EA, et al. Regulation of the Fanconi anemia pathway by a CUE ubiquitin-binding domain in the FANCD2 protein. Blood 2012;120:2109–17
  • Hoeller D, Hecker CM, Dikic I. Ubiquitin and ubiquitin-like proteins in cancer pathogenesis. Nat Rev Cancer 2006;6:776–88
  • Nakayama KI, Nakayama K. Ubiquitin ligases: cell-cycle control and cancer. Nat Rev Cancer 2006;6:369–81
  • Bernassola F, Karin M, Ciechanover A, Melino G. The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell 2008;14:10–21
  • Satija YK, Bhardwaj A, Das S. A portrayal of E3 ubiquitin ligases and deubiquitylases in cancer. Int J Cancer 2013;133:2759–68
  • Sgorbissa A, Potu H, Brancolini C. Isopeptidases in anticancer therapy: looking for inhibitors. Am J Transl Res 2010;2:235–47
  • Nicholson B, Marblestone JG, Butt TR, Mattern MR. Deubiquitinating enzymes as novel anticancer targets. Future Oncol 2007;3:191–9
  • Bienko M, Green CM, Crosetto N, et al. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 2005;310:1821–4
  • Guo C, Tang TS, Bienko M, et al. Ubiquitin-binding motifs in REV1 protein are required for its role in the tolerance of DNA damage. Mol Cell Biol 2006;26:8892–900
  • Masutani C, Kusumoto R, Yamada A, et al. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature 1999;399:700–4
  • Johnson RE, Kondratick CM, Prakash S, Prakash L. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 1999;285:263–5
  • Adams J. The proteasome: a suitable antineoplastic target. Nat Rev Cancer 2004;4:349–60
  • Richardson PG, Barlogie B, Berenson J, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med 2003;348:2609–17
  • Groll M, Berkers CR, Ploegh HL, Ovaa H. Crystal structure of the boronic acid-based proteasome inhibitor bortezomib in complex with the yeast 20S proteasome. Structure 2006;14:451–6
  • Hoeller D, Dikic I. Targeting the ubiquitin system in cancer therapy. Nature 2009;458:438–44
  • 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
  • Chauhan D, Tian Z, Nicholson B, et al. A small molecule inhibitor of ubiquitin-specific protease-7 induces apoptosis in multiple myeloma cells and overcomes Bortezomib resistance. Cancer Cell 2012;22:345–58
  • Verma R, Peters NR, D’Onofrio M, et al. Ubistatins inhibit proteasome-dependent degradation by binding the ubiquitin chain. Science 2004;306:117–20
  • Husnjak K, Elsasser S, Zhang NX, et al. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 2008;453:481–8
  • Hayden MS, Ghosh S. Shared principles in NF-B signaling. Cell 2008;132:344–62
  • Perkins ND. Integrating cell-signalling pathways with NF-kappa B and IKK function. Nat Rev Mol Cell Biol 2007;8:49–62
  • Scheidereit C. I kappa B kinase complexes: gateways to NF-kappa B activation and transcription. Oncogene 2006;25:6685–705
  • Vallabhapurapu S, Karin M. Regulation and function of NF-κB transcription factors in the immune system. Annu Rev Immunol 2009;27:693–733
  • Chiaravalli J, Fontan E, Fsihi H, et al. Direct inhibition of NF-κB activation by peptide targeting the NOA ubiquitin binding domain of NEMO. Biochem Pharmacol 2011;82:1163–74
  • Cornilescu G, Marquardt JL, Ottiger M, Bax A. Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J Am Chem Soc 1998;120:6836–7
  • Alam SL, Sun J, Payne M, et al. Ubiquitin interactions of NZF zinc fingers. EMBO J 2004;23:1411–21

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.