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Review Article

The role of allostery in the ubiquitin–proteasome system

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Pages 89-97 | Received 29 Aug 2012, Accepted 19 Oct 2012, Published online: 13 Dec 2012

References

  • Balakirev MY, Tcherniuk SO, Jaquinod M, et al. (2003). Otubains: a new family of cysteine proteases in the ubiquitin pathway. EMBO Rep 4:517–22
  • Bech-Otschir D, Helfrich A, Enenkel C, et al. (2009). Polyubiquitin substrates allosterically activate their own degradation by the 26S proteasome. Nat Struct Mol Biol 16:219–25
  • Bernier-Villamor V, Sampson DA, Matunis MJ, et al. (2002). Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108:345–56
  • Brzovic PS, Lissounov A, Christensen DE, et al. (2006). A UbcH5/ubiquitin noncovalent complex is required for processive BRCA1-directed ubiquitination. Mol Cell 21:873–80
  • Capili AD, Lima CD. (2007). Taking it step by step: mechanistic insights from structural studies of ubiquitin/ubiquitin-like protein modification pathways. Curr Opin Struct Biol 17:726–35
  • Cavanaugh A, Huang Y, Breitwieser GE. (2012). Behind the curtain: cellular mechanisms for allosteric modulation of calcium-sensing receptors. Brit J Pharmacol 165:1670–7
  • Ceccarelli DF, Tang X, Pelletier B, et al. (2011). An allosteric inhibitor of the human Cdc34 ubiquitin-conjugating enzyme. Cell 145:1075–87
  • Ciechanover A, Brundin P. (2003). The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 40:427–46
  • Coccetti P, Tripodi F, Tedeschi G, et al. (2008). The CK2 phosphorylation of catalytic domain of Cdc34 modulates its activity at the G1 to S transition in Saccharomyces cerevisiae. Cell Cycle 7:1391–401
  • da Fonseca PC, Morris EP. (2008). Structure of the human 26S proteasome: subunit radial displacements open the gate into the proteolytic core. J Biol Chem 283:23305–14
  • Das R, Mariano J, Tsai YC, et al. (2009). Allosteric activation of E2-RING finger-mediated ubiquitylation by a structurally defined specific E2-binding region of gp78. Mol Cell 34:674–85
  • Dou H, Buetow L, Hock A, et al. (2012a). Structural basis for autoinhibition and phosphorylation-dependent activation of c-Cbl. Nat Struct Mol Biol 19:184–92
  • Dou H, Buetow L, Sibbet GJ, et al. (2012b). BIRC7-E2 ubiquitin conjugate structure reveals the mechanism of ubiquitin transfer by a RING dimer. Nat Struct Mol Biol 19:876–83
  • Duda DM, Borg LA, Scott DC, et al. (2008). Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 134:995–1006
  • Duda DM, Scott DC, Calabrese MF, et al. (2011). Structural regulation of cullin-RING ubiquitin ligase complexes. Curr Opin Struct Biol 21:257–64
  • Dupre S, Haguenauer-Tsapis R. (2001). Deubiquitination step in the endocytic pathway of yeast plasma membrane proteins: crucial role of Doa4p ubiquitin isopeptidase. Mol Cellular Biol 21:4482–94
  • Fisk HA, Yaffe MP. (1999). A role for ubiquitination in mitochondrial inheritance in Saccharomyces cerevisiae. J Cell Biol 145:1199–208
  • Gaczynska M, Osmulski PA. (2011). Atomic force microscopy of proteasome assemblies. Methods Mol Biol 736:117–32
  • Gaczynska M, Osmulski PA, Gao Y, et al. (2003). Proline- and arginine-rich peptides constitute a novel class of allosteric inhibitors of proteasome activity. Biochemistry 42:8663–70
  • Goodey NM, Benkovic SJ. (2008). Allosteric regulation and catalysis emerge via a common route. Nat Chem Biol 4:474–82
  • Gunasekaran K, Ma B, Nussinov R. (2004). Is allostery an intrinsic property of all dynamic proteins? Proteins 57:433–43.
  • Herrmann J, Ciechanover A, Lerman LO, et al. (2004). The ubiquitin–proteasome system in cardiovascular diseases – a hypothesis extended. Cardiovasc Res 61:11–21
  • Hershko A. (2005). Early work on the ubiquitin proteasome system, an interview with Avram Hershko. Interview by CDD. Cell Death Differ 12:1158–61
  • Hofmann RM, Pickart CM. (1999). Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96:645–53
  • Huang DT, Hunt HW, Zhuang M, et al. (2007). Basis for a ubiquitin-like protein thioester switch toggling E1–E2 affinity. Nature 445:394–8
  • Huang DT, Paydar A, Zhuang M, et al. (2005). Structural basis for recruitment of Ubc12 by an E2 binding domain in NEDD8's E1. Mol Cell 17:341–50
  • Jackson S, Xiong Y. (2009). CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem Sci 34:562–70
  • Kar G, Keskin O, Gursoy A, Nussinov R. (2010). Allostery and population shift in drug discovery. Curr Opin Pharmacol 10:715–22
  • Karaca E, Tozluoglu M, Nussinov R, Haliloglu T. (2011). Alternative allosteric mechanisms can regulate the substrate and E2 in SUMO conjugation. J. Mol Biol 406:620–30
  • Karagoz GE, Duarte AM, Ippel H, et al. (2011). N-terminal domain of human Hsp90 triggers binding to the cochaperone p23. Proc Natl Acad Sci USA 108:580–5
  • Kenakin TP. (2012). Biased signalling and allosteric machines: new vistas and challenges for drug discovery. Brit J Pharmacol 165:1659–69
  • Klinger PP, Schubert U. (2005). The ubiquitin–proteasome system in HIV replication: potential targets for antiretroviral therapy. Expert Rev Anti-infective Therapy 3:61–79
  • Komander D, Clague MJ, Urbe S. (2009). Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10:550–63
  • Kumar S, Ma B, Tsai, CJ, et al. (2000). Folding and binding cascades: dynamic landscapes and population shifts. Protein Sci: Publ Protein Soc 9:10–19
  • Lamothe B, Besse A, Campos AD, et al. (2007). Site-specific Lys-63-linked tumor necrosis factor receptor-associated factor 6 auto-ubiquitination is a critical determinant of I kappa B kinase activation. J Biol Chem 282:4102–12
  • Lander GC, Estrin E, Matyskiela ME, et al. (2012). Complete subunit architecture of the proteasome regulatory particle. Nature 482:186–91
  • Lasker K, Forster F, Bohn S, et al. (2012). Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc Natl Acad Sci USA 109:380–7
  • Leonard TA, Hurley JH. (2011). Regulation of protein kinases by lipids. Curr Opin Struct Biol 21:785–91
  • Li J, Post M, Volk R, et al. (2000). PR39, a peptide regulator of angiogenesis. Nat Med 6:49–55
  • Li W, Tu D, Li L, et al. (2009). Mechanistic insights into active site-associated polyubiquitination by the ubiquitin-conjugating enzyme Ube2g2. Proc Natl Acad Sci USA 106:3722–7
  • Liu J, Nussinov R. (2008). Allosteric effects in the marginally stable von Hippel-Lindau tumor suppressor protein and allostery-based rescue mutant design. Proc Natl Acad Sci USA 105:901–6
  • Liu J, Nussinov R. (2009). The mechanism of ubiquitination in the cullin-RING E3 ligase machinery: conformational control of substrate orientation. PLoS Comput Biol 5:e1000527
  • Liu J, Nussinov R. (2010a). Molecular dynamics reveal the essential role of linker motions in the function of cullin-RING E3 ligases. J Mol Biol 396:1508–23
  • Liu J, Nussinov R. (2010b). Rbx1 flexible linker facilitates cullin-RING ligase function before neddylation and after deneddylation. Biophys J 99:736–44
  • Liu J, Nussinov R. (2011). Flexible cullins in cullin-RING E3 ligases allosterically regulate ubiquitination. J Biol Chem 286:40934–42
  • Lyumkis D, Doamekpor SK, Mario H, et al. (2013). Single-particle electron microscopy reveals extensive conformational variability of the Ltn1 E3 ligase, submitted
  • Ma B, Kumar S, Tsai CJ, et al. (1999). Folding funnels and binding mechanisms. Protein Eng 12:713–20
  • Ma B, Tsai CJ, Haliloglu T, et al. (2011). Dynamic allostery: linkers are not merely flexible. Structure 19:907–17
  • Mani A, Gelmann EP. (2005). The ubiquitin–proteasome pathway and its role in cancer. J Clin Oncol: OJ Amer Soc Clin Oncol 23:4776–89
  • Mao X, Li X, Sprangers R, et al. (2009). Clioquinol inhibits the proteasome and displays preclinical activity in leukemia and myeloma. Leukemia: OJ Leukemia Soc Amer Leukemia Res Fund UK 23:585–90
  • Nalepa G, Rolfe M, Harper JW. (2006). Drug discovery in the ubiquitin–proteasome system. Nat Rev Drug Discov 5:596–613
  • Nussinov R, Tsai CJ, Csermely P. (2011). Allo-network drugs: harnessing allostery in cellular networks. Trends Pharmacol Sci 32:686–93
  • Nussinov R, Tsai CJ, Xin F, et al. (2012). Allosteric post-translational modification codes. Trends Biochem Sci 37:447–55
  • Ogunjimi AA, Briant DJ, Pece-Barbara N, et al. (2005). Regulation of Smurf2 ubiquitin ligase activity by anchoring the E2 to the HECT domain. Mol Cell 19:297–308
  • Orlicky S, Tang X, Neduva V, et al. (2010). An allosteric inhibitor of substrate recognition by the SCF(Cdc4) ubiquitin ligase. Nat Biotechnol 28:733–7
  • Ozkan E, Yu H, Deisenhofer J. (2005). Mechanistic insight into the allosteric activation of a ubiquitin-conjugating enzyme by RING-type ubiquitin ligases. Proc Natl Acad Sci USA 102:18890–5
  • Pan Y, Tsai CJ, Ma B, et al. (2010). Mechanisms of transcription factor selectivity. Trends Genet 26:75–83
  • Papaleo E, Casiraghi N, Arrigoni A, et al. (2012). Loop 7 of e2 enzymes: an ancestral conserved functional motif involved in the e2-mediated steps of the ubiquitination cascade. PloS One 7:e40786
  • Papaleo E, Ranzani V, Tripodi F, et al. (2011). An acidic loop and cognate phosphorylation sites define a molecular switch that modulates ubiquitin charging activity in Cdc34-like enzymes. PLoS Comput Biol 7:e1002056
  • Pathare GR, Nagy I, Bohn S, et al. (2012). The proteasomal subunit Rpn6 is a molecular clamp holding the core and regulatory subcomplexes together. Proc Natl Acad Sci USA 109:149–54
  • Paul S. (2008). Dysfunction of the ubiquitin-proteasome system in multiple disease conditions: therapeutic approaches. BioEssays: News Rev Mol Cellular Dev Biol 30:1172–84
  • Pickart CM. (2000). Ubiquitin biology: an old dog learns an old trick. Nat Cell Biol i2:E139–41
  • Pruneda JN, Littlefield PJ, Soss SE, et al. (2012). Structure of an E3:E2 approximately Ub complex reveals an allosteric mechanism shared among RING/U-box ligases. Mol Cell 47:933–42
  • Reverter D, Lima CD. (2005). Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 435:687–92
  • Rual JF, Venkatesan K, Hao T, et al. (2005). Towards a proteome-scale map of the human protein-protein interaction network. Nature 437:1173–8
  • Ruschak AM, Slassi M, Kay LE, et al. (2011). Novel proteasome inhibitors to overcome bortezomib resistance. J Natl Cancer Inst 103:1007–17
  • Sanjo H, Zajonc DM, Braden R, et al. (2010). Allosteric regulation of the ubiquitin:NIK and ubiquitin:TRAF3 E3 ligases by the lymphotoxin-beta receptor. J Biol Chem 285:17148–55
  • Schulman BA, Harper JW. (2009). Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat Rev Mol Cell Biol 10:319–31
  • Souphron J, Waddell MB, Paydar A, et al. (2008). Structural dissection of a gating mechanism preventing misactivation of ubiquitin by NEDD8's E1. Biochemistry 47:8961–9
  • Spence J, Gali RR, Dittmar G, et al. (2000). Cell cycle-regulated modification of the ribosome by a variant multiubiquitin chain. Cell 102:67–76
  • Sprangers R, Li X, Mao X, et al. (2008). TROSY-based NMR evidence for a novel class of 20S proteasome inhibitors. Biochemistry 47:6727–34
  • Tatham MH, Kim S, Jaffray E, et al. (2005). Unique binding interactions among Ubc9, SUMO and RanBP2 reveal a mechanism for SUMO paralog selection. Nat Struct Mol Biol 12:67–74
  • Tozluoglu M, Karaca E, Nussinov R, et al. (2010). A mechanistic view of the role of E3 in sumoylation. PLoS Comput Biol 6:e1000913
  • Truong K, Su Y, Song J, Chen Y. (2011). Entropy-driven mechanism of an E3 ligase. Biochemistry 50:5757–66
  • Tsai CJ, Del Sol A, Nussinov R. (2009). Protein allostery, signal transmission and dynamics: a classification scheme of allosteric mechanisms. Mol Biosyst 5:207–16
  • Tsai CJ, Kumar S, Ma B, et al. (1999a). Folding funnels, binding funnels, and protein function. Protein Sci: Publ Protein Soc 8:1181–90
  • Tsai CJ, Ma B, Nussinov R. (1999b). Folding and binding cascades: shifts in energy landscapes. Proc Natl Acad Sci USA 96:9970–2
  • Tsai CJ, Nussinov R. (2011). Gene-specific transcription activation via long-range allosteric shape-shifting. Biochem J 439:15–25
  • Turner GC, Du F, Varshavsky A. (2000). Peptides accelerate their uptake by activating a ubiquitin-dependent proteolytic pathway. Nature 405:579–83
  • Ulrich HD, Jentsch S. (2000). Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J 19:3388–97
  • Varshavsky A. (2011). The N-end rule pathway and regulation by proteolysis. Protein Sci: Publ Protein Soc 20:1298–1345
  • Wang J, Maldonado MA. (2006). The ubiquitin–proteasome system and its role in inflammatory and autoimmune diseases. Cell Mol Immunol 3:255–61
  • Wang J, Schulman BA. (2009). (G2)BRinging an E2 to E3. Structure 17:916–7
  • Wenzel DM, Klevit RE. (2012). Following Ariadne's thread: a new perspective on RBR ubiquitin ligases. BMC Biol 10:24
  • Wiener R, Zhang X, Wang T. (2012). The mechanism of OTUB1-mediated inhibition of ubiquitination. Nature 483:618–22
  • Wood MR, Hopkins CR, Brogan JT, et al. (2011). “Molecular switches” on mGluR allosteric ligands that modulate modes of pharmacology. Biochemistry 50:2403–10
  • Xie Y, Varshavsky A. (1999). The E2–E3 interaction in the N-end rule pathway: the RING-H2 finger of E3 is required for the synthesis of multiubiquitin chain. EMBO J 18:6832–44
  • Yang Y, Kitagaki J, Wang H, et al. (2009). Targeting the ubiquitin-proteasome system for cancer therapy. Cancer Sci 100:24–8
  • Zheng N, Schulman BA, Song L, et al. (2002). Structure of the Cul1–Rbx1–Skp1–F boxSkp2 SCF ubiquitin ligase complex. Nature 416:703–9

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