The devil is in the details: comparison between COP9 signalosome (CSN) and the LID of the 26S proteasome
Tóm tắt
The COP9 signalosome (CSN) and the proteasomal LID are conserved macromolecular complexes composed of at least eight subunits with molecular weights of approximately 350 kDa. CSN and LID are part of the ubiquitin–proteasome pathway and cleave isopeptide linkages of lysine side chains on target proteins. CSN cleaves the isopeptide bond of ubiquitin-like protein Nedd8 from cullins, whereas the LID cleaves ubiquitin from target proteins sentenced for degradation. CSN and LID are structurally and functionally similar but the order of the assembly pathway seems to be different. The assembly differs in at least the last subunit joining the pre-assembled subcomplex. This review addresses the similarities and differences in structure, function and assembly of CSN and LID.
Tài liệu tham khảo
Axelrod DE, Gealt M, Pastushok M (1973) Gene control of developmental competence in Aspergillus nidulans. Dev Biol 34:9–15. doi:10.1016/0012-1606(73)90335-7
Beausoleil SA, Villén J, Gerber SA, Rush J, Gygi SP (2006) A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 24:1285–1292. doi:10.1038/nbt1240
Beck F, Unverdorben P, Bohn S, Schweitzer A, Pfeifer G, Sakata E, Nickell S, Plitzko JM, Villa E, Baumeister W, Förster F (2012) Near-atomic resolution structural model of the yeast 26S proteasome. Proc Natl Acad Sci USA 109:14870–14875. doi:10.1073/pnas.1213333109
Beckmann EA, Köhler AM, Meister C, Christmann M, Draht OW, Rakebrandt N, Valerius O, Braus GH (2015) Integration of the catalytic subunit activates deneddylase activity in vivo as final step in fungal COP9 signalosome assembly. Mol Microbiol 97:110–124. doi:10.1111/mmi.13017
Birol M, Enchev RI, Padilla A, Stengel F, Aebersold R, Betzi S, Yang Y, Hoh F, Peter M, Dumas C, Echalier A (2014) Structural and biochemical characterization of the Cop9 signalosome CSN5/CSN6 heterodimer. PLoS ONE 9:e105688. doi:10.1371/journal.pone.0105688
Bosu DR, Kipreos ET (2008) Cullin-RING ubiquitin ligases: global regulation and activation cycles. Cell Div 3. doi:10.1186/1747-1028-3-7
Braga GU, Rangel DE, Fernandes ÉK, Flint SD, Roberts DW (2015) Molecular and physiological effects of environmental UV radiation on fungal conidia. Curr Genet 61:405–425. doi:10.1007/s00294-015-0483-0
Braus GH, Irniger S, Bayram Ö (2010) Fungal development and the COP9 signalosome. Curr Opin Microbiol 13:672–676. doi:10.1016/j.mib.2010.09.011
Busch S, Eckert SE, Krappmann S, Braus GH (2003) The COP9 signalosome is an essential regulator of development in the filamentous fungus Aspergillus nidulans. Mol Microbiol 49:717–730. doi:10.1046/j.1365-2958.2003.03612.x
Busch S, Schwier EU, Nahlik K, Bayram Ö, Helmstaedt K, Draht OW, Krappmann S, Valerius O, Lipscomb WN, Braus GH (2007) An eight-subunit COP9 signalosome with an intact JAMM motif is required for fungal fruit body formation. Proc Natl Acad Sci USA 104:8089–8094. doi:10.1073/pnas.0702108104
Chamovitz DA (2009) Revisiting the COP9 signalosome as a transcriptional regulator. EMBO Rep 10:352–358. doi:10.1038/embor.2009.33
Chan Y, Yoon J, Wu JT, Kim HJ, Pan KT, Yim J, Chien CT (2008) DEN1 deneddylates non-cullin proteins in vivo. J Cell Sci 121:3218–3223. doi:10.1242/jcs.030445
Christmann M, Schmaler T, Gordon C, Huang X, Bayram Ö, Schinke J, Stumpf S, Dubiel W, Braus GH (2013) Control of multicellular development by the physically interacting deneddylases DEN1/DenA and COP9 signalosome. PLoS Genet. doi:10.1371/journal.pgen.1003275
Ciechanover A (1998) The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J 17:7151–7160. doi:10.1093/emboj/17.24.7151
Cope GA, Suh GS, Aravind L, Schwarz SE, Zipursky SL, Koonin EV, Deshaies RJ (2002) Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science 298:608–611. doi:10.1126/science.1075901
da Fonseca PC, He J, Morris EP (2012) Molecular model of the human 26S proteasome. Mol Cell 46:54–66. doi:10.1016/j.molcel.2012.03.026
Davy A, Bello P, Thierry-Mieg N, Vaglio P, Hitti J, Doucette-Stamm L, Thierry-Mieg D, Reboul J, Boulton S, Walhout AJ, Coux O, Vidal M (2001) A protein-protein interaction map of the Caenorhabditis elegans 26S proteasome. EMBO Rep 2:821–828. doi:10.1093/embo-reports/kve184
Deng XW, Dubiel W, Wei N, Hofmann K, Mundt K, Colicelli J, Kato J, Naumann M, Segal D, Seeger M, Carr A, Glickman M, Chamovitz DA (2000) Unified nomenclature for the COP9 signalosome and its subunits: an essential regulator of development. Trends Genet 16:202–203. doi:10.1016/S0168-9525(00)01982-X
Deshaies RJ (2014) Structural biology: corralling a protein-degradation regulator. Nature 512:145–146. doi:10.1038/nature13644
Dessau M, Halimi Y, Erez T, Chomsky-Hecht O, Chamovitz DA, Hirsch JA (2008) The Arabidopsis COP9 signalosome subunit 7 is a model PCI domain protein with subdomains involved in COP9 signalosome assembly. Plant Cell 20:2815–2834. doi:10.1105/tpc.107.053801
Echalier A, Pan Y, Birol M, Tavernier N, Pintard L, Hoh F, Ebel C, Galophe N, Claret FX, Dumas C (2013) Insights into the regulation of the human COP9 signalosome catalytic subunit, CSN5/Jab1. Proc Natl Acad Sci USA 110:1273–1278. doi:10.1073/pnas.1209345110
Ellisdon AM, Stewart M (2012) Structural biology of the PCI-protein fold. Bioarchitecture 2:118–123. doi:10.4161/bioa.21131
Enchev RI, Scott DC, da Fonseca PC, Schreiber A, Monda JK, Schulman BA, Peter M, Morris EP (2012) Structural basis for a reciprocal regulation between SCF and CSN. Cell Rep 2:616–627. doi:10.1016/j.celrep.2012.08.019
Estrin E, Lopez-Blanco JR, Chacón P, Martin A (2013) Formation of an intricate helical bundle dictates the assembly of the 26S proteasome lid. Structure 21:1624–1635. doi:10.1016/j.str.2013.06.023
Fang L, Wang X, Yamoah K, Chen PL, Pan ZQ, Huang L (2008) Characterization of the human COP9 signalosome complex using affinity purification and mass spectrometry. J Proteome Res 7:4914–4925. doi:10.1021/pr800574c
Fu H, Reis N, Lee Y, Glickman MH, Vierstra RD (2001) Subunit interaction maps for the regulatory particle of the 26S proteasome and the COP9 signalosome. EMBO J 20:7096–7107. doi:10.1093/emboj/20.24.7096
Fukunaga K, Kudo T, Toh-e A, Tanaka K, Saeki Y (2010) Dissection of the assembly pathway of the proteasome lid in Saccharomyces cerevisiae. Biochem Biophys Res Commun 396:1048–1053. doi:10.1016/j.bbrc.2010.05.061
Füzesi-Levi MG, Ben-Nissan G, Bianchi E, Zhou H, Deery MJ, Lilley KS, Levin Y, Sharon M (2014) Dynamic regulation of the COP9 signalosome in response to DNA damage. Mol Cell Biol 34:1066–1076. doi:10.1128/MCB.01598-13
Gerke J, Braus GH (2014) Manipulation of fungal development as source of novel secondary metabolites for biotechnology. Appl Microbiol Biotechnol 98:8443–8455. doi:10.1007/s00253-014-5997-8
Glickman MH, Rubin DM, Coux O, Wefes I, Pfeifer G, Cjeka Z, Baumeister W, Fried VA, Finley D (1998) A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94:615–623. doi:10.1016/S0092-8674(00)81603-7
Gusmaroli G, Figueroa P, Serino G, Deng XW (2007) Role of the MPN subunits in COP9 signalosome assembly and activity, and their regulatory interaction with Arabidopsis Cullin3-based E3 ligases. Plant Cell 19:564–581. doi:10.1105/tpc.106.047571
He Q, Cheng P, He Q, Liu Y (2005) The COP9 signalosome regulates the Neurospora circadian clock by controlling the stability of the SCFFWD-1 complex. Genes Dev 19:1518–1531. doi:10.1101/gad.1322205
Helmstaedt K, Schwier EU, Christmann M, Nahlik K, Westermann M, Harting R, Grond S, Busch S, Braus GH (2011) Recruitment of the inhibitor Cand1 to the cullin substrate adaptor site mediates interaction to the neddylation site. Mol Biol Cell 22:153–164. doi:10.1091/mbc.E10-08-0732
Horák J (2013) Regulations of sugar transporters: insights from yeast. Curr Genet 59:1–31. doi:10.1007/s00294-013-0388-8
Hotton SK, Callis J (2008) Regulation of cullin RING ligases. Annu Rev Plant Biol 59:467–489. doi:10.1146/annurev.arplant.58.032806.104011
Isono E, Saeki Y, Yokosawa H, Toh-e A (2004) Rpn7 Is required for the structural integrity of the 26 S proteasome of Saccharomyces cerevisiae. J Biol Chem 279:27168–27176. doi:10.1074/jbc.M314231200
Isono E, Saito N, Kamata N, Saeki Y, Toh-E A (2005) Functional analysis of Rpn6p, a lid component of the 26 S proteasome, using temperature-sensitive rpn6 mutants of the yeast Saccharomyces cerevisiae. J Biol Chem 280:6537–6547. doi:10.1074/jbc.M409364200
Isono E, Nishihara K, Saeki Y, Yashiroda H, Kamata N, Ge L, Ueda T, Kikuchi Y, Tanaka K, Nakano A, Toh-e A (2007) The assembly pathway of the 19S regulatory particle of the yeast 26S proteasome. Mol Biol Cell 18:569–580. doi:10.1091/mbc.E06-07-0635
Jesenberger V, Jentsch S (2002) Deadly encounter: ubiquitin meets apoptosis. Nat Rev Mol Cell Biol 3:112–121. doi:10.1038/nrm731
Kapelari B, Bech-Otschir D, Hegerl R, Schade R, Dumdey R, Dubiel W (2000) Electron microscopy and subunit-subunit interaction studies reveal a first architecture of COP9 signalosome. J Mol Biol 300:1169–1178. doi:10.1006/jmbi.2000.3912
Kato JY, Yoneda-Kato N (2009) Mammalian COP9 signalosome. Genes Cells 14:1209–1225. doi:10.1111/j.1365-2443.2009.01349.x
Kotiguda GG, Weinberg D, Dessau M, Salvi C, Serino G, Chamovitz DA, Hirsch JA (2012) The organization of a CSN5-containing subcomplex of the COP9 signalosome. J Biol Chem 287:42031–42041. doi:10.1074/jbc.M112.387977
Lammer D, Mathias N, Laplaza JM, Jiang W, Liu Y, Callis J, Goebl M, Estelle M (1998) Modification of yeast Cdc53p by the ubiquitin-related protein rub1p affects function of the SCFCdc4 complex. Genes Dev 12:914–926
Lander GC, Estrin E, Matyskiela ME, Bashore C, Nogales E, Martin A (2012) Complete subunit architecture of the proteasome regulatory particle. Nature 482:186–191. doi:10.1038/nature10774
Lasker K, Förster F, Bohn S, Walzthoeni T, Villa E, Unverdorben P, Beck F, Aebersold R, Sali A, Baumeister W (2012) Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc Natl Acad Sci U S A 109:1380–1387. doi:10.1073/pnas.1120559109
Leppert U, Henke W, Huang X, Müller JM, Dubiel W (2011) Post-transcriptional fine-tuning of COP9 signalosome subunit biosynthesis is regulated by the c-Myc/Lin28B/let-7 pathway. J Mol Biol 409:710–721. doi:10.1016/j.jmb.2011.04.041
Lingaraju GM, Bunker R, Cavadini S, Hess D, Hassiepen U, Renatus M, Fischer ES, Thomä NH (2014) Crystal structure of the human COP9 signalosome. Nature 512:161–165. doi:10.1038/nature13566
Mundt KE, Liu C, Carr AM (2002) Deletion mutants in COP9/signalosome subunits in fission yeast Schizosaccharomyces pombe display distinct phenotypes. Mol Biol Cell 13:493–502. doi:10.1091/mbc.01-10-0521
Pan ZQ, Kentsis A, Dias DC, Yamoah K, Wu K (2004) Nedd8 on cullin: building an expressway to protein destruction. Oncogene 23:1985–1997. doi:10.1038/sj.onc.1207414
Pathare GR, Nagy I, Śledź P, Anderson DJ, Zhou HJ, Pardon E, Steyaert J, Förster F, Bracher A, Baumeister W (2014) Crystal structure of the proteasomal deubiquitylation module Rpn8-Rpn11. Proc Natl Acad Sci USA 111:2984–2989. doi:10.1073/pnas.1400546111
Peth A, Berndt C, Henke W, Dubiel W (2007) Downregulation of COP9 signalosome subunits differentially affects the CSN complex and target protein stability. BMC Biochem 8. doi:10.1186/1471-2091-8-27
Pick E, Pintard L (2009) In the land of the rising sun with the COP9 signalosome and related zomes. Symposium on the COP9 signalosome, proteasome and eIF3. EMBO Rep 10:343–348. doi:10.1038/embor.2009.27
Pick E, Hofmann K, Glickman MH (2009) PCI Complexes: beyond the Proteasome, CSN, and eIF3 Troika. Mol Cell 35:260–264. doi:10.1016/j.molcel2009.07.009
Pick E, Golan A, Zimbler JZ, Guo L, Sharaby Y, Tsuge T, Hofmann K, Wei N (2012) The minimal deneddylase core of the COP9 signalosome excludes the Csn6 MPN- domain. PLoS One 7:e43980. doi:10.1371/journal.pone.0043980
Röhrig J, Kastner C, Fischer R (2013) Light inhibits spore germination through phytochrome in Aspergillus nidulans. Curr Genet 59:55–62. doi:10.1007/s00294-013-0387-9
Scheel H, Hofmann K (2005) Prediction of a common structural scaffold for proteasome lid, COP9-signalosome and eIF3 complexes. BMC Bioinformatics 6:71. doi:10.1186/1471-2105-6-71
Schreiner P, Chen X, Husnjak K, Randles L, Zhang N, Elsasser S, Finley D, Dikic I, Walters KJ, Groll M (2008) Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 453:548–552. doi:10.1038/nature06924
Seeger M, Kraft R, Ferrell K, Bech-Otschir D, Dumdey R, Schade R, Gordon C, Naumann M, Dubiel W (1998) A novel protein complex involved in signal transduction possessing similarities to 26S proteasome subunits. FASEB J 12:469–478. doi:10.1096/fj.1530-6860
Sharon M, Taverner T, Ambroggio XI, Deshaies RJ, Robinson CV (2006) Structural organization of the 19S proteasome lid: insights from MS of intact complexes. PLoS Biol 4:e267. doi:10.1371/journal.pbio.0040267
Sharon M, Mao H, Boeri Erba E, Stephens E, Zheng N, Robinson CV (2009) Symmetrical modularity of the COP9 signalosome complex suggests its multifunctionality. Structure 17:31–40. doi:10.1016/j.str.2008.10.012
Siergiejuk E, Scott DC, Schulman BA, Hofmann K, Kurz T, Peter M (2009) Cullin neddylation and substrate-adaptors counteract SCF inhibition by the CAND1-like protein Lag2 in Saccharomyces cerevisiae. EMBO J 28:3845–3856. doi:10.1038/emboj.2009.354
Spasser L, Brik A (2012) Chemistry and biology of the ubiquitin signal. Angew Chem Int Ed Engl 51:6840–6862. doi:10.1002/anie.201200020
Sun Y, Wilson MP, Majerus PW (2002) Inositol 1,3,4-trisphosphate 5/6-kinase associates with the COP9 signalosome by binding to CSN1. J Biol Chem 277:45759–45764. doi:10.1074/jbc.M208709200
Teichmann M, Dumay-Odelot H, Fribourg S (2012) Structural and functional aspects of winged-helix domains at the core of transcription initiation complexes. Transcription 3:2–7. doi:10.4161/trns.3.1.18917
Tomko RJ Jr, Hochstrasser M (2013) Molecular architecture and assembly of the eukaryotic proteasome. Annu Rev Biochem 82:415–445. doi:10.1146/annurev-biochem-060410-150257
Tomko RJ Jr, Hochstrasser M (2014) The intrinsically disordered Sem1 protein functions as a molecular tether during proteasome Lid biogenesis. Mol Cell 53:433–443. doi:10.1016/j.molcel.2013.12.009
Tsuge T, Matsui M, Wei N (2001) The subunit 1 of the COP9 signalosome suppresses gene expression through its N-terminal domain and incorporates into the complex through the PCI domain. J Mol Biol 305:1–9. doi:10.1006/jmbi.2000.4288
Uhle S, Medalia O, Waldron R, Dumdey R, Henklein P, Bech-Otschir D, Huang X, Berse M, Sperling J, Schade R, Dubiel W (2003) Protein kinase CK2 and protein kinase D are associated with the COP9 signalosome. EMBO J 22:1302–1312. doi:10.1093/emboj/cdg127
Verma R, Aravind L, Oania R, McDonald WH, Yates JR 3rd, Koonin EV, Deshaies RJ (2002) Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298:611–615. doi:10.1126/science.1075898
Wang Y, Devereux W, Stewart TM, Casero RA Jr (2002) Polyamine-modulated factor 1 binds to the human homologue of the 7a subunit of the Arabidopsis COP9 signalosome: implications in gene expression. Biochem J 366:79–86. doi:10.1042/BJ20020211
Wang X, Chen CF, Baker PR, Chen PL, Kaiser P, Huang L (2007) Mass spectrometric characterization of the affinity-purified human 26S proteasome complex. Biochemistry 46:3553–3565. doi:10.1021/bi061994u
Wauer T, Komander D (2014) The JAMM in the proteasome. Nat Struct Mol Biol 21:346–348. doi:10.1038/nsmb.2800
Wee S, Hetfeld B, Dubiel W, Wolf DA (2002) Conservation of the COP9/signalosome in budding yeast. BMC Genet. doi:10.1186/1471-2156-3-15
Wei N, Deng XW (2003) The COP9 signalosome. Annu Rev Cell Dev Biol 19:261–286. doi:10.1146/annurev.cellbio.19.111301.112449
Wei N, Serino G, Deng XW (2008) The COP9 signalosome: more than a protease. Trends Biochem Sci 33:592–600. doi:10.1016/j.tibs.2008.09.004
Worden EJ, Padovani C, Martin A (2014) Structure of the Rpn11-Rpn8 dimer reveals mechanisms of substrate deubiquitination during proteasomal degradation. Nat Struct Mol Biol 21:220–227. doi:10.1038/nsmb.2771
Wu K, Yamoah K, Dolios G, Gan-Erdene T, Tan P, Chen A, Lee CG, Wei N, Wilkinson KD, Wang R, Pan ZQ (2003) DEN1 is a dual function protease capable of processing the C terminus of Nedd8 and deconjugating hyper-neddylated CUL1. J Biol Chem 278:28882–28891. doi:10.1074/jbc.M302888200
Yoshida A, Yoneda-Kato N, Kato JY (2013) CSN5 specifically interacts with CDK2 and controls senescence in a cytoplasmic cyclin E-mediated manner. Sci Rep 3:1054. doi:10.1038/srep01054
Yu Z, Kleifeld O, Lande-Atir A, Bsoul M, Kleiman M, Krutauz D, Book A, Vierstra RD, Hofmann K, Reis N, Glickman MH, Pick E (2011) Dual function of Rpn5 in two PCI complexes, the 26S proteasome and COP9 signalosome. Mol Biol Cell 22:911–920. doi:10.1091/mbc.E10-08-0655