Dual function of Rpn5 in two PCI complexes, the 26S proteasome and COP9 signalosome

Molecular Biology of the Cell

Volumn 22, Issue 7, 2011, Pages 911-920

  Yu, Zanlin ^a   Kleifeld, Oded ^a   Lande Atir, Avigail ^a   Bsoul, Maisa ^b   Kleiman, Maya ^a   Krutauz, Daria ^a   Book, Adam ^c   Vierstra, Richard D ^c   Hofmann, Kay ^d   Reis, Noa ^a   Glickman, Michael H ^a   Pick, Elah ^b  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b UNIVERSITY OF HAIFA   (Israel)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d MILTENYI BIOTEC GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

26S PROTEASOME; COP9 SIGNALOSOME; CULLIN; NEDD8 PROTEIN; PROTEASOME; PROTEIN RPN5; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; ENZYME SUBUNIT; HYDROLYSIS; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE;

CULLIN PROTEINS; MOLECULAR WEIGHT; MULTIPROTEIN COMPLEXES; PEPTIDE HYDROLASES; PHENOTYPE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; PROTISTA; SACCHAROMYCES CEREVISIAE;

EID: 79953307883     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-08-0655     Document Type: Article

References (74)

1. Ambroggio XI, Rees DC, Deshaies RJ, JAMM: A metalloprotease-like zinc site in the proteasome and signalosome. PLoS Biol (2004). 2, e2.
2. Aravind L, Watanabe H, Lipman DJ, Koonin EV (2000). Lineage-specific loss and divergence of functionally linked genes in eukaryotes. Proc Natl Acad Sci USA 97, 11319-11324.
3. Baillat D, Hakimi MA, Naar AM, Shilatifard A, Cooch N, Shiekhattar R (2005). Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II. Cell 123, 265-276. (Pubitemid 41457216)
4. Bailly E, Reed SI (1999). Functional characterization of rpn3 uncovers a distinct 19S proteasomal subunit requirement for ubiquitin-dependent proteolysis of cell cycle regulatory proteins in budding yeast. Mol Cell Biol 19, 6872-6890. (Pubitemid 29441870)
5. Ben-Aroya S, Agmon N, Yuen K, Kwok T, McManus K, Kupiec M, Hieter P (2010). Proteasome nuclear activity affects chromosome stability by controlling the turnover of Mms22, a protein important for DNA repair. PLoS Genet 6, e1000852.
6. Besche HC, Haas W, Gygi SP, Goldberg AL (2009a). Isolation of mammalian 26S proteasomes and p97/VCP complexes using the ubiquitin-like domain from HHR23B reveals novel proteasome-associated proteins. Biochemistry 48, 2538-2549.
7. Besche HC, Peth A, Goldberg AL (2009b). Getting to first base in proteasome assembly. Cell 138, 25-28.
8. Bohn S, Beck F, Sakata E, Walzthoeni T, Beck M, Aebersold R, Forster F, Baumeister W, Nickell S (2010). Structure of the 26S proteasome from Schizosaccharomyces pombe at subnanometer resolution. Proc Natl Acad Sci USA 107, 20992-20997.
9. Book AJ, Gladman NP, Lee SS, Scalf M, Smith LM, Vierstra RD (2010). Af- finity purification of the Arabidopsis 26S proteasome reveals a diverse array of plant proteolytic complexes. J Biol Chem 285, 25554-25569.
10. Book AJ et al. (2009). The RPN5 subunit of the 26s proteasome is essential for gametogenesis, sporophyte development, and complex assembly in Arabidopsis. Plant Cell 21, 460-478.
11. Burks EA, Bezerra PP, Le H, Gallie DR, Browning KS (2001). Plant eIF3 sub-unit composition resembles mammalian eIF3 and has a novel subunit. J Biol Chem 276, 2122-2131. (Pubitemid 32109694)
12. Busch S, Schwier EU, Nahlik K, Bayram O, 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. (Pubitemid 47185880)
13. Chamovitz DA (2009). Revisiting the COP9 signalosome as a transcriptional regulator. EMBO Rep 10, 352-358.
14. Chang EC, Schwechheimer C (2004). ZOMES III: the interface between signalling and proteolysisMeeting on the COP9 signalosome, proteasome and eIF3. EMBO Rep 5, 1041-1045. (Pubitemid 39600201)
15. Cohen M, Stutz F, Belgareh N, Haguenauer-Tsapis R, Dargemont C (2003). Ubp3 requires a cofactor, Bre5, to specifically de-ubiquitinate the COPII protein, Sec23. Nat Cell Biol 5, 661-667. (Pubitemid 36818089)
16. Collins SR et al. (2007). Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446, 806-810. (Pubitemid 46582025)
17. 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. (Pubitemid 35215316)
18. 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. (Pubitemid 352844592)
19. Effantin G, Rosenzweig R, Glickman MH, Steven AC (2009). Electron microscopic evidence in support of á-solenoid models of proteasomal subunits Rpn1 and Rpn2. J Mol Biol 386, 1204-1211.
20. Elsasser S, Chandler-Militello D, Muller B, Hanna J, Finley D (2004). Rad23 and Rpn10 serve as alternative ubiquitin receptors for the proteasome. J Biol Chem 279, 26817-26822. (Pubitemid 38812515)
21. 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.
22. Faza MB, Kemmler S, Jimeno S, Gonzalez-Aguilera C, Aguilera A, Hurt E, Panse VG (2009). Sem1 is a functional component of the nuclear pore complex-associated messenger RNA export machinery. J Cell Biol 184, 833-846.
23. Finley D (2009). Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78, 477-513.
24. 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. (Pubitemid 34062301)
25. 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.
26. Gavin A-C et al. (2006). Proteome survey reveals modularity of the yeast cell machinery. Nature 440, 631.
27. Glickman MH, Coux O (2001). Purification and characterization of proteasomes from Saccharomyces cerevisiae. In: Current Protocols in Protein Science, vol. 24, New York: John Wiley & Sons, 21.25.21-21.25.17.
28. Glickman MH, Rubin DM, Coux O, Wefes I, Pfeifer G, Cjeka Z, Baumeister W, Fried VA, Finley D (1998a). A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94, 615-623. (Pubitemid 28427580)
29. Glickman MH, Rubin DM, Fried VA, Finley D (1998b). The regulatory particle of the S. cerevisiae proteasome. Mol Cell Biol 18, 3149-3162.
30. 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. (Pubitemid 41002996)
31. Hetfeld BK, Bech-Otschir D, Dubiel W (2005). Purification method of the COP9 signalosome from human erythrocytes. Methods Enzymol 398, 481-491. (Pubitemid 41578907)
32. Hetfeld BK, Helfrich A, Kapelari B, Scheel H, Hofmann K, Guterman A, Glickman M, Schade R, Kloetzel PM, Dubiel W (2005). The zinc finger of the CSN-associated deubiquitinating enzyme USP15 is essential to rescue the E3 ligase Rbx1. Curr Biol 15, 1217-1221. (Pubitemid 40950520)
33. Hinnebusch AG, Asano K, Olsen DS, Phan L, Nielsen KH, Valasek L (2004). Study of translational control of eukaryotic gene expression using yeast. Ann N Y Acad Sci 1038, 60-74. (Pubitemid 40577444)
34. Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y, Hofmann K, Walters KJ, Finley D, Dikic I (2008). Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453, 481-488. (Pubitemid 351733317)
35. Isono E et al. (2007). The assembly pathway of the 19S regulatory particle of the yeast 26S proteasome. Mol Biol Cell 18, 569-580. (Pubitemid 46213225)
36. 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. (Pubitemid 40341203)
37. 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.
38. Kato JY, Yoneda-Kato N (2009). Mammalian COP9 signalosome. Genes Cells 14, 1209-1225.
39. Kloetzel PM (2001). Antigen processing by the proteasome. Nat Rev Mol Cell Biol 2, 179-187.
40. Krogan NJ et al. (2006). Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637.
41. Longtine MS, McKenzie AR, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961. (Pubitemid 28328001)
42. Luke-Glaser S, Roy M, Larsen B, Le Bihan T, Metalnikov P, Tyers M, Peter M, Pintard L (2007). CIF-1, a shared subunit of the COP9/signalosome and eukaryotic initiation factor 3 complexes, regulates MEL-26 levels in the Caenorhabditis elegans embryo. Mol Cell Biol 27, 4526-4540. (Pubitemid 46906574)
43. Lyapina S, Cope G, Shevchenko A, Serino G, Tsuge T, Zhou C, Wolf DA, Wei N, Shevchenko A, Deshaies RJ (2001). Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science 292, 1382-1385. (Pubitemid 32476226)
44. Matiuhin Y, Kirkpatrick DS, Ziv I, Kim W, Dakshinamurthy A, Kleifeld O, Gygi SP, Reis N, Glickman MH (2008). Extraproteasomal Rpn10 restricts access of the polyubiquitin-binding protein Dsk2 to proteasome. Mol Cell 32, 415-425.
45. Mayor T, Russell Lipford J, Graumann J, Smith GT, Deshaies RJ (2005). Analysis of poly-ubiquitin conjugates reveals that the Rpn10 substrate receptor contributes to the turnover of multiple proteasome targets. Mol Cell Proteomics 4, 741-751. (Pubitemid 40873003)
46. Maytal-Kivity V, Pick E, Piran R, Hofmann K, Glickman MH (2003). The COP9 signalosome-like complex in S. cerevisiae and links to other PCI complexes. Int J Biochem Cell Biol 35, 706-715. (Pubitemid 36369518)
47. Maytal-Kivity V, Piran R, Pick E, Hofmann K, Glickman MH (2002a). COP9 signalosome components play a role in the mating pheromone response of S. cerevisiae. EMBO Rep 12, 1215-1221. (Pubitemid 36105013)
48. Maytal-Kivity V, Reis N, Hofmann K, Glickman MH (2002b). MPN+, a putative catalytic motif found in a subset of MPN domain proteins from eukaryotes and prokaryotes, is critical for Rpn11 function. BMC Biochem 3, 28.
49. Menon S, Rubio V, Wang X, Deng XW, Wei N (2005). Purification of the COP9 signalosome from porcine spleen, human cell lines, and Arabidopsis thaliana plants. Methods Enzymol 398, 468-481. (Pubitemid 41578906)
50. Mundt KE et al. (1999). The COP9/signalosome complex is conserved in fission yeast and has a role in S phase. Curr Biol 9, 1427-1430.
51. Pick E, Hofmann K, Glickman MH (2009). PCI complexes: beyond the proteasome, CSN, and eIF3 troika. Mol Cell 35, 260-264.
52. Pick E, Pintard L (2009). A journey to the land of the rising sun with the Cop9/signalosome and related Zomes. EMBO Rep 10, 343-348.
53. Rosel D, Kimmel AR (2006). The COP9 signalosome regulates cell proliferation of Dictyostelium discoideum. Eur J Cell Biol 85, 1023-1034. (Pubitemid 44317597)
54. Rosenzweig R, Osmulski PA, Gaczynska M, Glickman MH (2008). The central unit within the 19S regulatory particle of the proteasome. Nat Struct Mol Biol 15, 573-580. (Pubitemid 351799134)
55. Scheel H, Hofmann K (2005). Prediction of a common structural scaffold for proteasome lid, COP9-signalosome and eIF3 complexes. BMC Bioinformatics 6, 71.
56. Sha Z, Brill LM, Cabrera R, Kleifeld O, Scheliga JS, Glickman MH, Chang EC, Wolf DA (2009). The eIF3 interactome reveals the translasome, a supercomplex linking protein synthesis and degradation machineries. Mol Cell 36, 141-152.
57. Sha Z, Yen HC, Scheel H, Suo J, Hofmann K, Chang EC (2007). Isolation of the Schizosaccharomyces pombe proteasome subunit Rpn7 and a structure-function study of the proteasome-COP9-initiation factor domain. J Biol Chem 282, 32414-32423. (Pubitemid 350106423)
58. Shalev A, Valasek L, Pise-Masison CA, Radonovich M, Phan L, Clayton J, He H, Brady JN, Hinnebusch AG, Asano K (2001). Saccharomyces cerevisiae protein Pci8p and human protein eIF3e/Int-6 interact with the eIF3 core complex by binding to cognate eIF3b subunits. J Biol Chem 276, 34948-34957.
59. Sharon M, Taverner T, Ambroggio XI, Deshaies RJ, Robinson C (2006). Structural organization of the 19S proteasome lid: insights from MS of intact complexes. PLoS Biol 4, e267.
60. Takeuchi J, Fujimuro M, Yokosawa H, Tanaka K, Toh-e A (1999). Rpn9 is required for efficient assembly of the yeast 26S proteasome. Mol Cell Biol 10, 6575-6584. (Pubitemid 29441842)
61. Takeuchi J, Toh-e A (1999). Genetic evidence for interaction between components of the yeast 26S proteasome: combination of a mutation in RPN12 (a lid component gene) with mutations in RPT1 (an ATPase gene) causes synthetic lethality. Mol Gen Genet 262, 145-153. (Pubitemid 29423912)
62. Tomko RJ Jr, Funakoshi M, Schneider K, Wang J, Hochstrasser M (2010). Heterohexameric ring arrangement of the eukaryotic proteasomal ATPases: implications for proteasome structure and assembly. Mol Cell 38, 393-403.
63. 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. (Pubitemid 32039740)
64. Uetz P et al. (2000). A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403, 623-627. (Pubitemid 30103994)
65. Verma R, Aravind L, Oania R, McDonald WH, Yates JR III, Koonin EV, Deshaies RJ (2002). Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298, 611-615. (Pubitemid 35215317)
66. Wee S, Hetfeld B, Dubiel W, Wolf DA (2002). Conservation of the COP9/ signalosome in budding yeast. BMC Genet 3, 15.
67. Wei N, Serino G, Deng XW (2008a). The COP9 signalosome: more than a protease. Trends Biochem Sci 33, 592-600.
68. Wei SJ et al. (2008b). Identification of a specific motif of the DSS1 protein required for proteasome interaction and p53 protein degradation. J Mol Biol 383, 693-712.
69. Wilmes GM et al. (2008). A genetic interaction map of RNA-processing factors reveals links between Sem1/Dss1-containing complexes and mRNA export and splicing. Mol Cell 32, 735-746.
70. Yang P, Fu H, Walker J, Papa CM, Smalle J, Ju YM, Vierstra RD (2004). Purification of the Arabidopsis 26 S proteasome: biochemical and molecular analyses revealed the presence of multiple isoforms. J Biol Chem 279, 6401-6413. (Pubitemid 38248774)
71. Yao T, Cohen RE (2002). A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419, 403-407.
72. Zhou C, Arslan F, Wee S, Krishnan S, Ivanov AR, Oliva A, Leatherwood J, Wolf DA (2005). PCI proteins eIF3e and eIF3m define distinct translation initiation factor 3 complexes. BMC Biol 3, 14.
73. Zhou C, Seibert V, Geyer R, Rhee E, Lyapina S, Cope G, Deshaies RJ, Wolf DA (2001). The fission yeast COP9/signalosome is involved in cullin modification by ubiquitin-related Ned8p. BMC Biochem 2, 7.
74. Zhou M et al. (2008). Mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc Natl Acad Sci USA 105, 18139-18144.