The Protein Quality Control Machinery Regulates Its Misassembled Proteasome Subunits

PLoS Genetics

Volumn 11, Issue 4, 2015, Pages

  Peters, Lee Zeev ^a   Karmon, Ofri ^a   David Kadoch, Galit ^a   Hazan, Rotem ^a   Yu, Tzenlin ^b   Glickman, Michael H ^b   Ben Aroya, Shay ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 42; PROTEASOME; UBIQUITIN; UNCLASSIFIED DRUG; HSP42 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL PROTECTION; CONTROLLED STUDY; ENZYME SUBUNIT; METABOLIC PARAMETERS; METABOLIC REGULATION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN HOMEOSTASIS; PROTEIN METABOLISM; PROTEIN QUALITY CONTROL; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; UBIQUITIN PROTEASOME SYSTEM; CELL SURVIVAL; GENETICS; METABOLISM; PROTEIN FOLDING; REPRODUCTIVE FITNESS; UBIQUITINATION;

EUKARYOTA;

CELL SURVIVAL; GENETIC FITNESS; HEAT-SHOCK PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN; UBIQUITINATION;

EID: 84930353020     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005178     Document Type: Article

References (44)

1. Su H, Wang X, (2010) The ubiquitin-proteasome system in cardiac proteinopathy: a quality control perspective. Cardiovasc Res 85: 253–262. doi: 10.1093/cvr/cvp287 19696071
2. Kastle M, Grune T, (2012) Interactions of the proteasomal system with chaperones: protein triage and protein quality control. Prog Mol Biol Transl Sci 109: 113–160. doi: 10.1016/B978-0-12-397863-9.00004-3 22727421
3. Comyn SA, Chan GT, Mayor T, (2014) False start: Cotranslational protein ubiquitination and cytosolic protein quality control. J Proteomics 100C: 92–101.
4. Amm I, Sommer T, Wolf DH, (2014) Protein quality control and elimination of protein waste: the role of the ubiquitin-proteasome system. Biochim Biophys Acta 1843: 182–196. doi: 10.1016/j.bbamcr.2013.06.031 23850760
5. Hershko A, Ciechanover A, (1998) The ubiquitin system. Annu Rev Biochem 67: 425–479. 9759494
6. Tanaka K, (2009) The proteasome: overview of structure and functions. Proc Jpn Acad Ser B Phys Biol Sci 85: 12–36. 19145068
7. 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 20471955
8. Ciechanover A, (2005) Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ 12: 1178–1190. 16094394
9. Kaganovich D, Kopito R, Frydman J, (2008) Misfolded proteins partition between two distinct quality control compartments. Nature 454: 1088–1095. doi: 10.1038/nature07195 18756251
10. Spokoini R, Moldavski O, Nahmias Y, England JL, Schuldiner M, et al. (2012) Confinement to organelle-associated inclusion structures mediates asymmetric inheritance of aggregated protein in budding yeast. Cell Rep 2: 738–747. doi: 10.1016/j.celrep.2012.08.024 23022486
11. Brooks CL, Gu W, (2003) Ubiquitination, phosphorylation and acetylation: the molecular basis for p53 regulation. Curr Opin Cell Biol 15: 164–171. 12648672
12. Nasmyth K, (2002) Segregating sister genomes: the molecular biology of chromosome separation. Science 297: 559–565. 12142526
13. Ben-Aroya S, Agmon N, Yuen K, Kwok T, McManus K, et al. (2010) Proteasome nuclear activity affects chromosome stability by controlling the turnover of Mms22, a protein important for DNA repair. PLoS Genet 6: e1000852. doi: 10.1371/journal.pgen.1000852 20174551
14. Wilkinson CR, Wallace M, Morphew M, Perry P, Allshire R, et al. (1998) Localization of the 26S proteasome during mitosis and meiosis in fission yeast. EMBO J 17: 6465–6476. 9822592
15. Enenkel C, Lehmann A, Kloetzel PM, (1999) GFP-labelling of 26S proteasomes in living yeast: insight into proteasomal functions at the nuclear envelope/rough ER. Mol Biol Rep 26: 131–135. 10363659
16. Russell SJ, Steger KA, Johnston SA, (1999) Subcellular localization, stoichiometry, and protein levels of 26 S proteasome subunits in yeast. J Biol Chem 274: 21943–21952. 10419517
17. Ben-Aroya S, Coombes C, Kwok T, O'Donnell KA, Boeke JD, et al. (2008) Toward a comprehensive temperature-sensitive mutant repository of the essential genes of Saccharomyces cerevisiae. Mol Cell 30: 248–258. doi: 10.1016/j.molcel.2008.02.021 18439903
18. Isono E, Nishihara K, Saeki Y, Yashiroda H, Kamata N, et al. (2007) The assembly pathway of the 19S regulatory particle of the yeast 26S proteasome. Mol Biol Cell 18: 569–580. 17135287
19. Li X, Kusmierczyk AR, Wong P, Emili A, Hochstrasser M, (2007) beta-Subunit appendages promote 20S proteasome assembly by overcoming an Ump1-dependent checkpoint. EMBO J 26: 2339–2349. 17431397
20. Tarassov K, Messier V, Landry CR, Radinovic S, Serna Molina MM, et al. (2008) An in vivo map of the yeast protein interactome. Science 320: 1465–1470. doi: 10.1126/science.1153878 18467557
21. 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. 16869714
22. Sha Z, Yen HC, Scheel H, Suo J, Hofmann K, et al. (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. 17761670
23. 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. 11742986
24. Yu Z, Kleifeld O, Lande-Atir A, Bsoul M, Kleiman M, et al. (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 21289098
25. Leggett DS, Glickman MH, Finley D, (2005) Purification of proteasomes, proteasome subcomplexes, and proteasome-associated proteins from budding yeast. Methods Mol Biol 301: 57–70. 15917626
26. Escusa-Toret S, Vonk WI, Frydman J, (2013) Spatial sequestration of misfolded proteins by a dynamic chaperone pathway enhances cellular fitness during stress. Nat Cell Biol 15: 1231–1243. doi: 10.1038/ncb2838 24036477
27. Hill SM, Hao X, Liu B, Nystrom T, (2014) Life-span extension by a metacaspase in the yeast Saccharomyces cerevisiae. Science 344: 1389–1392. doi: 10.1126/science.1252634 24855027
28. Glickman MH, Rubin DM, Fried VA, Finley D, (1998) The regulatory particle of the Saccharomyces cerevisiae proteasome. Mol Cell Biol 18: 3149–3162. 9584156
29. Amen T, Kaganovich D, (2015) Dynamic droplets: the role of cytoplasmic inclusions in stress, function, and disease. Cell Mol Life Sci 72: 401–415. doi: 10.1007/s00018-014-1740-y 25283146
30. Weisberg SJ, Lyakhovetsky R, Werdiger AC, Gitler AD, Soen Y, et al. (2012) Compartmentalization of superoxide dismutase 1 (SOD1G93A) aggregates determines their toxicity. Proc Natl Acad Sci U S A 109: 15811–15816. 22967507
31. Haslbeck M, Miess A, Stromer T, Walter S, Buchner J, (2005) Disassembling protein aggregates in the yeast cytosol. The cooperation of Hsp26 with Ssa1 and Hsp104. J Biol Chem 280: 23861–23868. 15843375
32. Specht S, Miller SB, Mogk A, Bukau B, (2011) Hsp42 is required for sequestration of protein aggregates into deposition sites in Saccharomyces cerevisiae. J Cell Biol 195: 617–629. doi: 10.1083/jcb.201106037 22065637
33. Malinovska L, Kroschwald S, Munder MC, Richter D, Alberti S, (2012) Molecular chaperones and stress-inducible protein-sorting factors coordinate the spatiotemporal distribution of protein aggregates. Mol Biol Cell 23: 3041–3056. doi: 10.1091/mbc.E12-03-0194 22718905
34. Shiber A, Breuer W, Brandeis M, Ravid T, (2013) Ubiquitin conjugation triggers misfolded protein sequestration into quality control foci when Hsp70 chaperone levels are limiting. Mol Biol Cell 24: 2076–2087. doi: 10.1091/mbc.E13-01-0010 23637465
35. Kerem B, Rommens JM, Buchanan JA, Markiewicz D, Cox TK, et al. (1989) Identification of the cystic fibrosis gene: genetic analysis. Science 245: 1073–1080. 2570460
36. Rowe SM, Miller S, Sorscher EJ, (2005) Cystic fibrosis. N Engl J Med 352: 1992–2001. 15888700
37. Wolfe KJ, Cyr DM, (2011) Amyloid in neurodegenerative diseases: friend or foe? Semin Cell Dev Biol 22: 476–481. doi: 10.1016/j.semcdb.2011.03.011 21458579
38. Rott R, Szargel R, Haskin J, Bandopadhyay R, Lees AJ, et al. (2011) alpha-Synuclein fate is determined by USP9X-regulated monoubiquitination. Proc Natl Acad Sci U S A 108: 18666–18671. doi: 10.1073/pnas.1105725108 22065755
39. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, et al. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115–132. 9483801
40. Goldstein AL, McCusker JH, (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541–1553. 10514571
41. Longtine MS, McKenzie A,, 3rdDemarini DJ, NG Shah, A Wach, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953–961. 9717241
42. Peters LZ, Hazan R, Breker M, Schuldiner M, Ben-Aroya S, (2013) Formation and dissociation of proteasome storage granules are regulated by cytosolic pH. J Cell Biol 201: 663–671. doi: 10.1083/jcb.201211146 23690178
43. Lev I, Volpe M, Goor L, Levinton N, Emuna L, et al. (2013) Reverse PCA, a systematic approach for identifying genes important for the physical interaction between protein pairs. PLoS Genet 9: e1003838. doi: 10.1371/journal.pgen.1003838 24130505
44. Park SH, Kukushkin Y, Gupta R, Chen T, Konagai A, et al. (2013) PolyQ proteins interfere with nuclear degradation of cytosolic proteins by sequestering the Sis1p chaperone. Cell 154: 134–145. doi: 10.1016/j.cell.2013.06.003 23791384