Compartment-specific aggregases direct distinct nuclear and cytoplasmic aggregate deposition

EMBO Journal

Volumn 34, Issue 6, 2015, Pages 778-797

  Miller, Stephanie B M ^a,b   Ho, Chi Ting ^a,b   Winkler, Juliane ^a,b   Khokhrina, Maria ^a,b   Neuner, Annett ^a   Mohamed, Mohamed Y H ^a,b,d   Guilbride, D Lys ^a   Richter, Karsten ^b   Lisby, Michael ^c   Schiebel, Elmar ^a   Mogk, Axel ^a   Bukau, Bernd ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

chaperones; protein aggregation; protein disaggregation; proteostasis; ubiquitin proteasome system

Indexed keywords

AGGREGASE; BTN2 PROTEIN; CHAPERONE; DNA; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 42; NUCLEAR PROTEIN; PROTEIN; UNCLASSIFIED DRUG; AMINO ACID TRANSPORTER; BTN2 PROTEIN, S CEREVISIAE; HSP42 PROTEIN, S CEREVISIAE; PROTEIN AGGREGATE; SACCHAROMYCES CEREVISIAE PROTEIN;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; DNA DAMAGE; DNA REPLICATION; INTRANUCLEAR SPACE; JUXTANUCLEAR SITE; NONHUMAN; NUCLEAR IMPORT; NUCLEAR PORE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN QUALITY; QUALITY CONTROL; SACCHAROMYCES CEREVISIAE; UBIQUITINATION; YEAST; BIOLOGICAL MODEL; FLUORESCENCE MICROSCOPY; HELA CELL LINE; HUMAN; IMAGE PROCESSING; IMMUNOELECTRON MICROSCOPY; METABOLISM; PHYSIOLOGY; TIME LAPSE IMAGING; WESTERN BLOTTING;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

AMINO ACID TRANSPORT SYSTEMS; BLOTTING, WESTERN; CELL COMPARTMENTATION; CYTOSOL; HEAT-SHOCK PROTEINS; HELA CELLS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, FLUORESCENCE; MICROSCOPY, IMMUNOELECTRON; MODELS, BIOLOGICAL; PROTEIN AGGREGATES; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TIME-LAPSE IMAGING; UBIQUITINATION;

EID: 84924864644     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201489524     Document Type: Article

References (52)

1. Abelson JN, Guthrie C, Fink GR, (2003) Guide to Yeast Genetics and Molecular Biology. USA: Academic Press Inc
2. Berthold MR, Cebron N, Dill F, Gabriel TR, Kötter T, Meinl T, Ohl P, Sieb C, Thiel K, Wiswedel B, (2008) KNIME: The Konstanz Information Miner. In Data Analysis, Machine Learning and Applications, Preisach C, Burkhardt H, Schmidt-Thieme L, Decker R, (eds), Vol. 38, pp 319-326. Berlin, Heidelberg: Springer.
3. Chen B, Retzlaff M, Roos T, Frydman J, (2011) Cellular strategies of protein quality control. Cold Spring Harb Perspect Biol 3: a004374
4. Cherkasov V, Hofmann S, Druffel-Augustin S, Mogk A, Tyedmers J, Stoecklin G, Bukau B, (2013) Coordination of translational control and protein homeostasis during severe heat stress. Curr Biol 23: 2452-2462
5. Choi DH, Kwon SH, Kim JH, Bae SH, (2012) Saccharomyces cerevisiae Cmr1 protein preferentially binds to UV-damaged DNA in vitro. J Microbiol 50: 112-118
6. Cohen E, Bieschke J, Perciavalle RM, Kelly JW, Dillin A, (2006) Opposing activities protect against age-onset proteotoxicity. Science 313: 1604-1610
7. Douglas PM, Treusch S, Ren HY, Halfmann R, Duennwald ML, Lindquist S, Cyr DM, (2008) Chaperone-dependent amyloid assembly protects cells from prion toxicity. Proc Natl Acad Sci USA 105: 7206-7211
8. Eisele F, Wolf DH, (2008) Degradation of misfolded protein in the cytoplasm is mediated by the ubiquitin ligase Ubr1. FEBS Lett 582: 4143-4146
9. 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: 1231-1234
10. Fredrickson EK, Gallagher PS, Clowes Candadai SV, Gardner RG, (2013) Substrate recognition in nuclear protein quality control degradation is governed by exposed hydrophobicity that correlates with aggregation and insolubility. J Biol Chem 288: 6130-6139
11. Fredrickson EK, Rosenbaum JC, Locke MN, Milac TI, Gardner RG, (2011) Exposed hydrophobicity is a key determinant of nuclear quality control degradation. Mol Biol Cell 22: 2384-2395
12. Garcia-Mata R, Bebok Z, Sorscher EJ, Sztul ES, (1999) Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J Cell Biol 146: 1239-1254
13. Giddings TH Jr, O'Toole ET, Morphew M, Mastronarde DN, McIntosh JR, Winey M, (2001) Using rapid freeze and freeze-substitution for the preparation of yeast cells for electron microscopy and three-dimensional analysis. Methods Cell Biol 67: 27-42
14. Guerriero CJ, Weiberth KF, Brodsky JL, (2013) Hsp70 targets a cytoplasmic quality control substrate to the San1p ubiquitin ligase. J Biol Chem 288: 18506-18520
15. Gupta R, Kasturi P, Bracher A, Loew C, Zheng M, Villella A, Garza D, Hartl FU, Raychaudhuri S, (2011) Firefly luciferase mutants as sensors of proteome stress. Nat Methods 8: 879-884
16. Hartl FU, Bracher A, Hayer-Hartl M, (2011) Molecular chaperones in protein folding and proteostasis. Nature 475: 324-332
17. Heck JW, Cheung SK, Hampton RY, (2010) Cytoplasmic protein quality control degradation mediated by parallel actions of the E3 ubiquitin ligases Ubr1 and San1. Proc Natl Acad Sci USA 107: 1106-1111
18. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, Moreno-Borchart A, Doenges G, Schwob E, Schiebel E, Knop M, (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947-962
19. Johnston JA, Ward CL, Kopito RR, (1998) Aggresomes: a cellular response to misfolded proteins. J Cell Biol 143: 1883-1898
20. Jung G, Jones G, Masison DC, (2002) Amino acid residue 184 of yeast Hsp104 chaperone is critical for prion-curing by guanidine, prion propagation, and thermotolerance. Proc Natl Acad Sci USA 99: 9936-9941
21. Kaganovich D, Kopito R, Frydman J, (2008) Misfolded proteins partition between two distinct quality control compartments. Nature 454: 1088-1095
22. Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, Yao TP, (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115: 727-738
23. Knop M, Finger A, Braun T, Hellmuth K, Wolf DH, (1996) Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast. EMBO J 15: 753-763
24. Kopito RR, (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 10: 524-530
25. Kryndushkin DS, Shewmaker F, Wickner RB, (2008) Curing of the [URE3] prion by Btn2p, a Batten disease-related protein. EMBO J 27: 2725-2735
26. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685
27. Lelouard H, Gatti E, Cappello F, Gresser O, Camosseto V, Pierre P, (2002) Transient aggregation of ubiquitinated proteins during dendritic cell maturation. Nature 417: 177-182
28. 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
29. McClellan AJ, Scott MD, Frydman J, (2005) Folding and quality control of the VHL tumor suppressor proceed through distinct chaperone pathways. Cell 121: 739-748
30. Morimoto RI, (2011) The heat shock response: systems biology of proteotoxic stress in aging and disease. Cold Spring Harb Symp Quant Biol 76: 91-99
31. Nystrom T, Liu B, (2014) The mystery of aging and rejuvenation-a budding topic. Curr Opin Microbiol 18C: 61-67
32. Ogrodnik M, Salmonowicz H, Brown R, Turkowska J, Sredniawa W, Pattabiraman S, Amen T, Abraham AC, Eichler N, Lyakhovetsky R, Kaganovich D, (2014) Dynamic JUNQ inclusion bodies are asymmetrically inherited in mammalian cell lines through the asymmetric partitioning of vimentin. Proc Natl Acad Sci USA 111: 8049-8054
33. Ollion J, Cochennec J, Loll F, Escude C, Boudier T, (2013) TANGO: a generic tool for high-throughput 3D image analysis for studying nuclear organization. Bioinformatics 29: 1840-1841
34. Park SH, Kukushkin Y, Gupta R, Chen T, Konagai A, Hipp MS, Hayer-Hartl M, Hartl FU, (2013) PolyQ Proteins Interfere with Nuclear Degradation of Cytosolic Proteins by Sequestering the Sis1p Chaperone. Cell 154: 134-145
35. Parsell DA, Kowal AS, Singer MA, Lindquist S, (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372: 475-478
36. Prasad R, Kawaguchi S, Ng DT, (2010) A nucleus-based quality control mechanism for cytosolic proteins. Mol Biol Cell 21: 2117-2127
37. Rosenbaum JC, Gardner RG, (2011) How a disordered ubiquitin ligase maintains order in nuclear protein homeostasis. Nucleus 2: 264-270
38. Rujano MA, Bosveld F, Salomons FA, Dijk F, van Waarde MA, van der Want JJ, de Vos RA, Brunt ER, Sibon OC, Kampinga HH, (2006) Polarised asymmetric inheritance of accumulated protein damage in higher eukaryotes. PLoS Biol 4: e417
39. 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
40. 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
41. Sontag EM, Vonk WI, Frydman J, (2014) Sorting out the trash: the spatial nature of eukaryotic protein quality control. Curr Opin Cell Biol 26C: 139-146
42. 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
43. Spokoini R, Moldavski O, Nahmias Y, England JL, Schuldiner M, Kaganovich D, (2012) Confinement to organelle-associated inclusion structures mediates asymmetric inheritance of aggregated protein in budding yeast. Cell Rep 2: 738-747
44. Stirling PC, Bloom MS, Solanki-Patil T, Smith S, Sipahimalani P, Li Z, Kofoed M, Ben-Aroya S, Myung K, Hieter P, (2011) The complete spectrum of yeast chromosome instability genes identifies candidate CIN cancer genes and functional roles for ASTRA complex components. PLoS Genet 7: e1002057
45. Szebenyi G, Wigley WC, Hall B, Didier A, Yu M, Thomas P, Kramer H, (2007) Hook2 contributes to aggresome formation. BMC Cell Biol 8: 19
46. Szeto J, Kaniuk NA, Canadien V, Nisman R, Mizushima N, Yoshimori T, Bazett-Jones DP, Brumell JH, (2006) ALIS are stress-induced protein storage compartments for substrates of the proteasome and autophagy. Autophagy 2: 189-199
47. Tkach JM, Yimit A, Lee AY, Riffle M, Costanzo M, Jaschob D, Hendry JA, Ou J, Moffat J, Boone C, Davis TN, Nislow C, Brown GW, (2012) Dissecting DNA damage response pathways by analysing protein localization and abundance changes during DNA replication stress. Nat Cell Biol 14: 966-976
48. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, Page N, Robinson M, Raghibizadeh S, Hogue CW, Bussey H, Andrews B, Tyers M, Boone C, (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368
49. Tyedmers J, Mogk A, Bukau B, (2010) Cellular strategies for controlling protein aggregation. Nat Rev Mol Cell Biol 11: 777-788
50. Weisberg SJ, Lyakhovetsky R, Werdiger AC, Gitler AD, Soen Y, Kaganovich D, (2012) Compartmentalization of superoxide dismutase 1 (SOD1G93A) aggregates determines their toxicity. Proc Natl Acad Sci USA 109: 15811-15816
51. Wente SR, Rout MP, (2010) The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol 2: a000562
52. Zhou C, Slaughter BD, Unruh JR, Eldakak A, Rubinstein B, Li R, (2011) Motility and segregation of Hsp104-associated protein aggregates in budding yeast. Cell 147: 1186-1196