How the nucleus copes with proteotoxic stress

Current Biology

Volumn 24, Issue 10, 2014, Pages

  Shibata, Yoko ^a   Morimoto, Richard I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA;

FUNGAL PROTEIN;

ANIMAL; CELL NUCLEUS; CHEMISTRY; EUKARYOTIC CELL; HUMAN; METABOLISM; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES;

ANIMALS; CELL NUCLEUS; EUKARYOTIC CELLS; FUNGAL PROTEINS; HUMANS; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES;

EID: 84901012110     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2014.03.033     Document Type: Review

References (139)

1. F.U. Hartl, A. Bracher, and M. Hayer-Hartl Molecular chaperones in protein folding and proteostasis Nature 475 2011 324 332
2. E.T. Powers, R.I. Morimoto, A. Dillin, J.W. Kelly, and W.E. Balch Biological and chemical approaches to diseases of proteostasis deficiency Annu. Rev. Biochem. 78 2009 959 991
3. R.I. Morimoto Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging Genes Dev. 22 2008 1427 1438
4. D. Ron, and P. Walter Signal integration in the endoplasmic reticulum unfolded protein response Nat. Rev. Mol. Cell Biol. 8 2007 519 529
5. B.M. Baker, and C.M. Haynes Mitochondrial protein quality control during biogenesis and aging Trends Biochem. Sci. 36 2011 254 261
6. A. Buchberger, B. Bukau, and T. Sommer Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms Mol. Cell 40 2010 238 252
7. C.M. Haynes, and D. Ron The mitochondrial UPR - protecting organelle protein homeostasis J. Cell Sci. 123 2010 3849 3855
8. M. Neumann, D.M. Sampathu, L.K. Kwong, A.C. Truax, M.C. Micsenyi, T.T. Chou, J. Bruce, T. Schuck, M. Grossman, and C.M. Clark et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis Science 314 2006 130 133
9. I.A. Klement, P.J. Skinner, M.D. Kaytor, H. Yi, S.M. Hersch, H.B. Clark, H.Y. Zoghbi, and H.T. Orr Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice Cell 95 1998 41 53
10. S.W. Davies, M. Turmaine, B.A. Cozens, M. DiFiglia, A.H. Sharp, C.A. Ross, E. Scherzinger, E.E. Wanker, L. Mangiarini, and G.P. Bates Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation Cell 90 1997 537 548
11. P.S. Gallagher, M.L. Oeser, A.C. Abraham, D. Kaganovich, and R.G. Gardner Cellular maintenance of nuclear protein homeostasis Cell. Mol. Life Sci. 2013 epub ahead of print
12. J.M. Woulfe Abnormalities of the nucleus and nuclear inclusions in neurodegenerative disease: a work in progress Neuropathol. Appl. Neurobiol. 33 2007 2 42
13. H.H. Kampinga, and E.A. Craig The HSP70 chaperone machinery: J proteins as drivers of functional specificity Nat. Rev. Mol. Cell Biol. 11 2010 579 592
14. H. Rampelt, J. Kirstein-Miles, N.B. Nillegoda, K. Chi, S.R. Scholz, R.I. Morimoto, and B. Bukau Metazoan Hsp70 machines use Hsp110 to power protein disaggregation EMBO J. 31 2012 4221 4235
15. A. Matsuyama, R. Arai, Y. Yashiroda, A. Shirai, A. Kamata, S. Sekido, Y. Kobayashi, A. Hashimoto, M. Hamamoto, and Y. Hiraoka et al. ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe Nat. Biotechnol. 24 2006 841 847
16. W.K. Huh, J.V. Falvo, L.C. Gerke, A.S. Carroll, R.W. Howson, J.S. Weissman, and E.K. O'Shea Global analysis of protein localization in budding yeast Nature 425 2003 686 691
17. D.H. Lee, and A.L. Goldberg Proteasome inhibitors: valuable new tools for cell biologists Trends Cell Biol. 8 1998 397 403
18. D. Komander, and M. Rape The ubiquitin code Annu. Rev. Biochem. 81 2012 203 229
19. J. Pines, and C. Lindon Proteolysis: anytime, any place, anywhere? Nat. Cell Biol. 7 2005 731 735
20. V. Arndt, C. Rogon, and J. Hohfeld To be, or not to be-molecular chaperones in protein degradation Cell. Mol. Life Sci. 64 2007 2525 2541
21. S. Elsasser, and D. Finley Delivery of ubiquitinated substrates to protein-unfolding machines Nat. Cell Biol. 7 2005 742 749
22. J. Hanna, and D. Finley A proteasome for all occasions FEBS Lett. 581 2007 2854 2861
23. A. Varshavsky The ubiquitin system, an immense realm Annu. Rev. Biochem. 81 2012 167 176
24. A.M. Weissman, N. Shabek, and A. Ciechanover The predator becomes the prey: regulating the ubiquitin system by ubiquitylation and degradation. Nature reviews Mol. Cell Biol. 12 2011 605 620
25. R.R. Kopito Aggresomes, inclusion bodies and protein aggregation Trends Cell Biol. 10 2000 524 530
26. J. Tyedmers, A. Mogk, and B. Bukau Cellular strategies for controlling protein aggregation Nat. Rev. Mol. Cell Biol. 11 2010 777 788
27. E.M. Sontag, W.I. Vonk, and J. Frydman Sorting out the trash: the spatial nature of eukaryotic protein quality control Curr. Opin. Cell Biol. 26C 2014 139 146
28. D. Kaganovich, R. Kopito, and J. Frydman Misfolded proteins partition between two distinct quality control compartments Nature 454 2008 1088 1095
29. S. Escusa-Toret, W.I. Vonk, and J. Frydman Spatial sequestration of misfolded proteins by a dynamic chaperone pathway enhances cellular fitness during stress Nat. Cell Biol. 15 2013 1231 1243
30. R. Spokoini, O. Moldavski, Y. Nahmias, J.L. England, M. Schuldiner, and D. Kaganovich Confinement to organelle-associated inclusion structures mediates asymmetric inheritance of aggregated protein in budding yeast Cell Rep. 2 2012 738 747
31. A. Williams, L. Jahreiss, S. Sarkar, S. Saiki, F.M. Menzies, B. Ravikumar, and D.C. Rubinsztein Aggregate-prone proteins are cleared from the cytosol by autophagy: therapeutic implications Curr. Top. Dev. Biol. 76 2006 89 101
32. H.P. Harding, Y. Zhang, H. Zeng, I. Novoa, P.D. Lu, M. Calfon, N. Sadri, C. Yun, B. Popko, and R. Paules et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress Mol. Cell 11 2003 619 633
33. M.W. Hetzer, T.C. Walther, and I.W. Mattaj Pushing the envelope: structure, function, and dynamics of the nuclear periphery Annu. Rev. Cell Dev. Biol. 21 2005 347 380
34. B. Burke, and C.L. Stewart The nuclear lamins: flexibility in function. Nature reviews Mol. Cell Biol. 14 2013 13 24
35. D.L. Spector Nuclear domains J. Cell Sci. 114 2001 2891 2893
36. D. Kressler, E. Hurt, and J. Bassler Driving ribosome assembly Biochimica et biophysica acta 1803 2010 673 683
37. A. Taddei, H. Schober, and S.M. Gasser The budding yeast nucleus Cold Spring Harbor Perspect. Biol. 2 2010 a000612
38. S.L. Jaspersen, and M. Winey The budding yeast spindle pole body: structure, duplication, and function Annu. Rev. Cell Dev. Biol. 20 2004 1 28
39. A. Hoelz, E.W. Debler, and G. Blobel The structure of the nuclear pore complex Annu. Rev. Biochem. 80 2011 613 643
40. S. Bilokapic, and T.U. Schwartz 3D ultrastructure of the nuclear pore complex Curr. Opin. Cell Biol. 24 2012 86 91
41. H. Fried, and U. Kutay Nucleocytoplasmic transport: taking an inventory Cell. Mol. Life Sci. 60 2003 1659 1688
42. T. Guttler, and D. Gorlich Ran-dependent nuclear export mediators: a structural perspective EMBO J. 30 2011 3457 3474
43. S. Rodriguez-Navarro, and E. Hurt Linking gene regulation to mRNA production and export Curr. Opin. Cell Biol. 23 2011 302 309
44. S. Pechmann, F. Willmund, and J. Frydman The ribosome as a hub for protein quality control Mol. Cell 49 2013 411 421
45. M.A. D'Angelo, M. Raices, S.H. Panowski, and M.W. Hetzer Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells Cell 136 2009 284 295
46. R.J. Ellis Molecular chaperones: assisting assembly in addition to folding Trends Biochem. Sci. 31 2006 395 401
47. A. Philpott, T. Krude, and R.A. Laskey Nuclear chaperones Semin. Cell Dev. Biol. 11 2000 7 14
48. J.M. Velazquez, and S. Lindquist hsp70: nuclear concentration during environmental stress and cytoplasmic storage during recovery Cell 36 1984 655 662
49. W.J. Welch, and J.R. Feramisco Nuclear and nucleolar localization of the 72,000-dalton heat shock protein in heat-shocked mammalian cells J. Biol. Chem. 259 1984 4501 4513
50. W.J. Welch, and L.A. Mizzen Characterization of the thermotolerant cell. II. Effects on the intracellular distribution of heat-shock protein 70, intermediate filaments, and small nuclear ribonucleoprotein complexes J. Cell Biol. 106 1988 1117 1130
51. G. Akner, K. Mossberg, K.G. Sundqvist, J.A. Gustafsson, and A.C. Wikstrom Evidence for reversible, non-microtubule and non-microfilament-dependent nuclear translocation of hsp90 after heat shock in human fibroblasts Eur. J. Cell Biol. 58 1992 356 364
52. T. Langer, S. Rosmus, and H. Fasold Intracellular localization of the 90 kDA heat shock protein (HSP90alpha) determined by expression of a EGFP-HSP90alpha-fusion protein in unstressed and heat stressed 3T3 cells Cell Biol. Internat. 27 2003 47 52
53. J.K. Willsie, and J.S. Clegg Small heat shock protein p26 associates with nuclear lamins and HSP70 in nuclei and nuclear matrix fractions from stressed cells J. Cell. Biochem. 84 2002 601 614
54. H. Hattori, T. Kaneda, B. Lokeshwar, A. Laszlo, and K. Ohtsuka A stress-inducible 40 kDa protein (hsp40): purification by modified two-dimensional gel electrophoresis and co-localization with hsc70(p73) in heat-shocked HeLa cells J. Cell Sci. 104 1993 629 638
55. S. Daniel, G. Bradley, V.M. Longshaw, C. Soti, P. Csermely, and G.L. Blatch Nuclear translocation of the phosphoprotein Hop (Hsp70/Hsp90 organizing protein) occurs under heat shock, and its proposed nuclear localization signal is involved in Hsp90 binding Biochim. Biophys. Acta 1783 2008 1003 1014
56. V.M. Longshaw, J.P. Chapple, M.S. Balda, M.E. Cheetham, and G.L. Blatch Nuclear translocation of the Hsp70/Hsp90 organizing protein mSTI1 is regulated by cell cycle kinases J. Cell Sci. 117 2004 701 710
57. K.L. Milarski, and R.I. Morimoto Expression of human HSP70 during the synthetic phase of the cell cycle Proc. Natl. Acad. Sci. USA 83 1986 9517 9521
58. F. Melchior, and L. Gerace Mechanisms of nuclear protein import Curr. Opin. Cell Biol. 7 1995 310 318
59. D.C. Dezwaan, and B.C. Freeman HSP90: the Rosetta stone for cellular protein dynamics? Cell Cycle 7 2008 1006 1012
60. M. Furuta, S. Kose, M. Koike, T. Shimi, Y. Hiraoka, Y. Yoneda, T. Haraguchi, and N. Imamoto Heat-shock induced nuclear retention and recycling inhibition of importin alpha Genes Cells 9 2004 429 441
61. Y. Miyamoto, T. Saiwaki, J. Yamashita, Y. Yasuda, I. Kotera, S. Shibata, M. Shigeta, Y. Hiraoka, T. Haraguchi, and Y. Yoneda Cellular stresses induce the nuclear accumulation of importin alpha and cause a conventional nuclear import block J. Cell Biol. 165 2004 617 623
62. S. Kose, M. Furuta, and N. Imamoto Hikeshi, a nuclear import carrier for Hsp70s, protects cells from heat shock-induced nuclear damage Cell 149 2012 578 589
63. A. Chu, N. Matusiewicz, and U. Stochaj Heat-induced nuclear accumulation of hsc70s is regulated by phosphorylation and inhibited in confluent cells FASEB J. 15 2001 1478 1480
64. M. Udan-Johns, R. Bengoechea, S. Bell, J. Shao, M.I. Diamond, H.L. True, C.C. Weihl, and R.H. Baloh Prion-like nuclear aggregation of TDP-43 during heat shock is regulated by HSP40/70 chaperones Hum. Mol. Genet. 23 2014 157 170
65. S. Kim, E.A. Nollen, K. Kitagawa, V.P. Bindokas, and R.I. Morimoto Polyglutamine protein aggregates are dynamic Nat. Cell Biol. 4 2002 826 831
66. H. Tapia, and K.A. Morano Hsp90 nuclear accumulation in quiescence is linked to chaperone function and spore development in yeast Mol. Biol. Cell 21 2010 63 72
67. Z.S. Chughtai, R. Rassadi, N. Matusiewicz, and U. Stochaj Starvation promotes nuclear accumulation of the hsp70 Ssa4p in yeast cells J. Biol. Chem. 276 2001 20261 20266
68. X. Quan, R. Rassadi, B. Rabie, N. Matusiewicz, and U. Stochaj Regulated nuclear accumulation of the yeast hsp70 Ssa4p in ethanol-stressed cells is mediated by the N-terminal domain, requires the nuclear carrier Nmd5p and protein kinase C FASEB J. 18 2004 899 901
69. J.M. Tkach, and J.R. Glover Nucleocytoplasmic trafficking of the molecular chaperone Hsp104 in unstressed and heat-shocked cells Traffic 9 2008 39 56
70. J.M. Rossi, and S. Lindquist The intracellular location of yeast heat-shock protein 26 varies with metabolism J. Cell Biol. 108 1989 425 439
71. J.M. Tkach, A. Yimit, A.Y. Lee, M. Riffle, M. Costanzo, D. Jaschob, J.A. Hendry, J. Ou, J. Moffat, and C. Boone et al. Dissecting DNA damage response pathways by analysing protein localization and abundance changes during DNA replication stress Nat. Cell Biol. 14 2012 966 976
72. T. Makhnevych, P. Wong, O. Pogoutse, F.J. Vizeacoumar, J.F. Greenblatt, A. Emili, and W.A. Houry Hsp110 is required for spindle length control J. Cell Biol. 198 2012 623 636
73. A. Dasgupta, K.L. Ramsey, J.S. Smith, and D.T. Auble Sir Antagonist 1 (San1) is a ubiquitin ligase J. Biol. Chem. 279 2004 26830 26838
74. R.G. Gardner, Z.W. Nelson, and D.E. Gottschling Degradation-mediated protein quality control in the nucleus Cell 120 2005 803 815
75. Y. Matsuo, H. Kishimoto, K. Tanae, K. Kitamura, S. Katayama, and M. Kawamukai Nuclear protein quality is regulated by the ubiquitin-proteasome system through the activity of Ubc4 and San1 in fission yeast J. Biol. Chem. 286 2011 13775 13790
76. E.K. Fredrickson, P.S. Gallagher, S.V. Clowes Candadai, and R.G. Gardner Substrate recognition in nuclear protein quality control degradation is governed by exposed hydrophobicity that correlates with aggregation and insolubility J. Biol. Chem. 288 2013 6130 6139
77. E.K. Fredrickson, J.C. Rosenbaum, M.N. Locke, T.I. Milac, and R.G. Gardner Exposed hydrophobicity is a key determinant of nuclear quality control degradation Mol. Biol. Cell 22 2011 2384 2395
78. J.C. Rosenbaum, E.K. Fredrickson, M.L. Oeser, C.M. Garrett-Engele, M.N. Locke, L.A. Richardson, Z.W. Nelson, E.D. Hetrick, T.I. Milac, and D.E. Gottschling et al. Disorder targets misorder in nuclear quality control degradation: a disordered ubiquitin ligase directly recognizes its misfolded substrates Mol. Cell 41 2011 93 106
79. J.W. Heck, S.K. Cheung, and R.Y. Hampton Cytoplasmic protein quality control degradation mediated by parallel actions of the E3 ubiquitin ligases Ubr1 and San1 Proc. Natl. Acad. Sci. USA 107 2010 1106 1111
80. C.J. Guerriero, K.F. Weiberth, and J.L. Brodsky Hsp70 targets a cytoplasmic quality control substrate to the San1p ubiquitin ligase J. Biol. Chem. 288 2013 18506 18520
81. R. Prasad, S. Kawaguchi, and D.T. Ng A nucleus-based quality control mechanism for cytosolic proteins Mol. Biol. Cell 21 2010 2117 2127
82. M. Deng, and M. Hochstrasser Spatially regulated ubiquitin ligation by an ER/nuclear membrane ligase Nature 443 2006 827 831
83. T. Ravid, S.G. Kreft, and M. Hochstrasser Membrane and soluble substrates of the Doa10 ubiquitin ligase are degraded by distinct pathways EMBO J. 25 2006 533 543
84. R. Swanson, M. Locher, and M. Hochstrasser A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and Matalpha2 repressor degradation Genes Dev. 15 2001 2660 2674
85. N. Furth, O. Gertman, A. Shiber, O.S. Alfassy, I. Cohen, M.M. Rosenberg, N.K. Doron, A. Friedler, and T. Ravid Exposure of bipartite hydrophobic signal triggers nuclear quality control of Ndc10 at the endoplasmic reticulum/nuclear envelope Mol. Biol. Cell 22 2011 4726 4739
86. C.S. Hwang, A. Shemorry, and A. Varshavsky N-terminal acetylation of cellular proteins creates specific degradation signals Science 327 2010 973 977
87. R. Prasad, S. Kawaguchi, and D.T. Ng Biosynthetic mode can determine the mechanism of protein quality control Biochem. Biophys. Res. Commun. 425 2012 689 695
88. Z. Wang, and G. Prelich Quality control of a transcriptional regulator by SUMO-targeted degradation Mol. Cell. Biol. 29 2009 1694 1706
89. F. Kriegenburg, V. Jakopec, E.G. Poulsen, S.V. Nielsen, A. Roguev, N. Krogan, C. Gordon, U. Fleig, and R. Hartmann-Petersen A chaperone-assisted degradation pathway targets kinetochore proteins to ensure genome stability PLoS Genet. 10 2014 e1004140
90. S. Ghaemmaghami, W.K. Huh, K. Bower, R.W. Howson, A. Belle, N. Dephoure, E.K. O'Shea, and J.S. Weissman Global analysis of protein expression in yeast Nature 425 2003 737 741
91. S. Marguerat, A. Schmidt, S. Codlin, W. Chen, R. Aebersold, and J. Bahler Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells Cell 151 2012 671 683
92. S.H. Park, Y. Kukushkin, R. Gupta, T. Chen, A. Konagai, M.S. Hipp, M. Hayer-Hartl, and F.U. Hartl PolyQ proteins interfere with nuclear degradation of cytosolic proteins by sequestering the Sis1p chaperone Cell 154 2013 134 145
93. S.J. Russell, K.A. Steger, and S.A. Johnston Subcellular localization, stoichiometry, and protein levels of 26 S proteasome subunits in yeast J. Biol. Chem. 274 1999 21943 21952
94. D. Laporte, B. Salin, B. Daignan-Fornier, and I. Sagot Reversible cytoplasmic localization of the proteasome in quiescent yeast cells J. Cell Biol. 181 2008 737 745
95. M.H. Weberruss, A.F. Savulescu, J. Jando, T. Bissinger, A. Harel, M.H. Glickman, and C. Enenkel Blm10 facilitates nuclear import of proteasome core particles EMBO J. 32 2013 2697 2707
96. K. Takeda, and M. Yanagida Regulation of nuclear proteasome by Rhp6/Ubc2 through ubiquitination and destruction of the sensor and anchor Cut8 Cell 122 2005 393 405
97. H. Tatebe, and M. Yanagida Cut8, essential for anaphase, controls localization of 26S proteasome, facilitating destruction of cyclin and Cut2 Curr. Biol. 10 2000 1329 1338
98. L. Chen, L. Romero, S.M. Chuang, V. Tournier, K.K. Joshi, J.A. Lee, G. Kovvali, and K. Madura Sts1 plays a key role in targeting proteasomes to the nucleus J. Biol. Chem. 286 2011 3104 3118
99. K. Takeda, N.K. Tonthat, T. Glover, W. Xu, E.V. Koonin, M. Yanagida, and M.A. Schumacher Implications for proteasome nuclear localization revealed by the structure of the nuclear proteasome tether protein Cut8 Proc. Natl. Acad. Sci. USA 108 2011 16950 16955
100. N. Bader, T. Jung, and T. Grune The proteasome and its role in nuclear protein maintenance Exp. Gerontol. 42 2007 864 870
101. A. von Mikecz The nuclear ubiquitin-proteasome system J. Cell Sci. 119 2006 1977 1984
102. E.J. Bennett, N.F. Bence, R. Jayakumar, and R.R. Kopito Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation Mol. Cell 17 2005 351 365
103. A. Catic, C.Y. Suh, C.T. Hill, L. Daheron, T. Henkel, K.W. Orford, D.M. Dombkowski, T. Liu, X.S. Liu, and D.T. Scadden Genome-wide map of nuclear protein degradation shows NCoR1 turnover as a key to mitochondrial gene regulation Cell 155 2013 1380 1395
104. O. Ullrich, T. Reinheckel, N. Sitte, R. Hass, T. Grune, and K.J. Davies Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones Proc. Natl. Acad. Sci. USA 96 1999 6223 6228
105. J.S. Andersen, Y.W. Lam, A.K. Leung, S.E. Ong, C.E. Lyon, A.I. Lamond, and M. Mann Nucleolar proteome dynamics Nature 433 2005 77 83
106. Y.W. Lam, A.I. Lamond, M. Mann, and J.S. Andersen Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins Curr. Biol. 17 2007 749 760
107. A. Iwata, Y. Nagashima, L. Matsumoto, T. Suzuki, T. Yamanaka, H. Date, K. Deoka, N. Nukina, and S. Tsuji Intranuclear degradation of polyglutamine aggregates by the ubiquitin-proteasome system J. Biol. Chem. 284 2009 9796 9803
108. A. Janer, E. Martin, M.P. Muriel, M. Latouche, H. Fujigasaki, M. Ruberg, A. Brice, Y. Trottier, and A. Sittler PML clastosomes prevent nuclear accumulation of mutant ataxin-7 and other polyglutamine proteins J. Cell Biol. 174 2006 65 76
109. A.F. Savulescu, H. Shorer, O. Kleifeld, I. Cohen, R. Gruber, M.H. Glickman, and A. Harel Nuclear import of an intact preassembled proteasome particle Mol. Biol. Cell 22 2011 880 891
110. I. Kouranti, J.R. McLean, A. Feoktistova, P. Liang, A.E. Johnson, R.H. Roberts-Galbraith, and K.L. Gould A global census of fission yeast deubiquitinating enzyme localization and interaction networks reveals distinct compartmentalization profiles and overlapping functions in endocytosis and polarity PLoS Biol. 8 2010 e1000471
111. S.D. Boyd, K.Y. Tsai, and T. Jacks An intact HDM2 RING-finger domain is required for nuclear exclusion of p53 Nat. Cell Biol. 2 2000 563 568
112. J. Cornett, F. Cao, C.E. Wang, C.A. Ross, G.P. Bates, S.H. Li, and X.J. Li Polyglutamine expansion of huntingtin impairs its nuclear export Nat. Genet. 37 2005 198 204
113. P.J. Skinner, B.T. Koshy, C.J. Cummings, I.A. Klement, K. Helin, A. Servadio, H.Y. Zoghbi, and H.T. Orr Ataxin-1 with an expanded glutamine tract alters nuclear matrix-associated structures Nature 389 1997 971 974
114. M. Reichelt, L. Wang, M. Sommer, J. Perrino, A.M. Nour, N. Sen, A. Baiker, L. Zerboni, and A.M. Arvin Entrapment of viral capsids in nuclear PML cages is an intrinsic antiviral host defense against varicella-zoster virus PLoS Pathog. 7 2011 e1001266
115. C.M. Livingston, M.F. Ifrim, A.E. Cowan, and S.K. Weller Virus-Induced Chaperone-Enriched (VICE) domains function as nuclear protein quality control centers during HSV-1 infection PLoS Pathog. 5 2009 e1000619
116. L. Latonen, H.M. Moore, B. Bai, S. Jaamaa, and M. Laiho Proteasome inhibitors induce nucleolar aggregation of proteasome target proteins and polyadenylated RNA by altering ubiquitin availability Oncogene 30 2011 790 805
117. E.A. Nollen, F.A. Salomons, J.F. Brunsting, J.J. van der Want, O.C. Sibon, and H.H. Kampinga Dynamic changes in the localization of thermally unfolded nuclear proteins associated with chaperone-dependent protection Proc. Natl. Acad. Sci. USA 98 2001 12038 12043
118. T.E. Audas, M.D. Jacob, and S. Lee Immobilization of proteins in the nucleolus by ribosomal intergenic spacer noncoding RNA Mol. Cell 45 2012 147 157
119. T. Nystrom Spatial protein quality control and the evolution of lineage-specific ageing Phil. Trans. R. Soc. Lond. Series B. Biol. Sci. 366 2011 71 75
120. D.A. Sinclair, and L. Guarente Extrachromosomal rDNA circles-a cause of aging in yeast Cell 91 1997 1033 1042
121. A. Khmelinskii, P.J. Keller, H. Lorenz, E. Schiebel, and M. Knop Segregation of yeast nuclear pores Nature 466 2010 E1
122. G. Pereira, T.U. Tanaka, K. Nasmyth, and E. Schiebel Modes of spindle pole body inheritance and segregation of the Bfa1p-Bub2p checkpoint protein complex EMBO J. 20 2001 6359 6370
123. M. Hotz, C. Leisner, D. Chen, C. Manatschal, T. Wegleiter, J. Ouellet, D. Lindstrom, D.E. Gottschling, J. Vogel, and Y. Barral Spindle pole bodies exploit the mitotic exit network in metaphase to drive their age-dependent segregation Cell 148 2012 958 972
124. A. Iwata, J.C. Christianson, M. Bucci, L.M. Ellerby, N. Nukina, L.S. Forno, and R.R. Kopito Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation Proc. Natl. Acad. Sci. USA 102 2005 13135 13140
125. A. Rose, and C. Schlieker Alternative nuclear transport for cellular protein quality control Trends Cell Biol. 22 2012 509 514
126. D.C. Johnson, and J.D. Baines Herpesviruses remodel host membranes for virus egress Nat. Rev. Microbiol. 9 2011 382 394
127. S.D. Speese, J. Ashley, V. Jokhi, J. Nunnari, R. Barria, Y. Li, B. Ataman, A. Koon, Y.T. Chang, and Q. Li et al. Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling Cell 149 2012 832 846
128. M. Costanzo, A. Baryshnikova, J. Bellay, Y. Kim, E.D. Spear, C.S. Sevier, H. Ding, J.L. Koh, K. Toufighi, and S. Mostafavi et al. The genetic landscape of a cell Science 327 2010 425 431
129. C.J. Ryan, A. Roguev, K. Patrick, J. Xu, H. Jahari, Z. Tong, P. Beltrao, M. Shales, H. Qu, and S.R. Collins et al. Hierarchical modularity and the evolution of genetic interactomes across species Mol. Cell 46 2012 691 704
130. D.L. Lafontaine A 'garbage can' for ribosomes: how eukaryotes degrade their ribosomes Trends Biochem. Sci. 35 2010 267 277
131. C. Dez, J. Houseley, and D. Tollervey Surveillance of nuclear-restricted pre-ribosomes within a subnucleolar region of Saccharomyces cerevisiae EMBO J. 25 2006 1534 1546
132. E. Shor, C.A. Fox, and J.R. Broach The yeast environmental stress response regulates mutagenesis induced by proteotoxic stress PLoS Genet. 9 2013 e1003680
133. G. Chen, W.D. Bradford, C.W. Seidel, and R. Li Hsp90 stress potentiates rapid cellular adaptation through induction of aneuploidy Nature 482 2012 246 250
134. A.B. Oromendia, S.E. Dodgson, and A. Amon Aneuploidy causes proteotoxic stress in yeast Genes Dev. 26 2012 2696 2708
135. N. Pavelka, G. Rancati, J. Zhu, W.D. Bradford, A. Saraf, L. Florens, B.W. Sanderson, G.L. Hattem, and R. Li Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast Nature 468 2010 321 325
136. B.H. Toyama, J.N. Savas, S.K. Park, M.S. Harris, N.T. Ingolia, J.R. Yates 3rd, and M.W. Hetzer Identification of long-lived proteins reveals exceptional stability of essential cellular structures Cell 154 2013 971 982
137. C. Soto Unfolding the role of protein misfolding in neurodegenerative diseases Nat. Rev. Neurosci. 4 2003 49 60
138. G. Schilling, A.V. Savonenko, A. Klevytska, J.L. Morton, S.M. Tucker, M. Poirier, A. Gale, N. Chan, V. Gonzales, and H.H. Slunt et al. Nuclear-targeting of mutant huntingtin fragments produces Huntington's disease-like phenotypes in transgenic mice Hum. Mol. Genet. 13 2004 1599 1610
139. P. Manzerra, and I.R. Brown The neuronal stress response: nuclear translocation of heat shock proteins as an indicator of hyperthermic stress Exp. Cell Res. 229 1996 35 47