Mechanistic and Structural Insights into the Prion-Disaggregase Activity of Hsp104

Journal of Molecular Biology

Volumn 428, Issue 9, 2016, Pages 1870-1885

  Sweeny, Elizabeth A ^a   Shorter, James ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

disaggregase; Hsp104; prion

Indexed keywords

ADENOSINE TRIPHOSPHATE; HEAT SHOCK PROTEIN 104; SACCHAROMYCES CEREVISIAE PROTEIN; SUP35 PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN; HSP104 PROTEIN, S CEREVISIAE; MACROMOLECULE; PRION;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; DISAGGREGASE ACTIVITY; DRUG ACTIVITY; DRUG STRUCTURE; HUMAN; NONHUMAN; PRION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN SECRETION; PROTEIN SYNTHESIS; REVIEW; BIOLOGICAL MODEL; CHEMISTRY; ENZYMOLOGY; HYDROLYSIS; MACROMOLECULE; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SMALL ANGLE SCATTERING;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; HEAT-SHOCK PROTEINS; HYDROLYSIS; MACROMOLECULAR SUBSTANCES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PRIONS; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SCATTERING, SMALL ANGLE;

EID: 84960926930     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.11.016     Document Type: Review

References (167)

1. M.E. DeSantis, E.H. Leung, E.A. Sweeny, M.E. Jackrel, M. Cushman-Nick, A. Neuhaus-Follini, and et al. Operational plasticity enables Hsp104 to disaggregate diverse amyloid and nonamyloid clients Cell 151 2012 778 793
2. J. Shorter Hsp104: A weapon to combat diverse neurodegenerative disorders Neurosignals 16 2008 63 74
3. S. Vashist, M. Cushman, and J. Shorter Applying Hsp104 to protein-misfolding disorders Biochem. Cell Biol. 88 2010 1 13
4. M. Cushman-Nick, N.M. Bonini, and J. Shorter Hsp104 suppresses polyglutamine-induced degeneration post onset in a Drosophila MJD/SCA3 model PLoS Genet. 9 2013 e1003781
5. M.L. Duennwald, A. Echeverria, and J. Shorter Small heat shock proteins potentiate amyloid dissolution by protein disaggregases from yeast and humans PLoS Biol. 10 2012 e1001346
6. C. Lo Bianco, J. Shorter, E. Regulier, H. Lashuel, T. Iwatsubo, S. Lindquist, and et al. Hsp104 antagonizes alpha-synuclein aggregation and reduces dopaminergic degeneration in a rat model of Parkinson disease J. Clin. Invest. 118 2008 3087 3097
7. M.E. Jackrel, M.E. Desantis, B.A. Martinez, L.M. Castellano, R.M. Stewart, K.A. Caldwell, and et al. Potentiated hsp104 variants antagonize diverse proteotoxic misfolding events Cell 156 2014 170 182
8. J. Carmichael, J. Chatellier, A. Woolfson, C. Milstein, A.R. Fersht, and D.C. Rubinsztein Bacterial and yeast chaperones reduce both aggregate formation and cell death in mammalian cell models of Huntington's disease Proc. Natl. Acad. Sci. U. S. A. 97 2000 9701 9705
9. C. Vacher, L. Garcia-Oroz, and D.C. Rubinsztein Overexpression of yeast Hsp104 reduces polyglutamine aggregation and prolongs survival of a transgenic mouse model of Huntington's disease Hum. Mol. Genet. 14 2005 3425 3433
10. S.H. Satyal, E. Schmidt, K. Kitagawa, N. Sondheimer, S. Lindquist, J.M. Kramer, and et al. Polyglutamine aggregates alter protein folding homeostasis in Caenorhabditis elegans Proc. Natl. Acad. Sci. U. S. A. 97 2000 5750 5755
11. Y.H. Liu, Y.L. Han, J. Song, Y. Wang, Y.Y. Jing, Q. Shi, and et al. Heat shock protein 104 inhibited the fibrillization of prion peptide 106-126 and disassembled prion peptide 106-126 fibrils in vitro Int. J. Biochem. Cell Biol. 43 2011 768 774
12. Y. Kim, J.H. Park, J.Y. Jang, H. Rhim, and S. Kang Characterization and Hsp104-induced artificial clearance of familial ALS-related SOD1 aggregates Biochem. Biophys. Res. Commun. 434 2013 521 526
13. V. Perrin, E. Regulier, T. Abbas-Terki, R. Hassig, E. Brouillet, P. Aebischer, and et al. Neuroprotection by Hsp104 and Hsp27 in lentiviral-based rat models of Huntington's disease Mol. Ther. 15 2007 903 911
14. M.P. Torrente, and J. Shorter The metazoan protein disaggregase and amyloid depolymerase system: Hsp110, Hsp70, Hsp40, and small heat shock proteins Prion 7 2013 457 463
15. Y.S. Eisele, C. Monteiro, C. Fearns, S.E. Encalada, R.L. Wiseman, E.T. Powers, and et al. Targeting protein aggregation for the treatment of degenerative diseases Nat. Rev. Drug Discov. 14 2015 759 780
16. F. Arnold, J. Schnell, O. Zirafi, C. Sturzel, C. Meier, T. Weil, and et al. Naturally occurring fragments from two distinct regions of the prostatic acid phosphatase form amyloidogenic enhancers of HIV infection J. Virol. 86 2012 1244 1249
17. J. Munch, E. Rucker, L. Standker, K. Adermann, C. Goffinet, M. Schindler, and et al. Semen-derived amyloid fibrils drastically enhance HIV infection Cell 131 2007 1059 1071
18. N.R. Roan, J. Munch, N. Arhel, W. Mothes, J. Neidleman, A. Kobayashi, and et al. The cationic properties of SEVI underlie its ability to enhance human immunodeficiency virus infection J. Virol. 83 2009 73 80
19. L.M. Castellano, S.M. Bart, V.M. Holmes, D. Weissman, and J. Shorter Repurposing Hsp104 to antagonize seminal amyloid and counter HIV infection Chem. Biol. 22 2015 1074 1086
20. L.M. Castellano, and J. Shorter The surprising role of amyloid fibrils in HIV infection Biology 1 2012 58 80
21. L.M. Castellano, R.M. Hammond, V.M. Holmes, D. Weissman, and J. Shorter Epigallocatechin-3-gallate rapidly remodels pAP85-120, SEM1(45-107), and SEM2(49-107) seminal amyloid fibrils Biol. Open 4 2015 1206 1212
22. E. Lump, L.M. Castellano, C. Meier, J. Seeliger, N. Erwin, B. Sperlich, and et al. A molecular tweezer antagonizes seminal amyloids and HIV infection Elife 2015 10.7554/eLife.05397
23. S.J. Shire Formulation and manufacturability of biologics Curr. Opin. Biotechnol. 20 2009 708 714
24. M. Lebendiker, and T. Danieli Production of prone-to-aggregate proteins FEBS Lett. 588 2014 236 246
25. D.A. Parsell, A.S. Kowal, M.A. Singer, and S. Lindquist Protein disaggregation mediated by heat-shock protein Hsp104 Nature 372 1994 475 478
26. J.R. Glover, and S. Lindquist Hsp104, Hsp70, and Hsp40: A novel chaperone system that rescues previously aggregated proteins Cell 94 1998 73 82
27. J. Shorter, and S. Lindquist Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers Science 304 2004 1793 1797
28. S. DiSalvo, A. Derdowski, J.A. Pezza, and T.R. Serio Dominant prion mutants induce curing through pathways that promote chaperone-mediated disaggregation Nat. Struct. Mol. Biol. 18 2011 486 492
29. C.L. Klaips, M.L. Hochstrasser, C.R. Langlois, and T.R. Serio Spatial quality control bypasses cell-based limitations on proteostasis to promote prion curing Elife 2014 10.7554/eLife.04288
30. +] by causing dissolution of the prion seeds Eukaryot. Cell 13 2014 635 647
31. J. Shorter, and S. Lindquist Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions EMBO J. 27 2008 2712 2724
32. J. Shorter, and S. Lindquist Destruction or potentiation of different prions catalyzed by similar Hsp104 remodeling activities Mol. Cell 23 2006 425 438
33. T. Haslberger, A. Zdanowicz, I. Brand, J. Kirstein, K. Turgay, A. Mogk, and et al. Protein disaggregation by the AAA + chaperone ClpB involves partial threading of looped polypeptide segments Nat. Struct. Mol. Biol. 15 2008 641 650
34. J. Weibezahn, P. Tessarz, C. Schlieker, R. Zahn, Z. Maglica, S. Lee, and et al. Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB Cell 119 2004 653 665
35. R. Lum, M. Niggemann, and J.R. Glover Peptide and protein binding in the axial channel of Hsp104. Insights into the mechanism of protein unfolding J. Biol. Chem. 283 2008 30139 30150
36. R. Lum, J.M. Tkach, E. Vierling, and J.R. Glover Evidence for an unfolding/threading mechanism for protein disaggregation by Saccharomyces cerevisiae Hsp104 J. Biol. Chem. 279 2004 29139 29146
37. P. Tessarz, A. Mogk, and B. Bukau Substrate threading through the central pore of the Hsp104 chaperone as a common mechanism for protein disaggregation and prion propagation Mol. Microbiol. 68 2008 87 97
38. M.E. Jackrel, and J. Shorter Potentiated Hsp104 variants suppress toxicity of diverse neurodegenerative disease-linked proteins Dis. Model. Mech. 7 2014 1175 1184
39. M.E. Jackrel, and J. Shorter Reversing deleterious protein aggregation with re-engineered protein disaggregases Cell Cycle 13 2014 1379 1383
40. M.E. Jackrel, and J. Shorter Engineering enhanced protein disaggregases for neurodegenerative disease Prion 9 2015 90 109
41. E.A. Sweeny, M.E. Jackrel, M.S. Go, M.A. Sochor, B.M. Razzo, M.E. DeSantis, and et al. The Hsp104 N-terminal domain enables disaggregase plasticity and potentiation Mol. Cell 57 2015 836 849
42. A.J. Erives, and J.S. Fassler Metabolic and chaperone gene loss marks the origin of animals: Evidence for Hsp104 and Hsp78 chaperones sharing mitochondrial enzymes as clients PLoS One 10 2015 e0117192
43. E.C. Schirmer, J.R. Glover, M.A. Singer, and S. Lindquist HSP100/Clp proteins: A common mechanism explains diverse functions Trends Biochem. Sci. 21 1996 289 296
44. C.J. Shih, and M.C. Lai Analysis of the AAA + chaperone clpB gene and stress-response expression in the halophilic methanogenic archaeon Methanohalophilus portucalensis Microbiology 153 2007 2572 2583
45. C.J. Shih, and M.C. Lai Differentially expressed genes after hyper- and hypo-salt stress in the halophilic archaeon Methanohalophilus portucalensis Can. J. Microbiol. 56 2010 295 307
46. A. Finka, S.K. Sharma, and P. Goloubinoff Multi-layered molecular mechanisms of polypeptide holding, unfolding and disaggregation by HSP70/HSP110 chaperones Front. Mol. Biosci. 2 2015 29
47. R.U. Mattoo, S.K. Sharma, S. Priya, A. Finka, and P. Goloubinoff Hsp110 is a bona fide chaperone using ATP to unfold stable misfolded polypeptides and reciprocally collaborate with Hsp70 to solubilize protein aggregates J. Biol. Chem. 288 2013 21399 21411
48. H. Rampelt, J. Kirstein-Miles, N.B. Nillegoda, K. Chi, S.R. Scholz, R.I. Morimoto, and et al. Metazoan Hsp70 machines use Hsp110 to power protein disaggregation EMBO J. 31 2012 4221 4235
49. J. Shorter The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 and Hsp40 to catalyze protein disaggregation and reactivation in a cell-free system PLoS One 6 2011 e26319
50. X. Gao, M. Carroni, C. Nussbaum-Krammer, A. Mogk, N.B. Nillegoda, A. Szlachcic, and et al. Human Hsp70 disaggregase reverses Parkinson's-linked alpha-synuclein amyloid fibrils Mol. Cell 59 2015 781 793
51. N.B. Nillegoda, J. Kirstein, A. Szlachcic, M. Berynskyy, A. Stank, F. Stengel, and et al. Crucial HSP70 co-chaperone complex unlocks metazoan protein disaggregation Nature 524 2015 247 251
52. G.A. Newby, and S. Lindquist Blessings in disguise: Biological benefits of prion-like mechanisms Trends Cell Biol. 23 2013 251 259
53. S. Alberti, R. Halfmann, O. King, A. Kapila, and S. Lindquist A systematic survey identifies prions and illuminates sequence features of prionogenic proteins Cell 137 2009 146 158
54. J.S. Byers, and D.F. Jarosz Pernicious pathogens or expedient elements of inheritance: The significance of yeast prions PLoS Pathog. 10 2014 e1003992
55. D.M. Garcia, and D.F. Jarosz Rebels with a cause: Molecular features and physiological consequences of yeast prions FEMS Yeast Res. 14 2014 136 147
56. R. Halfmann, D.F. Jarosz, S.K. Jones, A. Chang, A.K. Lancaster, and S. Lindquist Prions are a common mechanism for phenotypic inheritance in wild yeasts Nature 482 2012 363 368
57. J. Shorter, and S. Lindquist Prions as adaptive conduits of memory and inheritance Nat. Rev. Genet. 6 2005 435 450
58. Y. Sanchez, and S.L. Lindquist HSP104 required for induced thermotolerance Science 248 1990 1112 1115
59. Y. Sanchez, J. Taulien, K.A. Borkovich, and S. Lindquist Hsp104 is required for tolerance to many forms of stress EMBO J. 11 1992 2357 2364
60. E.W.J. Wallace, J.L. Kear-Scott, E.V. Pilipenko, M.H. Schwartz, P.R. Laskowski, A.E. Rojek, and et al. Reversible, specific, active aggregates of endogenous proteins assemble upon heat stress Cell 162 2015 1286 1298
61. P. Tessarz, M. Schwarz, A. Mogk, and B. Bukau The yeast AAA + chaperone Hsp104 is part of a network that links the actin cytoskeleton with the inheritance of damaged proteins Mol. Cell. Biol. 29 2009 3738 3745
62. V. Andersson, S. Hanzen, B. Liu, M. Molin, and T. Nystrom Enhancing protein disaggregation restores proteasome activity in aged cells Aging 5 2013 802 812
63. N. Erjavec, L. Larsson, J. Grantham, and T. Nystrom Accelerated aging and failure to segregate damaged proteins in Sir2 mutants can be suppressed by overproducing the protein aggregation-remodeling factor Hsp104p Genes Dev. 21 2007 2410 2421
64. S.M. Hill, X. Hao, B. Liu, and T. Nystrom Life-span extension by a metacaspase in the yeast Saccharomyces cerevisiae Science 344 2014 1389 1392
65. B. Liu, L. Larsson, A. Caballero, X. Hao, D. Oling, J. Grantham, and et al. The polarisome is required for segregation and retrograde transport of protein aggregates Cell 140 2010 257 267
66. B. Liu, L. Larsson, V. Franssens, X. Hao, S.M. Hill, V. Andersson, and et al. Segregation of protein aggregates involves actin and the polarity machinery Cell 147 2011 959 961
67. C. Zhou, B.D. Slaughter, J.R. Unruh, A. Eldakak, B. Rubinstein, and R. Li Motility and segregation of Hsp104-associated protein aggregates in budding yeast Cell 147 2011 1186 1196
68. 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
69. S. Pattabiraman, and D. Kaganovich Imperfect asymmetry: The mechanism governing asymmetric partitioning of damaged cellular components during mitosis Bioarchitecture 4 2014 203 209
70. J. Saarikangas, and Y. Barral Protein aggregates are associated with replicative aging without compromising protein quality control Elife 2015 10.7554/eLife.06197
71. M. Coelho, A. Dereli, A. Haese, S. Kuhn, L. Malinovska, M.E. DeSantis, and et al. Fission yeast does not age under favorable conditions, but does so after stress Curr. Biol. 23 2013 1844 1852
72. M.E. DeSantis, and J. Shorter The elusive middle domain of Hsp104 and ClpB: Location and function Biochim. Biophys. Acta 2012 1823 29 39
73. V. Grimminger-Marquardt, and H.A. Lashuel Structure and function of the molecular chaperone Hsp104 from yeast Biopolymers 93 2010 252 276
74. P.I. Hanson, and S.W. Whiteheart AAA + proteins: Have engine, will work Nat. Rev. Mol. Cell Biol. 6 2005 519 529
75. D.A. Parsell, A.S. Kowal, and S. Lindquist Saccharomyces cerevisiae Hsp104 protein. Purification and characterization of ATP-induced structural changes J. Biol. Chem. 269 1994 4480 4487
76. E.C. Schirmer, C. Queitsch, A.S. Kowal, D.A. Parsell, and S. Lindquist The ATPase activity of Hsp104, effects of environmental conditions and mutations J. Biol. Chem. 273 1998 15546 15552
77. E.C. Schirmer, D.M. Ware, C. Queitsch, A.S. Kowal, and S.L. Lindquist Subunit interactions influence the biochemical and biological properties of Hsp104 Proc. Natl. Acad. Sci. U. S. A. 98 2001 914 919
78. D.A. Parsell, Y. Sanchez, J.D. Stitzel, and S. Lindquist Hsp104 is a highly conserved protein with two essential nucleotide-binding sites Nature 353 1991 270 273
79. M. Carroni, E. Kummer, Y. Oguchi, P. Wendler, D.K. Clare, I. Sinning, and et al. Head-to-tail interactions of the coiled-coil domains regulate ClpB activity and cooperation with Hsp70 in protein disaggregation Elife 3 2014 e02481
80. S. Lee, B. Sielaff, J. Lee, and F.T. Tsai CryoEM structure of Hsp104 and its mechanistic implication for protein disaggregation Proc. Natl. Acad. Sci. U. S. A. 107 2010 8135 8140
81. P. Wendler, J. Shorter, C. Plisson, A.G. Cashikar, S. Lindquist, and H.R. Saibil Atypical AAA + subunit packing creates an expanded cavity for disaggregation by the protein-remodeling factor Hsp104 Cell 131 2007 1366 1377
82. P. Wendler, J. Shorter, D. Snead, C. Plisson, D.K. Clare, S. Lindquist, and et al. Motor mechanism for protein threading through Hsp104 Mol. Cell 34 2009 81 92
83. S. Lee, M.E. Sowa, Y.H. Watanabe, P.B. Sigler, W. Chiu, M. Yoshida, and et al. The structure of ClpB: A molecular chaperone that rescues proteins from an aggregated state Cell 115 2003 229 240
84. M.E. DeSantis, E.A. Sweeny, D. Snead, E.H. Leung, M.S. Go, K. Gupta, and et al. Conserved distal loop residues in the Hsp104 and ClpB middle domain contact nucleotide-binding domain 2 and enable Hsp70-dependent protein disaggregation J. Biol. Chem. 289 2014 848 867
85. D. Xia, L. Esser, S.K. Singh, F. Guo, and M.R. Maurizi Crystallographic investigation of peptide binding sites in the N-domain of the ClpA chaperone J. Struct. Biol. 146 2004 166 179
86. J. Li, and B. Sha Crystal structure of the E. coli Hsp100 ClpB N-terminal domain Structure 11 2003 323 328
87. A. Pietrosiuk, E.D. Lenherr, S. Falk, G. Bonemann, J. Kopp, H. Zentgraf, and et al. Molecular basis for the unique role of the AAA + chaperone ClpV in type VI protein secretion J. Biol. Chem. 286 2011 30010 30021
88. F. Wang, Z. Mei, Y. Qi, C. Yan, Q. Hu, J. Wang, and et al. Structure and mechanism of the hexameric MecA-ClpC molecular machine Nature 471 2011 331 335
89. J.H. Lo, T.A. Baker, and R.T. Sauer Characterization of the N-terminal repeat domain of Escherichia coli ClpA-A class I Clp/HSP100 ATPase Protein Sci. 10 2001 551 559
90. A. Mogk, C. Schlieker, C. Strub, W. Rist, J. Weibezahn, and B. Bukau Roles of individual domains and conserved motifs of the AAA + chaperone ClpB in oligomerization, ATP hydrolysis, and chaperone activity J. Biol. Chem. 278 2003 17615 17624
91. T. Ishikawa, M.R. Maurizi, and A.C. Steven The N-terminal substrate-binding domain of ClpA unfoldase is highly mobile and extends axially from the distal surface of ClpAP protease J. Struct. Biol. 146 2004 180 188
92. S. Lee, J.M. Choi, and F.T. Tsai Visualizing the ATPase cycle in a protein disaggregating machine: Structural basis for substrate binding by ClpB Mol. Cell 25 2007 261 271
93. S.K. Park, K.I. Kim, K.M. Woo, J.H. Seol, K. Tanaka, A. Ichihara, and et al. Site-directed mutagenesis of the dual translational initiation sites of the clpB gene of Escherichia coli and characterization of its gene products J. Biol. Chem. 268 1993 20170 20174
94. P. Beinker, S. Schlee, Y. Groemping, R. Seidel, and J. Reinstein The N terminus of ClpB from Thermus thermophilus is not essential for the chaperone activity J. Biol. Chem. 277 2002 47160 47166
95. M.E. Barnett, M. Nagy, S. Kedzierska, and M. Zolkiewski The amino-terminal domain of ClpB supports binding to strongly aggregated proteins J. Biol. Chem. 280 2005 34940 34945
96. N. Tanaka, Y. Tani, H. Hattori, T. Tada, and S. Kunugi Interaction of the N-terminal domain of Escherichia coli heat-shock protein ClpB and protein aggregates during chaperone activity Protein Sci. 13 2004 3214 3221
97. S.M. Doyle, J.R. Hoskins, and S. Wickner DnaK chaperone-dependent disaggregation by caseinolytic peptidase B (ClpB) mutants reveals functional overlap in the N-terminal domain and nucleotide-binding domain-1 pore tyrosine J. Biol. Chem. 287 2012 28470 28479
98. S. Mizuno, Y. Nakazaki, M. Yoshida, and Y.H. Watanabe Orientation of the amino-terminal domain of ClpB affects the disaggregation of the protein FEBS J. 279 2012 1474 1484
99. T. Zhang, E.A. Ploetz, M. Nagy, S.M. Doyle, S. Wickner, P.E. Smith, and et al. Flexible connection of the N-terminal domain in ClpB modulates substrate binding and the aggregate reactivation efficiency Proteins 80 2012 2758 2768
100. G.C. Hung, and D.C. Masison N-terminal domain of yeast Hsp104 chaperone is dispensable for thermotolerance and prion propagation but necessary for curing prions by Hsp104 overexpression Genetics 173 2006 611 620
101. S.M. Doyle, J. Shorter, M. Zolkiewski, J.R. Hoskins, S. Lindquist, and S. Wickner Asymmetric deceleration of ClpB or Hsp104 ATPase activity unleashes protein-remodeling activity Nat. Struct. Mol. Biol. 14 2007 114 122
102. L.M. Iyer, D.D. Leipe, E.V. Koonin, and L. Aravind Evolutionary history and higher order classification of AAA + ATPases J. Struct. Biol. 146 2004 11 31
103. J.P. Erzberger, and J.M. Berger Evolutionary relationships and structural mechanisms of AAA + proteins Annu. Rev. Biophys. Biomol. Struct. 35 2006 93 114
104. D.A. Hattendorf, and S.L. Lindquist Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants EMBO J. 21 2002 12 21
105. J. Krzewska, G. Konopa, and K. Liberek Importance of two ATP-binding sites for oligomerization, ATPase activity and chaperone function of mitochondrial Hsp78 protein J. Mol. Biol. 314 2001 901 910
106. 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
107. T. Haslberger, J. Weibezahn, R. Zahn, S. Lee, F.T. Tsai, B. Bukau, and et al. M domains couple the ClpB threading motor with the DnaK chaperone activity Mol. Cell 25 2007 247 260
108. B. Sielaff, and F.T. Tsai The M-domain controls Hsp104 protein remodeling activity in an Hsp70/Hsp40-dependent manner J. Mol. Biol. 402 2010 30 37
109. M.E. Jackrel, K. Yee, A. Tariq, A.I. Chen, and J. Shorter Disparate mutations confer therapeutic gain of Hsp104 function ACS Chem. Biol. 2015 10.1021/acschembio.5b00765
110. M. Miot, M. Reidy, S.M. Doyle, J.R. Hoskins, D.M. Johnston, O. Genest, and et al. Species-specific collaboration of heat shock proteins (Hsp) 70 and 100 in thermotolerance and protein disaggregation Proc. Natl. Acad. Sci. U. S. A. 108 2011 6915 6920
111. F. Seyffer, E. Kummer, Y. Oguchi, J. Winkler, M. Kumar, R. Zahn, and et al. Hsp70 proteins bind Hsp100 regulatory M domains to activate AAA + disaggregase at aggregate surfaces Nat. Struct. Mol. Biol. 19 2012 1347 1355
112. J. Lee, J.H. Kim, A.B. Biter, B. Sielaff, S. Lee, and F.T. Tsai Heat shock protein (Hsp) 70 is an activator of the Hsp104 motor Proc. Natl. Acad. Sci. U. S. A. 110 2013 8513 8518
113. Y. Oguchi, E. Kummer, F. Seyffer, M. Berynskyy, B. Anstett, R. Zahn, and et al. A tightly regulated molecular toggle controls AAA + disaggregase Nat. Struct. Mol. Biol. 19 2012 1338 1346
114. J.E. Dulle, K.C. Stein, and H.L. True Regulation of the hsp104 middle domain activity is critical for yeast prion propagation PLoS One 9 2014 e87521
115. R.G. Mackay, C.W. Helsen, J.M. Tkach, and J.R. Glover The C-terminal extension of Saccharomyces cerevisiae Hsp104 plays a role in oligomer assembly Biochemistry 47 2008 1918 1927
116. T. Abbas-Terki, O. Donze, P.A. Briand, and D. Picard Hsp104 interacts with Hsp90 cochaperones in respiring yeast Mol. Cell. Biol. 21 2001 7569 7575
117. A.G. Cashikar, E.C. Schirmer, D.A. Hattendorf, J.R. Glover, M.S. Ramakrishnan, D.M. Ware, and et al. Defining a pathway of communication from the C-terminal peptide binding domain to the N-terminal ATPase domain in a AAA protein Mol. Cell 9 2002 751 760
118. J.M. Tkach, and J.R. Glover Amino acid substitutions in the C-terminal AAA + module of Hsp104 prevent substrate recognition by disrupting oligomerization and cause high temperature inactivation J. Biol. Chem. 279 2004 35692 35701
119. H. Saibil Chaperone machines for protein folding, unfolding and disaggregation Nat. Rev. Mol. Cell Biol. 14 2013 630 642
120. A. Mogk, E. Kummer, and B. Bukau Cooperation of Hsp70 and Hsp100 chaperone machines in protein disaggregation Front. Mol. Biosci. 2 2015 22
121. T. Li, C.L. Weaver, J. Lin, E.C. Duran, J.M. Miller, and A.L. Lucius Escherichia coli ClpB is a non-processive polypeptide translocase Biochem. J. 470 2015 39 52
122. M. Reidy, M. Miot, and D.C. Masison Prokaryotic chaperones support yeast prions and thermotolerance and define disaggregation machinery interactions Genetics 192 2012 185 193
123. M. Reidy, R. Sharma, S. Shastry, B.L. Roberts, I. Albino-Flores, S. Wickner, and et al. Hsp40s specify functions of Hsp104 and Hsp90 protein chaperone machines PLoS Genet. 10 2014 e1004720
124. K.A. Tipton, K.J. Verges, and J.S. Weissman In vivo monitoring of the prion replication cycle reveals a critical role for Sis1 in delivering substrates to Hsp104 Mol. Cell 32 2008 584 591
125. A.H. Yuan, S.J. Garrity, E. Nako, and A. Hochschild Prion propagation can occur in a prokaryote and requires the ClpB chaperone Elife 3 2014 e02949
126. F. Gasset-Rosa, A.S. Coquel, M. Moreno-Del Alamo, P. Chen, X. Song, A.M. Serrano, and et al. Direct assessment in bacteria of prionoid propagation and phenotype selection by Hsp70 chaperone Mol. Microbiol. 91 2014 1070 1087
127. V.V. Kushnirov, and M.D. Ter-Avanesyan Structure and replication of yeast prions Cell 94 1998 13 16
128. P. Satpute-Krishnan, S.X. Langseth, and T.R. Serio Hsp104-dependent remodeling of prion complexes mediates protein-only inheritance PLoS Biol. 5 2007 e24
129. J.E. Dulle, R.E. Bouttenot, L.A. Underwood, and H.L. True Soluble oligomers are sufficient for transmission of a yeast prion but do not confer phenotype J. Cell Biol. 203 2013 197 204
130. J.E. Dulle, and H.L. True Low activity of select Hsp104 mutants is sufficient to propagate unstable prion variants Prion 7 2013 394 403
131. P. Wendler, and H.R. Saibil Cryo electron microscopy structures of Hsp100 proteins: Crowbars in or out? Biochem. Cell Biol. 88 2010 89 96
132. B. Chen, T.A. Sysoeva, S. Chowdhury, L. Guo, S. De Carlo, J.A. Hanson, and et al. Engagement of arginine finger to ATP triggers large conformational changes in NtrC1 AAA + ATPase for remodeling bacterial RNA polymerase Structure 18 2010 1420 1430
133. J.M. Davies, H. Tsuruta, A.P. May, and W.I. Weis Conformational changes of p97 during nucleotide hydrolysis determined by small-angle x-ray scattering Structure 13 2005 183 195
134. A. Roll-Mecak, and R.D. Vale Structural basis of microtubule severing by the hereditary spastic paraplegia protein spastin Nature 451 2008 363 367
135. T.A. Sysoeva, S. Chowdhury, L. Guo, and B.T. Nixon Nucleotide-induced asymmetry within ATPase activator ring drives sigma54-RNAP interaction and ATP hydrolysis Genes Dev. 27 2013 2500 2511
136. E. Arias-Palomo, V.L. O'Shea, I.V. Hood, and J.M. Berger The bacterial DnaC helicase loader is a DnaB ring breaker Cell 153 2013 438 448
137. A.S. Meyer, J.R. Gillespie, D. Walther, I.S. Millet, S. Doniach, and J. Frydman Closing the folding chamber of the eukaryotic chaperonin requires the transition state of ATP hydrolysis Cell 113 2003 369 381
138. B. Nagar, and J. Kuriyan SAXS and the working protein Structure 13 2005 169 170
139. R. Krishnan, and S.L. Lindquist Structural insights into a yeast prion illuminate nucleation and strain diversity Nature 435 2005 765 772
140. P.M. Tessier, and S. Lindquist Prion recognition elements govern nucleation, strain specificity and species barriers Nature 447 2007 556 561
141. +] Nat. Struct. Mol. Biol. 16 2009 598 605
142. H. Wang, M.L. Duennwald, B.E. Roberts, L.M. Rozeboom, Y.L. Zhang, A.D. Steele, and et al. Direct and selective elimination of specific prions and amyloids by 4,5-dianilinophthalimide and analogs Proc. Natl. Acad. Sci. U. S. A. 105 2008 7159 7164
143. B.E. Roberts, M.L. Duennwald, H. Wang, C. Chung, N.P. Lopreiato, E.A. Sweeny, and et al. A synergistic small-molecule combination directly eradicates diverse prion strain structures Nat. Chem. Biol. 5 2009 936 946
144. J. Shorter Emergence and natural selection of drug-resistant prions Mol. BioSyst. 6 2010 1115 1130
145. M.E. DeSantis, and J. Shorter Hsp104 drives "protein-only" positive selection of Sup35 prion strains encoding strong [PSI(+)] Chem. Biol. 19 2012 1400 1410
146. J. Dong, C.E. Castro, M.C. Boyce, M.J. Lang, and S. Lindquist Optical trapping with high forces reveals unexpected behaviors of prion fibrils Nat. Struct. Mol. Biol. 17 2010 1422 1430
147. +] prion by overexpression of 104-kDa heat shock protein (Hsp104) J. Biol. Chem. 287 2012 542 556
148. S.V. Paushkin, V.V. Kushnirov, V.N. Smirnov, and M.D. Ter-Avanesyan Propagation of the yeast prion-like [psi +] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor EMBO J. 15 1996 3127 3134
149. Y.O. Chernoff, S.L. Lindquist, B. Ono, S.G. Inge-Vechtomov, and S.W. Liebman Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi +] Science 268 1995 880 884
150. J. O'Driscoll, D. Clare, and H. Saibil Prion aggregate structure in yeast cells is determined by the Hsp104-Hsp110 disaggregase machinery J. Cell Biol. 211 2015 145 158
151. C.W. Helsen, and J.R. Glover A new perspective on Hsp104-mediated propagation and curing of the yeast prion [PSI (+)] Prion 6 2012 234 239
152. +] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104 J. Biol. Chem. 278 2003 49636 49643
153. J. Winkler, J. Tyedmers, B. Bukau, and A. Mogk Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation J. Cell Biol. 198 2012 387 404
154. M. Reidy, and D.C. Masison Yeast prions help identify and define chaperone interaction networks Curr. Pharm. Biotechnol. 15 2014 1008 1018
155. M.L. Wohlever, T.A. Baker, and R.T. Sauer Roles of the N domain of the AAA + Lon protease in substrate recognition, allosteric regulation and chaperone activity Mol. Microbiol. 91 2014 66 78
156. R.T. Sauer, and T.A. Baker AAA + proteases: ATP-fueled machines of protein destruction Annu. Rev. Biochem. 80 2011 587 612
157. J. Hinnerwisch, B.G. Reid, W.A. Fenton, and A.L. Horwich Roles of the N-domains of the ClpA unfoldase in binding substrate proteins and in stable complex formation with the ClpP protease J. Biol. Chem. 280 2005 40838 40844
158. S. Cranz-Mileva, F. Imkamp, K. Kolygo, Z. Maglica, W. Kress, and E. Weber-Ban The flexible attachment of the N-domains to the ClpA ring body allows their use on demand J. Mol. Biol. 378 2008 412 424
159. G. Thibault, and W.A. Houry Role of the N-terminal domain of the chaperone ClpX in the recognition and degradation of lambda phage protein O J. Phys. Chem. B 116 2012 6717 6724
160. D. Barthelme, J.Z. Chen, J. Grabenstatter, T.A. Baker, and R.T. Sauer Architecture and assembly of the archaeal Cdc48∗20S proteasome Proc. Natl. Acad. Sci. U. S. A. 111 2014 E1687 E1694
161. F. Zhang, Z. Wu, P. Zhang, G. Tian, D. Finley, and Y. Shi Mechanism of substrate unfolding and translocation by the regulatory particle of the proteasome from Methanocaldococcus jannaschii Mol. Cell 34 2009 485 496
162. A. Gerega, B. Rockel, J. Peters, T. Tamura, W. Baumeister, and P. Zwickl VAT, the thermoplasma homolog of mammalian p97/VCP, is an N domain-regulated protein unfoldase J. Biol. Chem. 280 2005 42856 42862
163. A. Rothballer, N. Tzvetkov, and P. Zwickl Mutations in p97/VCP induce unfolding activity FEBS Lett. 581 2007 1197 1201
164. D.I. Svergun, M.V. Petoukhov, and M.H. Koch Determination of domain structure of proteins from x-ray solution scattering Biophys. J. 80 2001 2946 2953
165. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and et al. UCSF Chimera - A visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
166. R. Rosenzweig, P. Farber, A. Velyvis, E. Rennella, M.P. Latham, and L.E. Kay ClpB N-terminal domain plays a regulatory role in protein disaggregation Proc. Natl. Acad. Sci. U. S. A. 2015 10.1073/pnas.1512783112
167. R. Rosenzweig, S. Morad, A. Zarrine-Afsar, J.R. Glover, and L.E. Kay Unraveling the mechanism of protein disaggregation through a ClpB-DnaK interaction Science 339 2013 1080 1083