Small heat shock proteins potentiate amyloid dissolution by protein disaggregases from yeast and humans

PLoS Biology

Volumn 10, Issue 6, 2012, Pages

  Duennwald, Martin L ^a   Echeverria, AnaLisa ^a   Shorter, James ^b  

^a BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID; CHAPERONE; FUNGAL PROTEIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 104; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 26; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 42; HEAT SHOCK PROTEIN 70; PROTEIN SUP35; UNCLASSIFIED DRUG; HSP26 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SMALL HEAT SHOCK PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DEPOLYMERIZATION; DISSOLUTION; DOWN REGULATION; EX VIVO STUDY; HUMAN; IN VITRO STUDY; NONHUMAN; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; TEMPERATURE SENSITIVITY; UPREGULATION; YEAST; CHEMISTRY; METABOLISM; PRION; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

AMYLOID; HEAT-SHOCK PROTEINS; HEAT-SHOCK PROTEINS, SMALL; HUMANS; PRIONS; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84863683967     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001346     Document Type: Article

References (95)

1. Cushman M, Johnson B. S, King O. D, Gitler A. D, Shorter J, (2010) Prion-like disorders: blurring the divide between transmissibility and infectivity. J Cell Sci 123: 1191-1201.
2. Goldschmidt L, Teng P. K, Riek R, Eisenberg D, (2010) Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proc Natl Acad Sci U S A 107: 3487-3492.
3. Chiti F, Dobson C. M, (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333-366.
4. Fowler D. M, Koulov A. V, Alory-Jost C, Marks M. S, Balch W. E, et al. (2006) Functional amyloid formation within mammalian tissue. PLoS Biol 4: e6 doi:10.1371/journal.pbio.0040006.
5. Watt B, van Niel G, Fowler D. M, Hurbain I, Luk K. C, et al. (2009) N-terminal domains elicit formation of functional Pmel17 amyloid fibrils. J Biol Chem 284: 35543-35555.
6. Fowler D. M, Koulov A. V, Balch W. E, Kelly J. W, (2007) Functional amyloid-from bacteria to humans. Trends Biochem Sci 32: 217-224.
7. Cegelski L, Pinkner J. S, Hammer N. D, Cusumano C. K, Hung C. S, et al. (2009) Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat Chem Biol 5: 913-919.
8. Shorter J, Lindquist S, (2005) Prions as adaptive conduits of memory and inheritance. Nat Rev Genet 6: 435-450.
9. Si K, Choi Y. B, White-Grindley E, Majumdar A, Kandel E. R, (2010) Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell 140: 421-435.
10. True H. L, Lindquist S. L, (2000) A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407: 477-483.
11. Tyedmers J, Madariaga M. L, Lindquist S, (2008) Prion switching in response to environmental stress. PLoS Biol 6: e294 doi:10.1371/journal.pbio.0060294.
12. Eaglestone S. S, Cox B. S, Tuite M. F, (1999) Translation termination efficiency can be regulated in Saccharomyces cerevisiae by environmental stress through a prion-mediated mechanism. EMBO J 18: 1974-1981.
13. Halfmann R, Jarosz D. F, Jones S. K, Chang A, Lancaster A. K, et al. (2012) Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482: 363-368.
14. Suzuki G, Shimazu N, Tanaka M, (2012) A yeast prion, Mod5, promotes acquired drug resistance and cell survival under environmental stress. Science 336: 355-359.
15. Scheibel T, Parthasarathy R, Sawicki G, Lin X. M, Jaeger H, et al. (2003) Conducting nanowires built by controlled self-assembly of amyloid fibers and selective metal deposition. Proc Natl Acad Sci U S A 100: 4527-4532.
16. Knowles T. P, Oppenheim T. W, Buell A. K, Chirgadze D. Y, Welland M. E, (2010) Nanostructured films from hierarchical self-assembly of amyloidogenic proteins. Nat Nanotechnol 5: 204-207.
17. Knowles T. P, Buehler M. J, (2011) Nanomechanics of functional and pathological amyloid materials. Nat Nanotechnol 6: 469-479.
18. Raynes J. K, Pearce F. G, Meade S. J, Gerrard J. A, (2011) Immobilization of organophosphate hydrolase on an amyloid fibril nanoscaffold: towards bioremediation and chemical detoxification. Biotechnol Prog 27: 360-367.
19. Baldwin A. J, Bader R, Christodoulou J, MacPhee C. E, Dobson C. M, et al. (2006) Cytochrome display on amyloid fibrils. J Am Chem Soc 128: 2162-2163.
20. Haslbeck M, Franzmann T, Weinfurtner D, Buchner J, (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12: 842-846.
21. Waters E. R, Lee G. J, Vierling E, (1996) Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 47: 325-338.
22. McHaourab H. S, Godar J. A, Stewart P. L, (2009) Structure and mechanism of protein stability sensors: chaperone activity of small heat shock proteins. Biochemistry 48: 3828-3837.
23. Ecroyd H, Carver J. A, (2009) Crystallin proteins and amyloid fibrils. Cell Mol Life Sci 66: 62-81.
24. Lee G. J, Roseman A. M, Saibil H. R, Vierling E, (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J 16: 659-671.
25. Mogk A, Schlieker C, Friedrich K. L, Schonfeld H. J, Vierling E, et al. (2003) Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J Biol Chem 278: 31033-31042.
26. 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.
27. Haslbeck M, Walke S, Stromer T, Ehrnsperger M, White H. E, et al. (1999) Hsp26: a temperature-regulated chaperone. EMBO J 18: 6744-6751.
28. Haslbeck M, Braun N, Stromer T, Richter B, Model N, et al. (2004) Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J 23: 638-649.
29. Benesch J. L, Aquilina J. A, Baldwin A. J, Rekas A, Stengel F, et al. (2010) The quaternary organization and dynamics of the molecular chaperone HSP26 are thermally regulated. Chem Biol 17: 1008-1017.
30. White H. E, Orlova E. V, Chen S, Wang L, Ignatiou A, et al. (2006) Multiple distinct assemblies reveal conformational flexibility in the small heat shock protein Hsp26. Structure 14: 1197-1204.
31. Franzmann T. M, Menhorn P, Walter S, Buchner J, (2008) Activation of the chaperone Hsp26 is controlled by the rearrangement of its thermosensor domain. Mol Cell 29: 207-216.
32. Franzmann T. M, Wuhr M, Richter K, Walter S, Buchner J, (2005) The activation mechanism of Hsp26 does not require dissociation of the oligomer. J Mol Biol 350: 1083-1093.
33. Cashikar A. G, Duennwald M, Lindquist S. L, (2005) A chaperone pathway in protein disaggregation. Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J Biol Chem 280: 23869-23875.
34. Specht S, Miller S. B, 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.
35. Raman B, Ban T, Sakai M, Pasta S. Y, Ramakrishna T, et al. (2005) AlphaB-crystallin, a small heat-shock protein, prevents the amyloid fibril growth of an amyloid beta-peptide and beta2-microglobulin. Biochem J 392: 573-581.
36. Waudby C. A, Knowles T. P, Devlin G. L, Skepper J. N, Ecroyd H, et al. (2010) The interaction of alphaB-crystallin with mature alpha-synuclein amyloid fibrils inhibits their elongation. Biophys J 98: 843-851.
37. Rekas A, Adda C. G, Andrew Aquilina J, Barnham K. J, Sunde M, et al. (2004) Interaction of the molecular chaperone alphaB-crystallin with alpha-synuclein: effects on amyloid fibril formation and chaperone activity. J Mol Biol 340: 1167-1183.
38. Hsu A. L, Murphy C. T, Kenyon C, (2003) Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300: 1142-1145.
39. McGlinchey R. P, Kryndushkin D, Wickner R. B, (2011) Suicidal [PSI+] is a lethal yeast prion. Proc Natl Acad Sci U S A 108: 5337-5341.
40. Krishnan R, Lindquist S. L, (2005) Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 435: 765-772.
41. Roberts B. E, Duennwald M. L, Wang H, Chung C, Lopreiato N. P, et al. (2009) A synergistic small-molecule combination directly eradicates diverse prion strain structures. Nat Chem Biol 5: 936-946.
42. Wang H, Duennwald M. L, Roberts B. E, Rozeboom L. M, Zhang Y. L, et al. (2008) Direct and selective elimination of specific prions and amyloids by 4,5-dianilinophthalimide and analogs. Proc Natl Acad Sci U S A 105: 7159-7164.
43. Serio T. R, Cashikar A. G, Kowal A. S, Sawicki G. J, Moslehi J. J, et al. (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289: 1317-1321.
44. Tanaka M, Chien P, Naber N, Cooke R, Weissman J. S, (2004) Conformational variations in an infectious protein determine prion strain differences. Nature 428: 323-328.
45. Scheibel T, Lindquist S. L, (2001) The role of conformational flexibility in prion propagation and maintenance for Sup35p. Nat Struct Biol 8: 958-962.
46. Scheibel T, Bloom J, Lindquist S. L, (2004) The elongation of yeast prion fibers involves separable steps of association and conversion. Proc Natl Acad Sci U S A 101: 2287-2292.
47. Mukhopadhyay S, Krishnan R, Lemke E. A, Lindquist S, Deniz A. A, (2007) A natively unfolded yeast prion monomer adopts an ensemble of collapsed and rapidly fluctuating structures. Proc Natl Acad Sci U S A 104: 2649-2654.
48. Shorter J, Lindquist S, (2004) Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 304: 1793-1797.
49. Shorter J, Lindquist S, (2006) Destruction or potentiation of different prions catalyzed by similar Hsp104 remodeling activities. Mol Cell 23: 425-438.
50. DePace A. H, Weissman J. S, (2002) Origins and kinetic consequences of diversity in Sup35 yeast prion fibers. Nat Struct Biol 9: 389-396.
51. Tessier P. M, Lindquist S, (2007) Prion recognition elements govern nucleation, strain specificity and species barriers. Nature 447: 556-561.
52. Dong J, Castro C. E, Boyce M. C, Lang M. J, Lindquist S, (2010) Optical trapping with high forces reveals unexpected behaviors of prion fibrils. Nat Struct Mol Biol 17: 1422-1430.
53. Nevzglyadova O. V, Artemov A. V, Mittenberg A. G, Solovyov K. V, Kostyleva E. I, et al. (2009) Prion-associated proteins in yeast: comparative analysis of isogenic [PSI+] and [psi-] strains. Yeast 26: 611-631.
54. Lo Bianco C, Shorter J, Regulier E, Lashuel H, Iwatsubo T, et al. (2008) Hsp104 antagonizes alpha-synuclein aggregation and reduces dopaminergic degeneration in a rat model of Parkinson disease. J Clin Invest 118: 3087-3097.
55. Shorter J, Lindquist S, (2008) Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions. Embo J 27: 2712-2724.
56. DiSalvo S, Derdowski A, Pezza J. A, Serio T. R, (2011) Dominant prion mutants induce curing through pathways that promote chaperone-mediated disaggregation. Nat Struct Mol Biol 18: 486-492.
57. Sweeny E. A, Shorter J, (2008) Prion proteostasis: Hsp104 meets its supporting cast. Prion 2: 135-140.
58. Liu Y. H, Han Y. L, Song J, Wang Y, Jing Y. Y, et al. (2011) 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: 768-774.
59. Shorter J, (2008) Hsp104: a weapon to combat diverse neurodegenerative disorders. Neurosignals 16: 63-74.
60. Bieschke J, Cohen E, Murray A, Dillin A, Kelly J. W, (2009) A kinetic assessment of the C. elegans amyloid disaggregation activity enables uncoupling of disassembly and proteolysis. Protein Sci 18: 2231-2241.
61. Shorter J, (2011) The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 and Hsp40 to catalyze protein disaggregation and reactivation in a cell-free system. PLoS One 6: e26319 doi:10.1371/journal.pone.0026319.
62. Carulla N, Caddy G. L, Hall D. R, Zurdo J, Gairi M, et al. (2005) Molecular recycling within amyloid fibrils. Nature 436: 554-558.
63. Platt G. W, Xue W. F, Homans S. W, Radford S. E, (2009) Probing dynamics within amyloid fibrils using a novel capping method. Angew Chem Int Ed Engl 48: 5705-5707.
64. Sanchez L, Madurga S, Pukala T, Vilaseca M, Lopez-Iglesias C, et al. (2011) Abeta40 and Abeta42 amyloid fibrils exhibit distinct molecular recycling properties. J Am Chem Soc 133: 6505-6508.
65. Maji S. K, Perrin M. H, Sawaya M. R, Jessberger S, Vadodaria K, et al. (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325: 328-332.
66. Maji S. K, Schubert D, Rivier C, Lee S, Rivier J. E, et al. (2008) Amyloid as a depot for the formulation of long-acting drugs. PLoS Biol 6: e17 doi:10.1371/journal.pbio.0060017.
67. Carulla N, Zhou M, Giralt E, Robinson C. V, Dobson C. M, (2010) Structure and intermolecular dynamics of aggregates populated during amyloid fibril formation studied by hydrogen/deuterium exchange. Acc Chem Res 43: 1072-1079.
68. Olofsson A, Sauer-Eriksson A. E, Ohman A, (2009) Amyloid fibril dynamics revealed by combined hydrogen/deuterium exchange and nuclear magnetic resonance. Anal Biochem 385: 374-376.
69. Kayed R, Head E, Thompson J. L, McIntire T. M, Milton S. C, et al. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300: 486-489.
70. Derkatch I. L, Chernoff Y. O, Kushnirov V. V, Inge-Vechtomov S. G, Liebman S. W, (1996) Genesis and variability of [PSI+] prion factors in Saccharomyces cerevisiae. Genetics 144: 1375-1386.
71. Ter-Avanesyan M. D, Kushnirov V. V, Dagkesamanskaya A. R, Didichenko S. A, Chernoff Y. O, et al. (1993) Deletion analysis of the SUP35 gene of the yeast Saccharomyces cerevisiae reveals two non-overlapping functional regions in the encoded protein. Mol Microbiol 7: 683-692.
72. Patino M. M, Liu J. J, Glover J. R, Lindquist S, (1996) Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 273: 622-626.
73. Derkatch I. L, Bradley M. E, Hong J. Y, Liebman S. W, (2001) Prions affect the appearance of other prions: the story of [PIN+]. Cell 106: 171-182.
74. Derkatch I. L, Uptain S. M, Outeiro T. F, Krishnan R, Lindquist S. L, et al. (2004) Effects of Q/N-rich, polyQ, and non-polyQ amyloids on the de novo formation of the [PSI+] prion in yeast and aggregation of Sup35 in vitro. Proc Natl Acad Sci U S A 101: 12934-12939.
75. Bagriantsev S. N, Gracheva E. O, Richmond J. E, Liebman S. W, (2008) Variant-specific [PSI+] infection is transmitted by Sup35 polymers within [PSI+] aggregates with heterogeneous protein composition. Mol Biol Cell 19: 2433-2443.
76. Chernoff Y. O, Lindquist S. L, Ono B, Inge-Vechtomov S. G, Liebman S. W, (1995) Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [PSI+]. Science 268: 880-884.
77. Spillantini M. G, Schmidt M. L, Lee V. M, Trojanowski J. Q, Jakes R, et al. (1997) Alpha-synuclein in Lewy bodies. Nature 388: 839-840.
78. Luk K. C, Kehm V. M, Zhang B, O'Brien P, Trojanowski J. Q, et al. (2012) Intracerebral inoculation of pathological alpha-synuclein initiates a rapidly progressive neurodegenerative alpha-synucleinopathy in mice. J Exp Med 209: 975-986.
79. Scherzinger E, Lurz R, Turmaine M, Mangiarini L, Hollenbach B, et al. (1997) Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90: 549-558.
80. Wotton D, Freeman K, Shore D, (1996) Multimerization of Hsp42p, a novel heat shock protein of Saccharomyces cerevisiae, is dependent on a conserved carboxyl-terminal sequence. J Biol Chem 271: 2717-2723.
81. Kaganovich D, Kopito R, Frydman J, (2008) Misfolded proteins partition between two distinct quality control compartments. Nature 454: 1088-1095.
82. Tyedmers J, Treusch S, Dong J, McCaffery J. M, Bevis B, et al. (2010) Prion induction involves an ancient system for the sequestration of aggregated proteins and heritable changes in prion fragmentation. Proc Natl Acad Sci U S A 107: 8633-8638.
83. Yamamoto A, Lucas J. J, Hen R, (2000) Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell 101: 57-66.
84. Mallucci G, Dickinson A, Linehan J, Klohn P. C, Brandner S, et al. (2003) Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302: 871-874.
85. Vacher C, Garcia-Oroz L, Rubinsztein D. C, (2005) Overexpression of yeast hsp104 reduces polyglutamine aggregation and prolongs survival of a transgenic mouse model of Huntington's disease. Hum Mol Genet 14: 3425-3433.
86. Perrin V, Regulier E, Abbas-Terki T, Hassig R, Brouillet E, et al. (2007) Neuroprotection by Hsp104 and Hsp27 in lentiviral-based rat models of Huntington's disease. Mol Ther 15: 903-911.
87. Vashist S, Cushman M, Shorter J, (2010) Applying Hsp104 to protein-misfolding disorders. Biochem Cell Biol 88: 1-13.
88. Sweeny E. A, Desantis M. E, Shorter J, (2011) Purification of Hsp104, a protein disaggregase. J Vis Exp 55: e3190.
89. Raviol H, Bukau B, Mayer M. P, (2006) Human and yeast Hsp110 chaperones exhibit functional differences. FEBS Lett 580: 168-174.
90. Sadlish H, Rampelt H, Shorter J, Wegrzyn R. D, Andreasson C, et al. (2008) Hsp110 chaperones regulate prion formation and propagation in S. cerevisiae by two discrete activities. PLoS One 3: e1763 doi:10.1371/journal.pone.0001763.
91. Onodera O, Roses A. D, Tsuji S, Vance J. M, Strittmatter W. J, et al. (1996) Toxicity of expanded polyglutamine-domain proteins in Escherichia coli. FEBS Lett 399: 135-139.
92. Fredenburg R. A, Rospigliosi C, Meray R. K, Kessler J. C, Lashuel H. A, et al. (2007) The impact of the E46K mutation on the properties of alpha-synuclein in its monomeric and oligomeric states. Biochemistry 46: 7107-7118.
93. Douglas P. M, Treusch S, Ren H. Y, Halfmann R, Duennwald M. L, et al. (2008) Chaperone-dependent amyloid assembly protects cells from prion toxicity. Proc Natl Acad Sci U S A 105: 7206-7211.
94. Liu J. J, Sondheimer N, Lindquist S. L, (2002) Changes in the middle region of Sup35 profoundly alter the nature of epigenetic inheritance for the yeast prion [PSI+]. Proc Natl Acad Sci U S A 99 (Suppl 4): 16446-16453.
95. Arnold C. E, Wittrup K. D, (1994) The stress response to loss of signal recognition particle function in Saccharomyces cerevisiae. J Biol Chem 269: 30412-30418.