Hsp90 inhibits α-synuclein aggregation by interacting with soluble oligomers

Journal of Molecular Biology

Volumn 425, Issue 22, 2013, Pages 4614-4628

  Daturpalli, Soumya ^a   Waudby, Christopher A ^b   Meehan, Sarah ^a   Jackson, Sophie E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

aggregation; amyloid; cytoprotective; Parkinson's disease; thioflavin T assay

Indexed keywords

ALPHA SYNUCLEIN; HEAT SHOCK PROTEIN 90; OLIGOMER;

ARTICLE; LEWY BODY; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

EID: 84886728386     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.08.006     Document Type: Article

References (57)

1. H. Braak, U. Rüb, W.P. Gai, and K. Del Tredici Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen J Neural Transm 110 2003 517 536
2. C.A. Davie A review of Parkinson's disease Br Med Bull 86 2008 109 127
3. A.B. Singleton, M. Farrer, J. Johnson, A. Singleton, S. Hague, and J. Kachergus α-Synuclein locus triplication causes Parkinson's disease Science 302 2003 841-841
4. J. Li, V.N. Uversky, and A.L. Fink Effect of familial Parkinson's disease point mutations A30P and A53T on the structural properties, aggregation, and fibrillation of human α-synuclein Biochemistry 40 2001 11604 11613
5. I. Cantuti-Castelvetri, J. Klucken, M. Ingelsson, K. Ramasamy, P.J. McLean, and M.P. Frosch Alpha-synuclein and chaperones in dementia with Lewy bodies J Neuropathol Exp Neurol 64 2005 1058 1066
6. W. Dauer, N. Kholodilov, M. Vila, A.C. Trillat, R. Goodchild, and K.E. Larsen Resistance of α-synuclein null mice to the parkinsonian neurotoxin MPTP Proc Natl Acad Sci USA 99 2002 14524 14529
7. K.A. Conway, J.D. Harper, and P.T. Lansbury Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease Nat Med 4 1998 1318 1320
8. K.A. Conway, S.J. Lee, J.C. Rochet, T.T. Ding, R.E. Williamson, and P.T. Lansbury Acceleration of oligomerization, not fibrillization, is a shared property of both α-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy Proc Natl Acad Sci USA 97 2000 571 576
9. C.W. Bertoncini, C.O. Fernandez, C. Griesinger, T.M. Jovin, and M. Zweckstetter Familial mutants of α-synuclein with increased neurotoxicity have a destabilized conformation J Biol Chem 280 2005 30649 30652
10. M.M. Dedmon, K. Lindorff-Larsen, J. Christodoulou, M. Vendruscolo, and C.M. Dobson Mapping long-range interactions in α-synuclein using spin-label NMR and ensemble molecular dynamics simulations J Am Chem Soc 127 2005 476 477
11. H. Heise, M.S. Celej, S. Becker, D. Riedel, A. Pelah, and A. Kumar Solid-state NMR reveals structural differences between fibrils of wild-type and disease-related A53T mutant α-synuclein J Mol Biol 380 2008 444 450
12. A.R. Saha, J. Hill, M.A. Utton, A.A. Asuni, S. Ackerley, and A.J. Grierson Parkinson's disease α-synuclein mutations exhibit defective axonal transport in cultured neurons J Cell Sci 117 2004 1017 1024
13. N. Ostrerova-Golts, L. Petrucelli, J. Hardy, J.M. Lee, M. Farer, and B. Wolozin The A53T α-synuclein mutation increases iron-dependent aggregation and toxicity J Neurosci 20 2000 6048 6054
14. S.J. Wood, J. Wypych, S. Steavenson, J.C. Louis, M. Citron, and A.L. Biere α-Synuclein fibrillogenesis is nucleation-dependent: implications for the pathogenesis of Parkinson's disease J Biol Chem 274 1999 19509 19512
15. M. Arimon, V. Grimminger, F. Sanz, and H.A. Lashuel Hsp104 targets multiple intermediates on the amyloid pathway and suppresses the seeding capacity of Aβ fibrils and protofibrils J Mol Biol 384 2008 1157 1173
16. C.J. Huang, H. Cheng, S. Hao, H. Zhou, X. Zhang, and J. Gao Heat shock protein 70 inhibits α-synuclein fibril formation via interactions with diverse intermediates J Mol Biol 364 2006 323 336
17. C. Roodveldt, C.W. Bertoncini, A. Andersson, A.T. van der Goot, S.T. Hsu, and R. Fernández-Montesinos Chaperone proteostasis in Parkinson's disease: stabilization of the Hsp70/α-synuclein complex by Hip EMBO J 28 2009 3758 3770
18. A. Rekas, L. Jankova, D.C. Thorn, R. Cappai, and J.A. Carver Monitoring the prevention of amyloid fibril formation by α-crystallin. Temperature dependence and the nature of the aggregating species FEBS J 274 2007 6290 6304
19. C.A. Waudby, T.P. Knowles, G.L. Devlin, J.N. Skepper, H. Ecroyd, and J.A. Carver The interaction of αB-crystallin with mature α-synuclein amyloid fibrils inhibits their elongation Biophys J 98 2010 843 851
20. P. Csermely, T. Schnaider, C. Soti, Z. Prohászka, and G. Nardai The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review Pharmacol Ther 79 1998 129 168
21. J.C. Young, I. Moarefi, and F.U. Hartl Hsp90: a specialized but essential protein-folding tool J Cell Biol 154 2001 267 273
22. S.H. McLaughlin, H.W. Smith, and S.E. Jackson Stimulation of the weak ATPase activity of human Hsp90 by a client protein J Mol Biol 315 2002 787 798
23. S.C. Onuoha, S.R. Mukund, E.T. Coulstock, B. Sengerovà, J. Shaw, and S.H. McLaughlin Mechanistic studies on Hsp90 inhibition by ansamycin derivatives J Mol Biol 372 2007 287 297
24. M.P. Hernandez, W.P. Sullivan, and D.O. Toft The assembly and intermolecular properties of the Hsp70-Hop-Hsp90 molecular chaperone complex J Biol Chem 277 2002 38294 38304
25. B.D. Johnson, R.J. Schumacher, E.D. Ross, and D.O. Toft Hop modulates Hsp70/Hsp90 interactions in protein folding J Biol Chem 273 1998 3679 3686
26. J. Trepel, M. Mollapour, G. Giaccone, and L. Neckers Targeting the dynamic HSP90 complex in cancer Nat Rev Cancer 10 2010 537 549
27. P. Putcha, K.M. Danzer, L.R. Kranich, A. Scott, M. Silinski, and S. Mabbett Brain-permeable small-molecule inhibitors of Hsp90 prevent α-synuclein oligomer formation and rescue α-synuclein-induced toxicity J Pharmacol Exp Ther 332 2010 849 857
28. J.Y. Zou, Y. Guo, T. Guettouche, D.F. Smith, and R. Voellmy Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1 Cell 94 1998 471 480
29. J. Kakimura, Y. Kitamura, K. Takata, M. Umeki, S. Suzuki, and K. Shibagaki Microglial activation and amyloid-β clearance induced by exogenous heat-shock proteins FASEB J 16 2002 601
30. P.J. McLean, H. Kawamata, S. Shariff, J. Hewett, N. Sharma, and K. Ueda TorsinA and heat shock proteins act as molecular chaperones: suppression of alpha-synuclein aggregation J Neurochem 83 2002 846 854
31. K. Uryu, C. Richter-Landsberg, W. Welch, E. Sun, O. Goldbaum, and E.H. Norris Convergence of heat shock protein 90 with ubiquitin in filamentous α-synuclein inclusions of α-synucleinopathies Am J Pathol 168 2006 947 961
32. G.S. Jeon, S.W. Park, D.W. Kim, J.H. Seo, J. Cho, and S.Y. Lim Glial expression of the 90-kDa heat shock protein (HSP90) and the 94-kDa glucose-regulated protein (GRP94) following an excitotoxic lesion in the mouse hippocampus Glia 48 2004 250 258
33. S.F. Falsone, A.J. Kungl, A. Rek, R. Cappai, and K. Zangger The molecular chaperone Hsp90 modulates intermediate steps of amyloid assembly of the Parkinson-related protein α-synuclein J Biol Chem 284 2009 31190 31199
34. B. Panaretou, C. Prodromou, S.M. Roe, R. O'Brien, J.E. Ladbury, and P.W. Piper ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo EMBO J 17 1998 4829 4836
35. C.K. Vaughan, P.W. Piper, L.H. Pearl, and C. Prodromou A common conformationally coupled ATPase mechanism for yeast and human cytoplasmic HSP90s FEBS J 276 2009 199 209
36. V.N. Uversky, J. Li, and A.L. Fink Evidence for a partially folded intermediate in α-synuclein fibril formation J Biol Chem 276 2001 10737 10744
37. D.W. Dickson, H.A. Crystal, C. Bevona, W. Honer, I. Vincent, and P. Davies Correlations of synaptic and pathological markers with cognition of the elderly Neurobiol Aging 16 1995 285 298
38. T.P.J. Knowles, C.A. Waudby, G.L. Devlin, S.I. Cohen, A. Aguzzi, and M. Vendruscolo An analytical solution to the kinetics of breakable filament assembly Science 326 2009 1533 1537
39. R. Kayed, E. Head, F. Sarsoza, T. Saing, C.W. Cotman, and M. Necula Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers Mol Neurodegener 2 2007 18
40. V.N. Uversky α-Synuclein misfolding and neurodegenerative diseases Curr Protein Pept Sci 9 2008 507 540
41. J.M. Barral, S.A. Broadley, G. Schaffar, and F.U. Hartl Roles of molecular chaperones in protein misfolding diseases Semin Cell Dev Biol 15 2004 17 29
42. U. Jakob, H. Lilie, I. Meyer, and J. Buchner Transient interaction of Hsp90 with early unfolding intermediates of citrate synthase. Implications for heat shock in vivo J Biol Chem 270 1995 7288 7294
43. O. Genest, M. Reidy, T.O. Street, J.R. Hoskins, J.L. Camberg, and D.A. Agard Uncovering a region of heat shock protein 90 important for client binding in E. coli and chaperone function in yeast Mol Cell 49 2013 464 473
44. C.K. Vaughan, U. Gohlke, F. Sobott, V.M. Good, M.M. Ali, and C. Prodromou Structure of an Hsp90-Cdc37-Cdk4 complex Mol Cell 23 2006 697 707
45. L. Giehm, C.L. Oliveira, G. Christiansen, J.S. Pedersen, and D.E. Otzen SDS-induced fibrillation of α-synuclein: an alternative fibrillation pathway J Mol Biol 401 2010 115 133
46. S. Campioni, B. Mannini, M. Zampagni, A. Pensalfini, C. Parrini, and E. Evangelisti A causative link between the structure of aberrant protein oligomers and their toxicity Nat Chem Biol 6 2010 140 147
47. M.S. Celej, R. Sarroukh, E. Goormaghtigh, G.D. Fidelio, J.M. Ruysschaert, and V. Raussens Toxic prefibrillar α-synuclein amyloid oligomers adopt a distinctive antiparallel β-sheet structure Biochem J 443 2012 719 726
48. S.K. Wandinger, K. Richter, and J. Buchner The Hsp90 chaperone machinery J Biol Chem 283 2008 18473 18477
49. T.O. Street, L.A. Lavery, and D.A. Agard Substrate binding drives large-scale conformational changes in the Hsp90 molecular chaperone Mol Cell 42 2011 96 105
50. N. Cremades, S.I. Cohen, E. Deas, A.Y. Abramov, A.Y. Chen, and A. Orte Direct observation of the interconversion of normal and toxic forms of α-synuclein Cell 149 2012 1048 1059
51. H.R. Xie, L.S. Hu, and G.Y. Li SH-SY5Y human neuroblastoma cell line: in vitro cell model of dopaminergic neurons in Parkinson's disease Chin Med J 123 2010 1086 1092
52. S.H. McLaughlin, L.A. Ventouras, B. Lobbezoo, and S.E. Jackson Independent ATPase activity of Hsp90 subunits creates a flexible assembly platform J Mol Biol 344 2004 813 826
53. S.C. Onuoha, E.T. Coulstock, J.G. Grossmann, and S.E. Jackson Structural studies on the co-chaperone Hop and its complexes with Hsp90 J Mol Biol 379 2008 732 744
54. R.C. Rivers, J.R. Kumita, G.G. Tartaglia, M.M. Dedmon, A. Pawar, and M. Vendruscolo Molecular determinants of the aggregation behavior of alpha- and beta-synuclein Protein Sci 17 2008 887 898
55. C.A. Waudby, T.P. Knowles, G.L. Devlin, J.N. Skepper, H. Ecroyd, and J.A. Carver The interaction of αB-crystallin with mature α-synuclein amyloid fibrils inhibits their elongation Biophys J 98 2010 843 851
56. É. Karászi, K. Jakab, L. Homolya, G. Szakács, Z. Holló, and B. Telek Calcein assay for multidrug resistance reliably predicts therapy response and survival rate in acute myeloid leukaemia Br J Haematol 112 2001 308 314
57. M.V. Berridge, P.M. Herst, and A.S. Tan Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction Biotechnol Annu Rev 11 2005 127 152