Heat Shock Protein 70 Inhibits α-Synuclein Fibril Formation via Interactions with Diverse Intermediates

Journal of Molecular Biology

Volumn 364, Issue 3, 2006, Pages 323-336

  Huang, Chunjuan ^a,b   Cheng, Han ^a,b   Hao, Shufeng ^a   Zhou, Hui ^a,b   Zhang, Xujia ^a   Gao, Jianen ^c   Sun, Qi Hong ^c   Hu, Hongyu ^d   Wang, Chih chen ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

^d INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

Author keywords

chaperone; fibril; heat shock protein 70; intermediate; synuclein

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ALPHA SYNUCLEIN; CHAPERONE; HEAT SHOCK PROTEIN 70; NUCLEAR PROTEIN;

ARTICLE; MEMBRANE PERMEABILITY; MEMBRANE VESICLE; NEUROFILAMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION;

EID: 33750873994     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.08.062     Document Type: Article

References (50)

1. Dauer W., and Przedborski S. Parkinson's disease: mechanisms and models. Neuron 39 (2003) 889-909
2. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276 (1997) 2045-2047
3. McKeith I.G., Perry E.K., and Perry R.H. Report of the second dementia withLewy body international workshop: diagnosis and treatment. Neurology 53 (1999) 902-905
4. Kruger R., Kuhn W., Muller T., Woitalla D., Graeber M., Kosel S., et al. Ala30Pro mutation in the gene encodingalpha-synuclein in Parkinson's disease. Nature Genet. 18 (1998) 106-108
5. Zarranz J.J., Alegre J., Gomez-Esteban J.C., Lezcano E., Ros R., Ampuero I., et al. The new mutation, E46K, of alpha-synucleincauses Parkinson and Lewy body dementia. Ann. Neurol. 55 (2004) 164-173
6. Feany M.B., and Bender W.W. A Drosophila model of Parkinson's disease. Nature 404 (2000) 394-398
7. Masliah E., Rockenstein E., Veinbergs I., Mallory M., Hashimoto M., Takeda A., et al. Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders. Science 287 (2000) 1265-1269
8. Kirik D., Annett L.E., Burger C., Muzyczka N., Mandel R.J., and Björklund A. Nigrostriatal α-synucleinopathy induced by viral vector-mediated overexpression of human α-synuclein: a new primate model of Parkinson's disease. Proc. Natl Acad. Sci. USA 100 (2003) 2884-2889
9. Conway K.A., Lee S.J., Rochet J.C., Ding T.T., Williamson R.E., and Lansbury Jr. P.T. 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
10. Conway K.A., Harper J.D., and Lansbury Jr. P.T. Accelerated in vitro fibril formation by a mutant α-synuclein linked to early-onset Parkinson disease. Nature Med. 4 (1998) 1318-1320
11. Volles M.J., Lee S.J., Rochet J.C., Shtilerman M.D., Ding T.T., Kessler J.C., and Lansbury Jr. P.T. Vesicle permeabilization by protofibrillar α-synuclein: implications for the pathogenesis and treatment of Parkinson's disease. Biochemistry 40 (2001) 7812-7819
12. Volles M.J., and Lansbury Jr. P.T. Vesicle permeabilzation by protofibrillar α-synuclein is sensitive to Parkinson's disease-linked mutations and occurs by a pore-like mechanism. Biochemistry 41 (2002) 4595-4602
13. Snyder H., Mensah K., Theisler C., Lee J., Matouschek A., and Wolozin B. Aggregated and monomeric α-synuclein bind to the S6′ proteasomal protein and inhibit proteasomal function. J. Biol. Chem. 278 (2003) 11753-11759
14. Lindersson E., Beedholms R., Hojrup P., Moos T., Gai W., Gendil K.B., and Jensen P.H. Proteasomal inhibition by α-synuclein filaments and oligomers. J. Biol. Chem. 279 (2004) 12924-12934
15. Macario A.J., Lange M., Ahring B.K., and De Macario E.C. Stress genes and proteins in the archaea. Microbiol. Mol. Biol. Rev. 63 (1999) 923-967
16. Hartl F.U., and Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295 (2002) 1852-1858
17. Uchida K., Kuroki K., Yoshino T., Yamaguchi R., and Tateyama S. Immunohistochemical study of constituents other than β-protein in canine senile plaques and cerebral amyloid angiopathy. Acta Neuropathologica 93 (1997) 277-284
18. Stenoien D.L., Cummings1 C.J., Adams H.P., Mancini M.G., Patel K., DeMartino G.N., et al. Polyglutamine-expanded androgen receptors form aggregates that sequester heat shock proteins, proteasome components and SRC-1, and are suppressed by the HDJ-2 chaperone. Hum. Mol. Genet. 8 (1999) 731-741
19. Auluck P.K., Chan H.Y., Trojanowski J.Q., Lee V.M., and Bonini N.M. Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295 (2002) 865-868
20. Muchowski P.J., Schaffar G., Sittler A., Wanker E.E., Hayer-Hartl M.K., and Hartl F.U. Hsp70 and Hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc. Natl Acad. Sci. USA 97 (2000) 7841-7846
21. Schaffar G., Breuer P., Boteva R., Behrends C., Tzvetkov N., Strippel N., et al. Cellular toxicity of polyglutamine expansion proteins: mechanism of transcription factor deactivation. Mol. Cell 15 (2004) 95-105
22. Klucken J., Shin Y., Masliah E., Hyman B.T., and Mclean P.J. Hsp70 reduces α-synuclein aggregation and toxicity. J. Biol. Chem. 279 (2004) 25497-25502
23. Dedmon M.M., Christodoulou J., Wilson M.R., and Dobson C.M. Heat shock protein 70 inhibits α-synuclein fibril formation via preferential binding to prefibrillar speices. J. Biol. Chem. 280 (2005) 14733-14740
24. Rekas A., Adda C.G., Aquilina J.A., Barnham K.J., Sunde M., Galatis D., et al. Interaction of the molecular chaperone αB-crystallin with α-synuclein: effects on amyloid fibril formation and chaperone activity. J. Mol. Biol. 340 (2004) 1167-1183
25. Freeman B.C., Myers M.P., Schumacher R., and Morimoto R.I. Identification of a regulatory motif in Hsp70 that affect ATPase activity, substrate binding and interaction with HDJ-1. EMBO J. 14 (1995) 2281-2292
26. Mayer M.P., Schröder H., Rüdiger S., Paal K., Laufen T., and Bukau B. Multi-step mechanism of substrate-binding determines chaperone activity of Hsp70. Nature Struct. Biol. 7 (2000) 586-593
27. Rüdiger S., Buchberger A., and Bukau B. Interaction of Hsp70 chaperones with substrates. Nature Struct. Biol. 4 (1997) 342-349
28. Miao B., Davis J., and Craig E.A. The Hsp70 family - an overview. In: Gething M.-J. (Ed). Guidebook to Molecular Chaperones and Protein - Folding Catalysts (1997), Oxford University Press, Oxford 3-13
29. Huang C.J., Ren G.P., Zhou H., and Wang C.C. A new method for purification of recombinant human α-synuclein in Escherichia coli. Protein Expr. Purif. 42 (2005) 173-177
30. Naiki H., Higuchi K., Hosokawa M., and Takeda T. Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1. Anal. Biochem. 177 (1989) 244-249
31. Wood S.J., Wypych J., Steavenson S., Louis J.C., Citron M., and Biere A.L. α-Synuclein fibrillogenesis is nucleation-dependent. J. Biol. Chem. 274 (1999) 19509-19512
32. Dedmon M.M., Lindorff-Larsen K., Christodoulou J., Vendruscolo M., and Dobson C.M. Mapping long-range interactions in α-synuclein using spin-label NMR and ensemble molecular dynamics simulations. J. Am. Chem. Soc. 127 (2005) 476-477
33. Uversky V.N., Li J., and Fink A.L. Evidence for a partially folded intermediate in a-synuclein fibril formation. J. Biol. Chem. 276 (2001) 10738-10744
34. Rochet J., Conway K.A., and Lansbury Jr. P.T. Inhibition of fibrillization and accumulation of prefibrillar oligomers in mixtures of human and mouse α-synuclein. Biochemistry 39 (2000) 10619-10626
35. Volles M.J., and Lansbury Jr. P.T. Zeroing in on the pathogenic form of α-synuclein and its mechanism of neurotoxicity in Parkinson's Disease. Biochemistry 42 (2003) 7871-7878
36. Gosavi N., Lee H.J., Lee J.S., Patel S., and Lee S.J. Golgi fragmentation occurs in the cells with prefibrillar α-synuclein aggregates and precedes the formation of fibrillar inclusion. J. Biol. Chem. 277 (2002) 48984-48992
37. Irizarry M.C., Kim T.W., McNamara M., Tanzi R.E., George J.M., Clayton D.F., and Hyman B.T. Characterization of the precursor protein of the non-Aβ component of senile plaques (NACP) in the human central nervous system. J. Neuropathol. Exp. Neurol. 55 (1996) 889-895
38. Kahle P.J., Neumann M., Ozmen L., Muller V., Jacobsen H., Schindzielorz A., et al. Subcellular localization of wild-type and Parkinson's disease-associated mutant α-synuclein in human transgenic mouse brain. J. Neurosci. 20 (2000) 6365-6373
39. Fortin D.L., Troyer M.D., Nakamura K., Kubo S., Anthony M.D., and Edwards R.H. Lipid rafts mediate the synaptic localization of α-synuclein. J. Neurosci. 24 (2004) 6715-6723
40. Glickman M.H., and Ciechanover A. The ubiquitin-proteasome protelytic pathway: destruction for the sake of construction. Physiol. Rev. 82 (2002) 373-428
41. Shorter J., and Lindquist S. Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 304 (2004) 1793-1797
42. Ohno M., Kitabatake N., and Tani F. Role of the C-terminal region of mouse inducible Hsp72 in the recognition of peptide substrate for chaperone activity. FEBS Letters 576 (2004) 381-386
43. Narhi L., Wood S.J., Steavenson S., Jiang Y., Wu G.M., Anafi D., et al. Both familial Parkinson's disease mutations accelerate a-synuclein aggregation. J. Biol. Chem. 274 (1999) 9843-9846
44. Bradford M.M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal. Biochem. 72 (1976) 248-254
45. Nielsen L., Khurana R., Coats A., Frokjaer S., Brange J., Vyas S., et al. Effect of environmental factors on kinetics of insulin fibril formation: elucidation of the molecular mechanism. Biochemistry 40 (2001) 6036-6046
46. Yagi H., Kusaka E., Hongo K., Mizobata T., and Kawata Y. Amyloid fibril formation of α-synuclein is accelerated by preformed amyloid seeds of other proteins: implications for the mechanism of transmissibale conformational diseases. J. Biol. Chem. 280 (2005) 38609-38616
47. Weissmann G., Collins T., Evers A., and Dunham P. Membrane perturbation: studies employing a calcium-sensitive dye, arsenazo III, in liposomes. Proc. Natl Acad. Sci. USA 73 (1976) 510-514
48. 2+)-ATPase in reconstituted vesicles. Biochim. Biophys. Acta 904 (1987) 36-44
49. Hoyer W., Antony T., Cherny D., Heim G., Jovin T.M., and Subramaniam V. Dependence of alpha-synuclein aggregate morphology on solution conditions. J. Mol. Biol. 322 (2002) 383-393
50. Barral J.M., Broadley S.A., Schaffar G., and Hartl F.U. Roles of molecular chaperones in protein misfolding diseases. Semin. Cell. Dev. Biol. 15 (2004) 17-29