Isolation of short peptide fragments from α-synuclein fibril core identifies a residue important for fibril nucleation: A possible implication for diagnostic applications

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1804, Issue 10, 2010, Pages 2077-2087

  Yagi, Hisashi ^a,b,c   Takeuchi, Hideki ^b   Ogawa, Shiho ^b   Ito, Naomi ^a   Sakane, Isao ^a,b   Hongo, Kunihiro ^a,b   Mizobata, Tomohiro ^a,b   Goto, Yuji ^c   Kawata, Yasushi ^a,b  

^a TOTTORI UNIVERSITY   (Japan)

^b TOTTORI UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

Synuclein; Amyloid fibril; Fibril core peptide region; Neurodegenerative disease; Parkinson's disease

Indexed keywords

ALANYLVALYLALANYLGLUTAMINYLLYSYLTHREONYLVALINE; ALANYLVALYLALANYLGLUTAMINYLLYSYLTHREONYLVALYLGLUTAMYLGLYCYLALANYLGLYCYLSERYLISOLEUCYLALANINE; ALPHA SYNUCLEIN; AMYLOID; GLYCINE; INSULIN; LYSOZYME; PEPTIDE DERIVATIVE; PEPTIDE FRAGMENT; PHENYLALANINE; PROTEINASE; SYNTHETIC PEPTIDE; THREONYLVALYLGLUTAMYLGLYCYLALANYLGLYCYLSERINE; THREONYLVALYLGLUTAMYLGLYCYLALANYLGLYCYLSERYLISOLEUCYLALANYLALANYLALANYLTHREONYLGLYCYLPHENYLALANYLVALYLLYSINE; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DRUG IDENTIFICATION; ELECTROSPRAY MASS SPECTROMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOLATION PROCEDURE; MASS SPECTROMETRY; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION;

ALPHA-SYNUCLEIN; AMINO ACID SEQUENCE; AMYLOID; CIRCULAR DICHROISM; HUMANS; INSULIN; LEWY BODIES; MICROSCOPY, ATOMIC FORCE; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; THIAZOLES;

EID: 77956063815     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2010.07.007     Document Type: Article

References (68)

1. Goedert M. Alpha-synuclein and neurodegenerative diseases. Nat. Rev. Neurosci. 2001, 2:492-501.
2. Selkoe D.J. Folding proteins in fatal ways. Nature 2003, 426:900-904.
3. Shastry B.S. Neurodegenerative disorders of protein aggregation. Neurochem. Int. 2003, 43:1-7.
4. Waxman E.A., Giasson B.I. Molecular mechanisms of alpha-synuclein neurodegeneration. Biochim. Biophys. Acta 2009, 1792:616-624.
5. Westermark G.T., Johnson K.H., Westermark P. Staining methods for identification of amyloid in tissue. Methods Enzymol. 1999, 309:3-25.
6. Tan S.Y., Pepys M.B. Amyloidosis. Histopathology 1994, 25:403-414.
7. Carrell R.W., Lomas D.A. Conformational disease. Lancet 1997, 350:134-138.
8. Sunde M., Blake C. The structure of amyloid fibrils by electron microscopy and X-ray diffraction. Adv. Protein Chem. 1997, 50:123-159.
9. Sipe J.D., Cohen A.S. Review: history of the amyloid fibril. J. Struct. Biol. 2000, 130:88-98.
10. Lauren J., Gimbel D.A., Nygaard H.B., Gilbert J.W., Strittmatter S.M. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 2009, 457:1128-1132.
11. Sakono M., Zako T. Amyloid oligomers: formation and toxicity of Abeta oligomers. FEBS J. 2010, 277:1348-1358.
12. Kitamura A., Kubota H. Amyloid oligomers: dynamics and toxicity in the cytosol and nucleus. FEBS J. 2010, 277:1369-1379.
13. Wright P.E., Dyson H.J. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 1999, 293:321-331.
14. Eliezer D. Biophysical characterization of intrinsically disordered proteins. Curr. Opin. Struct. Biol. 2009, 19:23-30.
15. Weinreb P.H., Zhen W., Poon A.W., Conway K.A., Lansbury P.T. NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry 1996, 35:13709-13715.
16. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E.S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W.G., Lazzarini A.M., Duvoisin R.C., Di Iorio G., Golbe L.I., Nussbaum R.L. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 1997, 276:2045-2047.
17. Kruger R., Kuhn W., Muller T., Woitalla D., Graeber M., Kosel S., Przuntek H., Epplen J.T., Schols L., Riess O. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Genet. 1998, 18:106-108.
18. Zarranz J.J., Alegre J., Gomez-Esteban J.C., Lezcano E., Ros R., Ampuero I., Vidal L., Hoenicka J., Rodriguez O., Atares B., Llorens V., Gomez Tortosa E., del Ser T., Munoz D.G., de Yebenes J.G. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann. Neurol. 2004, 55:164-173.
19. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., Goedert M. Alpha-synuclein in Lewy bodies. Nature 1997, 388:839-840.
20. Uversky V.N., Li J., Fink A.L. Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson's disease and heavy metal exposure. J. Biol. Chem. 2001, 276:44284-44296.
21. Uversky V.N., Li J., Fink A.L. Pesticides directly accelerate the rate of alpha-synuclein fibril formation: a possible factor in Parkinson's disease. FEBS Lett. 2001, 500:105-108.
22. Uversky V.N., Li J., Fink A.L. Trimethylamine-N-oxide-induced folding of alpha-synuclein. FEBS Lett. 2001, 509:31-35.
23. Munishkina L.A., Phelan C., Uversky V.N., Fink A.L. Conformational behavior and aggregation of alpha-synuclein in organic solvents: modeling the effects of membranes. Biochemistry 2003, 42:2720-2730.
24. Uversky V.N., Lee H.J., Li J., Fink A.L., Lee S.J. Stabilization of partially folded conformation during alpha-synuclein oligomerization in both purified and cytosolic preparations. J. Biol. Chem. 2001, 276:43495-43498.
25. Uversky V.N., Li J., Fink A.L. Evidence for a partially folded intermediate in alpha-synuclein fibril formation. J. Biol. Chem. 2001, 276:10737-10744.
26. Conway K.A., Harper J.D., Lansbury P.T. Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat. Med. 1998, 4:1318-1320.
27. Conway K.A., Harper J.D., Lansbury P.T. Fibrils formed in vitro from α-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid. Biochemistry 2000, 39:2552-2563.
28. Conway K.A., Lee S.J., Rochet J.C., Ding T.T., Williamson R.E., Lansbury P.T. Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc. Natl Acad. Sci. USA 2000, 97:571-576.
29. Goldberg M.S., Lansbury P.T. Is there a cause-and-effect relationship between alpha-synuclein fibrillization and Parkinson's disease?. Nat. Cell Biol. 2000, 2:E115-E119.
30. Yagi H., Kusaka E., Hongo K., Mizobata T., Kawata Y. Amyloid fibril formation of alpha-synuclein is accelerated by preformed amyloid seeds of other proteins: implications for the mechanism of transmissible conformational diseases. J. Biol. Chem. 2005, 280:38609-38616.
31. Jimenez J.L., Nettleton E.J., Bouchard M., Robinson C.V., Dobson C.M., Saibil H.R. The protofilament structure of insulin amyloid fibrils. Proc. Natl Acad. Sci. USA 2002, 99:9196-9201.
32. Krebs M.R., Wilkins D.K., Chung E.W., Pitkeathly M.C., Chamberlain A.K., Zurdo J., Robinson C.V., Dobson C.M. Formation and seeding of amyloid fibrils from wild-type hen lysozyme and a peptide fragment from the beta-domain. J. Mol. Biol. 2000, 300:541-549.
33. Higurashi T., Yagi H., Mizobata T., Kawata Y. Amyloid-like fibril formation of co-chaperonin GroES: nucleation and extension prefer different degrees of molecular compactness. J. Mol. Biol. 2005, 351:1057-1069.
34. Giasson B.I., Forman M.S., Higuchi M., Golbe L.I., Graves C.L., Kotzbauer P.T., Trojanowski J.Q., Lee V.M. Initiation and synergistic fibrillization of tau and alpha-synuclein. Science 2003, 300:636-640.
35. Lucking C.B., Brice A. Alpha-synuclein and Parkinson's disease. Cell. Mol. Life Sci. 2000, 57:1894-1908.
36. Forman M.S., Schmidt M.L., Kasturi S., Perl D.P., Lee V.M., Trojanowski J.Q. Tau and alpha-synuclein pathology in amygdala of Parkinsonism-dementia complex patients of Guam. Am. J. Pathol. 2002, 160:1725-1731.
37. Wirths O., Bayer T.A. Alpha-synuclein, A beta and Alzheimer's disease. Prog. Neuropsychopharmacol. Biol. Psychiatry 2003, 27:103-108.
38. Hardy J. The relationship between amyloid and tau. J. Mol. Neurosci. 2003, 20:203-206.
39. Ueda K., Fukushima H., Masliah E., Xia Y., Iwai A., Yoshimoto M., Otero D.A., Kondo J., Ihara Y., Saitoh T. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl Acad. Sci. USA 1993, 90:11282-11286.
40. Giasson B.I., Murray I.V., Trojanowski J.Q., Lee V.M. A hydrophobic stretch of 12 amino acid residues in the middle of alpha-synuclein is essential for filament assembly. J. Biol. Chem. 2001, 276:2380-2386.
41. Waxman E.A., Mazzulli J.R., Giasson B.I. Characterization of hydrophobic residue requirements for alpha-synuclein fibrillization. Biochemistry 2009, 48:9427-9436.
42. Miake H., Mizusawa H., Iwatsubo T., Hasegawa M. Biochemical characterization of the core structure of alpha-synuclein filaments. J. Biol. Chem. 2002, 277:19213-19219.
43. Qin Z., Hu D., Han S., Hong D.P., Fink A.L. Role of different regions of alpha-synuclein in the assembly of fibrils. Biochemistry 2007, 46:13322-13330.
44. Heise H., Hoyer W., Becker S., Andronesi O.C., Riedel D., Baldus M. Molecular-level secondary structure, polymorphism, and dynamics of full-length alpha-synuclein fibrils studied by solid-state NMR. Proc. Natl Acad. Sci. USA 2005, 102:15871-15876.
45. Vilar M., Chou H.T., Luhrs T., Maji S.K., Riek-Loher D., Verel R., Manning G., Stahlberg H., Riek R. The fold of alpha-synuclein fibrils. Proc. Natl Acad. Sci. USA 2008, 105:8637-8642.
46. Uversky V.N., Fink A.L. Amino acid determinants of alpha-synuclein aggregation: putting together pieces of the puzzle. FEBS Lett. 2002, 522:9-13.
47. Narhi L., Wood S.J., Steavenson S., Jiang Y., Wu G.M., Anafi D., Kaufman S.A., Martin F., Sitney K., Denis P., Louis J.C., Wypych J., Biere A.L., Citron M. Both familial Parkinson's disease mutations accelerate alpha-synuclein aggregation. J. Biol. Chem. 1999, 274:9843-9846.
48. Sakiyama F., Masaki T. Lysyl endopeptidase of Achromobacter lyticus. Methods Enzymol. 1994, 244:126-137.
49. Ban T., Hamada D., Hasegawa K., Naiki H., Goto Y. Direct observation of amyloid fibril growth monitored by thioflavin T fluorescence. J. Biol. Chem. 2003, 278:16462-16465.
50. Ban T., Hoshino M., Takahashi S., Hamada D., Hasegawa K., Naiki H., Goto Y. Direct observation of Abeta amyloid fibril growth and inhibition. J. Mol. Biol. 2004, 344:757-767.
51. Serpell L.C. Alzheimer's amyloid fibrils: structure and assembly. Biochim. Biophys. Acta 2000, 1502:16-30.
52. Zurdo J., Guijarro J.I., Dobson C.M. Preparation and characterization of purified amyloid fibrils. J. Am. Chem. Soc. 2001, 123:8141-8142.
53. Monti M., Amoresano A., Giorgetti S., Bellotti V., Pucci P. Limited proteolysis in the investigation of beta2-microglobulin amyloidogenic and fibrillar states. Biochim. Biophys. Acta 2005, 1753:44-50.
54. Frare E., Mossuto M.F., Polverino de Laureto P., Dumoulin M., Dobson C.M., Fontana A. Identification of the core structure of lysozyme amyloid fibrils by proteolysis. J. Mol. Biol. 2006, 361:551-561.
55. Yagi H., Sato A., Yoshida A., Hattori Y., Hara M., Shimamura J., Sakane I., Hongo K., Mizobata T., Kawata Y. Fibril formation of hsp10 homologue proteins and determination of fibril core regions: differences in fibril core regions dependent on subtle differences in amino acid sequence. J. Mol. Biol. 2008, 377:1593-1606.
56. Klunk W.E., Pettegrew J.W., Abraham D.J. Quantitative evaluation of congo red binding to amyloid-like proteins with a beta-pleated sheet conformation. J. Histochem. Cytochem. 1989, 37:1273-1281.
57. Dische F.E., Wernstedt C., Westermark G.T., Westermark P., Pepys M.B., Rennie J.A., Gilbey S.G., Watkins P.J. Insulin as an amyloid-fibril protein at sites of repeated insulin injections in a diabetic patient. Diabetologia 1988, 31:158-161.
58. Pepys M.B., Hawkins P.N., Booth D.R., Vigushin D.M., Tennent G.A., Soutar A.K., Totty N., Nguyen O., Blake C.C., Terry C.J., et al. Human lysozyme gene mutations cause hereditary systemic amyloidosis. Nature 1993, 362:553-557.
59. Wood S.J., Wypych J., Steavenson S., Louis J.C., Citron M., Biere A.L. alpha-synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease. J. Biol. Chem. 1999, 274:19509-19512.
60. Pawar A.P., Dubay K.F., Zurdo J., Chiti F., Vendruscolo M., Dobson C.M. Prediction of "aggregation-prone" and "aggregation-susceptible" regions in proteins associated with neurodegenerative diseases. J. Mol. Biol. 2005, 350:379-392.
61. Uversky V.N., Fink A.L. Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim. Biophys. Acta 2004, 1698:131-153.
62. Hoyer W., Cherny D., Subramaniam V., Jovin T.M. Impact of the acidic C-terminal region comprising amino acids 109-140 on alpha-synuclein aggregation in vitro. Biochemistry 2004, 43:16233-16242.
63. Makin O.S., Atkins E., Sikorski P., Johansson J., Serpell L.C. Molecular basis for amyloid fibril formation and stability. Proc. Natl Acad. Sci. USA 2005, 102:315-320.
64. Levy M., Garmy N., Gazit E., Fantini J. The minimal amyloid-forming fragment of the islet amyloid polypeptide is a glycolipid-binding domain. FEBS J. 2006, 273:5724-5735.
65. Chou P.Y., Fasman G.D. Conformational parameters for amino acids in helical, beta-sheet, and random coil regions calculated from proteins. Biochemistry 1974, 13:211-222.
66. Andersen C.B., Yagi H., Manno M., Martorana V., Ban T., Christiansen G., Otzen D.E., Goto Y., Rischel C. Branching in amyloid fibril growth. Biophys. J. 2009, 96:1529-1536.
67. Ban T., Morigaki K., Yagi H., Kawasaki T., Kobayashi A., Yuba S., Naiki H., Goto Y. Real-time and single fibril observation of the formation of amyloid beta spherulitic structures. J. Biol. Chem. 2006, 281:33677-33683.
68. Yagi H., Ban T., Morigaki K., Naiki H., Goto Y. Visualization and classification of amyloid beta supramolecular assemblies. Biochemistry 2007, 46:15009-15017.