Conformational Plasticity of the Gerstmann-Sträussler-Scheinker Disease Peptide as Indicated by Its Multiple Aggregation Pathways

Journal of Molecular Biology

Volumn 381, Issue 5, 2008, Pages 1349-1361

  Natalello, Antonino ^a,b   Prokorov, Valery V ^c   Tagliavini, Fabrizio ^d   Morbin, Michela ^d   Forloni, Gianluigi ^e   Beeg, Marten ^e   Manzoni, Claudia ^e   Colombo, Laura ^e   Gobbi, Marco ^e   Salmona, Mario ^e   Doglia, Silvia Maria ^a,b  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b Consorzio Nazionale Interuniversitario per le Scienze fisiche della Materia ^*  (Italy)

^c SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^d DEPARTMENT OF NEUROSURGERY   (Italy)

^e MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

amyloid; atomic force microscopy; Fourier transform infrared spectroscopy; prion; protein aggregation

Indexed keywords

PRION PROTEIN; PROTEIN PRP 82-146;

ARTICLE; ATOMIC FORCE MICROSCOPY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON MICROSCOPY; GERSTMANN STRAUSSLER SCHEINKER SYNDROME; HUMAN; INFRARED SPECTROSCOPY; KINETICS; PLASTICITY; PRIORITY JOURNAL; PROTEIN AGGREGATION;

EID: 48749090708     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.06.063     Document Type: Article

References (60)

1. Prusiner S.B. Prions. Proc. Natl Acad. Sci. USA 95 (1998) 13363-13383
2. Prusiner S.B. Molecular biology of prion diseases. Science 252 (1991) 1515-1522
3. Pan K.M., Baldwin M., Nguyen J., Gasset M., Serban A., Groth D., et al. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc. Natl Acad. Sci. USA 90 (1993) 10962-10966
4. Zahn R., Liu A., Luhrs T., Riek R., Von Schroetter C., Garcia F.L., et al. NMR solution structure of the human prion protein. Proc. Natl Acad. Sci. USA 97 (2000) 145-150
5. Tagliavini F., Prelli F., Ghiso J., Bugiani O., Serban D., Prusiner S.B., et al. Amyloid protein of Gerstmann-Straussler-Scheinker disease (Indiana kindred) is an 11 kd fragment of prion protein with an N-terminal glycine at codon 58. EMBO J. 10 (1991) 513-519
6. Tagliavini F., Prelli F., Porro M., Rossi G., Giaccone G., Farlow M.R., et al. Amyloid fibrils in Gerstmann-Straussler-Scheinker disease (Indiana and Swedish kindreds) express only PrP peptides encoded by the mutant allele. Cell 79 (1994) 695-703
7. Tagliavini F., Lievens P.M.J., Tranchant C., Warter J.M., Mohr M., Giaccone G., et al. A 7-kDa prion protein (PrP) fragment, an integral component of the PrP region required for infectivity, is the major amyloid protein in Gerstmann-Straussler-Scheinker disease A117V. J. Biol. Chem. 276 (2001) 6009-6015
8. Piccardo P., Seiler C., Dlouhy S.R., Young K., Farlow M.R., Prelli F., et al. Proteinase-K-resistant prion protein isoforms in Gerstmann-Straussler-Scheinker disease (Indiana kindred). J. Neuropathol. Exp. Neurol. 55 (1996) 1157-1163
9. Piccardo P., Dlouhy S.R., Lievens P.M., Young K., Bird T.D., Nochlin D., et al. Phenotypic variability of Gerstmann-Straussler-Scheinker disease is associated with prion protein heterogeneity. J. Neuropathol. Exp. Neurol. 57 (1998) 979-988
10. Parchi P., Chen S.G., Brown P., Zou W., Capellari S., Budka H., et al. Different patterns of truncated prion protein fragments correlate with distinct phenotypes in P102L Gerstmann-Straussler-Scheinker disease. Proc. Natl Acad. Sci. USA 95 (1998) 8322-8327
11. Muramoto T., Scott M., Cohen F.E., and Prusiner S.B. Recombinant scrapie-like prion protein of 106 amino acids is soluble. Proc. Natl Acad. Sci. USA 93 (1996) 15457-15462
12. Supattapone S., Bosque P., Muramoto T., Wille H., Aagaard C., Peretz D., et al. Prion protein of 106 residues creates an artificial transmission barrier for prion replication in transgenic mice. Cell 96 (1999) 869-878
13. Salmona M., Morbin M., Massignan T., Colombo L., Mazzoleni G., Capobianco R., et al. Structural properties of Gerstmann-Straussler-Scheinker disease amyloid protein. J. Biol. Chem. 278 (2003) 48146-48153
14. Bahadi R., Farrelly P.V., Kenna B.L., Kourie J.I., Tagliavini F., Forloni G., and Salmona M. Channels formed with a mutant prion protein PrP(82-146) homologous to a 7-kDa fragment in diseased brain of GSS patients. Am. J. Physiol.: Cell Physiol. 285 (2003) C862-C872
15. Gobbi M., Colombo L., Morbin M., Mazzoleni G., Accardo E., Vanoni M., et al. Gerstmann-Straussler-Scheinker disease amyloid protein polymerizes according to the "dock-and-lock" model. J. Biol. Chem. 281 (2006) 843-849
16. Tagliavini F., Forloni G., Colombo L., Rossi G., Girola L., Canciani B., et al. Tetracycline affects abnormal properties of synthetic PrP peptides and PrP(Sc) in vitro. J. Mol. Biol. 300 (2000) 1309-1322
17. Ricchelli F., Buggio R., Drago D., Salmona M., Forloni G., Negro A., et al. Aggregation/fibrillogenesis of recombinant human prion protein and Gerstmann-Straussler-Scheinker disease peptides in the presence of metal ions. Biochemistry 45 (2006) 6724-6732
18. Fioriti L., Angeretti N., Colombo L., De Luigi A., Colombo A., Manzoni C., et al. Neurotoxic and gliotrophic activity of a synthetic peptide homologous to Gerstmann-Straussler-Scheinker disease amyloid protein. J. Neurosci. 27 (2007) 1576-1583
19. Zandomeneghi G., Krebs M.R.H., McCammon M.G., and Fandrich M. FTIR reveals structural differences between native beta-sheet proteins and amyloid fibrils. Protein Sci. 13 (2004) 3314-3321
20. Jones E.M., and Surewicz W.K. Fibril conformation as the basis of species- and strain-dependent seeding specificity of mammalian prion amyloids. Cell 121 (2005) 63-72
21. Ollesch J., Kunnemann E., Glockshuber R., and Gerwert K. Prion protein alpha-to-beta transition monitored by time-resolved Fourier transform infrared spectroscopy. Appl. Spectrosc. 61 (2007) 1025-1031
22. Stohr J., Weinmann N., Wille H., Kaimann T., Nagel-Steger L., Birkmann E., et al. Mechanisms of prion protein assembly into amyloid. Proc. Natl Acad. Sci. USA 105 (2008) 2409-2414
23. Sun Y., Breydo L., Makarava N., Yang Q.Y., Bocharova O.V., and Baskakov I.V. Site-specific conformational studies of prion protein (PrP) amyloid fibrils revealed two cooperative folding domains within amyloid structure. J. Biol. Chem. 282 (2007) 9090-9097
24. Susi H., and Byler D.M. Resolution-enhanced Fourier transform infrared spectroscopy of enzymes. Methods Enzymol. 130 (1986) 290-311
25. Barth A., and Zscherp C. What vibrations tell us about proteins. Q. Rev. Biophys. 35 (2002) 369-430
26. Goormaghtigh E., Raussens V., and Ruysschaert J.M. Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes. Biochim. Biophys. Acta 1422 (1999) 105-185
27. Arrondo J.L.R., and Goni F.M. Structure and dynamics of membrane proteins as studied by infrared spectroscopy. Prog. Biophys. Mol. Biol. 72 (1999) 367-405
28. Arrondo J.L.R., Muga A., Castresana J., and Goni F.M. Quantitative studies of the structure of proteins in solution by Fourier-transform infrared spectroscopy. Prog. Biophys. Mol. Biol. 59 (1993) 23-56
29. Seshadri S., Khurana R., and Fink A.L. Fourier transform infrared spectroscopy in analysis of protein deposits. Methods Enzymol. 309 (1999) 559-576
30. Natalello A., Doglia S.M., Carey J., and Grandori R. Role of flavin mononucleotide in the thermostability and oligomerization of Escherichia coli stress-defense protein WrbA. Biochemistry 46 (2007) 543-553
31. Peralvarez-Marin A., Barth A., and Graslund A. Time-resolved infrared spectroscopy of pH-induced aggregation of the Alzheimer Abeta1-28 peptide. J. Mol. Biol. 379 (2008) 589-596
32. Ami D., Natalello A., Taylor G., Tonon G., and Maria Doglia S. Structural analysis of protein inclusion bodies by Fourier transform infrared microspectroscopy. Biochim. Biophys. Acta 1764 (2006) 793-799
33. Sokolowski F., Modler A.J., Masuch R., Zirwer D., Baier M., Lutsch G., et al. Formation of critical oligomers is a key event during conformational transition of recombinant Syrian hamster prion protein. J. Biol. Chem. 278 (2003) 40481-40492
34. Natalello A., Ami D., Brocca S., Lotti M., and Doglia S.M. Secondary structure, conformational stability and glycosylation of a recombinant Candida rugosa lipase studied by Fourier-transform infrared spectroscopy. Biochem. J. 385 (2005) 511-517
35. Laws D.D., Bitter H.L., Liu K., Ball H.L., Kaneko K., Wille H., et al. Solid-state NMR studies of the secondary structure of a mutant prion protein fragment of 55 residues that induces neurodegeneration. Proc. Natl Acad. Sci. USA 98 (2001) 11686-11690
36. Ban T., Hoshino M., Takahashi S., Hamada D., Hasegawa K., Naiki H., and Goto Y. Direct observation of Abeta amyloid fibril growth and inhibition. J. Mol. Biol. 344 (2004) 757-767
37. Le Vine III H. Quantification of beta-sheet amyloid fibril structures with thioflavin T. Methods Enzymol. 309 (1999) 274-284
38. Yagi H., Ban T., Morigaki K., Naiki H., and Goto Y. Visualization and classification of amyloid beta supramolecular assemblies. Biochemistry 46 (2007) 15009-15017
39. Ding T.T., Lee S.J., Rochet J.C., and Lansbury P.T. Annular alpha-synuclein protofibrils are produced when spherical protofibrils are incubated in solution or bound to brain-derived membranes. Biochemistry 41 (2002) 10209-10217
40. Nandi P.K., Bera A., and Sizaret P.Y. Osmolyte trimethylamine N-oxide converts recombinant α-helical prion protein to its soluble β-structured form at high temperature. J. Mol. Biol. 362 (2006) 810-820
41. Kajava A.V., Squire J.M., and Parry D.A.D. β-Structures in fibrous proteins. Adv. Protein Chem. 73 (2006) 1-15
42. Lashuel H.A., Petre B.M., Wall J., Simon M., Nowak R.J., Walz T., and Lansbury P.T. α-Synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J. Mol. Biol. 322 (2002) 1089-1102
43. Khurana R., Ionescu-Zanetti C., Pope M., Li J., Nielson L., Ramirez-Alvarado M., et al. A general model for amyloid fibril assembly based on morphological studies using atomic force microscopy. Biophys. J. 85 (2003) 1135-1144
44. Kad N.M., Myers S.L., Smith D.P., Alastair Smith D., Radford S.E., and Thomson N.H. Hierarchical assembly of beta2-microglobulin amyloid in vitro revealed by atomic force microscopy. J. Mol. Biol. 330 (2003) 785-797
45. Jansen R., Dzwolak W., and Winter R. Amyloidogenic self-assembly of insulin aggregates probed by high resolution atomic force microscopy. Biophys. J. 88 (2005) 1344-1353
46. Viles J.H., Donne D., Kroon G., Prusiner S.B., Cohen F.E., Dyson H.J., and Wright P.E. Local structural plasticity of the prion protein. Analysis of NMR relaxation dynamics. Biochemistry 40 (2001) 2743-2753
47. Spassov S., Beekes M., and Naumann D. Structural differences between TSEs strains investigated by FT-IR spectroscopy. Biochim. Biophys. Acta 1760 (2006) 1138-1149
48. Natalello A., Santarella R., Doglia S.M., and de Marco A. Physical and chemical perturbations induce the formation of protein aggregates with different structural features. Protein Expr. Purif. 58 (2008) 356-361
49. Lasch P., Beekes M., Schmitt J., and Naumann D. Detection of preclinical scrapie from serum by infrared spectroscopy and chemometrics. Anal. Bioanal. Chem. 387 (2007) 1791-1800
50. Watzlawik J., Skora L., Frense D., Griesinger C., Zweckstetter M., Schulz-Schaeffer W.J., and Kramer M.L. Prion protein helix1 promotes aggregation but is not converted into beta-sheet. J. Biol. Chem. 281 (2006) 30242-30250
51. Decatur S.M. Elucidation of residue-level structure and dynamics of polypeptides via isotope-edited infrared spectroscopy. Acc. Chem. Res. 39 (2006) 169-175
52. Yamada N., Ariga K., Naito M., Matsubara K., and Koyama E. Regulation of beta-sheet structures within amyloid-like beta-sheet assemblage from tripeptide derivatives. J. Am. Chem. Soc. 120 (1998) 12192-12199
53. Chitnumsub P., Fiori W.R., Lashuel H.A., Diaz H., and Kelly J.W. The nucleation of monomeric parallel beta-sheet-like structures and their self-assembly in aqueous solution. Bioorg. Med. Chem. 7 (1999) 39-59
54. Kodali R., and Wetzel R. Polymorphism in the intermediates and products of amyloid assembly. Curr. Opin. Struct. Biol. 17 (2007) 48-57
55. Chamberlain A.K., MacPhee C.E., Zurdo J., Morozova-Roche L.A., Hill H.A.O., Dobson C.M., and Davis J.J. Ultrastructural organization of amyloid fibrils by atomic force microscopy. Biophys. J. 79 (2000) 3282-3293
56. Lin X.J., Zhang F., Xie Y.Y., Bao W.J., He J.H., and Hu H.Y. Secondary structural formation of alpha-synuclein amyloids as revealed by g-factor of solid-state circular dichroism. Biopolymers 83 (2006) 226-232
57. Collinge J. Molecular neurology of prion disease. J. Neurol., Neurosurg. Psychiatry 76 (2005) 906-919
58. Klinov D., and Magonov S. True molecular resolution in tapping-mode atomic force microscopy with high-resolution probes. Appl. Phys. Lett. 84 (2004) 2697-2699
59. San Paulo A., and Garcia R. High-resolution imaging of antibodies by tapping-mode atomic force microscopy: attractive and repulsive tip-sample interaction regimes. Biophys. J. 78 (2000) 1599-1605
60. Prokhorov V.V., and Saunin S.A. Probe-surface interaction mapping in amplitude modulation atomic force microscopy by integrating amplitude-distance and amplitude-frequency curves. Appl. Phys. Lett. 91 (2007) 23122