Critical region for amyloid fibril formation of mouse prion protein: Unusual amyloidogenic properties of the helix 2 peptide

Biochemistry

Volumn 47, Issue 50, 2008, Pages 13242-13251

  Yamaguchi, Kei Ichi ^a   Matsumoto, Tomoharu ^a   Kuwata, Kazuo ^a  

^a GIFU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEINS; SEED; SELF ASSEMBLED MONOLAYERS;

AMYLOID FIBRIL FORMATIONS; AMYLOID FIBRILS; CONFORMATIONAL CONVERSIONS; CRITICAL REGIONS; CROSS REACTIVITIES; FIBRIL FORMATIONS; GAIN INSIGHTS; LAG TIMES; PEPTIDE FRAGMENTS; PRION PROTEINS; RANDOM CONFORMATIONS; REPLICATION PROCESSES; STRUCTURAL ELEMENTS; STRUCTURAL MECHANISMS;

AMINES;

AMYLOID; HELIX 2 PEPTIDE; HELIX 3 PEPTIDE; PEPTIDE; PEPTIDE FRAGMENT; PRION PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BETA SHEET; BETA TURN; CROSS REACTION; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; AMYLOID; ANIMALS; BASE SEQUENCE; MICE; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PRIONS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY;

EID: 57649136747     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801562w     Document Type: Article

References (57)

1. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13388.
2. Collinge, J. (2001) Prion diseases of humans and animals: Their causes and molecular basis. Annu. Rev. Neurosci. 24, 519-550.
3. Aguzzi, A., and Polymenidou, M. (2004) Mammalian prion biology: One century of evolving concepts. Cell 116, 313-327.
4. Weissmann, C. (2004) The state of the prion. Nat. Rev. Microbiol. 2, 861-871.
5. Legname, G., Baskakov, I. V., Nguyen, H.-O. B., Riesner, D., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (2004) Synthetic mammalian prions. Science 305, 673-676.
6. Bocharova, O. V., Breydo, L., Parfenov, A. S., Salnikov, V. V., and Baskakov, I. V. (2005) In vitro conversion of full-length mammalian prion protein produces amyloid form with physical properties of PrPSc. J. Mol. Biol. 346, 645-659.
7. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R., and Wüthrich, K. (1996) NMR structure of the mouse prion protein domain PrP(121-231). Nature 382, 180-182.
8. Muramoto, T., Scott, M., Cohen, F. E., and Prusiner, S. B. (1996) Recombinant scrapie-like prion protein of 106 amino acids is soluble. Proc. Natl. Acad. Sci. U.S.A. 93, 15457-15462.
9. Gasset, M., Baldwin, M. A., Lloyd, D. H., Gabriel, J.-M., Holtzman, D. M., Cohen, F., Fletterick, R., and Prusiner, S. B. (1992) Predicted α-helical regions of the prion protein when synthesized as peptides form amyloid. Proc. Natl. Acad. Sci. U.SA. 89, 10940-10944.
10. Tagliavini, F., Prelli, F., Verga, L., Giaccone, G., Sarma, R., Gorevic, P., Chetti, B., Passerini, F., Ghibaudi, E., Forloni, G., Salmona, M., Bugiani, O., and Frangione, B. (1993) Synthetic peptides homologous to prion protein residues 106-147 form amyloid-like fibrils in vitro. Proc. Natl. Acad. Sci. U.S.A. 90, 9678-9682.
11. Jones, E. M., and Surewicz, W. K. (2005) Fibril conformation as the basis of species- and strain-dependent seeding specificity of mammalian prion amyloids. Cell 121, 63-72.
12. Natalello, A., Prokorov, V. V., Tagliavini, F., Morbin, M., Forloni, G., Beeg, M., Manzoni, C., Colombo, L., Gobbi, M., Salmona, M., and Doglia, S. M. (2008) Conformational plasticity of the Gerstmann-Sträussler-Scheinker disease peptide as indicated by its multiple aggregation pathways. J. Mol. Biol. 381, 1349-1361.
13. Salmona, M., Malesani, P., De Gioia, L., Gorla, S., Bruschi, M., Molinari, A., Della Vedova, F., Pedrotti, B., Marrari, M. A., Awan, T., Bugiani, O., Forloni, G., and Tagliavini, F. (1999) Molecular determinants of the physicochemical properties of a critical prion protein region comprising residues 106-126. Biochem. J. 342, 207-214.
14. Nguyen, J. T., Inouye, H., Baldwin, M. A., Fletterick, R. J., Cohen, F. E., Prusiner, S. B., and Kirschner, D. A. (1995) X-ray diffraction of scrapie prion rods and PrP peptides. J. Mol. Biol. 252, 412-422.
15. Kuwata, K., Matumoto, T., Cheng, H., Nagayama, K., James, T. L., and Roder, H. (2003) NMR-detected hydrogen exchange and molecular dynamics simulations provide structural insight into fibril formation of prion protein fragment 106-126. Proc. Natl. Acad. Sci. U.S.A. 100, 14790-14795.
16. Govaerts, C., Wille, H., Prusiner, S. B., and Cohen, F. E. (2004) Evidence for assembly of prions with left-handed β-helices into trimers. Proc. Natl. Acad. Sci. U.S.A. 101, 8342-8347.
17. Baskakov, I. V., Aagaard, C., Mehlhorn, I., Wille, H., Groth, D., Baldwin, M. A., Prusiner, S. B., and Cohen, F. E. (2000) Self-assembly of recombinant prion protein of 106 residues. Biochemistry 39, 2792-2804.
18. Lu, X., Wintrode, P. L., and Surewicz, W. K. (2007) β-Sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange. Proc. Natl. Acad. Sci. U.S.A. 104, 1510-1515.
19. Viles, J. H., Cohen, F. E., Prusiner, S. B., Goodin, D. B., Wright, P. E., and Dyson, H. J. (1999) Copper binding to the prion protein: Structural implications of four identical cooperative binding sites. Proc. Natl. Acad. Sci. U.S.A. 96, 2042-2047.
20. Khurana, R., Coleman, C., Ionescu-Zanetti, C., Carter, S. A., Krishna, V., Grover, R. K., Roy, R., and Singh, S. (2005) Mechanism of thioflavin T binding to amyloid fibrils. J Struct. Biol. 151, 229-238.
21. Meehan, S., Knowles, T. P. J., Baldwin, A. J., Smith, J. F., Squires, A. M., Clements, P., Treweek, T. M., Ecroyd, H., Tartaglia, G. G., Vendruscolo, M., MacPhee, C. E., Dobson, C. M., and Carver, J. A. (2007) Characterization of amyloid fibril formation by small heat-shock chaperone proteins human αA-, αB- and R120G αB-crystallins. J. Mol. Biol. 372, 470-484.
22. 2-microglobulin fragment are induced by fluorine-substituted alcohols. J. Mol. Biol. 363, 279-288.
23. Fezoui, Y., and Teplow, D. B. (2002) Kinetic studies of amyloid β-protein fibril assembly. J. Biol. Chem. 277, 36948-36954.
24. Plakoutsi, G., Bemporad, F., Calamai, M., Taddei, N., Dobson, C. M., and Chiti, F. (2005) Evidence for a mechanism of amyloid formation involving molecular reorganisation within native-like precursor aggregates. J. Mol. Biol. 351, 910-922.
25. Seshadri, S., Khurana, R., and Fink, A. L. (1999) Fourier transform infrared spectroscopy in analysis of protein deposits. Methods Enzymol. 309, 559-576.
26. Barth, A., and Zscherp, C. (2002) What vibrations tell us about proteins. Q. Rev. Biophys. 35, 369-430.
27. Zandomeneghi, G., Krebs, M. R. H., Mccammon, M. G., and Fändrich, M. (2004) FTIR reveals structural differences between native β-sheet proteins and amyloid fibrils. Protein Sci. 13, 3314-3321.
28. Watzlawik, J., Skora, L., Frense, D., Griesinger, C., Zweckstetter, M., Schulz-Schaeffer, W. J., and Kramer, M. L. (2006) Prion protein helix1 promotes aggregation but is not converted into β-sheet. J. Biol. Chem. 281, 30242-30250.
29. Goormaghtigh, E., Cabiaux, V., and Ruysschaert, J.-M. (1994) Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. III. Secondary structures. Subcell. Biochem. 23, 405-450.
30. Bandekar, J., and Krimm, S. (1979) Vibrational analysis of peptides, polypeptides, and proteins: Characteristic amide bands of β-turns. Proc. Natl. Acad. Sci. U.S.A. 76, 774-777.
31. Bandekar, J. (1992) Amide modes and protein conformation. Biochim. Biophys. Acta 1120, 123-143.
32. 1-28 peptide. J. Mol. Biol. 379, 589-596.
33. Atarashi, R., Moore, R. A., Sim, V. L., Hughson, A. G., Dorward, D. W., Onwubiko, H. A., Priola, S. A., and Caughey, B. (2007) Ultrasensitive detection of scrapie prion protein using seeded conversion of recombinant prion protein. Nat. Methods 4, 645-650.
34. 2- microglobulin. J. Biol. Chem. 280, 32843-32848.
35. Telling, G. C., Scott, M., Mastrianni, J., Gabizon, R., Torchia, M., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (1995) Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell 83, 79-90.
36. Kuwata, K., Li, H., Yamada, H., Legname, G., Prusiner, S. B., Akasaka, K., and James, T. L. (2002) Locally disordered conformer of the hamster prion protein: A crucial intermediate to PrPSc? Biochemistry 41, 12277-12283.
37. Chiti, F., Taddei, N., Baroni, F., Capanni, C., Stefani, M., Ramponi, G., and Dobson, C. M. (2002) Kinetic partitioning of protein folding and aggregation. Nat. Struct. Biol. 9, 137-143.
38. Chiti, F., Stefani, M., Taddei, N., Ramponi, G., and Dobson, C. M. (2003) Rationalization of the effects of mutations on peptide and protein aggregation rates. Nature 424, 805-808.
39. Hollósi, M., Kövér, K. E., Holly, S., Radics, L., and Fasman, G. D. (1987) β-Turns in bridged proline-containing cyclic peptide models. Biopolymers 26, 1555-1572.
40. 2 cyclic hexapeptides. Preferred β-turn conformers and implications for β-turns in proteins. Biochemistry 20, 4730-4738.
41. Rose, G. D., Gierasch, L. M., and Smith, J. A. (1985) Turns in peptides and proteins. Adv. Protein Chem. 37, 1-109.
42. Yamaguchi, K., Takahashi, S., Kawai, T., Naiki, H., and Goto, Y. (2005) Seeding-dependent propagation and maturation of amyloid fibril conformation. J. Mol. Biol. 352, 952-960.
43. 2-microblobulin fragments probed by solid-state NMR. Proc. Natl. Acad. Sci. U.S.A. 103, 18119-18124.
44. Saiki, M., Honda, S., Kawasaki, K., Zhou, D., Kaito, A., Konakahara, T., and Morii, H. (2005) Higher-order molecular packing in amyloid-like fibrils constructed with linear arrangements of hydrophobic and hydrogen-bonding side-chains. J. Mol. Biol. 348, 983-998.
45. Sternberg, M. J. E., and Thornton, J. M. (1977) On the conformation of proteins: An analysis of β-pleated sheets. J. Mol. Biol. 110, 285-296.
46. Tycko, R. (2006) Molecular structure of amyloid fibrils: Insights from solid-state NMR. Q. Rev. Biophys. 39, 1-55.
47. Wasmer, C., Lange, A., Van Melckebeke, H., Siemer, A. B., Riek, R., and Meier, B. H. (2008) Amyloid fibrils of the HET-s(218-289) prion form a β solenoid with a triangular hydrophobic core. Science 319, 1523-1526.
48. C helix 1 in the hydrophilic seeding of prion aggregates. Proc. Natl. Acad. Sci. U.S.A. 96, 11293-11298.
49. López De La Paz, M., Goldie, K., Zurdo, J., Lacroix, E., Dobson, C. M., Hoenger, A., and Serrano, L. (2002) De novo designed peptide-based amyloid fibrils. Proc. Natl. Acad. Sci. U.S.A. 99, 16052-16057.
50. Kyte, J., and Doolittle, R. F. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
51. Deléage, G., and Roux, B. (1987) An algorithm for protein secondary structure prediction based on class prediction. Protein Eng. 1, 289-294.
52. King, R. D., and Sternberg, M. J. E. (1996) Identification and application of the concepts important for accurate and reliable protein secondary structure prediction. Protein Sci. 5, 2298-2310.
53. Garnier, J., Gibrat, J. F., and Robson, B. (1996) GOR method for predicting protein secondary structure from amino acid sequence. Methods Enzymol. 266, 540-553.
54. Guermeur, Y. (1997) Combinaison de classifieurs statistiques, Application a la prediction de structure secondaire des proteines. Ph.D. Thesis, Université Paris 6, France.
55. Rost, B., and Sander, C. (1993) Prediction of protein secondary structure at better than 70% accuracy. J. Mol. Biol. 232, 584-599.
56. Geourjon, C., and Deléage, G. (1995) SOPMA: Significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput. Appl. Biosci. 11, 681-684.
57. Deléage, G., Combet, C., Blanchet, C., and Geourjon, C. (2001) ANTHEPROT: An integrated protein sequence analysis software with client/server capabilities. Comput. Biol. Med. 31, 259-267.