Observation of intermediate states of the human prion protein by high pressure NMR spectroscopy

BMC Structural Biology

Volumn 6, Issue , 2006, Pages

  Kachel, Norman ^a   Kremer, Werner ^a   Zahn, Ralph ^b,c   Kalbitzer, Hans Robert ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b ETH ZURICH   (Switzerland)

^c Alicon AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN;

ARTICLE; ATMOSPHERIC PRESSURE; CONFORMATIONAL TRANSITION; ENTHALPY; HUMAN; HYDROSTATIC PRESSURE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTON NUCLEAR MAGNETIC RESONANCE;

HUMANS; MAGNETIC RESONANCE IMAGING; MODELS, MOLECULAR; MOLECULAR CONFORMATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PRESSURE; PRIONS; PROTEIN FOLDING; PROTEIN ISOFORMS;

ANIMALIA;

EID: 33748176879     PISSN: 14726807     EISSN: 14726807     Source Type: Journal    
DOI: 10.1186/1472-6807-6-16     Document Type: Article

References (60)

1. Weissmann C, Enari M, Klohn PC, Rossi D, Flechsig E: Transmission of prions. PNAS 2002, 99(Suppl 4):16378-16383.
2. Prusiner SB: Prions. PNAS 1998, 95:13363-13383.
3. Prusiner SB: Novel proteinaceous infectious particles cause scrapie. Science 1982, 216:136-144.
4. Bueler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, Weissmann C: Mice devoid of PrP are resistant to scrapie. Cell 1993, 73:1339-1347.
5. Sailer A, Bueler H, Fischer M, Aguzzi A, Weissmann C: No propagation of prions in mice devoid of PrP. Cell 1994, 77:967-968.
6. Fischer M, Rulicke T, Raeber A, Sailer A, Moser M, Oesch B, Brandner S, Aguzzi A, Weissmann C: Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J 1996, 15:1255-1264.
7. Horiuchi M, Caughey B: Prion protein interconversions and the transmissible spongiform encephalopathies. Structure Fold Des 1999, 7:R231-R240.
8. Legname G, Baskakov IV, Nguyen HO, Riesner D, Cohen FE, DeArmond SJ, Prusiner SB: Synthetic mammalian prions. Science 2004, 305:673-676.
9. Collinge J: Prion diseases of humans and animals: their causes and molecular basis. Annu Rev Neurosci 2001, 24:519-550.
10. Prusiner SB, Scott M, Foster D, Pan KM, Groth D, Mirenda C, Torchia M, Yang SL, Serban D, Carlson GA, et al.: Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 1990, 63:673-686.
11. Chen SG, Gambetti P: A journey through the species barrier. Neuron 2002, 34:854-856.
12. Peretz D, Williamson RA, Legname G, Matsunaga Y, Vergara J, Burton DR, DeArmond SJ, Prusiner SB, Scott MR: A change in the conformation of prions accompanies the emergence of a new prion strain. Neuron 2002, 34:921-932.
13. King CY, Diaz-Avalos R: Protein-only transmission of three yeast prion strains. Nature 2004, 428:319-323.
14. Tanaka M, Chien P, Naber N, Cooke R, Weissman JS: Conformational variations in an infectious protein determine prion strain differences. Nature 2004, 428:323-328.
15. Chien P, Weissman JS, DePace AH: Emerging principles of conformation-based prion inheritance. Annual Review of Biochemistry 2004, 73:617-656.
16. Vanik DL, Surewicz KA, Surewicz WK: Molecular basis of barriers for interspecies transmissibility of mammalian prions. Mol Cell 2004, 14:139-145.
17. James TL, Liu H, Ulyanov NB, Farr-Jones S, Zhang H, Donne DG, Kaneko K, Groth D, Mehlhorn I, Prusiner SB, et al.: Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform. PNAS 1997, 94:10086-10091.
18. Donne DG, Viles JH, Groth D, Mehlhorn I, James TL, Cohen FE, Prusiner SB, Wright PE, Dyson HJ: Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible. PNAS 1997, 94:13452-13457.
19. Zahn R, Liu A, Luhrs T, Riek R, von Schroetter C, Lopez GF, Billeter M, Calzolai L, Wider G, Wuthrich K: NMR solution structure of the human prion protein. PNAS 2000, 97:145-150.
20. Calzolai L, Zahn R: Influence of pH on NMR Structure and Stability of the Human Prion Protein Globular Domain. J Biol Chem 2003, 278:35592-35596.
21. Knaus KJ, Morillas M, Swietnicki W, Malone M, Surewicz WK, Yee VC: Crystal structure of the human prion protein reveals a mechanism for oligomerization. Nat Struct Biol 2001, 8:770-774.
22. Lopez GF, Zahn R, Riek R, Wuthrich K: NMR structure of the bovine prion protein. PNAS 2000, 97:8334-8339.
23. Hornemann S, Glockshuber R: A scrapie-like unfolding intermediate of the prion protein domain PrP(121-231) induced by acidic pH. PNAS 1998, 95:6010-6014.
24. Jackson GS, Hosszu LL, Power A, Hill AF, Kenney J, Saibil H, Craven CJ, Waltho JP, Clarke AR, Collinge J: Reversible conversion of monomeric human prion protein between native and fibrilogenic conformations. Science 1999, 283:1935-1937.
25. Inoue K, Yamada H, Akasaka K, Herrmann C, Kremer W, Maurer T, Doker R, Kalbitzer HR: Pressure-induced local unfolding of the Ras binding domain of RalGDS. Nat Struct Biol 2000, 7:547-550.
26. Foguel D, Silva JL: New insights into the mechanisms of protein misfolding and aggregation in amyloidogenic diseases derived from pressure studies. Biochemistry 2004, 43:11361-11370.
27. Silva JL, Foguel D, Royer CA: Pressure provides new insights into protein folding, dynamics and structure. Trends Biochem Sci 2001, 26:612-618.
28. Kamatari YO, Kitahara R, Yamada H, Yokoyama S, Akasaka K: High-pressure NMR spectroscopy for characterizing folding intermediates and denatured states of proteins. Methods 2004, 34:133-143.
29. Torrent J, Alvarez-Martinez MT, Heitz F, Liautard JP, Balny C, Lange R: Alternative prion structural changes revealed by high pressure. Biochemistry 2003, 42:1318-1325.
30. Torrent J, Alvarez-Martinez MT, Harricane MC, Heitz F, Liautard JP, Balny C, Lange R: High pressure induces scrapie-like prion protein misfolding and amyloid fibril formation. Biochemistry 2004, 43:7162-7170.
31. Torrent J, Alvarez-Martinez MT, Liautard JP, Balny C, Lange R: The role of the 132-160 region in prion protein conformational transitions. Protein Sci 2005, 14:956-967.
32. Cordeiro Y, Kraineva J, Ravindra R, Lima LM, Gomes MPB, Foguel D, Winter R, Silva JL: Hydration and packing effects on prion folding and {beta}-sheet conversion: high pressure spectroscopy and pressure perturbation calorimetry studies. J Biol Chem 2004, 279:32354-32359.
33. Martins SM, Chapeaurouge A, Ferreira ST: Folding intermediates of the prion protein stabilized by hydrostatic pressure and low temperature. J Biol Chem 2003, 278:50449-50455.
34. Kuwata K, Li H, Yamada H, Legname G, Prusiner SB, Akasaka K, James TL: Locally disordered conformer of the hamster prion protein: a crucial intermediate to PrPSc? Biochemistry 2002, 41:12277-12283.
35. Zahn R: The octapeptide repeats in mammalian prion protein constitute a pH-dependent folding and aggregation site. J Mol Biol 2003, 334:477-488.
36. Arnold MR, Kremer W, Ludemann HD, Kalbitzer HR: 1H-NMR parameters of common amino acid residues measured in aqueous solutions of the linear tetrapeptides Gly-Gly-X-Ala at pressures between 0.1 and 200 MPa. Biophys Chem 2002, 96:129-140.
37. Maurer T, Meier S, Kachel N, Munte CE, Hasenbein S, Koch B, Hengstenberg W, Kalbitzer HR: High-resolution structure of the Histidine-Containing Phosphocarrier Protein (HPr) from Staphylococcus aureus and characterization of its interaction with the bifunctional HPr Kinase/Phosphorylase. J Bacteriol 2004, 186:5906-5918.
38. Stanley EM, Batten RC: Viscosity of water at high pressures and moderate temperatures. J Phys Chem 1969, 73:1187-1191.
39. Akasaka K, Li H: Low-lying excited states of proteins revealed from nonlinear pressure shifts in 1H and 15N NMR. Biochemistry 2001, 40:8665-8671.
40. Castilla J, Saa P, Hetz C, Soto C: In vitro generation of infectious scrapie prions. Cell 2005, 121:195-206.
41. Tanaka M, Chien P, Yonekura K, Weissman JS: Mechanism of cross-species prion transmission: An infectious conformation compatible with two highly divergent yeast prion proteins. Cell 2005, 121:49-62.
42. Jones EM, Surewicz WK: Fibril conformation as the basis of species-and strain-dependent seeding specificity of mammalian prion amyloids. Cell 2005, 121:63-72.
43. Baskakov IV, Legname G, Baldwin MA, Prusiner SB, Cohen FE: Pathway complexity of prion protein assembly into amyloid. J Biol Chem 2002, 277:21140-21148.
44. Schwarzinger S, Kroon GJ, Foss TR, Chung J, Wright PE, Dyson HJ: Sequence-dependent correction of random coil NMR chemical shifts. J Am Chem Soc 2001, 123:2970-2978.
45. Wille H, Michelitsch MD, Guenebaut V, Supattapone S, Serban A, Cohen FE, Agard DA, Prusiner SB: Structural studies of the scrapie prion protein by electron crystallography. PNAS 2002, 99:3563-3568.
46. Govaerts C, Wille H, Prusiner SB, Cohen FE: Evidence for assembly of prions with left-handed {beta}-helices into trimers. PNAS 2004:0402254101.
47. Hummer G, Garde S, Garcia AE, Paulaitis ME, Pratt LR: The pressure dependence of hydrophobic interactions is consistent with the observed pressure denaturation of proteins. PNAS 1998, 95:1552-1555.
48. Nicholson EM, Mo H, Prusiner SB, Cohen FE, Marqusee S: Differences between the prion protein and its homolog Doppel: a partially structured state with implications for scrapie formation. J Mol Biol 2002, 316:807-815.
49. Hosszu LL, Baxter NJ, Jackson GS, Power A, Clarke AR, Waltho JP, Craven CJ, Collinge J: Structural mobility of the human prion protein probed by backbone hydrogen exchange. Nat Struct Biol 1999, 6:740-743.
50. Heppner FL, Musahl C, Arrighi I, Klein MA, Rulicke T, Oesch B, Zinkernagel RM, Kalinke U, Aguzzi A: Prevention of scrapie pathogenesis by transgenic expression of anti-prion protein antibodies. Science 2001, 294:178-182.
51. Peretz D, Williamson RA, Kaneko K, Vergara J, Leclerc E, Schmitt-Ulms G, Mehlhorn IR, Legname G, Wormald MR, Rudd PM, et al.: Antibodies inhibit prion propagation and clear cell cultures of prion infectivity. Nature 2001, 412:739-743.
52. Zahn R, von Schroetter C, Wuthrich K: Human prion proteins expressed in Escherichia coli and purified by high-affinity column refolding. FEBS Lett 1997, 417:400-404.
53. Yamada H: Pressure-resisting glass cell for high pressure, high resolution NMR measurement. Rev Sci Instrum 1974, 45:640-642.
54. Price WE, Ludemann HD: NMR and diaphragm cell techniques for the study of molecular dynamics in fluids. In High Pressure Techniques in Chemistry and Physics: A Practical Approach Edited by: Holzapfel WB, Isaacs NS. Oxford: Oxford University Press; 1997:225.
55. Arnold MR, Kalbitzer HR, Kremer W: High-sensitivity sapphire cells for high pressure NMR spectroscopy on proteins. J Magn Reson 2003, 161:127-131.
56. Kremer W, Arnold MR, Kachel N, Kalbitzer HR: The use of high-sensitivity sapphire cells in high pressure NMR spectroscopy and its application to proteins. Spectroscopy 2004, 18:271-278.
57. Pervushin K, Riek R, Wider G, Wuthrich K: Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. PNAS 1997, 94:12366-12371.
58. Gronwald W, Kalbitzer HR: Automated structure determination of proteins by NMR spectroscopy. Prog Nucl Mag Res Sp 2004, 44:33-96.
59. AUREMOL Homepage [http://www.auremol.de]
60. Koradi R, Billeter M, Wuthrich K: MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 1996, 14:51-32.