The elusive intermediate on the folding pathway of the prion protein

FEBS Journal

Volumn 275, Issue 6, 2008, Pages 1323-1335

  Jenkins, David C ^a   Sylvester, Ian D ^a   Pinheiro, Teresa J T ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Denaturant unfolding; Molten globule; Phase diagram; Prion conversion; Prion diseases

Indexed keywords

PRION PROTEIN;

ARTICLE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING; THERMODYNAMICS;

ANIMALS; CIRCULAR DICHROISM; CRICETINAE; FLUORESCENCE; MUTATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PRPC PROTEINS; TRYPTOPHAN;

EID: 40349108841     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06293.x     Document Type: Article

References (64)

1. Collinge J (2005) Molecular neurology of prion disease. J Neurol Neurosurg Psychiatry 76, 906 919.
2. Oesch B, Westaway D, Walchli M, McKinley MP, Kent SB, Aebersold R, Barry RA, Tempst P, Teplow DB, Hood LE et al. (1985) A cellular gene encodes scrapie PrP 27-30 protein. Cell 40, 735 746.
3. Chesebro B, Race R, Wehrly K, Nishio J, Bloom M, Lechner D, Bergstrom S, Robbins K, Mayer L, Keith JM et al. (1985) Identification of scrapie prion protein-specific mRNA in scrapie-infected and uninfected brain. Nature 315, 331 333.
4. Stahl N, Baldwin MA, Teplow DB, Hood L, Gibson BW, Burlingame AL Prusiner SB (1993) Structural studies of the scrapie prion protein using mass spectrometry and amino acid sequencing. Biochemistry 32, 1991 2002.
5. Liu H, Farr-Jones S, Ulyanov NB, Llinas M, Marqusee S, Groth D, Cohen FE, Prusiner SB James TL (1999) Solution structure of Syrian hamster prion protein rPrP(90-231). Biochemistry 38, 5362 5377.
6. James TL, Liu H, Ulyanov NB, Farr-Jones S, Zhang H, Donne DG, Kaneko K, Groth D, Mehlhorn I, Prusiner SB et al. (1997) Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform. Proc Natl Acad Sci USA 94, 10086 10091.
7. Donne DG, Viles JH, Groth D, Mehlhorn I, James TL, Cohen FE, Prusiner SB, Wright PE Dyson HJ (1997) Structure of the recombinant full-length hamster prion protein PrP(29-231): the N-terminus is highly flexible. Proc Natl Acad Sci USA 94, 13452 13457.
8. Riek R, Hornemann S, Wider G, Billeter M, Glockshuber R Wuthrich K (1996) NMR structure of the mouse prion protein domain PrP(121-321). Nature 382, 180 182.
9. Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, Mehlhorn I, Huang Z, Fletterick RJ, Cohen FE et al. (1993) Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci USA 90, 10962 10966.
10. Meyer RK, McKinley MP, Bowman KA, Braunfeld MB, Barry RA Prusiner SB (1986) Separation and properties of cellular and scrapie prion proteins. Proc Natl Acad Sci USA 83, 2310 2314.
11. McKinley MP, Bolton DC Prusiner SB (1983) A protease-resistant protein is a structural component of the scrapie prion. Cell 35, 57 62.
12. Prusiner SB, Scott MR, DeArmond SJ Cohen FE (1998) Prion protein biology. Cell 93, 337 348.
13. Apetri AC, Maki K, Roder H Surewicz WK (2006) Early intermediate in human prion protein folding as evidenced by ultrarapid mixing experiments. J Am Chem Soc 128, 11673 11678.
14. Apetri AC, Surewicz K Surewicz WK (2004) The effect of disease-associated mutations on the folding pathway of human prion protein. J Biol Chem 279, 18008 18014.
15. Apetri AC Surewicz WK (2002) Kinetic intermediate in the folding of human prion protein. J Biol Chem 277, 44589 44592.
16. Swietnicki W, Petersen R, Gambetti P Surewicz WK (1997) pH-dependent stability and conformation of the recombinant human prion protein PrP(90-231). J Biol Chem 272, 27517 27520.
17. Swietnicki W, Morillas M, Chen SG, Gambetti P Surewicz WK (2000) Aggregation and fibrillization of the recombinant human prion protein huPrP90-231. Biochemistry 39, 424 431.
18. Hosszu LL, Wells MA, Jackson GS, Jones S, Batchelor M, Clarke AR, Craven CJ, Waltho JP Collinge J (2005) Definable equilibrium states in the folding of human prion protein. Biochemistry 44, 16649 16657.
19. Kuwata K, Li H, Yamada H, Legname G, Prusiner SB, Akasaka K James TL (2002) Locally disordered conformer of the hamster prion protein: a crucial intermediate to PrPSc? Biochemistry 41, 12277 12283.
20. Nicholson EM, Mo H, Prusiner SB, Cohen FE Marqusee S (2002) Differences between the prion protein and its homolog doppel: a partially structured state with implications for scrapie formation. J Mol Biol 316, 807 815.
21. Martins SM, Chapeaurouge A Ferreira ST (2003) Folding intermediates of the prion protein stabilized by hydrostatic pressure and low temperature. J Biol Chem 278, 50449 50455.
22. Bolton DC, McKinley MP Prusiner SB (1982) Identification of a protein that purifies with the scrapie prion. Science 218, 1309 1311.
23. Smith CJ, Clarke AR, Chia WN, Irons LI, Atkinson T Holbrook JJ (1991) Detection and characterization of intermediates in the folding of large proteins by the use of genetically inserted tryptophan probes. Biochemistry 30, 1028 1036.
24. Tew DJ Bottomley SP (2001) Probing the equilibrium denaturation of the serpin alpha(1)-antitrypsin with single tryptophan mutants; evidence for structure in the urea unfolded state. J Mol Biol 313, 1161 1169.
25. Wildegger G, Liemann S Glockshuber R (1999) Extremely rapid folding of the C-terminal domain of the prion protein without kinetic intermediates. Nat Struct Biol 6, 550 553.
26. Riek R, Hornemann S, Wider G, Glockshuber R Wuthrich K (1997) mPrP(23-231). FEBS Lett 413, 282 288.
27. Grimsley JK, Scholtz JM, Pace CN Wild JR (1997) Organophosphorous hydrolase is a remarkably stable enzyme that unfolds through a homodimeric intermediate. Biochemistry 36, 14366 14374.
28. Staiano M, Scognamiglio V, Rossi M, D'Auria S, Stepanenko OV, Kuznetsova IM Turoverov KK (2005) Unfolding and refolding of the glutamine-binding protein from Escherichia coli and its complex with glutamine induced by guanidine hydrochloride. Biochemistry 44, 5625 5633.
29. Kuznetsova IM, Turoverov KK Uversky VN (2004) Use of the phase diagram method to analyze the protein unfolding-refolding reactions: fishing out the 'invisible' intermediates. J Proteome Res 3, 485 494.
30. Bushmarina NA, Kuznetsova IM, Biktashev AG, Turoverov KK Uversky VN (2001) Partially folded conformations in the folding pathway of bovine carbonic anhydrase II: a fluorescence spectroscopic analysis. Chembiochem 2, 813 821.
31. Zhang H, Stockel J, Mehlhorn I, Groth D, Baldwin MA, Prusiner SB, James TL Cohen FE (1997) Physical studies of conformational plasticity in a recombinant prion protein. Biochemistry 36, 3543 3553.
32. Jackson GS, Hill AF, Joseph C, Hosszu LL, Power A, Waltho JP, Clarke AR Collinge J (1999) Multiple folding pathways for heterologously expressed human prion protein. Biochim Biophys Acta 1431, 1 13.
33. Ptitsyn OB (1992) The molten globule state. In Protein Folding (Creighton TE ed pp. 243 300. Freeman, New York, NY.
34. Kelly SM Price NC (1997) The application of circular dichroism to studies of protein folding and unfolding. Biochim Biophys Acta 1338, 161 185.
35. Cohen FE, Pan KM, Huang Z, Baldwin M, Fletterick RJ Prusiner SB (1994) Structural clues to prion replication. Science 264, 530 531.
36. Hornemann S Glockshuber R (1998) A scrapie-like unfolding intermediate of the prion protein domain PrP(121-231) induced by acidic pH. Proc Natl Acad Sci USA 95, 6010 6014.
37. Fersht AR (1997) Nucleation mechanisms in protein folding. Curr Opin Struct Biol 7, 3 9.
38. Daggett V Fersht AR (2003) Is there a unifying mechanism for protein folding? Trends Biochem Sci 28, 18 25.
39. Uversky VN Fink AL (2002) The chicken-egg scenario of protein folding revisted. FEBS Lett 515, 79 83.
40. Bocharova OV, Breydo L, Parfenov AS, Salnikov VV Baskakov IV (2005) In vitro conversion of full-length mammalian prion protein produces amyloid form with physical properties of PrP(Sc). J Mol Biol 346, 645 659.
41. Baskakov IV, Legname G, Baldwin MA, Prusiner SB Cohen FE (2002) Pathway complexity of prion protein assembly into amyloid. J Biol Chem 277, 21140 21148.
42. Legname G, Nguyen HO, Peretz D, Cohen FE, DeArmond SJ Prusiner SB (2006) Continuum of prion protein structures enciphers a multitude of prion isolate-specified phenotypes. Proc Natl Acad Sci USA 103, 19105 19110.
43. Legname G, Baskakov IV, Nguyen HO, Riesner D, Cohen FE, DeArmond SJ Prusiner SB (2004) Synthetic mammalian prions. Science 305, 673 676.
44. Hosszu LL, Baxter NJ, Jackson GS, Power A, Clarke AR, Waltho JP, Craven CJ Collinge J (1999) Structural mobility of the human prion protein probed by backbone hydrogen exchange. Nat Struct Biol 6, 740 743.
45. Glockshuber R (2001) Folding dynamics and energetics of recombinant prion proteins. Adv Protein Chem 57, 83 105.
46. Morillas M, Vanik DL Surewicz WK (2001) On the mechanism of alpha-helix to beta-sheet transition in the recombinant prion protein. Biochemistry 40, 6982 6987.
47. Gerber R, Tahiri-Alaoui A, Hore PJ James W (2007) Oligomerization of the human prion protein proceeds via a molten globule intermediate. J Biol Chem 282, 6300 6307.
48. Booth DR, Sunde M, Bellotti V, Robinson CV, Hutchinson WL, Fraser PE, Hawkins PN, Dobson CM, Radford SE, Blake CCF et al. (1997) Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis. Nature 385, 787 793.
49. Pertinhez TA, Bouchard M, Tomlinson EJ, Wain R, Ferguson SJ, Dobson CM Smith LJ (2001) Amyloid fibril formation by a helical cytochrome. FEBS Lett 495, 184 186.
50. Stahl N, Borchelt DR Prusiner SB (1990) Differential release of cellular and scrapie prion proteins from cellular membranes by phosphatidylinositol- specific phospholipase C. Biochemistry 29, 5405 5412.
51. Safar J, Ceroni M, Gajdusek DC Gibbs CJ Jr. (1991) Differences in the membrane interaction of scrapie amyloid precursor proteins in normal and scrapie- or Creutzfeldt-Jakob disease-infected brains. J Infect Dis 163, 488 494.
52. Borchelt D, Taraboulos A Prusiner S (1992) Evidence for synthesis of scrapie prion proteins in the endocytic pathway. J Biol Chem 267, 16188 16199.
53. Caughey B, Raymond GJ, Ernst D Race RE (1991) N-terminal truncation of the scrapie-associated form of PrP by lysosomal protease(s): implications regarding the site of conversion of PrP to the protease-resistant state. J Virol 65, 6597 6603.
54. Goto Y Fink AL (1989) Conformational states of beta-lactamase: molten-globule states at acidic and alkaline pH with high salt. Biochemistry 28, 945 952.
55. De Filippis V, de Laureto PP, Toniutti N Fontana A (1996) Acid-induced molten globule state of a fully active mutant of human interleukin-6. Biochemistry 35, 11503 11511.
56. van der Goot FG, Gonzalez-Manas JM, Lakey JH Pattus F (1991) A 'molten-globule' membrane-insertion intermediate of the pore-forming domain of colicin A. Nature 354, 408 410.
57. Pinheiro TJ, Cheng H, Seeholzer SH Roder H (2000) Direct evidence for the cooperative unfolding of cytochrome c in lipid membranes from H-(2)H exchange kinetics. J Mol Biol 303, 617 626.
58. Sanghera N Pinheiro TJ (2002) Binding of prion protein to lipid membranes and implications for prion conversion. J Mol Biol 315, 1241 1256.
59. Kazlauskaite J, Sanghera N, Sylvester I, Venien-Bryan C Pinheiro TJ (2003) Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization. Biochemistry 42, 3295 3304.
60. Mehlhorn I, Groth D, Stockel J, Moffat B, Reilly D, Yansura D, Willett WS, Baldwin M, Fletterick R, Cohen FE et al. (1996) High-level expression and characterization of a purified 142-residue polypeptide of the prion protein. Biochemistry 35, 5528 5537.
61. Gill SC von Hippel PH (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182, 319 326.
62. Pace CN (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol 131, 266 280.
63. Santoro MM Bolen DW (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27, 8063 8068.
64. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC Ferrin TE (2004) UCSF chimera - a visualization system for exploratory research and analysis. J Comput Chem 25, 1605 1612.