Rapid folding of the prion protein captured by pressure-jump

European Biophysics Journal

Volumn 38, Issue 5, 2009, Pages 625-635

  Jenkins, David C ^a   Pearson, David S ^b   Harvey, Andrew ^a   Sylvester, Ian D ^a   Geeves, Michael A ^b   Pinheiro, Teresa J T ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF KENT   (United Kingdom)

Author keywords

Folding intermediate; Folding kinetics; Pressure jump; Prion conversion; Prion folding; Tryptophan mutant

Indexed keywords

PRION PROTEIN; TRYPTOPHAN;

ARTICLE; CIRCULAR DICHROISM; FLUORESCENCE SPECTROSCOPY; MUTANT; NONHUMAN; PRESSURE; PROTEIN FOLDING; PROTEIN STABILITY; THERMODYNAMICS;

ANIMALS; CIRCULAR DICHROISM; CRICETINAE; KINETICS; MESOCRICETUS; MUTATION; PEPTIDE FRAGMENTS; PRESSURE; PRIONS; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN RENATURATION; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, FLUORESCENCE; TEMPERATURE; THERMODYNAMICS;

EID: 67349217669     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-009-0420-6     Document Type: Article

References (50)

1. Sc-like) conformation Biochim Biophys Acta 1645 228 240 (Pubitemid 38229282)
2. AC Apetri WK Surewicz 2002 Kinetic intermediate in the folding of human prion protein J Biol Chem 277 44589 44592 10.1074/jbc.C200507200 (Pubitemid 36159046)
3. AC Apetri K Surewicz WK Surewicz 2004 The effect of disease-associated mutations on the folding pathway of human prion protein J Biol Chem 279 18008 18014 10.1074/jbc.M313581200 (Pubitemid 38560570)
4. AC Apetri K Maki H Roder WK Surewicz 2006 Early intermediate in human prion protein folding as evidenced by ultrarapid mixing experiments J Am Chem Soc 128 11673 11678 10.1021/ja063880b (Pubitemid 44338858)
5. DC Bolton MP McKinley SB Prusiner 1982 Identification of a protein that purifies with the scrapie prion Science 218 1309 1311 10.1126/science.6815801
6. D Borchelt A Taraboulos S Prusiner 1992 Evidence for synthesis of scrapie prion proteins in the endocytic pathway J Biol Chem 267 16188 16199
7. B Caughey GJ Raymond D Ernst RE Race 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
8. B Chesebro R Race K Wehrly J Nishio M Bloom D Lechner S Bergstrom K Robbins L Mayer JM Keith C Garon A Haase 1985 Identification of scrapie prion protein-specific mRNA in scrapie-infected and uninfected brain Nature 315 331 333 10.1038/315331a0 (Pubitemid 15044624)
9. FE Cohen KM Pan Z Huang M Baldwin RJ Fletterick SB Prusiner 1994 Structural clues to prion replication Science 264 530 531 10.1126/science. 7909169 (Pubitemid 24185856)
10. J Collinge 2005 Molecular neurology of prion disease J Neurol Neurosurg Psychiatry 76 906 919 10.1136/jnnp.2004.048660 (Pubitemid 40909547)
11. Y Cordeiro J Kraineva M Gomes M Lopes VR Martins L Lima D Foguel R Winter JL Silva 2005 The amino-terminal PrP domain is crucial to modulate prion misfolding and aggregation Biophys J 89 2667 2676 10.1529/biophysj.105.067603 (Pubitemid 41401056)
12. Y Cordeiro J Kraineva MP Gomes MH Lopes VR Martins LM Lima D Foguel R Winter JL Silva 2005 The amino-terminal PrP domain is crucial to modulate prion misfolding and aggregation Biophys J 89 2667 2676 10.1529/biophysj.105.067603 (Pubitemid 41401056)
13. Y Cordeiro J Kraineva R Winter JL Silva 2005 Volume and energy folding landscape of prion protein revealed by pressure Braz J Med Biol Res 38 1195 1201 10.1590/S0100-879X2005000800006 (Pubitemid 41167283)
14. SJ DeArmond H Sanchez F Yehiely Y Qiu A Ninchak-Casey V Daggett AP Camerino J Cayetano M Rogers D Groth M Torchia P Tremblay MR Scott FE Cohen SB Prusiner 1997 Selective neuronal targeting in prion disease Neuron 19 1337 1348 10.1016/S0896-6273(00)80424-9 (Pubitemid 28030552)
15. DG Donne JH Viles D Groth I Mehlhorn TL James FE Cohen SB Prusiner PE Wright HJ Dyson 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 10.1073/pnas.94.25.13452 (Pubitemid 28009603)
16. J Font J Torrent M Ribo DV Laurents C Balny M Vilanova R Lange 2006 Pressure-jump induced kinetics reveals a hydration dependent folding/unfolding mechanism of ribonuclease A Biophys J 91 2264 2274 (Pubitemid 44352408)
17. SC Gill PH von Hippel 1989 Calculation of protein extinction coefficients from amino acid sequence data Anal Biochem 182 319 326 10.1016/0003-2697(89) 90602-7 (Pubitemid 19277112)
18. N Guex MC Peitsch 1997 SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling Electrophoresis 18 2714 2723 10.1002/elps.1150181505 (Pubitemid 28059943)
19. S Hornemann R Glockshuber 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 10.1073/pnas.95.11.6010 (Pubitemid 28248955)
20. LL Hosszu MA Wells GS Jackson S Jones M Batchelor AR Clarke CJ Craven JP Waltho J Collinge 2005 Definable equilibrium states in the folding of human prion protein Biochemistry 44 16649 16657 10.1021/bi051277k (Pubitemid 41832045)
21. GS Jackson AF Hill C Joseph LL Hosszu A Power JP Waltho AR Clarke J Collinge 1999 Multiple folding pathways for heterologously expressed human prion protein Biochim Biophys Acta 1431 1 13 (Pubitemid 29182716)
22. M Jacob G Holtermann D Perl J Reinstein T Schindler MA Geeves FX Schmid 1999 Microsecond folding of the cold shock protein measured by a pressure-jump technique Biochemistry 38 2882 2891 10.1021/bi982487i (Pubitemid 29131794)
23. TL James H Liu NB Ulyanov S Farr-Jones H Zhang DG Donne K Kaneko D Groth I Mehlhorn SB Prusiner FE Cohen 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 10.1073/pnas.94.19.10086 (Pubitemid 27406998)
24. DC Jenkins ID Sylvester TJ Pinheiro 2008 The elusive intermediate on the folding pathway of the prion protein FEBS J 275 1323 1335 10.1111/j.1742-4658. 2008.06293.x
25. J Kazlauskaite N Sanghera I Sylvester C Venien-Bryan TJ Pinheiro 2003 Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization Biochemistry 42 3295 3304 10.1021/bi026872q (Pubitemid 36348638)
26. K Kuwata H Li H Yamada G Legname SB Prusiner K Akasaka TL James 2002 Locally disordered conformer of the hamster prion protein: a crucial intermediate to PrPSc? Biochemistry 41 12277 12283 10.1021/bi026129y
27. Lakowicz JR (1999) Protein fluorescence, 2nd edn. Kluwer Academic/Plenum Publishers, New York
28. S Liemann R Glockshuber 1999 Influence of amino acid substitutions related to inherited human prion diseases on the thermodynamic stability of the cellular prion protein Biochemistry 38 3258 3267 10.1021/bi982714g (Pubitemid 29148900)
29. H Liu S Farr-Jones NB Ulyanov M Llinas S Marqusee D Groth FE Cohen SB Prusiner TL James 1999 Solution structure of Syrian hamster prion protein rPrP(90-231) Biochemistry 38 5362 5377 10.1021/bi982878x (Pubitemid 29211221)
30. MP McKinley DC Bolton SB Prusiner 1983 A protease-resistant protein is a structural component of the scrapie prion Cell 35 57 62 10.1016/0092-8674(83) 90207-6 (Pubitemid 14240218)
31. I Mehlhorn D Groth J Stockel B Moffat D Reilly D Yansura WS Willett M Baldwin R Fletterick FE Cohen R Vandlen D Henner SB Prusiner 1996 High-level expression and characterization of a purified 142-residue polypeptide of the prion protein Biochemistry 35 5528 5537 10.1021/bi952965e (Pubitemid 26136530)
32. RK Meyer MP McKinley KA Bowman MB Braunfeld RA Barry SB Prusiner 1986 Separation and properties of cellular and scrapie prion proteins Proc Natl Acad Sci USA 83 2310 2314 10.1073/pnas.83.8.2310 (Pubitemid 16026876)
33. EM Nicholson H Mo SB Prusiner FE Cohen S Marqusee 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 10.1006/jmbi.2001.5347 (Pubitemid 34729256)
34. B Oesch D Westaway M Walchli MP McKinley SB Kent R Aebersold RA Barry P Tempst DB Teplow LE Hood 1985 A cellular gene encodes scrapie PrP 27-30 protein Cell 40 735 746 10.1016/0092-8674(85)90333-2 (Pubitemid 15240279)
35. CN Pace 1986 Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol 131 266 280 10.1016/0076-6879(86)31045-0 (Pubitemid 16002205)
36. KM Pan M Baldwin J Nguyen M Gasset A Serban D Groth I Mehlhorn Z Huang RJ Fletterick FE Cohen SB Prusiner 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 10.1073/pnas.90.23.10962 (Pubitemid 23354348)
37. DS Pearson G Holtermann P Ellison C Cremo MA Geeves 2002 A novel pressure-jump apparatus for the microvolume analysis of protein-ligand and protein-protein interactions: its application to nucleotide binding to skeletal-muscle and smooth-muscle myosin subfragment-1 Biochem J 366 643 651 10.1042/BJ20020462
38. SB Prusiner 1998 Prions Proc Natl Acad Sci USA 95 13363 13383 10.1073/pnas.95.23.13363 (Pubitemid 28525623)
39. SB Prusiner MR Scott SJ DeArmond FE Cohen 1998 Prion protein biology Cell 93 337 348 10.1016/S0092-8674(00)81163-0 (Pubitemid 28232079)
40. R Riek S Hornemann G Wider M Billeter R Glockshuber K Wuthrich 1996 NMR structure of the mouse prion protein domain PrP(121-321) Nature 382 180 182 10.1038/382180a0 (Pubitemid 26242887)
41. H Roder W Colon 1997 Kinetic role of early intermediates in protein folding Curr Opin Struct Biol 7 15 28 10.1016/S0959-440X(97)80004-8 (Pubitemid 27092376)
42. N Sanghera TJ Pinheiro 2002 Binding of prion protein to lipid membranes and implications for prion conversion J Mol Biol 315 1241 1256 10.1006/jmbi.2001.5322 (Pubitemid 34729301)
43. MM Santoro DW Bolen 1988 Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants Biochemistry 27 8063 8068 10.1021/bi00421a014 (Pubitemid 18254049)
44. N Stahl MA Baldwin DB Teplow L Hood BW Gibson AL Burlingame SB Prusiner 1993 Structural studies of the scrapie prion protein using mass spectrometry and amino acid sequencing Biochemistry 32 1991 2002 10.1021/bi00059a016 (Pubitemid 23086050)
45. W Swietnicki R Petersen P Gambetti WK Surewicz 1997 pH-dependent stability and conformation of the recombinant human prion protein PrP(90-231) J Biol Chem 272 27517 27520 10.1074/jbc.272.44.27517 (Pubitemid 27473537)
46. W Swietnicki RB Petersen P Gambetti WK Surewicz 1998 Familial mutations and the thermodynamic stability of the recombinant human prion protein J Biol Chem 273 31048 31052 10.1074/jbc.273.47.31048 (Pubitemid 28533111)
47. W Swietnicki M Morillas SG Chen P Gambetti WK Surewicz 2000 Aggregation and fibrillization of the recombinant human prion protein huPrP90-231 Biochemistry 39 424 431 10.1021/bi991967m (Pubitemid 30056478)
48. GJA Vidugiris DM Truckses JL Markley CA Royer 1996 High-pressure denaturation of staphylococcal nuclease proline-to-glycine substitution mutants Biochemistry 35 3857 3864 10.1021/bi952012g (Pubitemid 26102178)
49. G Wildegger S Liemann R Glockshuber 1999 Extremely rapid folding of the C-terminal domain of the prion protein without kinetic intermediates Nat Struct Biol 6 550 553 10.1038/9323 (Pubitemid 29252834)
50. H Zhang J Stockel I Mehlhorn D Groth MA Baldwin SB Prusiner TL James FE Cohen 1997 Physical studies of conformational plasticity in a recombinant prion protein Biochemistry 36 3543 3553 10.1021/bi961965r (Pubitemid 27143508)