Highly polar environments catalyze the unfolding of PrPC helix 1

European Biophysics Journal

Volumn 39, Issue 8, 2010, Pages 1177-1192

  Lingenheil, Martin ^a   Denschlag, Robert ^a   Tavan, Paul ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Dielectric constant; Helix 1; Molecular dynamics; Peptide studies; Prion protein; Secondary structure

Indexed keywords

METHANOL; PEPTIDE; PRION PROTEIN; SOLVENT; WATER;

ALGORITHM; ARTICLE; CHEMISTRY; HUMAN; KINETICS; MOLECULAR DYNAMICS; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; STATIC ELECTRICITY; TEMPERATURE;

ALGORITHMS; HUMANS; KINETICS; METHANOL; MOLECULAR DYNAMICS SIMULATION; PEPTIDES; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PRPC PROTEINS; SOLVENTS; STATIC ELECTRICITY; TEMPERATURE; WATER;

EID: 77955657922     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-009-0570-6     Document Type: Article

References (82)

1. Allen MP, Tildesley DJ (1987) Computer simulations of liquids. Oxford University Press, Oxford
2. DOV Alonso A Cham V Daggett 2002 Simulations of biomolecules: characterization of the early steps in the ph-induced conformational conversion of the hamster, bovine and human forms of the prion protein Phil Trans R Soc Lond A 360 1165 1178 10.1098/rsta.2002.0986 1:CAS:528:DC%2BD38XmtVWhu7c%3D
3. HJC Berendsen JPM Postma WF van Gunsteren A Di Nola JR Haak 1984 Molecular dynamics with coupling to an external bath J Chem Phys 81 3684 3690 10.1063/1.448118 1:CAS:528:DyaL2cXmtlGksbY%3D
4. L Calzolai R Zahn 2003 Influence of ph on nmr structure and stability of the human prion protein globular domain J Biol Chem 278 35592 35596 10.1074/jbc.M303005200 1:CAS:528:DC%2BD3sXntVajs7c%3D 12826672 (Pubitemid 37102332)
5. BW Caughey A Dong KS Bhat D Ernst SF Hayes WS Caughey 1991 Secondary structure-analysis of the scrapie-associated protein prp 27-30 in water by infrared-spectroscopy Biochemistry 30 7672 7680 10.1021/bi00245a003 1:CAS:528:DyaK3MXks12mt7g%3D 1678278
6. NJ Cobb FD Sönnichsen H Mchaourab WK Surewicz 2007 Molecular architecture of human prion protein amyloid: a parallel, in-register β-structure Proc Natl Acad Sci USA 104 18946 18951 10.1073/pnas.0706522104 1:CAS:528:DC%2BD2sXhsVSru7nO 18025469
7. 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 1:CAS:528:DyaK2cXkslOrsrg%3D 7909169
8. S Colacino G Tiana RA Broglia G Colombo 2006 The determinants of stability in the human prion protein: insights into folding and misfolding from the analysis of the change in the stabilization energy distribution in different conditions Prot Struct Funct Bioinf 62 698 707 10.1002/prot.20804 1:CAS:528:DC%2BD28XhsVGru78%3D (Pubitemid 43191256)
9. A De Simone A Zagari P Derreumaux 2007 Structural and hydration properties of the partially unfolded states of the prion protein Biophys J 93 1284 1292 10.1529/biophysj.107.108613 1:CAS:528:DC%2BD2sXosFCjurY%3D 17483173 (Pubitemid 47330908)
10. ML DeMarco V Daggett 2004 From conversion to aggregation: Protofibril formation of the prion protein Proc Natl Acad Sci USA 101 2293 2298 10.1073/pnas.0307178101 1:CAS:528:DC%2BD2cXhvVOis70%3D 14983003 (Pubitemid 38269305)
11. R Denschlag M Lingenheil P Tavan 2008 Efficiency reduction and pseudo-convergence in replica exchange sampling of peptide folding-unfolding equilibria Chem Phys Lett 458 244 248 10.1016/j.cplett.2008.04.114 1:CAS:528:DC%2BD1cXmsFChtbg%3D
12. R Denschlag M Lingenheil P Tavan 2009 Optimal temperature ladders on replica exchange Chem Phys Lett 473 193 195 10.1016/j.cplett.2009.03.053 1:CAS:528:DC%2BD1MXkslGjtbg%3D
13. C. Proc Natl Acad Sci USA 101 15335 15340 10.1073/pnas.0404235101 1:CAS:528:DC%2BD2cXhtVKhsb3J 15494440 (Pubitemid 39441542)
14. F Eghiaian T Daubenfeld Y Quenet M van Audenhaege AP Bouin G van der Rest J Grosclaude H Rezaei 2007 Diversity in prion protein oligomerization pathways results from domain expansion as revealed by hydrogen/deuterium exchange and disulfide linkage Proc Natl Acad Sci USA 104 7414 7419 10.1073/pnas.0607745104 1:CAS:528:DC%2BD2sXlslWqtr8%3D 17442756 (Pubitemid 47185920)
15. M Eichinger H Grubmuller H Heller P Tavan 1997 Famusamm: an algorithm for rapid evaluation of electrostatic interactions in molecular dynamics simulations J Comput Chem 18 1729 1749 10.1002/(SICI)1096-987X(19971115)18: 14<1729::AID-JCC3>3.0.CO;2-M 1:CAS:528:DyaK2sXmvVKhtLk%3D
16. M Eigen 1996 Prionics or the kinetic basis of prion diseases Biophys Chem 63 A1 A18 10.1016/S0301-4622(96)02250-8 1:CAS:528:DyaK28XnsFymsrs%3D 8981746 (Pubitemid 26421976)
17. A Fernández A Crespo S Maddipati R Scott 2008 Bottom-up engineering of peptide cell translocators based on environmentally modulated quadrupole switches ACS nano 2 61 68 10.1021/nn700239j 19206548 (Pubitemid 351585765)
18. C Govaerts H Wille SB Prusiner FE Cohen 2004 Evidence for assembly of prions with left-handed β-helices into trimers Proc Natl Acad Sci USA 101 8342 8347 10.1073/pnas.0402254101 1:CAS:528:DC%2BD2cXkvFOmsLs%3D 15155909 (Pubitemid 38736577)
19. JS Griffith 1967 Self-replication and scrapie Nature 215 1043 1044 10.1038/2151043a0 1:STN:280:DyaF1c%2Fht1amtw%3D%3D 4964084
20. J Gsponer P Ferrara A Calfisch 2001 Flexibility of the murine prion protein and its Asp178Asn mutant investigated by molecular dynamics simulations J Mol Graphics Modell 20 169 182 10.1016/S1093-3263(01)00117-6 1:CAS:528:DC%2BD3MXos1Cmt78%3D (Pubitemid 33135513)
21. JR Hesp NDH Raven JM Sutton 2007 A role for His155 in binding of human prion peptide 144-167 to immobilised prion protein Biochem Biophys Res Commun 362 695 699 10.1016/j.bbrc.2007.08.050 1:CAS:528:DC%2BD2sXhtVWitLbM 17761148 (Pubitemid 47376683)
22. T Hirschberger M Stork B Schropp KF Winklhofer J Tatzelt P Tavan 2006 Structural instability of the prion protein upon M205S/R mutations revealed by molecular dynamics simulations Biophys J 90 3908 3918 10.1529/biophysj.105. 075341 1:CAS:528:DC%2BD28XltF2mtrg%3D 16513786 (Pubitemid 43846109)
23. XH Huang M Hagen B Kim RA Friesner RH Zhou BJ Berne 2007 Replica exchange with solute tempering: efficiency in large scale systems J Phys Chem B 111 5405 5410 10.1021/jp068826w 1:CAS:528:DC%2BD2sXkt1Knt7w%3D 17439169 (Pubitemid 46854533)
24. N Jamin YM Coic C Landon L Ovtracht F Baleux JM Neumann A Sanson 2002 Most of the structural elements of the globular domain of murine prion protein form fibrils with predominant beta-sheet structure FEBS Lett 529 256 260 10.1016/S0014-5793(02)03353-7 1:CAS:528:DC%2BD38Xns1ant7o%3D 12372610
25. JT Jarrett PT Lansbury Jr 1993 Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie Cell 73 1055 1058 10.1016/0092-8674(93)90635-4 1:CAS:528: DyaK3sXksVKnsL8%3D 8513491 (Pubitemid 23180480)
26. HF Ji HY Zhang LA Shen 2005 The role of electrostatic interaction in triggering the unraveling of stable helix 1 in normal prion protein. A molecular dynamics simulation investigation J Biomol Struct Dyn 22 563 570 1:CAS:528:DC%2BD2MXisVWhs74%3D 15702928
27. WL Jorgensen J Chandrasekhar JD Madura RW Impey ML Klein 1983 Comparison of simple potential functions for simulating liquid water J Chem Phys 79 926 935 10.1063/1.445869 1:CAS:528:DyaL3sXksF2htL4%3D
28. W Kabsch C Sander 1983 Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 22 2577 2637 10.1002/bip.360221211 1:CAS:528:DyaL2cXkslegtQ%3D%3D 6667333
29. HG Katzgraber S Trebst DA Huse M Troyer 2006 Feedback-optimized parallel tempering Monte Carlo J Stat Mech P 03018 1742 5468
30. DK Klimov D Thirumalai 2003 Dissecting the assembly of a beta(16-22) amyloid peptides into antiparallel beta sheets Structure 11 295 307 10.1016/S0969-2126(03)00031-5 1:CAS:528:DC%2BD3sXhvFait7w%3D 12623017 (Pubitemid 36287693)
31. SA Kozin G Bertho AK Mazur H Rabesona JP Girault T Haertle M Takahashi P Debey GHB Hoa 2001 Sheep prion protein synthetic peptide spanning helix 1 and beta-strand 2 (residues 142-166) shows beta-hairpin structure in solution J Biol Chem 276 46364 46370 10.1074/jbc.M108014200 1:CAS:528:DC%2BD3MXptVymtbk%3D 11577109
32. V Kraeutler WF van Gunsteren PH Hünenberger 2001 A fast SHAKE algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations J Comput Chem 22 501 508 10.1002/1096- 987X(20010415)22:5<501::AID-JCC1021>3.0.CO;2-V (Pubitemid 32291686)
33. JPM Langedijk G Fuentes R Boshuizen AMJJ Bonvin 2006 Two-rung model of a left-handed β-helix for prions explains species barrier and strain variation in transmissible spongiform encephalopathies J Mol Biol 360 907 920 10.1016/j.jmb.2006.05.042 1:CAS:528:DC%2BD28XmslKjsbY%3D 16782127 (Pubitemid 43993917)
34. Y Levy OM Becker 2002 Conformational polymorphism of wild-type and mutant prion proteins: energy landscape analysis Prot Struct Funct Genet 47 458 468 10.1002/prot.10095 1:CAS:528:DC%2BD38XksVyqu7w%3D (Pubitemid 34614725)
35. M Lingenheil R Denschlag R Reichold P Tavan 2008 The "hot-solvent/ cold-solute" problem revisited J Chem Theory Comput 4 1293 1306 10.1021/ct8000365 1:CAS:528:DC%2BD1cXotFyitLk%3D
36. AZ Liu P Riek R Zahn S Hornemann R Glockshuber K Wuthrich 1999 Peptides and proteins in neurodegenerative disease: helix propensity of a polypeptide containing helix 1 of the mouse prion protein studied by NMR and CD spectroscopy Biopolymers 51 145 152 10.1002/(SICI)1097-0282(1999)51:2<145::AID-BIP4>3. 0.CO;2-4 1:CAS:528:DyaK1MXkslGgu7o%3D 10397798 (Pubitemid 29352517)
37. P Liu B Kim RA Friesner BJ Berne 2005 Replica exchange with solute tempering: a method for sampling biological systems in explicit water Proc Natl Acad Sci USA 102 13749 13754 10.1073/pnas.0506346102 1:CAS:528: DC%2BD2MXhtVOqsb3P 16172406 (Pubitemid 41377651)
38. X Lu PL Wintrode WK Surewicz 2007 β-sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange Proc Natl Acad Sci USA 104 1510 1515 10.1073/pnas.0608447104 1:CAS:528: DC%2BD2sXhslaktr4%3D 17242357 (Pubitemid 46214621)
39. AD MacKerell Jr M Feig CL Brooks III 2004 Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J Comput Chem 25 1400 1415 10.1002/jcc.20065 1:CAS:528:DC%2BD2cXlsVOgt7c%3D 15185334
40. AD MacKerell D Bashford M Bellott RL Dunbrack JD Evanseck MJ Field S Fischer J Gao H Guo S Ha D Joseph-McCarthy L Kuchnir K Kuczera FTK Lau C Mattos S Michnick T Ngo DT Nguyen B Prodhom WE Reiher B Roux M Schlenkrich JC Smith R Stote J Straub M Watanabe J Wiorkiewicz-Kuczera D Yin M Karplus 1998 All-atom empirical potential for molecular modeling and dynamics studies of proteins J Phys Chem B 102 3586 3616 10.1021/jp973084f 1:CAS:528:DyaK1cXivVOlsb4%3D
41. G Mathias B Egwolf M Nonella P Tavan 2003 A fast multipole method combined with a reaction field for long-range electrostatics in molecular dynamics simulations: the effects of truncation on the properties of water J Chem Phys 118 10847 10860 10.1063/1.1574774 1:CAS:528:DC%2BD3sXksFynsrY%3D
42. S Megy G Bertho SA Kozin P Debey GHB Hoa JP Girault 2004 Possible role of region 152-156 in the structural duality of a peptide fragment from sheep prion protein Protein Sci 13 3151 3160 10.1110/ps.04745004 1:CAS:528: DC%2BD2cXhtVCjsLrK 15537751 (Pubitemid 39557786)
43. C helix 1 in the hydrophilic seeding of prion aggregates Proc Natl Acad Sci USA 96 11293 11298 10.1073/pnas.96.20.11293 1:CAS:528:DyaK1MXmvVCms7Y%3D 10500170 (Pubitemid 29487374)
44. LM Mukherjee E Grunwald 1958 Physical properties and hydrogen bonding in the system ethanol-2,2,2-trifluoroethanol J Phys Chem 62 1311 1314 10.1021/j150568a034 1:CAS:528:DyaG1MXhsVKktw%3D%3D
45. V Munoz L Serrano 1994 Elucidating the folding problem of helical peptides using empirical parameters Nature Struct Biol 1 399 409 10.1038/nsb0694-399 1:CAS:528:DyaK2cXmvFKmurc%3D 7664054 (Pubitemid 2083893)
46. V Munoz L Serrano 1995 Elucidating the folding problem of helical peptides using empirical parameters. II. Helix macrodipole effects and rational modification of the helical content of natural peptides J Mol Biol 245 275 296 10.1006/jmbi.1994.0023 1:CAS:528:DyaK2MXjtFGjsL4%3D 7844817
47. W Nadler UHE Hansmann 2008 Optimized explicit-solvent replica exchange molecular dynamics from scratch J Phys Chem B 112 10386 10387 10.1021/jp805085y 1:CAS:528:DC%2BD1cXptFCrsbc%3D 18671362
48. W Nadler JH Meinke UHE Hansmann 2008 Folding proteins by first-passage-times-optimized replica exchange Phys Rev E 78 061,905 10.1103/PhysRevE.78.061905
49. JW Nelson NR Kallenbach 1986 Stabilization of the ribonuclease s-peptide α-helix by trifluoroethanol Prot Struct Funct Genet 1 211 217 10.1002/prot.340010303 1:CAS:528:DyaL2sXltFGqtLs%3D
50. C Niedermeier P Tavan 1996 Fast version of the structure adapted multipole method-efficient calculation of electrostatic forces in protein dynamics Mol Simul 17 57 66 10.1080/08927029608024094 1:CAS:528: DyaK28XmtFKqs7s%3D
51. Sc J Virol 80 8521 8529 10.1128/JVI.00366-06 1:CAS:528:DC%2BD28XovVOjt7k%3D 16912302 (Pubitemid 44384864)
52. KM Pan M Baldwin J Nguyen M Gasset A Serban D Groth I Mehlhorn ZW Huang RJ Fletterick FE Cohen SB Prusiner 1993 Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins Proc Natl Acad Sci USA 90 10962 10966 10.1073/pnas.90.23.10962 1:CAS:528: DyaK2cXkvVCnug%3D%3D 7902575 (Pubitemid 23354348)
53. Sc aggregates J Virol 79 12355 12364 10.1128/JVI.79.19.12355-12364. 2005 1:CAS:528:DC%2BD2MXhtVGls7fP 16160162 (Pubitemid 41346097)
54. J Pankiewicz F Prelli MS Sy RJ Kascsak RB Kascsak DS Spinner RI Carp HC Meeker M Sadowski T Wisniewski 2006 Clearance and prevention of prion infection in cell culture by anti-PrP antibodies Eur J Neurosci 23 2635 2647 10.1111/j.1460-9568.2006.04805.x 16817866 (Pubitemid 43801455)
55. M Pappalardo D Milardi D Grasso C La Rosa 2007 Steered molecular dynamics studies reveal different unfolding pathways of prions from mammalian and non-mammalian species New J Chem 31 901 905 10.1039/b700764g 1:CAS:528:DC%2BD2sXmt1GjtLg%3D (Pubitemid 47324752)
56. SB Prusiner 1982 Novel proteinaceous infectious particles cause scrapie Science 216 136 144 10.1126/science.6801762 1:CAS:528:DyaL38XhsFyqtro%3D 6801762
57. SB Prusiner 1998 Prions Proc Natl Acad Sci USA 95 13363 13383 10.1073/pnas.95.23.13363 1:CAS:528:DyaK1cXnsVGhsbY%3D 9811807 (Pubitemid 28525623)
58. Reichold R (2009) Rechnergestützte Beschreibung der Struktur und Dynamik von Peptiden und ihren Bausteinen. Doktorarbeit, Fakultät für Physik, LMU München
59. E Rosta NV Buchete G Hummer 2009 Thermostat artifacts in replica exchange molecular dynamics simulations J Chem Theory Comput 5 1393 1399 10.1021/ct800557h 1:CAS:528:DC%2BD1MXktlSlsb0%3D 20046980
60. G Schaftenaar J Noordik 2000 Molden: a pre- and post-processing program for molecular and electronic structures J Comput Aid Mol Des 14 123 134 10.1023/A:1008193805436 1:CAS:528:DC%2BD3cXhslant7c%3D (Pubitemid 30110670)
61. S Schwarzinger AHC Horn J Ziegler H Sticht 2006 Rare large scale subdomain motions in prion protein can initiate aggregation J Biomol Struct Dyn 23 581 590 1:CAS:528:DC%2BD28XkvVCnt7k%3D 16615804
62. GJ Sharman N Kenward HE Williams M Landon RJ Mayer MS Searle 1998 Prion protein fragments spanning helix 1 and both strands of beta sheet (residues 125-170) show evidence for predominantly helical propensity by CD and NMR Fold Des 3 313 320 10.1016/S1359-0278(98)00043-1 1:CAS:528:DyaK1cXnt1Gltb8%3D 9806936 (Pubitemid 28494096)
63. M Shen KF Freed 2002 Long time dynamics of Met-Enkephalin: comparison of explicit and implicit solvent models Biophys J 82 1791 1808 10.1016/S0006- 3495(02)75530-6 1:CAS:528:DC%2BD38XivFKis7o%3D
64. KR Shoemaker PS Kim EJ York JM Stewart RL Baldwin 1987 Tests of the helix dipole model for stabilization of α-helices Nature 326 563 567 10.1038/326563a0 1:CAS:528:DyaL2sXktVart74%3D 3561498 (Pubitemid 17051328)
65. L Solforosi A Bellon M Schaller JT Cruite GC Abalos RA Williamson 2007 Toward molecular dissection of prpc-prpsc interaction J Biol Chem 282 7465 7471 10.1074/jbc.M610051200 1:CAS:528:DC%2BD2sXitlSrt7k%3D 17218310 (Pubitemid 47093641)
66. JO Speare TS Rush ME Bloom B Caughey 2003 The role of helix 1 aspartates and salt bridges in the stability and conversion of prion protein J Biol Chem 278 12522 12529 10.1074/jbc.M211599200 1:CAS:528:DC%2BD3sXisVOntbc%3D 12551897 (Pubitemid 36800241)
67. M Stork A Giese HA Kretzschmar P Tavan 2005 Molecular dynamics simulations indicate a possible role of parallel β-helices in seeded aggregation of poly-Gln Biophys J 88 2442 2451 10.1529/biophysj.104.052415 1:CAS:528:DC%2BD2MXjtFCjsL4%3D 15665127 (Pubitemid 40976115)
68. WK Surewicz EM Jones AC Apetri 2006 The emerging principles of mammalian prion propagation and transmissibility barriers: insight from studies in vitro Acc Chem Res 39 654 662 10.1021/ar050226c 1:CAS:528:DC%2BD28XkslWlsL0%3D 16981682
69. A Tahiri-Alaoui M Bouchard J Zurdo W James 2003 Competing intrachain interactions regulate the formation of beta-sheet fibrils in bovine PrP peptides Protein Sci 12 600 608 10.1110/ps.0236703 1:CAS:528:DC%2BD3sXhsFKmtbs%3D 12592030 (Pubitemid 36241116)
70. C J Neurosci Res 62 293 301 10.1002/1097-4547(20001015) 62:2<293::AID-JNR14>3.0.CO;2-Y 1:CAS:528:DC%2BD3cXns1aqur8%3D 11020222
71. van der Spoel D, Lindahl E, Hess B, van Buuren AR, Apol E, Meulenhoff PJ, Tieleman DP, Sijbers ALTM, Feenstra KA, van Drunen R, Berendsen HJC (2005) Gromacs User Manual version 3.3. http://www.gromacs.org
72. R Walser AE Mark WF van Gunsteren 1999 On the validity of Stoke's law at the molecular level Chem Phys Lett 303 583 586 10.1016/S0009-2614(99)00266-3 1:CAS:528:DyaK1MXisFCktLw%3D
73. R Walser AE Mark WF van Gunsteren 2000 The effect of force-field parameters on properties of liquids: parametrization of a simple three-site model for methanol J Chem Phys 112 10450 10459 10.1063/1.481680 1:CAS:528:DC%2BD3cXjvVOksbw%3D
74. J Watzlawik L Skora D Frense C Griesinger M Zweckstetter WJ Schulz-Schaeffer ML Kramer 2006 Prion protein helix 1 promotes aggregation but is not converted into beta-sheet J Biol Chem 281 30242 30250 10.1074/jbc. M605141200 1:CAS:528:DC%2BD28XhtVahsbjO 17012240 (Pubitemid 44537031)
75. H Wille SB Prusiner 1999 Ultrastructural studies on scrapie prion protein crystals obtained from reverse micellar solutions Biophys J 76 1048 1062 10.1016/S0006-3495(99)77270-X 1:CAS:528:DyaK1MXnsVaktg%3D%3D 9916037
76. RA Williamson D Peretz C Pinilla H Ball RB Bastidas R Rozenshteyn RA Houghten SB Prusiner DR Burton 1998 Mapping the prion protein using recombinant antibodies J Virol 72 9413 9418 1:CAS:528:DyaK1cXmslaht7k%3D 9765500
77. Wohlfarth C (2008) Static dielectric constants of pure liquids and binary liquid mixtures, Landolt-Börnstein: numerical data and functional relationships in science and technology-new series. Physical Chemistry, vol 17. Springer, London
78. K Wüthrich R Riek 2001 Three-dimensional structures of prion proteins Adv Protein Chem 57 55 82 10.1016/S0065-3233(01)57018-7 11447697 (Pubitemid 32622680)
79. S Yu S Yin C Li P Wong B Chang F Xiao SC Kang H Yan G Xiao P Tien MS Sy 2007 Aggregation of prion protein with insertion mutations is proportional to the number of inserts Biochem J 403 343 351 10.1042/BJ20061592 1:CAS:528:DC%2BD2sXjsVWrtL4%3D 17187581 (Pubitemid 46596591)
80. R Zahn A Liu T Lührs R Riek C von Schroetter F López- García M Billeter L Calzolai G Wider K Wüthrich 2000 NMR solution structure of the human prion protein Proc Natl Acad Sci USA 97 145 150 10.1073/pnas.97.1.145 1:CAS:528:DC%2BD3cXjvVCrtg%3D%3D 10618385 (Pubitemid 30055798)
81. Sc conversion process J Biol Chem 278 50175 50181 10.1074/jbc.M305234200 1:CAS:528:DC%2BD3sXpslSqsLY%3D 12952977 (Pubitemid 37548856)
82. DM Zuckerman E Lyman 2006 A second look at canonical sampling of biomolecules using replica exchange simulation J Chem Theory Comput 2 1200 1202 10.1021/ct0600464 1:CAS:528:DC%2BD28XlsFakurc%3D