Comparative analysis of essential collective dynamics and NMR-derived flexibility profiles in evolutionarily diverse prion proteins

References

• Harris DA. Cellular biology of prion diseases. Clin Microbiol Rev 1999; 12:429 - 444
   PubMed Web of Science ®Google Scholar
• Prusiner SB. Prions. Proc Natl Acad Sci USA 1998; 95:13363 - 13383
   PubMed Web of Science ®Google Scholar
• Weissmann C. The state of the prion. Nat Rev Microbiology 2004; 2:861 - 871
   PubMed Web of Science ®Google Scholar
• Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science 1982; 216:136 - 144
   PubMed Web of Science ®Google Scholar
• Caughey BW, Dong A, Bhat KS, Ernst D, Hayes SF, Caughey WS. Secondary structure-analysis of the scrapie-associated protein PrP 27–30 in water by infraredspectroscopy. Biochemistry 1991; 30:7672 - 7680
   PubMed Web of Science ®Google Scholar
• Sunde M, Serpell LC, Bartlam M, Fraser PE, Pepys MB, Blake CCF. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J Mol Biol 1997; 273:729 - 739
   PubMed Web of Science ®Google Scholar
• Sunde M, Blake CCF. From the globular to the fibrous state: protein structure and structural conversion in amyloid formation. Q Rev Biophys 1998; 31:1 - 39
   PubMed Web of Science ®Google Scholar
• Pan KM, Baldwin M, Gasset MN, Serban A, Groth D, Mehlhorn I, et al. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci USA 1993; 90:10962 - 10966
   PubMed Web of Science ®Google Scholar
• Jackson GS, Hill AF, Joseph C, Hosszu L, Power A, Waltho JP, et al. Multiple folding pathways for heterologously expressed human prion protein. Biochim Biophys Acta 1999; 1431:1 - 13
   PubMed Web of Science ®Google Scholar
• Wille H, Michelitsch MD, Guenebaut V, Supattapone S, Serban A, Cohen FE, et al. Structural studies of the scrapie prion protein by electron crystallography. Proc Natl Acad Sci USA 2002; 99:3563 - 3568
   PubMed Web of Science ®Google Scholar
• Diringer H, Gelderblom H, Hilmert H, Ozel M, Edelbluth C, Kimberlin RH. Scrapie infectivity, fibrils and low molecular weight protein. Nature 1983; 306:476 - 478
   PubMed Web of Science ®Google Scholar
• Hartley DM, Walsh DM, Ye CPP, Diehl T, Vasquez S, Vassilev PM, et al. Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J Neurosci 1999; 19:8876 - 88s84
   PubMed Web of Science ®Google Scholar
• Bucciantini M, Giannoni E, Chiti F, Baroni F, Formigli L, Zurdo JS, et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 2002; 416:507 - 511
   PubMed Web of Science ®Google Scholar
• Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003; 300:486 - 489
   PubMed Web of Science ®Google Scholar
• Silveira JR, Raymond GJ, Hughson AG, Race RE, Sim VL, Hayes SF, et al. The most infectious prion protein particles. Nature 2005; 437:257 - 261
   PubMed Web of Science ®Google Scholar
• Cobb NJ, Sonnichsen FD, Mchaourab H, Surewicz WK. Molecular architecture of human prion protein amyloid: a parallel, in-register β-structure. Proc Natl Acad Sci USA 2007; 104:18946 - 18951
   PubMed Web of Science ®Google Scholar
• Govaerts C, Wille H, Prusiner SB, Cohen FE. Evidence for assembly of prions with left-handed α-helices into trimers. Proc Natl Acad Sci USA 2004; 101:8342 - 8347
   PubMed Web of Science ®Google Scholar
• Lu X, Wintrode PL, Surewicz WK. β-Sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange. Proc Natl Acad Sci USA 2007; 104:1510 - 1515
   PubMed Web of Science ®Google Scholar
• Saborio GP, Permanne B, Soto C. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 2001; 411:810 - 813
   PubMed Web of Science ®Google Scholar
• Smirnovas V, Baron GS, Offerdahl DK, Raymond GJ, Caughey B, Surewicz WK. Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange. Nature Strut Molec Biol 2011; 18:504 - 506
   PubMed Web of Science ®Google Scholar
• Huang Z, Prusiner SB, Cohen FE. Scrapie prions: a three-dimensional model of an infectious fragment. Fold Des 1996; 1:13 - 19
   PubMedGoogle Scholar
• Gu W, Wang T, Zhu J, Shi Y, Liu H. Molecular dynamics simulation of the unfolding of the human prion protein domain under low pH and high temperature conditions. Biophys Chem 2003; 104:79 - 94
   PubMed Web of Science ®Google Scholar
• Dima RI, Thirumalai D. Probing the instabilities in the dynamics of helical fragments from mouse PrP. Proc Natl Acad Sci USA 2004; 101:15335 - 15340
   PubMed Web of Science ®Google Scholar
• Langella E, Improta R, Barone V. Checking the pH-induced conformational transition of prion protein by molecular dynamics simulations: effect of protonation of histidine residues. Biophys J 2004; 87:3623 - 3632
   PubMed Web of Science ®Google Scholar
• De Simone A, Dodson GG, Verma CS, Zagari A, Fraternali F. Prion and water: Tight and dynamical hydration sites have a key role in structural stability. Proc Natl Acad Sci USA 2005; 102:7535 - 7540
   PubMed Web of Science ®Google Scholar
• Barducci A, Chelli R, Procacci P, Schettino V. Misfolding pathways of the prion protein probed by molecular dynamics simulations. Biophys J 2005; 88:1334 - 1343
   PubMed Web of Science ®Google Scholar
• Langella E, Improta R, Crescenzi O, Barone V. Assessing the acid-base and conformational properties of histidine residues in human prion protein (125–228) by means of p calculations and molecular dynamics simulations. Proteins: Struct Funct Bioinf 2006; 64:167 - 177
   PubMed Web of Science ®Google Scholar
• De Simone A, Spadaccini R, Temussi PA, Fraternali F. Toward the understanding of MNEI sweetness from hydration map surfaces. Biophys J 2006; 90:3052 - 3061
   PubMed Web of Science ®Google Scholar
• Barducci A, Chelli R, Procacci P, Schettino V, Gervasio FL, Parrinello M. Metadynamics simulation of prion protein: β-structure stability and the early stages of misfolding. J Am Chem Soc 2006; 128:2705 - 2710
   PubMed Web of Science ®Google Scholar
• De Simone A, Zagari A, Derreumaux P. Structural and hydration properties of the partially unfolded states of the prion protein. Biophys J 2007; 93:1284 - 1292
   PubMed Web of Science ®Google Scholar
• DeMarco L, Daggett V. Molecular mechanism for low pH triggered misfolding of the human prion protein. Biochemistry 2007; 46:3045 - 3054
   PubMed Web of Science ®Google Scholar
• Apetri AC, Vanik DL, Surewicz WK. Polymorphism at residue 129 modulates the conformational conversion of the D178N variant of human prion protein 90–231. Biochemistry 2005; 44:15880 - 15888
   PubMed Web of Science ®Google Scholar
• Scheraga HA, Khalili M, Liwo A. Protein-folding dynamics: Overview of molecular simulation techniques. Annu Rev Phys Chem 2007; 58:57 - 83
   PubMed Web of Science ®Google Scholar
• Brown WM, Martin S, Pollock SN, Coutsias EA, Watson JP. Algorithmic dimensionality reduction for molecular structure analysis. J Chem Phys 2008; 129:64118
   Web of Science ®Google Scholar
• Loeffler HH, Kitao A. Collective dynamics of periplasmic glutamine binding protein upon domain closure. Biophys J 2009; 97:2541 - 2549
   PubMed Web of Science ®Google Scholar
• Hayward S, Go N. Collective variable description of native protein dynamics. Annu Rev Phys Chem 1995; 46:223 - 250
   PubMed Web of Science ®Google Scholar
• Amadei A, Linssen ABM, Berendsen HJC. Essential dynamics of proteins. Proteins: Struct Funct and Gen 1999; 17:412 - 425
   Web of Science ®Google Scholar
• Garcia AE. Large-amplitude nonlinear motions in proteins. Phys Rev Lett 1992; 68:2696 - 2699
   PubMed Web of Science ®Google Scholar
• Kitao A, Go N. Investigating protein dynamics in collective coordinate space. Curr Opin Struct Biol 1999; 9:164 - 169
   PubMed Web of Science ®Google Scholar
• Berendsen HJC, Hayward S. Collective protein dynamics in relation to function. Curr Opin Struct Biol 2000; 10:165 - 169
   PubMed Web of Science ®Google Scholar
• Yang LW, Bahar I. Coupling between catalytic site and collective dynamics; a requirement for mechanochemical activity of enzymes. Structure 2005; 13:893 - 904
   PubMed Web of Science ®Google Scholar
• Tournier AL, Smith JC. Principal components of the protein dynamical transition. Phys Rev Lett 2003; 91:208106
   PubMed Web of Science ®Google Scholar
• Arnold GE, Ornstein RL. Molecular dynamics study of time-correlated protein domain motions and molecular flexibility: cytochrome P450BM-3. Biophys 1997; 73:1147 - 1159
   PubMed Web of Science ®Google Scholar
• Emberly EG, Mukhopadhyay R, Wingreen NS, Tang C. Flexibility of α-helices: Results of a statistical analysis of database protein structures. J Mol Biol 2003; 327:229 - 237
   PubMed Web of Science ®Google Scholar
• Emberly EG, Mukhopadhyay R, Tang C, Wingreen NS. Flexibility of β-sheets: Principal component analysis of database protein structures. Proteins: Struct Funct Bioinf 2004; 55:91 - 98
   PubMed Web of Science ®Google Scholar
• Yesylevsky SO, Kharkyanen VN, Demchenko AP. Dynamic protein domains: Identification, interdependence and stability. Biophys J 2006; 91:670 - 685
   PubMed Web of Science ®Google Scholar
• Stepanova M. Dynamics of essential collective motions in proteins: Theory. Phys Rev E 2007; 76:1 - 16
   Web of Science ®Google Scholar
• Blinov N, Berjanskii M, Wishart DS, Stepanova M. Structural domains and main-chain flexibility in prion proteins. Biochemistry 2009; 48:1488 - 1497
   PubMed Web of Science ®Google Scholar
• Mori H. Transport, Collective motion and Brownian motion. Prog Theor Phys 1965; 33:423 - 454
   Web of Science ®Google Scholar
• Berjanskii MV, Wishart DS. A simple method to predict protein flexibility using secondary chemical shifts. J Am Chem Soc 2005; 127:14970 - 14971
   PubMed Web of Science ®Google Scholar
• Berjanskii M, Wishart DS. NMR: prediction of protein flexibility. Nat Protoc 2006; 1:683 - 688
   PubMed Web of Science ®Google Scholar
• Berjanskii MV, Wishart DS. Application of the random coil index to studying protein flexibility. J Biomol NMR 2008; 40:31 - 48
   PubMed Web of Science ®Google Scholar
• Moore RA, Vorberg I, Priola SA. Peters CJ, Calisher CH. Species barriers in prion diseases. Nature: mechanisms of viral emergence and persistence 2005; Vienna Springer-Verlag 187 - 202; http://dx.doi.org/10.1007/3-211-29981-5_15
   Google Scholar
• Kedarisetti KD, Dick S, Kurgan L. Searching for factors that distinguish disease-prone and disease-resistant prions via sequence analysis. Bioinform Biol Insights 2008; 2:133 - 144
   PubMedGoogle Scholar
• Goldmann W, O'Neil G, Cheung F, Charleson F, Ford P, Hunter N. PrP (prion) gene expression in sheep may be modulated by alternative polyadenylation of its messenger RNA. J Gen Virol 1999; 80:2275 - 2283
   PubMed Web of Science ®Google Scholar
• Xie Zh, O'Rouke K, Dong Zh, Jenny AL, Langenberg JA, Belay ED, et al. Chronic wasting disease of elk and deer and Creutzfeldt-Jakob disease. J Biol Chem 2006; 281:4199 - 4205
   PubMed Web of Science ®Google Scholar
• Kurt TD, Telling GC, Zabel MD, Hoover EA. Trans-species amplification of PrPC WD and correlation with rigid loop 170N. Virology 2009; 387:235 - 243
   PubMed Web of Science ®Google Scholar
• Gossert AD, Bonjour S, Lysek DA, Fiorito F, Wuthrich K. Prion protein NMR structures of elk and of mouse/elk hybrids. Proc Natl Acad Sci USA 2005; 102:646 - 650
   PubMed Web of Science ®Google Scholar
• Lopez Garcia F, Zahn R, Riek R, Wuthrich K. NMR structure of the bovine prion protein. Proc Natl Acad Sci USA 2000; 97:8334 - 8339
   PubMed Web of Science ®Google Scholar
• Lysek DA, Schorn C, Nivon LG, Esteve-Moya V, Christen B, Calzolai L, et al. Prion protein NMR structures of cats, dogs, pigs and sheep. Proc Natl Acad Sci USA 2005; 102:640 - 645
   PubMed Web of Science ®Google Scholar
• Liu H, Farr-Jones S, Ulyanov NB, Llinas M, Marqusee S, Groth D, et al. Solution structure of Syrian hamster prion protein rPrP(90–231). Biochemistry 1999; 38:5362 - 5377
   PubMed Web of Science ®Google Scholar
• Zahn R, Liu L, Luhrs T, Riek R, von Schroetter C, Garcia LF, et al. NMR solution structure of the human prion protein. Proc Natl Acad Sci USA 2000; 97:145 - 150
   PubMed Web of Science ®Google Scholar
• Perez DR, Wuthrich K. NMR assignment of the Xenopus laevis prion protein fragment xlPrP (98–226). J Biomol NMR 2005; 31:260
   PubMed Web of Science ®Google Scholar
• Calzolai L, Lysek DA, Wuthrich K. NMR assignment of the turtle prion protein fragment tPrP(121–225). J Biomol NMR 2004; 30:97
   Google Scholar
• Lysek DA, Calzolai L, Wuthrich K. NMR assignment of the chicken prion protein fragments chPrP(128–242) and chPrP(25–242). J Biomol NMR 2004; 30:97
   Google Scholar
• Garcia FL, Zahn R, Riek R, Wuthrich K. NMR structure of the bovine prion protein. Proc Natl Acad Sci USA 2000; 97:8334 - 8339
   PubMed Web of Science ®Google Scholar
• Kachel N, Kremer W, Zahn R, Kalbitzer HR. Observation of intermediate states of the human prion protein by high pressure NMR spectroscopy. BMC Struct Biol 2006; 6:1 - 18
   PubMed Web of Science ®Google Scholar
• Julien O, Chatterjee S, Thiessen A, Graether SP, Sykes BD. Differential stability of the bovine prion protein upon urea unfolding. Prot Sci 2009; 18:2172 - 2182
   PubMed Web of Science ®Google Scholar
• Soto C. Constraining the loop, releasing prion infectivity. Proc Natl Acad Sci USA 2009; 106:10 - 11
   PubMed Web of Science ®Google Scholar
• Kaneko K, Zulianello L, Scott M, Cooper CM, Wallace AC, James TL, et al. Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proc Natl Acad Sci USA 1997; 94:10069 - 10074
   PubMed Web of Science ®Google Scholar
• James TL, Liu H, Ulyanov NB, Farr-Jones S, Zhang H, Donne DG, Cohen FE. Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform. Proc Natl Acad Sci USA 1997; 94:10086 - 10091
   PubMed Web of Science ®Google Scholar
• Calzolai L, Lysek AD, Perez DR, Guntert P, Wuthrich K. Prion protein NMR structures of chickens, turtles and frogs. Proc Natl Acad Sci USA 2005; 102:651 - 655
   PubMed Web of Science ®Google Scholar
• Sigurdson CJ, Nilsson KPR, Hornemann S, Heikenwalder M, Manco G, Schwarz P, et al. De novo generation of a transmissible spongiform encephalopathy by mouse transgenesis. Proc Natl Acad Sci USA 2009; 106:304 - 309
   PubMed Web of Science ®Google Scholar
• Lindahl E, Hess B, van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J Mol Model 2001; 7:306 - 317
   Web of Science ®Google Scholar
• Scott WRP, Hünenberger PH, Tironi IG, Mark AE, Billeter SR, Fennen J, et al. The GROMOS biomolecular simulation program package. J Phys Chem A 1999; 103:3596 - 3607
   Web of Science ®Google Scholar
• DeMarco ML, Daggett V. Characterization of cell-surface prion protein relative to its recombinant analogue: insights from molecular dynamics simulations of diglycosylated, membrane-bound human prion protein. J Neurochem 2009; 109:60 - 73
   PubMed Web of Science ®Google Scholar
• Zhong L, Xie J. Investigation of the effect of glycosylation on human prion protein by molecular dynamics. J Biomol Struct Dyn 2009; 26:525 - 533
   PubMed Web of Science ®Google Scholar
• Liu DC, Nocedal J. On the limited memory BFGS method for large-scale optimization. Math Program 1989; 45:503 - 528
   Web of Science ®Google Scholar
• Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR. Molecular dynamics with coupling to an external bath. J Chem Phys 1984; 81:3684 - 3690
   Web of Science ®Google Scholar
• Hess B, Bekker B, Berendsen HJC, Fraaije JGEM. LINCS: A linear constraint solver for molecular simulations. J Comput Chem 1997; 18:1463 - 1472
   Web of Science ®Google Scholar
• Darden T, York D, Pedersen L. Particle Mesh Ewald—an N.Log (N) method for Ewald Sums in large systems. J Chem Phys 1993; 98:10089 - 10092
   Web of Science ®Google Scholar
• Jain AK, Murty MN, Flynn PJ. Data clustering: A review. ACM Comput Surv 1999; 31:264 - 323
   Web of Science ®Google Scholar
• Ulrich EL, Akutsu H, Doreleijers JF, Harano Y, Ioannidis YE, Lin J, et al. BioMagResBank. Nucleic Acids Res 2008; 36:402 - 408 http://www.bmrb.wisc.edu/
   PubMed Web of Science ®Google Scholar
• Humphrey W, Dalke A, Schulten K. VMD: Visual Molecular Dynamics. J Mol Graphics 1996; 14:33 - 38
   PubMed Web of Science ®Google Scholar