Solution structure and dynamics of the I214V mutant of the rabbit prion protein

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Wen, Yi ^a   Li, Jun ^a,c   Xiong, Minqian ^a   Peng, Yu ^a   Yao, Wenming ^a   Hong, Jing ^a   Lin, Donghai ^a,b  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^b XIAMEN UNIVERSITY   (China)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; MUTANT PROTEIN; PRION PROTEIN; VALINE;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; PRION DISEASE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STABILITY; PROTEIN STRUCTURE; VIRUS TRANSMISSION; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; MUTATION; NUCLEAR MAGNETIC RESONANCE; PRION; RABBIT; STATIC ELECTRICITY;

ORYCTOLAGUS CUNICULUS;

ANIMALS; HYDROGEN BONDING; MODELS, MOLECULAR; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PRIONS; PROTEIN CONFORMATION; RABBITS; STATIC ELECTRICITY;

EID: 78049286310     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013273     Document Type: Article

References (64)

1. Prusiner SB (1998) Prions. Proc Natl Acad Sci USA 95: 13363-13383.
2. Legname G, Baskakov IV, Nguyen HO, Riesner D, Cohen FE, et al. (2004) Synthetic mammalian prions. Science 305: 673-676.
3. Castilla J, Saa P, Hetz C, Soto C (2005) In vitro generation of infectious scrapie prions. Cell 121: 195-206.
4. Wang F, Wang X, Yuan CG, Ma J (2010) Generating a Prion with Bacterially Expressed Recombinant Prion Protein. Science 327: 1132-1135.
5. Riek R, Hornemann S, Wider G, Billeter M, Glockshuber R, et al. (1996) NMR structure of the mouse prion protein domain PrP(121-231). Nature 382: 180-182.
6. Donne DG, Viles JH, Groth D, Mehlhorn I, James TL, et al. (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.
7. James TL, Liu H, Ulyanov NB, Farr-Jones S, Zhang H, 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.
8. Riek R, Wider G, Billeter M, Hornemann S, Glockshuber R, et al. (1998) Prion protein NMR structure and familial human spongiform encephalopathies. Proc Natl Acad Sci USA 95: 11667-11672.
9. Liu H, Farr-Jones S, Ulyanov NB, Llinas M, Marqusee S, et al. (1999) Solution structure of Syrian hamster prion protein rPrP(90-231). Biochemistry 38: 5362-5377.
10. Lopez Garcia F, Zahn R, Riek R, Wuthrich K (2000) NMR structure of the bovine prion protein. Proc Natl Acad Sci USA 97: 8334-8339.
11. Zahn R, Liu A, Luhrs T, Riek R, von Schroetter C, et al. (2000) NMR solution structure of the human prion protein. Proc Natl Acad Sci USA 97: 145-150.
12. Hornemann S, Schorn C, Wuthrich K (2004) NMR structure of the bovine prion protein isolated from healthy calf brains. EMBO Rep 5: 1159-1164.
13. Gossert AD, Bonjour S, Lysek DA, Fiorito F, Wuthrich K (2005) Prion protein NMR structures of elk and of mouse/elk hybrids. Proc Natl Acad Sci USA 102: 646-650.
14. Lysek DA, Schorn C, Nivon LG, Esteve-Moya V, Christen B, et al. (2005) Prion protein NMR structures of cats, dogs, pigs, and sheep. Proc Natl Acad Sci USA 102: 640-645.
15. Christen B, Perez DR, Hornemann S, Wuthrich K (2008) NMR structure of the bank vole prion protein at 20 degrees C contains a structured loop of residues 165-171. J Mol Biol 383: 306-312.
16. Christen B, Hornemann S, Damberger FF, Wuthrich K (2009) Prion protein NMR structure from tammar wallaby (Macropus eugenii) shows that the beta2- alpha2 loop is modulated by long-range sequence effects. J Mol Biol 389: 833-845.
17. Wille H, Michelitsch MD, Guenebaut V, Supattapone S, Serban A, et al. (2002) Structural studies of the scrapie prion protein by electron crystallography. Proc Natl Acad Sci USA 99: 3563-3568.
18. Govaerts C, Wille H, Prusiner SB, Cohen FE (2004) Evidence for assembly of prions with left-handed beta-helices into trimers. Proc Natl Acad Sci USA 101: 8342-8347.
19. Cobb NJ, Sonnichsen FD, McHaourab H, Surewicz WK (2007) Molecular architecture of human prion protein amyloid: a parallel, in-register betastructure. Proc Natl Acad Sci USA 104: 18946-18951.
20. Lu X, Wintrode PL, Surewicz WK (2007) Beta-sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange. Proc Natl Acad Sci USA 104: 1510-1515.
21. Walsh P, Simonetti K, Sharpe S (2009) Core structure of amyloid fibrils formed by residues 106-126 of the human prion protein. Structure 17: 417-426.
22. Prusiner SB (1996) Molecular biology and pathogenesis of prion diseases. Trends Biochem Sci 21: 482-487.
23. Prusiner SB (1997) Prion diseases and the BSE crisis. Science 278: 245-251.
24. Hunter N (1997) PrP genetics in sheep and the applications for scrapie and BSE. Trends Microbiol 5: 331-334.
25. Westaway D, Zuliani V, Cooper CM, Da Costa M, Neuman S, et al. (1994) Homozygosity for prion protein alleles encoding glutamine-171 renders sheep susceptible to natural scrapie. Genes Dev 8: 959-969.
26. Belt PB, Muileman IH, Schreuder BE, Bos-deRuijter J, Gielkens AL, et al. (1995) Identification of five allelic variants of the sheep PrP gene and their association with natural scrapie. J Gen Virol 76: 509-517.
27. Clouscard C, Beaudry P, Elsen JM, Milan D, Dussaucy M, et al. (1995) Different allelic effects of the codons 136 and 171 of the prion protein gene in sheep with natural scrapie. J Gen Virol 76: 2097-2101.
28. Gibbs CJ, Jr., Gajdusek DC (1973) Experimental subacute spongiform virus encephalopathies in primates and other laboratory animals. Science 182: 67-68.
29. Vorberg I, Groschup MH, Pfaff E, Priola SA (2003) Multiple amino acid residues within the rabbit prion protein inhibit formation of its abnormal isoform. J Virol 77: 2003-2009.
30. Wen Y, Li J, Yao W, Xiong M, Hong J, et al. (2010) Unique structural characteristics of the rabbit prion protein. J Biol Chem (in press).
31. Peng JW, Wagner G (1992) Mapping of the spectral densities of N-H bond motions in eglin c using heteronuclear relaxation experiments. Biochemistry 31: 8571-8586.
32. Peng JW, Wagner G (1992) Mapping of Spectral Density Functions Using Heteronuclear NMR Relaxation Measurements. J Magn Reson 98: 308-332.
33. Farrow NA, Zhang O, Szabo A, Torchia DA, Kay LE (1995) Spectral density function mapping using 15N relaxation data exclusively. J Biomol NMR 6: 153-162.
34. O'Sullivan DB, Jones CE, Abdelraheim SR, Brazier MW, Toms H, et al. (2009) Dynamics of a truncated prion protein, PrP(113-231), from (15)N NMR relaxation: order parameters calculated and slow conformational fluctuations localized to a distinct region. Protein Sci 18: 410-423.
35. Dyson HJ, Wright PE (2002) Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance. Adv Protein Chem 62: 311-340.
36. Lefevre JF, Dayie KT, Peng JW, Wagner G (1996) Internal mobility in the partially folded DNA binding and dimerization domains of GAL4: NMR analysis of the N-H spectral density functions. Biochemistry 35: 2674-2686.
37. Lipari G, Szabo A (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J Am Chem Soc 104: 4546-4559.
38. Lipari G, Szabo A (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J Am Chem Soc 104: 4559-4570.
39. Clore GM, Szabo A, Bax A, Kay LE, Driscoll PC, et al. (1990) Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen- 15 nuclear magnetic relaxation of proteins. J Am Chem Soc 112: 4989-4991.
40. Kirby L, Agarwal S, Graham JF, Goldmann W, Gill AC (2010) Inverse correlation of thermal lability and conversion efficiency for five prion protein polymorphic variants. Biochemistry 49: 1448-1459.
41. Calzolai L, Lysek DA, Guntert P, von Schroetter C, Riek R, et al. (2000) NMR structures of three single-residue variants of the human prion protein. Proc Natl Acad Sci USA 97: 8340-8345.
42. Zhang Y, Swietnicki W, Zagorski MG, Surewicz WK, Sonnichsen FD (2000) Solution structure of the E200K variant of human prion protein. Implications for the mechanism of pathogenesis in familial prion diseases. J Biol Chem 275: 33650-33654.
43. Cordeiro Y, Machado F, Juliano L, Juliano MA, Brentani RR, et al. (2001) DNA converts cellular prion protein into the beta-sheet conformation and inhibits prion peptide aggregation. J Biol Chem 276: 49400-49409.
44. Lima LM, Cordeiro Y, Tinoco LW, Marques AF, Oliveira CL, et al. (2006) Structural insights into the interaction between prion protein and nucleic acid. Biochemistry 45: 9180-9187.
45. Telling GC, Scott M, Mastrianni J, Gabizon R, Torchia M, et al. (1995) Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell 83: 79-90.
46. Kaneko K, Zulianello L, Scott M, Cooper CM, Wallace AC, et al. (1997) Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proc Natl Acad Sci USA 94: 10069-10074.
47. Kay LE (1998) Protein dynamics from NMR. Nat Struct Biol 5 Suppl: 513-517.
48. Viles JH, Donne D, Kroon G, Prusiner SB, Cohen FE, et al. (2001) Local structural plasticity of the prion protein. Analysis of NMR relaxation dynamics. Biochemistry 40: 2743-2753.
49. Blinov N, Berjanskii M, Wishart DS, Stepanova M (2009) Structural domains and main-chain flexibility in prion proteins. Biochemistry 48: 1488-1497.
50. Bae SH, Legname G, Serban A, Prusiner SB, Wright PE, et al. (2009) Prion proteins with pathogenic and protective mutations show similar structure and dynamics. Biochemistry 48: 8120-8128.
51. Kay LE, Muhandiram DR, Wolf G, Shoelson SE, Forman-Kay JD (1998) Correlation between binding and dynamics at SH2 domain interfaces. Nat Struct Biol 5: 156-163.
52. Tzeng SR, Kalodimos CG (2009) Dynamic activation of an allosteric regulatory protein. Nature 462: 368-372.
53. Privalov PL, Makhatadze GI (1990) Heat capacity of proteins. II. Partial molar heat capacity of the unfolded polypeptide chain of proteins: protein unfolding effects. J Mol Biol 213: 385-391.
54. Alonso DO, Dill KA (1991) Solvent denaturation and stabilization of globular proteins. Biochemistry 30: 5974-5985.
55. Dill KA, Shortle D (1991) Denatured states of proteins. Annu Rev Biochem 60: 795-825.
56. Privalov PL, Makhatadze GI (1992) Contribution of hydration and non-covalent interactions to the heat capacity effect on protein unfolding. J Mol Biol 224: 715-723.
57. Zhang J (2010) Studies on the structural stability of rabbit prion probed by molecular dynamics simulations of its wild-type and mutants. J Theor Biol 264: 119-122.
58. 2+ Binding by Calbindin D9k. J Am Chem Soc 115: 9832-9833.
59. Yang D, Kay LE (1996) Contributions to conformational entropy arising from bond vector fluctuations measured from NMR-derived order parameters: application to protein folding. J Mol Biol 263: 369-382.
60. Yin SM, Zheng Y, Tien P (2003) On-column purification and refolding of recombinant bovine prion protein: using its octarepeat sequences as a natural affinity tag. Protein Expr Purif 32: 104-109.
61. Koradi R, Billeter M, Wuthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14: 51-55, 29-32.
62. Spyracopoulos L (2006) A suite of Mathematica notebooks for the analysis of protein main chain 15N NMR relaxation data. J Biomol NMR 36: 215-224.
63. Cole R, Loria JP (2003) FAST-Modelfree: a program for rapid automated analysis of solution NMR spin-relaxation data. J Biomol NMR 26: 203-213.
64. Wishart DS, Sykes BD (1994) The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J Biomol NMR 4: 171-180