The unfolding of the prion protein sheds light on the mechanisms of prion susceptibility and species barrier

Biochemistry

Volumn 48, Issue 36, 2009, Pages 8551-8558

  Robinson, Philip J ^a   Pinheiro, Teresa J T ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; BARRIER EFFECTS; CIRCULAR DICHROISM; EQUILIBRIUM INTERMEDIATE; FOLDING PROPERTIES; HIGH-RESOLUTION STRUCTURES; MISFOLDING; NEURODEGENERATIVE DISORDERS; PRION DISEASE; PRION PROTEIN; SECONDARY STRUCTURES; TERTIARY STRUCTURES; TRYPTOPHAN MUTANT; WILD TYPES;

AMINES; DICHROISM; ORGANIC ACIDS;

AMINO ACIDS;

ARGININE; PRION PROTEIN; TRYPTOPHAN;

ARTICLE; CIRCULAR DICHROISM; CODON; FLUORESCENCE ANALYSIS; MUTATION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS; WILD TYPE;

ANIMALS; ARGININE; CRICETINAE; GENETIC PREDISPOSITION TO DISEASE; GLUTAMINE; MICE; MUTAGENESIS, SITE-DIRECTED; PRION DISEASES; PRIONS; PROTEIN DENATURATION; PROTEIN FOLDING; SPECIES SPECIFICITY; THERMODYNAMICS; TRYPTOPHAN;

CRICETINAE; OVIS ARIES;

EID: 70149110670     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901070t     Document Type: Article

References (48)

1. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383.
2. Mead, S. (2006) Prion disease genetics. Eur. J. Hum. Genet. 14, 273-281.
3. Goldmann, W. (2008) PrP genetics in ruminant transmissible spongiform encephalopathies. Vet. Res. 39, 30.
4. Westaway, D., Zuliani, V., Cooper, C. M., Da Costa, M., Neuman, S., Jenny, A. L., Detwiler, L., and Prusiner, S. B. (1994) Homozygosity for prion protein alleles encoding glutamine-171 renders sheep susceptible to natural scrapie. Genes Dev. 8, 959-969. (Pubitemid 24137243)
5. Belt, P. B., Muileman, I. H., Schreuder, B. E., Bos-de Ruijter, J., Gielkens, A. L., and Smits, M. A. (1995) Identification of five allelic variants of the sheep PrP gene and their association with natural scrapie. J. Gen. Virol. 76 (Part 3), 509-517.
6. Clouscard, C., Beaudry, P., Elsen, J. M., Milan, D., Dussaucy, M., Bounneau, C., Schelcher, F., Chatelain, J., Launay, J. M., and Laplanche, J. L. (1995) Different allelic effects of the codons 136 and 171 of the prion protein gene in sheep with natural scrapie. J. Gen. Virol. 76 (Part 8), 2097-2101.
7. Hunter, N. (2007) Scrapie: uncertainties, biology and molecular approaches. Biochim. Biophys. Acta 1772, 619-628.
8. Goldmann, W., Hunter, N., Smith, G., Foster, J., and Hope, J. (1994) PrP genotype and agent effects in scrapie: change in allelic interaction with different isolates of agent in sheep, a natural host of scrapie. J. Gen. Virol. 75 (Part 5), 989-995.
9. Kaneko, K., Zulianello, L., Scott, M., Cooper, C. M., Wallace, A. C., James, T. L., Cohen, F. E., and Prusiner, S. B. (1997) Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proc. Natl. Acad. Sci. U.S.A. 94, 10069-10074.
10. Perrier, V., Kaneko, K., Safar, J., Vergara, J., Tremblay, P., DeArmond, S. J., Cohen, F. E., Prusiner, S. B., and Wallace, A. C. (2002) Dominant-negative inhibition of prion replication in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 99, 13079-13084.
11. Caplazi, P. A., O'Rourke, K. I., and Baszler, T. V. (2004) Resistance to scrapie in PrP ARR/ARQ heterozygous sheep is not caused by preferential allelic use. J. Clin. Pathol. 57, 647-650.
12. Lee, C. I., Yang, Q., Perrier, V., and Baskakov, I. V. (2007) The dominant-negative effect of the Q218K variant of the prion protein does not require protein X. Protein Sci. 16, 2166-2173. (Pubitemid 47481651)
13. Beringue, V., Vilotte, J. L., and Laude, H. (2008) Prion agent diversity and species barrier. Vet. Res. 39, 47.
14. Scott, M., Foster, D., Mirenda, C., Serban, D., Coufal, F., Walchli, M., Torchia, M., Groth, D., Carlson, G., and DeArmond, S. J.; et al. (1989) Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell 59, 847-857. (Pubitemid 20022375)
15. Chiti, F., and Dobson, C. M. (2009) Amyloid formation by globular proteins under native conditions. Nat. Chem. Biol. 5, 15-22.
16. Jenkins, D. C., Sylvester, I. D., and Pinheiro, T. J. (2008) The elusive intermediate on the folding pathway of the prion protein. FEBS J. 275, 1323-1335. (Pubitemid 351342226)
17. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326.
18. Greenfield, N. J. (2006) Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nat. Protoc. 1, 2527-2535.
19. Santoro, M. M., and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27, 8063-8068.
20. Kuznetsova, I. M., Turoverov, K. K., and Uversky, V. N. (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.
21. Hosszu, L. L., Wells, M. A., Jackson, G. S., Jones, S., Batchelor, M., Clarke, A. R., Craven, C. J., Waltho, J. P., and Collinge, J. (2005) Definable equilibrium states in the folding of human prion protein. Biochemistry 44, 16649-16657. (Pubitemid 41832045)
22. Evans, P., Slingsby, C., and Wallace, B. A. (2008) Association of partially folded lens betaB2-crystallins with the alpha-crystallin molecular chaperone. Biochem. J. 409, 691-699. (Pubitemid 351214195)
23. Liemann, S., and Glockshuber, R. (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. (Pubitemid 129501385)
24. Wildegger, G., Liemann, S., and Glockshuber, R. (1999) Extremely rapid folding of the C-terminal domain of the prion protein without kinetic intermediates. Nat. Struct. Biol. 6, 550-553.
25. Martins, S. M., Chapeaurouge, A., and Ferreira, S. T. (2003) Folding intermediates of the prion protein stabilized by hydrostatic pressure and low temperature. J. Biol. Chem. 278, 50449-50455.
26. Rezaei, H., Choiset, Y., Eghiaian, F., Treguer, E., Mentre, P., Debey, P., Grosclaude, J., and Haertle, T. (2002) Amyloidogenic unfolding intermediates differentiate sheep prion protein variants. J. Mol. Biol. 322, 799-814.
27. Rezaei, H., Marc, D., Choiset, Y., Takahashi, M., Hui Bon Hoa, G., Haertle, T., Grosclaude, J., and Debey, P. (2000) High yield purification and physico-chemical properties of full-length recombinant allelic variants of sheep prion protein linked to scrapie susceptibility. Eur. J. Biochem. 267, 2833-2839.
28. Paludi, D., Thellung, S., Chiovitti, K., Corsaro, A., Villa, V., Russo, C., Ianieri, A., Bertsch, U., Kretzschmar, H. A., Aceto, A., and Florio, T. (2007) Different structural stability and toxicity of PrP-(ARR) and PrP(ARQ) sheep prion protein variants. J. Neurochem. 103, 2291-2300. (Pubitemid 350173570)
29. Horiuchi, M., and Caughey, B. (1999) Prion protein interconversions and the transmissible spongiform encephalopathies. Structure 7, R231-R240. (Pubitemid 29482978)
30. Eghiaian, F., Grosclaude, J., Lesceu, S., Debey, P., Doublet, B., Treguer, E., Rezaei, H., and Knossow, M. (2004) Insight into the PrPC→PrPSc conversion from the structures of antibody-bound ovine prion scrapie-susceptibility variants. Proc. Natl. Acad. Sci. U.S.A. 101, 10254-10259.
31. Bujdoso, R., Burke, D. F., and Thackray, A. M. (2005) Structural differences between allelic variants of the ovine prion protein revealed by molecular dynamics simulations. Proteins 61, 840-849.
32. De Simone, A., Zagari, A., and Derreumaux, P. (2007) Structural and hydration properties of the partially unfolded states of the prion protein. Biophys. J. 93, 1284-1292. (Pubitemid 47330908)
33. Chebaro, Y., and Derreumaux, P. (2009) The conversion of helix H2 to beta-sheet is accelerated in the monomer and dimer of the prion protein upon T183A mutation. J. Phys. Chem. B 113, 6942-6948.
34. Eghiaian, F., Daubenfeld, T., Quenet, Y., van Audenhaege, M., Bouin, A. P., van der Rest, G., Grosclaude, J., and Rezaei, H. (2007) Diversity in prion protein oligomerization pathways results from domain expansion as revealed by hydrogen/deuterium exchange and disulfide linkage. Proc. Natl. Acad. Sci. U.S.A. 104, 7414-7419.
35. DeMarco, M. L., and Daggett, V. (2007) Molecular mechanism for low pH triggered misfolding of the human prion protein. Biochemistry 46, 3045-3054. (Pubitemid 46449128)
36. Gossert, A. D., Bonjour, S., Lysek, D. A., Fiorito, F., and Wuthrich, K. (2005) Prion protein NMR structures of elk and of mouse/elk hybrids. Proc. Natl. Acad. Sci. U.S.A. 102, 646-650.
37. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R., and Wuthrich, K. (1996) NMR structure of the mouse prion protein domain PrP(121-321). Nature 382, 180-182. (Pubitemid 26242887)
38. Zahn, R., Liu, A., Luhrs, T., Riek, R., von Schroetter, C., Lopez Garcia, F., Billeter, M., Calzolai, L., Wider, G., and Wuthrich, K. (2000) NMR solution structure of the human prion protein. Proc. Natl. Acad. Sci. U.S.A. 97, 145-150.
39. Sigurdson, C. J., Nilsson, K. P., Hornemann, S., Heikenwalder, M., Manco, G., Schwarz, P., Ott, D., Rulicke, T., Liberski, P. P., Julius, C., Falsig, J., Stitz, L., Wuthrich, K., and Aguzzi, A. (2009) De novo generation of a transmissible spongiform encephalopathy by mouse transgenesis. Proc. Natl. Acad. Sci. U.S.A. 106, 304-309.
40. Soto, C. (2009) Constraining the loop, releasing prion infectivity. Proc. Natl. Acad. Sci. U.S.A. 106, 10-11.
41. Kim, P. S., and Baldwin, R. L. (1982) Specific intermediates in the folding reactions of small proteins and the mechanism of protein folding. Annu. Rev. Biochem. 51, 459-489.
42. Daggett, V., and Fersht, A. R. (2003) Is there a unifying mechanism for protein folding? Trends Biochem. Sci. 28, 18-25.
43. Settanni, G., Hoang, T. X., Micheletti, C., and Maritan, A. (2002) Folding pathways of prion and doppel. Biophys. J. 83, 3533-3541.
44. Breydo, L., Bocharova, O. V., Makarava, N., Salnikov, V. V., Anderson, M., and Baskakov, I. V. (2005) Methionine oxidation interferes with conversion of the prion protein into the fibrillar proteinase K-resistant conformation. Biochemistry 44, 15534-15543. (Pubitemid 41706137)
45. Thirumalai, D., Klimov, D. K., and Dima, R. I. (2003) Emerging ideas on the molecular basis of protein and peptide aggregation. Curr. Opin. Struct. Biol. 13, 146-159.
46. Kimberlin, R. H., Cole, S., and Walker, C. A. (1987) Temporary and permanent modifications to a single strain of mouse scrapie on transmission to rats and hamsters. J. Gen. Virol. 68 (Part 7), 1875-1881.
47. Kremer, W., Kachel, N., Kuwata, K., Akasaka, K., and Kalbitzer, H. R. (2007) Species-specific differences in the intermediate states of human and Syrian hamster prion protein detected by high pressure NMR spectroscopy. J. Biol. Chem. 282, 22689-22698.
48. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera;a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.