Relative and regional stabilities of the hamster, mouse, rabbit, and bovine prion proteins toward urea unfolding assessed by nuclear magnetic resonance and circular dichroism spectroscopies

Biochemistry

Volumn 50, Issue 35, 2011, Pages 7536-7545

  Julien, Olivier ^a   Chatterjee, Subhrangsu ^a   Bjorndahl, Trent C ^a   Sweeting, Braden ^b,c   Acharya, Sandipta ^a   Semenchenko, Valentyna ^d   Chakrabartty, Avijit ^b,c,e   Pai, Emil F ^b,c   Wishart, David S ^a,d   Sykes, Brian D ^a   Cashman, Neil R ^f  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD SPECTROSCOPY; GLOBAL STABILITY; HIGH RESOLUTION; HIS-TAG; HYDROPHOBIC REGIONS; MAMMALIAN PRION PROTEINS; PRION PROTEIN; RANK ORDER; REGIONAL STABILITY; SPECTROSCOPIC MEASUREMENTS;

DICHROISM; MAMMALS; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS; RESONANCE; UREA;

CIRCULAR DICHROISM SPECTROSCOPY;

POLYHISTIDINE TAG; PRION PROTEIN; UREA;

ANIMAL EXPERIMENT; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; COW; DENATURATION; HAMSTER; HYDROPHOBICITY; MOUSE; MUTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTON NUCLEAR MAGNETIC RESONANCE; RABBIT;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; CIRCULAR DICHROISM; CRICETINAE; CRICETULUS; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PRIONS; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEIN UNFOLDING; RABBITS; SPECIES SPECIFICITY; UREA;

BOVINAE; CRICETINAE; MAMMALIAN PRION; MESOCRICETUS AURATUS; ORYCTOLAGUS CUNICULUS;

EID: 80052254268     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200731e     Document Type: Article

References (51)

1. Prusiner, S. B. (1982) Novel proteinaceous infectious particles cause scrapie Science 216, 136-144 (Pubitemid 12089840)
2. Prusiner, S. B. (1998) Prions Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383 (Pubitemid 28525623)
3. Collinge, J. (2001) Prion diseases of humans and animals: Their causes and molecular basis Annu. Rev. Neurosci. 24, 519-550 (Pubitemid 32695238)
4. Aguzzi, A., Sigurdson, C., and Heikenwaelder, M. (2008) Molecular mechanisms of prion pathogenesis Annu. Rev. Pathol. 3, 11-40 (Pubitemid 351488275)
5. Caughey, B. and Baron, G. S. (2006) Prions and their partners in crime Nature 443, 803-810 (Pubitemid 44622685)
6. Weissmann, C. (2004) The state of the prion Nat. Rev. Microbiol. 2, 861-871 (Pubitemid 39561804)
7. Caughey, B. W., Dong, A., Bhat, K. S., Ernst, D., Hayes, S. F., and Caughey, W. S. (1991) Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy Biochemistry 30, 7672-7680
8. Safar, J., Roller, P. P., Gajdusek, D. C., and Gibbs, C. J. J. (1993) Thermal stability and conformational transitions of scrapie amyloid (prion) protein correlate with infectivity Protein Sci. 2, 2206-2216 (Pubitemid 23354723)
9. Pan, K. M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., Cohen, F. E., and Prusiner, S. B. (1993) Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins Proc. Natl. Acad. Sci. U.S.A. 90, 10962-10966
10. Rieger, R., Edenhofer, F., Lasmezas, C. I., and Weiss, S. (1997) The human 37-kDa laminin receptor precursor interacts with the prion protein in eukaryotic cells Nat. Med. 3, 1383-1388 (Pubitemid 28011039)
11. Telling, G. C., Scott, M., Mastrianni, J., Gabizon, R., Torchia, M., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (1995) Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein Cell 83, 79-90
12. Mouillet-Richard, S., Ermonval, M., Chebassier, C., Laplanche, J. L., Lehmann, S., Launay, J. M., and Kellermann, O. (2000) Signal transduction through prion protein Science 289, 1925-1928
13. Brown, D. R., Qin, K., Herms, J. W., Madlung, A., Manson, J., Strome, R., Fraser, P. E., Kruck, T., von Bohlen, A., Schulz-Schaeffer, W., Giese, A., Westaway, D., and Kretzschmar, H. (1997) The cellular prion protein binds copper in vivo Nature 390, 684-687 (Pubitemid 28016355)
14. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R., and Wuthrich, K. (1996) NMR structure of the mouse prion protein domain PrP(121-231) Nature 382, 180-182 (Pubitemid 26242887)
15. Julien, O., Graether, S. P., and Sykes, B. D. (2009) Monitoring prion protein stability by NMR J. Toxicol. Environ. Health, Part A 72, 1069-1074
16. DeMarco, M. L. and Daggett, V. (2004) From conversion to aggregation: Protofibril formation of the prion protein Proc. Natl. Acad. Sci. U.S.A. 101, 2293-2298 (Pubitemid 38269305)
17. DeMarco, M. L., Silveira, J., Caughey, B., and Daggett, V. (2006) Structural properties of prion protein protofibrils and fibrils: An experimental assessment of atomic models Biochemistry 45, 15573-15582 (Pubitemid 46032478)
18. Wille, H., Michelitsch, M. D., Guenebaut, V., Supattapone, S., Serban, A., Cohen, F. E., Agard, D. A., and Prusiner, S. B. (2002) Structural studies of the scrapie prion protein by electron crystallography Proc. Natl. Acad. Sci. U.S.A. 99, 3563-3568 (Pubitemid 34252147)
19. Govaerts, C., Wille, H., Prusiner, S. B., and Cohen, F. E. (2004) Evidence for assembly of prions with left-handed β-helices into trimers Proc. Natl. Acad. Sci. U.S.A. 101, 8342-8347 (Pubitemid 38736577)
20. Wasmer, C., Lange, A., Van Melckebeke, H., Siemer, A. B., Riek, R., and Meier, B. H. (2008) Amyloid fibrils of the HET-s(218-289) prion form a β solenoid with a triangular hydrophobic core Science 319, 1523-1526 (Pubitemid 351398180)
21. Cobb, N. J., Sonnichsen, F. D., McHaourab, H., and Surewicz, W. K. (2007) Molecular architecture of human prion protein amyloid: A parallel, in-register β-structure Proc. Natl. Acad. Sci. U.S.A. 104, 18946-18951
22. Smirnovas, V., Baron, G. S., Offerdahl, D. K., Raymond, G. J., Caughey, B., and Surewicz, W. K. (2011) Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange Nat. Struct. Mol. Biol. 18, 504-506
23. Barducci, A., Chelli, R., Procacci, P., Schettino, V., Gervasio, F. L., and Parrinello, M. (2006) Metadynamics simulation of prion protein: β-Structure stability and the early stages of misfolding J. Am. Chem. Soc. 128, 2705-2710 (Pubitemid 43328887)
24. Paramithiotis, E., Pinard, M., Lawton, T., LaBoissiere, S., Leathers, V. L., Zou, W. Q., Estey, L. A., Lamontagne, J., Lehto, M. T., Kondejewski, L. H., Francoeur, G. P., Papadopoulos, M., Haghighat, A., Spatz, S. J., Head, M., Will, R., Ironside, J., ORourke, K., Tonelli, Q., Ledebur, H. C., Chakrabartty, A., and Cashman, N. R. (2003) A prion protein epitope selective for the pathologically misfolded conformation Nat. Med. 9, 893-899 (Pubitemid 36889932)
25. 15N NMR relaxation: Order parameters calculated and slow conformational fluctuations localized to a distinct region Protein Sci. 18, 410-423
26. Julien, O., Chatterjee, S., Thiessen, A., Graether, S. P., and Sykes, B. D. (2009) Differential stability of the bovine prion protein upon urea unfolding Protein Sci. 18, 2172-2182
27. Barlow, R. M. and Rennie, J. C. (1976) The fate of ME7 scrapie infection in rats, guinea-pigs and rabbits Res. Vet. Sci. 21, 110-111
28. Gibbs, C. J. J. and Gajdusek, D. C. (1973) Experimental subacute spongiform virus encephalopathies in primates and other laboratory animals Science 182, 67-68
29. Vorberg, I., Groschup, M. H., Pfaff, E., and Priola, S. A. (2003) Multiple amino acid residues within the rabbit prion protein inhibit formation of its abnormal isoform J. Virol. 77, 2003-2009 (Pubitemid 36110012)
30. Priola, S. A. and Chesebro, B. (1995) A single hamster PrP amino acid blocks conversion to protease-resistant PrP in scrapie-infected mouse neuroblastoma cells J. Virol. 69, 7754-7758
31. Castilla, J., Gonzalez-Romero, D., Saa, P., Morales, R., De Castro, J., and Soto, C. (2008) Crossing the species barrier by PrP(Sc) replication in vitro generates unique infectious prions Cell 134, 757-768
32. Barria, M. A., Telling, G. C., Gambetti, P., Mastrianni, J. A., and Soto, C. (2011) Generation of a New Form of Human PrPSc in Vitro by Interspecies Transmission from Cervid Prions J. Biol. Chem. 286, 7490-7495
33. Baskakov, I. V., Legname, G., Gryczynski, Z., and Prusiner, S. B. (2004) The peculiar nature of unfolding of the human prion protein Protein Sci. 13, 586-595 (Pubitemid 38252555)
34. Baskakov, I. V., Legname, G., Baldwin, M. A., Prusiner, S. B., and Cohen, F. E. (2002) Pathway complexity of prion protein assembly into amyloid J. Biol. Chem. 277, 21140-21148 (Pubitemid 34952249)
35. Zahn, R., von Schroetter, C., and Wuthrich, K. (1997) Human prion proteins expressed in Escherichia coli and purified by high-affinity column refolding FEBS Lett. 417, 400-404 (Pubitemid 27511631)
36. Baryshnikova, O. K., Williams, T. C., and Sykes, B. D. (2008) Internal pH indicators for biomolecular NMR J. Biomol. NMR 41, 5-7
37. Khan, M. Q., Sweeting, B., Mulligan, V. K., Arslan, P. E., Cashman, N. R., Pai, E. F., and Chakrabartty, A. (2010) Prion disease susceptibility is affected by β-structure folding propensity and local side-chain interactions in PrP Proc. Natl. Acad. Sci. U.S.A. 107, 19808-19813
38. Greene, R. F. J. and Pace, C. N. (1974) Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, α-chymotrypsin, and β-lactoglobulin J. Biol. Chem. 249, 5388-5393
39. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol. 131, 266-280 (Pubitemid 16002205)
40. Hornemann, S., Schorn, C., and Wuthrich, K. (2004) NMR structure of the bovine prion protein isolated from healthy calf brains EMBO Rep. 5, 1159-1164 (Pubitemid 40103610)
41. Chakroun, N., Prigent, S., Dreiss, C. A., Noinville, S., Chapuis, C., Fraternali, F., and Rezaei, H. (2010) The oligomerization properties of prion protein are restricted to the H2H3 domain FASEB J. 24, 3222-3231
42. Adrover, M., Pauwels, K., Prigent, S., de Chiara, C., Xu, Z., Chapuis, C., Pastore, A., and Rezaei, H. (2010) Prion fibrillization is mediated by a native structural element that comprises helices H2 and H3 J. Biol. Chem. 285, 21004-21012
43. 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 (Pubitemid 40282719)
44. Soto, C. (2009) Constraining the loop, releasing prion infectivity Proc. Natl. Acad. Sci. U.S.A. 106, 10-11
45. Deleault, N. R., Harris, B. T., Rees, J. R., and Supattapone, S. (2007) Formation of native prions from minimal components in vitro Proc. Natl. Acad. Sci. U.S.A. 104, 9741-9746 (Pubitemid 47175337)
46. Wang, F., Wang, X., Yuan, C. G., and Ma, J. (2010) Generating a prion with bacterially expressed recombinant prion protein Science 327, 1132-1135
47. Blinov, N., Berjanskii, M., Wishart, D. S., and Stepanova, M. (2009) Structural domains and main-chain flexibility in prion proteins Biochemistry 48, 1488-1497
48. Guest, W. C., Cashman, N. R., and Plotkin, S. S. (2010) Electrostatics in the stability and misfolding of the prion protein: Salt bridges, self energy, and solvation Biochem. Cell Biol. 88, 371-381
49. 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
50. Wen, Y., Li, J., Yao, W., Xiong, M., Hong, J., Peng, Y., Xiao, G., and Lin, D. (2010) Unique structural characteristics of the rabbit prion protein J. Biol. Chem. 285, 31682-31693
51. Li, L., Guest, W., Huang, A., Plotkin, S. S., and Cashman, N. R. (2009) Immunological mimicry of PrPC-PrPSc interactions: Antibody-induced PrP misfolding Protein Eng., Des. Sel. 22, 523-529