Recombinant Prion Protein Refolded with Lipid and RNA Has the Biochemical Hallmarks of a Prion but Lacks In Vivo Infectivity

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Timmes, Andrew G ^a   Moore, Roger A ^a   Fischer, Elizabeth R ^a   Priola, Suzette A ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 PALMITOYL 2 OLEOYL SN GLYCERO 3 PHOSPHOGLYCEROL; GLYCEROL DERIVATIVE; LIPID; PRION PROTEIN; PROTEINASE; RECOMBINANT PROTEIN; RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; BIOASSAY; BIOCHEMISTRY; BRAIN TISSUE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INFECTION SENSITIVITY; MOUSE; NONHUMAN; PRION DISEASE; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; PROTEIN RNA BINDING; TISSUE HOMOGENATE;

ANIMALS; BRAIN; CELL LINE; DETERGENTS; FEMALE; LIPIDS; MICE; PRIONS; PROTEIN REFOLDING; PROTEOLYSIS; PRPC PROTEINS; PRPSC PROTEINS; RECOMBINANT PROTEINS; RNA; SOLUBILITY;

EID: 84880771972     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071081     Document Type: Article

References (68)

1. Priola SA, Vorberg I, (2006) Molecular aspects of disease pathogenesis in the transmissible spongiform encephalopathies. Mol Biotechnol 33: 71-88.
2. Castilla J, Saa P, Hetz C, Soto C, (2005) In vitro generation of infectious scrapie prions. Cell 121: 195-206.
3. Deleault NR, Harris BT, Rees JR, Supattapone S, (2007) Formation of native prions from minimal components in vitro. Proc Natl Acad Sci U S A 104: 9741-9746.
4. Castilla J, Gonzalez-Romero D, Saa P, Morales R, De Castro J, et al. (2008) Crossing the species barrier by PrP(Sc) replication in vitro generates unique infectious prions. Cell 134: 757-768.
5. Green KM, Castilla J, Seward TS, Napier DL, Jewell JE, et al. (2008) Accelerated high fidelity prion amplification within and across prion species barriers. PLoS Pathog 4: e1000139.
6. Bieschke J, Weber P, Sarafoff N, Beekes M, Giese A, et al. (2004) Autocatalytic self-propagation of misfolded prion protein. Proc Natl Acad Sci U S A 101: 12207-12211.
7. Klingeborn M, Race B, Meade-White KD, Chesebro B, (2011) Lower specific infectivity of protease-resistant prion protein generated in cell-free reactions. Proc Natl Acad Sci U S A 108: E1244-E1253.
8. Shikiya RA, Bartz JC, (2011) In vitro generation of high-titer prions. J Virol 85: 13439-13442.
9. Weber P, Giese A, Piening N, Mitteregger G, Thomzig A, et al. (2006) Cell-free formation of misfolded prion protein with authentic prion infectivity. Proc Natl Acad Sci U S A 103: 15818-15823.
10. Smirnovas V, Baron GS, Offerdahl DK, Raymond GJ, Caughey B, et al. (2011) Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange. Nat Struct Mol Biol 18: 504-506.
11. Legname G, Baskakov IV, Nguyen HO, Riesner D, Cohen FE, et al. (2004) Synthetic mammalian prions. Science 305: 673-676.
12. Makarava N, Kovacs GG, Bocharova O, Savtchenko R, Alexeeva I, et al. (2010) Recombinant prion protein induces a new transmissible prion disease in wild-type animals. Acta Neuropathol 119: 177-187.
13. Kim JI, Cali I, Surewicz K, Kong Q, Raymond GJ, et al. (2010) Mammalian prions generated from bacterially expressed prion protein in the absence of any mammalian cofactors. J Biol Chem 285: 14083-14087.
14. Wang F, Wang X, Yuan CG, Ma J, (2010) Generating a prion with bacterially expressed recombinant prion protein. Science 327: 1132-1135.
15. Makarava N, Kovacs GG, Savtchenko R, Alexeeva I, Ostapchenko VG, et al. (2012) A new mechanism for transmissible prion diseases. J Neurosci 32: 7345-7355.
16. Raymond GJ, Race B, Hollister JR, Offerdahl DK, Moore RA, et al. (2012) Isolation of novel synthetic prion strains by amplification in transgenic mice coexpressing wild-type and anchorless prion proteins. J Virol 86: 11763-11778.
17. Colby DW, Giles K, Legname G, Wille H, Baskakov IV, et al. (2009) Design and construction of diverse mammalian prion strains. Proc Natl Acad Sci U S A 106: 20417-20422.
18. Deleault NR, Lucassen RW, Supattapone S, (2003) RNA molecules stimulate prion protein conversion. Nature 425: 717-720.
19. Wang F, Zhang Z, Wang X, Li J, Zha L, et al. (2012) Genetic informational RNA is not required for recombinant prion infectivity. J Virol 86: 1874-1876.
20. Deleault NR, Piro JR, Walsh DJ, Wang F, Ma J, et al. (2012) Isolation of phosphatidylethanolamine as a solitary cofactor for prion formation in the absence of nucleic acids. Proc Natl Acad Sci U S A 109: 8546-8551.
21. Taggart C, Cervantes-Laurean D, Kim G, McElvaney NG, Wehr N, et al. (2000) Oxidation of either methionine 351 or methionine 358 in alpha 1-antitrypsin causes loss of anti-neutrophil elastase activity. J Biol Chem 275: 27258-27265.
22. Apffel A, Fischer S, Goldberg G, Goodley PC, Kuhlmann FE, (1995) Enhanced sensitivity for peptide mapping with electrospray liquid chromatography-mass spectrometry in the presence of signal suppression due to trifluoroacetic acid-containing mobile phases. J Chromatogr A 712: 177-190.
23. Stevens LA, Levine RL, Gochuico BR, Moss J, (2009) ADP-ribosylation of human defensin HNP-1 results in the replacement of the modified arginine with the noncoded amino acid ornithine. Proc Natl Acad Sci U S A 106: 19796-19800.
24. Atarashi R, Moore RA, Sim VL, Hughson AG, Dorward DW, et al. (2007) Ultrasensitive detection of scrapie prion protein using seeded conversion of recombinant prion protein. Nat Methods 4: 645-650.
25. Zahn R, von SC, Wuthrich K, (1997) Human prion proteins expressed in Escherichia coli and purified by high-affinity column refolding. FEBS Lett 417: 400-404.
26. Wang F, Wang X, Ma J, (2011) Conversion of bacterially expressed recombinant prion protein. Methods 53: 208-213.
27. Levine RL, (2006) Fixation of nitrogen in an electrospray mass spectrometer. Rapid Commun Mass Spectrom 20: 1828-1830.
28. Chen M, Cook KD, (2007) Oxidation artifacts in the electrospray mass spectrometry of Abeta Peptide. Anal Chem 79: 2031-2036.
29. Morand K, Talbo G, Mann M, (1993) Oxidation of peptides during electrospray ionization. Rapid Commun Mass Spectrom 7: 738-743.
30. Caughey B, Raymond GJ, Ernst D, Race RE, (1991) N-terminal truncation of the scrapie-associated form of PrP by lysosomal protease(s): implications regarding the site of conversion of PrP to the protease-resistant state. J Virol 65: 6597-6603.
31. Hammond DN, Lee HJ, Tonsgard JH, Wainer BH, (1990) Development and characterization of clonal cell lines derived from septal cholinergic neurons. Brain Res 512: 190-200.
32. Greil CS, Vorberg IM, Ward AE, Meade-White KD, Harris DA, et al. (2008) Acute cellular uptake of abnormal prion protein is cell type and scrapie-strain independent. Virology 379: 284-293.
33. McNally KL, Ward AE, Priola SA, (2009) Cells expressing anchorless prion protein are resistant to scrapie infection. J Virol 83: 4469-4475.
34. Vorberg I, Raines A, Priola SA, (2004) Acute formation of protease-resistant prion protein does not always lead to persistent scrapie infection in vitro. J Biol Chem 279: 29218-29225.
35. Leblanc P, Hasenkrug K, Ward A, Myers L, Messer RJ, et al. (2012) Co-infection with the friend retrovirus and mouse scrapie does not alter prion disease pathogenesis in susceptible mice. PLoS One 7: e30872.
36. Atarashi R, Wilham JM, Christensen L, Hughson AG, Moore RA, et al. (2008) Simplified ultrasensitive prion detection by recombinant PrP conversion with shaking. Nat Methods 5: 211-212.
37. McKinley MP, Bolton DC, Prusiner SB, (1983) A protease-resistant protein is a structural component of the scrapie prion. Cell 35: 57-62.
38. Baral PK, Wieland B, Swayampakula M, Polymenidou M, Rahman MH, et al. (2012) Structural studies on the folded domain of the human prion protein bound to the Fab fragment of the antibody POM1. Acta Crystallogr D Biol Crystallogr 68: 1501-1512.
39. Oesch B, Westaway D, Walchli M, McKinley MP, Kent SB, et al. (1985) A cellular gene encodes scrapie PrP 27-30 protein. Cell 40: 735-746.
40. Hjelmeland LM, Chrambach A, (1984) Solubilization of functional membrane proteins. Methods Enzymol 104: 305-318.
41. Hill AF, Antoniou M, Collinge J, (1999) Protease-resistant prion protein produced in vitro lacks detectable infectivity. J Gen Virol 80 (Pt 1): 11-14.
42. Race R, Meade-White K, Raines A, Raymond GJ, Caughey B, et al. (2002) Subclinical scrapie infection in a resistant species: persistence, replication, and adaptation of infectivity during four passages. J Infect Dis 186Suppl 2: S166-S170.
43. Race RE, Ernst D, (1992) Detection of proteinase K-resistant prion protein and infectivity in mouse spleen by 2 weeks after scrapie agent inoculation. J Gen Virol 73 (Pt 12): 3319-3323.
44. Vorberg I, Priola SA, (2002) Molecular basis of scrapie strain glycoform variation. J Biol Chem 277: 36775-36781.
45. Baron GS, Magalhaes AC, Prado MA, Caughey B, (2006) Mouse-adapted scrapie infection of SN56 cells: greater efficiency with microsome-associated versus purified PrP-res. J Virol 80: 2106-2117.
46. Deleault NR, Walsh DJ, Piro JR, Wang F, Wang X, et al. (2012) Cofactor molecules maintain infectious conformation and restrict strain properties in purified prions. Proc Natl Acad Sci U S A 109: E1938-E1946.
47. Piro JR, Wang F, Walsh DJ, Rees JR, Ma J, et al. (2011) Seeding specificity and ultrastructural characteristics of infectious recombinant prions. Biochemistry 50: 7111-7116.
48. Merz PA, Somerville RA, Wisniewski HM, Iqbal K, (1981) Abnormal fibrils from scrapie-infected brain. Acta Neuropathol 54: 63-74.
49. Prusiner SB, McKinley MP, Bowman KA, Bolton DC, Bendheim PE, et al. (1983) Scrapie prions aggregate to form amyloid-like birefringent rods. Cell 35: 349-358.
50. Drochmans P, (1962) [Morphology of glycogen. Electron microscopic study of the negative stains of particulate glycogen]. J Ultrastruct Res 6: 141-163.
51. Calder PC, (1991) Glycogen structure and biogenesis. Int J Biochem 23: 1335-1352.
52. Bocharova OV, Breydo L, Salnikov VV, Gill AC, Baskakov IV, (2005) Synthetic prions generated in vitro are similar to a newly identified subpopulation of PrPSc from sporadic Creutzfeldt-Jakob Disease. Protein Sci 14: 1222-1232.
53. Bocharova OV, Makarava N, Breydo L, Anderson M, Salnikov VV, et al. (2006) Annealing prion protein amyloid fibrils at high temperature results in extension of a proteinase K-resistant core. J Biol Chem 281: 2373-2379.
54. Zou WQ, Capellari S, Parchi P, Sy MS, Gambetti P, et al. (2003) Identification of novel proteinase K-resistant C-terminal fragments of PrP in Creutzfeldt-Jakob disease. J Biol Chem 278: 40429-40436.
55. Satoh K, Muramoto T, Tanaka T, Kitamoto N, Ironside JW, et al. (2003) Association of an 11-12 kDa protease-resistant prion protein fragment with subtypes of dura graft-associated Creutzfeldt-Jakob disease and other prion diseases. J Gen Virol 84: 2885-2893.
56. Silveira JR, Raymond GJ, Hughson AG, Race RE, Sim VL, et al. (2005) The most infectious prion protein particles. Nature 437: 257-261.
57. Wolschner C, Giese A, Kretzschmar HA, Huber R, Moroder L, et al. (2009) Design of anti- and pro-aggregation variants to assess the effects of methionine oxidation in human prion protein. Proc Natl Acad Sci U S A 106: 7756-7761.
58. Colombo G, Meli M, Morra G, Gabizon R, Gasset M, (2009) Methionine sulfoxides on prion protein Helix-3 switch on the alpha-fold destabilization required for conversion. PLoS One 4: e4296.
59. Younan ND, Nadal RC, Davies P, Brown DR, Viles JH, (2012) Methionine oxidation perturbs the structural core of the prion protein and suggests a generic misfolding pathway. J Biol Chem 287: 28263-28275.
60. Breydo L, Bocharova OV, Makarava N, Salnikov VV, Anderson M, et al. (2005) Methionine oxidation interferes with conversion of the prion protein into the fibrillar proteinase K-resistant conformation. Biochemistry 44: 15534-15543.
61. Chesebro B, Trifilo M, Race R, Meade-White K, Teng C, et al. (2005) Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308: 1435-1439.
62. Chesebro B, Race B, Meade-White K, LaCasse R, Race R, et al. (2010) Fatal transmissible amyloid encephalopathy: a new type of prion disease associated with lack of prion protein membrane anchoring. PLoS Pathog 6: e1000800.
63. Sim VL, Caughey B, (2009) Ultrastructures and strain comparison of under-glycosylated scrapie prion fibrils. Neurobiol Aging 30: 2031-2042.
64. Panza G, Stohr J, Birkmann E, Riesner D, Willbold D, et al. (2008) Aggregation and amyloid fibril formation of the prion protein is accelerated in the presence of glycogen. Rejuvenation Res 11: 365-369.
65. Luk KC, Kehm VM, Zhang B, O'Brien P, Trojanowski JQ, et al. (2012) Intracerebral inoculation of pathological alpha-synuclein initiates a rapidly progressive neurodegenerative alpha-synucleinopathy in mice. J Exp Med 209: 975-986.
66. Kane MD, Lipinski WJ, Callahan MJ, Bian F, Durham RA, et al. (2000) Evidence for seeding of beta-amyloid by intracerebral infusion of Alzheimer brain extracts in beta-amyloid precursor protein-transgenic mice. J Neurosci 20: 3606-3611.
67. Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, et al. (2006) Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 313: 1781-1784.
68. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, et al. (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11: 909-913.