The reconstitution of mammalian prion infectivity de novo

FEBS Journal

Volumn 274, Issue 3, 2007, Pages 576-587

  Baskakov, Ilia V ^a,b  

^a University of Maryland School of Medicine ^*  (United States)

^b UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

Author keywords

Amyloid fibrils; Conformational adaptation; In vitro conversion; Prion diseases; Prion protein; Synthetic prions

Indexed keywords

AMYLOID; MUTANT PROTEIN; PRION PROTEIN; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE;

ALPHA HELIX; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CIS TRANS ISOMERISM; CREUTZFELDT JAKOB DISEASE; HUMAN; HYPOTHESIS; INCUBATION TIME; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN STRUCTURE; SHORT SURVEY; STRUCTURE ANALYSIS;

AMYLOID; ANIMALS; HUMANS; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; PRION DISEASES; PRIONS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY;

FUNGI; MAMMALIA; MAMMALIAN PRION;

EID: 33846446694     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05630.x     Document Type: Short Survey

References (101)

1. Prusiner SB (1998) Prions (Les Prix Nobel Lecture). In Les Prix Nobel (Frängsmyr T, ed.), pp. 268-323. Almqvist & Wiksell International, Stockholm.
2. Gajdusek DC (1988) Transmissible and non-transmissible amyloidoses: autocatalytic post-translational conversion of host precursor proteins to β-pleated sheet configurations. J Neuroimmunol 20, 95-110.
3. Legname G, Baskakov IV, Nguyen H-OB, Riesner D, Cohen FE, DeArmond SJ & Prusiner SB (2004) Synthetic mammalian prions. Science 305, 673-676.
4. Castilla J, Saa P, Hetz C & Soto C (2005) In vitro generation of infectious scrapie prions. Cell 121, 195-206.
5. Dumpitak C, Beekes M, Weinmann N, Metzger S, Winklhofer KF, Tatzelt J & Riesner D (2006) The polysaccharide scaffold of PrP 27-30 is a common compound of natural prions and consists of a-linked polyglucose. Biol Chem 386, 1149-1155.
6. Appel TR, Dumpitak C, Matthiesen U & Riesner D (1999) Prion rods contain an inert polysaccharide scaffold. Biol Chem 380, 1295-1306.
7. Klein TR, Kirsch D, Kaufmann R & Riesner D (1998) Prion rods contain small amounts of two sphingolipids as revealed by thin-layer chromatography and mass spectrometry. Biol Chem 379, 655-666.
8. Safar JG, Kellings K, Serban A, Groth D, Cleaver JE, Prusiner SB & Riesner D (2005) Search for a prionspecific nucleic acid. J Virol 79, 10796-10806.
9. Meyer N, Rosenbaum V, Schmidt B, Gilles K, Mirenda C, Groth D, Prusiner SB & Riesner D (1991) Search for a putative scrapie genome in purified prion fractions reveals a paucity of nucleic acids. J Gen Virol 72, 37-49.
10. Zou W, Zheng J, Gray DM, Gambetti P & Chen SG (2004) Antibody to DNA detect scrapie but not normal prion protein. Proc Acad Natl Sci USA 101, 1380-1385.
11. Deleault NR, Lucassen RW & Supattapone S (2003) RNA molecules stimulate prion protein conversion. Nature 425, 717-720.
12. Deleault NR, Geoghegan JC, Nishina K, Kascsak R, Williamson RA & Supattapone S (2005) Protease-resistant prion protein amplification reconstituted with partially purified substrates and synthetic polyanions. J Biol Chem 280, 26873-26879.
13. Wong C, Xiong LW, Horiuchi M, Raymond L, Wehrly K, Chesebro B & Caughey B (2001) Sulfated glycans and elevated temperature stimulate PrP (Sc)-dependent cell-free formation of protease-resistant prion protein. EMBO J 20, 377-386.
14. Warner RG, Hundt C, Weiss S & Turnbull JE (2002) Identification of the heparan sulfate binding sites in the cellular prion protein. J Biol Chem 277, 18421-18430.
15. Wille H, Michelitsch MD, Guenebaut V, Supattapone S, Serban A, Cohen FE, Agard DA & Prusiner SB (2002) Structural studies of the scrapie prion protein by electron crystallography. Proc Acad Natl Sci USA 99, 3563-3568.
16. Govaerts C, Wille H, Prusiner SB & Cohen FE (2004) Evidance for assembly of prions with left-handed b-helices into trimers. Proc Acad Natl Sci USA 101, 8342-8347.
17. DeMarco ML & Daggett V (2004) From conversion to aggregation: protofibrils formation of the prion protein. Proc Acad Natl Sci USA 101, 2293-2298.
18. Dima RI & Thirumalai D (2004) Probing the instabilities in the dynamics of helical fragments from mouse PrPC. Proc Natl Acad Sci USA 101, 15335-15340.
19. Eghiaian F, Grosclaude J, Lesceu S, Debey P, Doublet B, Treguer E, Rezaei H & Knossow M (2004) Insight into the PrPC → PrPSc conversion from the structures of antibody-bound ovine prion scrapie susceptibility variants. Proc Acad Natl Sci USA 101, 10254-10259.
20. Kocisko DA, Lansbury PT Jr & Caughey B (1996) Partial unfolding and refolding of scrapie-associated prion protein: evidence for a critical 16-kDa C-terminal domain. Biochemistry 35, 13434-13442.
21. Peretz D, Williamson RA, Matsunaga Y, Serban H, Pinilla C, Bastidas RB, Rozenshteyn R, James TL, Houghten RA, Cohen FE et al. (1997) A conformational transition at the N terminus of the prion protein features in formation of the scrapie isoform. J Mol Biol 273, 614-622.
22. Khalili-Shirazi A, Summers L, Linehan J, Mallinson G, Anstee D, Hawke S, Jackson GS & Collinge J (2005) PrP glycoforms are associated in a strain-specific ratio in native PrPSc. J Gen Virol 86, 2635-2644.
23. Haire LF, Whyte SM, Vasisht N, Gill AC, Verma C, Dodson EJ, Dodson GG & Bayley PM (2004) The crystal structure of the globular domain of sheep prion protein. J Mol Biol 336, 1175-1183.
24. Ziegler J, Sticht H, Marx UC, Muller W, Rosch P & Schwarzinger S (2003) CD and NMR studies of prion protein (PrP) helix 1. J Biol Chem 278, 50175-50181.
25. Pan K-M, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, Mehlhorn I, Huang Z, Fletterick RJ, Cohen FE et al. (1993) Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci USA 90, 10962-10966.
26. Caughey BW, Dong A, Bhat KS, Ernst D, Hayes SF & Caughey WS (1991) Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. Biochemistry 30, 7672-7680.
27. Lasmézas CI, Deslys J-P, Robain O, Jaegly A, Beringue V, Peyrin J-M, Fournier J-G, Hauw J-J, Rossier J & Dormont D (1997) Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein. Science 275, 402-405.
28. Tremblay P, Ball HL, Kaneko K, Groth D, Hegde RS, Cohen FE, DeArmond S, Prusiner SB & Safar J (2004) Mutant PrPSc conformers induced by a synthetic peptide and several prion strains. J Virol 78, 2088-2099.
29. Manuelidis L, Fritch W & Xi Y-G (1997) Evolution of a strain of CJD that induces BSE-like plaques. Science 277, 94-98.
30. Barron RM, Thomson V, Jameison E, Melton DW, Ironside J, Will R & Manson JC (2001) Changing a single amino acid in the N-terminus of murine PrP alters TSE incubation time across three species barrier. EMBO J 20, 5070-5078.
31. Novitskaya V, Makarava N, Bellon A, Bocharova OV, Bronstein IB, Williamson RA & Baskakov IV (2006) Probing the conformation of the prion protein within a single amyloid fibril using a novel immunoconformational assay. J Biol Chem 281, 15536-15545.
32. Sc)-specific epitope defined by a monoclonal antibody. Nature 389, 74-77.
33. Paramithiotis E, Pinard M, Lawton T, LaBoissiere S, Leathers VL, Zou WQ, Estey LA, Lamontagne J, Lehto MT, Kondejewski LH et al. (2003) A prion protein epitope selective for the pathologically misfolded conformation. Nat Med 9, 893-899.
34. Moroncini G, Kanu N, Solforosi L, Abalos G, Telling GC, Head M, Ironside J, Brockes JP, Burton DR & Williamson RA (2004) Motif-grafted antibodies containing the replicative interface of cellular PrP are specific for PrPSc. Proc Acad Natl Sci USA 101, 10404-10409.
35. Bessen RA, Kocisko DA, Raymond GJ, Nandan S, Lansbury PT & Caughey B (1995) Non-genetic propagation of strain-specific properties of scrapie prion protein. Nature 375, 698-700.
36. Saborio GP, Permanne B & Soto C (2001) Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411, 810-813.
37. Caughey B, Kocisko DA, Raymond GJ & Lansbury PT Jr (1995) Aggregates of scrapie-associated prion protein induce the cell-free conversion of protease-sensitive prion protein to the protease-resistant state. Chem Biol 2, 807-817.
38. Horiuchi M, Chabry J & Caughey B (1999) Specific binding of normal prion protein to the scrapie form via a localized domain initiates its conversion to the protease-resistant state. EMBO J 18, 3193-3203.
39. Horiuchi M, Priola SA, Chabry J & Caughey B (2000) Interactions between heterologous forms of prion protein: binding, inhibition of conversion, and species barriers. Proc Natl Acad Sci USA 97, 5836-5841.
40. Kocisko DA, Priola SA, Raymond GJ, Chesebro B, Lansbury PT Jr & Caughey B (1995) Species specificity in the cell-free conversion of prion protein to protease-resistant forms: a model for the scrapie species barrier. Proc Natl Acad Sci USA 92, 3923-3927.
41. Supattapone S (2004) Prion protein conversion in vitro. J Mol Med 82, 348-356.
42. Weber P, Giese A, Piening N, Mitteregger G, Thomzig A, Beekes M & Kretzschmar HA (2006) Cell-free formation of misfolded prion protein with authentic prion infectivity. Proc Acad Natl Sci USA 103, 15823.
43. Lucassen R, Nishina K & Supattapone S (2003) In vitro amplification of protease-resistant prion protein requires free sulfhydryl groups. Biochemistry 42, 4127-4135.
44. Castilla J, Saa P & Soto C (2005) Detection of prions in blood. Nat Med 11, 982-985.
45. Nishina K, Deleault NR, Mahal S, Baskakov I, Luhrs T, Riek R & Supattapone S (2006) The stoichiometry of host PrPC glycoforms modulates the efficiency of PrPSc formation in vitro. Biochemistry 45, 14129-14139.
46. Bieschke J, Weber P, Sarafoff N, Beekes M, Giese A & Kretzschmar H (2004) Autocatalytic self-propagation of misfolded prion protein. Proc Acad Natl Sci USA 101, 12207-12211.
47. Chesebro B, Trifilo M, Race M, Meade-White K, Teng C, LaCasse R, Raymond L, Favara C, Baron G, Priola S et al. (2005) Anchorless prion protein result in infectious amyloid disease without clinical scrapie. Science 308, 1435-1439.
48. Lehmann S & Harris DA (1997) Blockade of glycosylation promotes acquisition of scrapie-like properties by the prion protein in cultured cells. J Biol Chem 272, 21479-21487.
49. Neuendorf E, Weber A, Saalmueller A, Schatzl H, Reifenberg K, Pfaff E & Groschup MH (2004) Glycosylation deficiency at either one of the two glycan attachment sites of cellular prion protein preserves susceptibility to bovine spongiform encephalopathy and scrapie infections. J Biol Chem 279, 53306-53316.
50. Sc formation in neuroblastoma cells infected with different prion strains. J Gen Virol 81, 2555-2563.
51. Taraboulos A, Rogers M, Borchelt DR, McKinley MP, Scott M, Serban D & Prusiner SB (1990) Acquisition of protease resistance by prion proteins in scrapie-infected cells does not require asparagine-linked glycosylation. Proc Natl Acad Sci USA 87, 8262-8266.
52. Hornemann S, Schorn C & Wuthrich K (2004) NMR structure of bovine prion protein isolated from healthy calf brain. EMBO Report 5, 1159-1164.
53. Hicks MR, Gill AC, Bath IK, Rullay AK, Sylvester ID, Crout DH & Pinheiro TJ (2006) Synthesis and structural characterization of a mimetic membrane-anchored prion protein. FEBS J 273, 1285-1299.
54. Lu KP (2004) Pinning down cell signaling, cancer, and Alzheimer's disease. Trends Biochem Sci 29, 200-209.
55. Eakin CM, Berman AJ & Miranker AD (2006) A native to amyloidogenic transition regulated by a backbone trigger. Nat Struct Mol Biol 13, 295-297.
56. Goldgaber D, Goldfarb LG, Brown P, Asher DM, Brown WT, Lin S, Teener JW, Feinstone SM, Rubenstein R, Kascsak RJ et al. (1989) Mutations in familial Creutzfeldt-Jakob disease and Gerstmann-Sträussler-Scheinker's syndrome. Exp Neurol 106, 204-206.
57. Jackson GS, Hosszu LLP, Power A, Hill AF, Kenney J, Saibil H, Craven CJ, Waltho JP, Clarke AR & Collinge J (1999) Reversible conversion of monomeric human prion protein between native and fibrilogenic conformations. Science 283, 1935-1937.
58. Baskakov IV, Legname G, Prusiner SB & Cohen FE (2001) Folding of prion protein to its native α-helical conformation is under kinetic control. J Biol Chem 276, 19687-19690.
59. Rezaei H, Choiset Y, Eghiaian F, Treguer E, Mentre P, Debey P, Grosclaude J & Haertle T (2002) Amyloidogenic unfolding intermediates differentiate sheep prion protein variants. J Mol Biol 322, 799-814.
60. Lee S & Eisenberg D (2003) Seeded conversion of recombinant prion protein to a disulfide-bonded oligomer by a reduction-oxidation process. Nat Struc Biol 10, 725-730.
61. Kazlauskaite J, Sanghera N, Sylvester I, Venien-Bryan C & Pinheiro TJ (2003) Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization. Biochemistry 42, 3295-3304.
62. Sokolowski F, Modler AJ, Masuch R, Zirwer D, Baier M, Lutsch GMDA, Gast K & Naumann D (2003) Formation of critical oligomers is a key event during conformational transition of recombinant syrian hamster prion protein. J Biol Chem 278, 40481-40492.
63. Torrent J, Alvarez-Martinez MT, Heitz F, Liautard JP, Balny C & Lange R (2003) Alternative prion structural changes revealed by high pressure. Biochemistry 42, 1318-1325.
64. Cordeiro Y, Machado F, Juliano L, Juliano MA, Brentani RR, Foguel D & Silva JL (2001) DNA converts cellular prion protein into the beta-sheet conformation and inhibits prion peptide aggregation. J Biol Chem 276, 49400-49409.
65. Swietnicki W, Morillas M, Chen SG, Gambetti P & Surewicz WK (2000) Aggregation and fibrillization of the recombinant human prion protein huPrP90-231. Biochemistry 39, 424-431.
66. Cordeiro Y, Lima LMTR, Gomes MPB, Foguel D & Silva JL (2004) Modulation of prion protein oligomerization, aggregation, and b-sheet conversion by 4,4′-dianilino-1,1′-binaphthyl-5,5′-sulfonate (bis-ANS). J Biol Chem 279, 5346-5352.
67. Caughey B, Brown K, Raymond GJ, Katzenstein GE & Thresher W (1994) Binding of the protease-sensitive form of PrP (prion protein) to sulfated glycosaminoglycan and Congo red. J Virol 68, 2135-2141.
68. Gabus C, Derrington E, Leblanc P, Chnaiderman J, Dormont D, Swietnicki W, Morillas M, Surewicz WK, Marc D, Nandi P et al. (2004) The prion protein has RNA binding chaperoning properties characteristic of nucleocapsid protein NCP7 of HIV-1. J Biol Chem 276, 19301-19309.
69. Adler V, Zeiler B, Kryukov V, Kascsak R, Rubenstein R & Grossman A (2003) Small, highly structured RNAs participate in the conversion of human recombinant PrPsen to PrPres in vitro. J Mol Biol 332, 47-57.
70. Sanghera N & Pinheiro TJ (2002) Binding of prion protein to lipid membranes and implications for prion conversion. J Mol Biol 315, 1241-1256.
71. Critchley P, Kazlauskaite J, Eason R & Pinheiro TJ (2004) Binding of prion proteins to lipid membranes. Biochem Biophys Res Commun 313, 559-567.
72. Nandi PK, Leclerc E & Marc D (2002) Unusual property of prion protein unfolding in neutral salt solution. Biochemistry 41, 11017-11024.
73. Morillas M, Vanik DL & Surewicz WK (2001) On the mechanism of α-helix to β-sheet transition in the recombinant prion protein. Biochemistry 40, 6982-6987.
74. Nandi PK & Leclerc E (1999) Polymerization of murine recombinant prion protein in nucleic acid solution. Arch Virol 144, 1751-1763.
75. Millhauser GL (2004) Copper binding in the prion protein. Acc Chem Res 37, 79-85.
76. Bocharova OV, Breydo L, Salnikov VV & Baskakov IV (2005) Cu(II) inhibits in vitro conversion of prion protein into amyloid fibrils. Biochemistry 44, 6776-6787.
77. +] factor by in vitro-converted Sup35 protein. Science 289, 595-599.
78. Maddelein ML, Dos Reis S, Duvezin-Caubet S, Coulary-Salin B & Saupe SJ (2002) Amyloid aggregates of the HET-s prion protein are infectious. Proc Acad Natl Sci USA 99, 7402-7407.
79. Tanaka M, Chien P, Naber N, Cooke R & Weissman JS (2004) Conformational variations in an infectious protein determine prion strain differences. Nature 6980, 323-328.
80. Baskakov IV, Legname G, Baldwin MA, Prusiner SB & Cohen FE (2002) Pathway complexity of prion protein assembly into amyloid. J Biol Chem 277, 21140-21148.
81. Kazlauskaite J, Young A, Gardner CE, Macpherson JV, Venien-Bryan C & Pinheiro TJ (2005) An unusual soluble b-turn-rich conformation of prion is involved in fibril formation and toxic to neuronal cells. Biochem Biophys Res Commun 328, 292-305.
82. Leffer K-W, Wille H, Stohr J, Junger E, Prusiner SB & Riesner D (2005) Assembly of natural and recombinant prion protein into fibrils. Biol Chem 386, 569-580.
83. Leffer K-W, Schell J, Jansen K, Lucassen R, Kaimann T, Nagel-Steger L, Tatzelt J & Riesner D (2004) The structural transition of the prion protein into its pathogenic conformation is induced by unmasking hydrophobic sites. J Mol Biol 344, 839-853.
84. Silveira JR, Raymond GJ, Hughson A, Race RE, Sim VL, Hayes SF & Caughey B (2005) The most infectious prion protein particles. Nature 437, 257-261.
85. Baskakov IV (2004) Autocatalytic conversion of recombinant prion proteins displays a species barrier. J Biol Chem 279, 586-595.
86. Bocharova OV, Breydo L, Parfenov AS, Salnikov VV & Baskakov IV (2005) In vitro conversion of full length mammalian prion protein produces amyloid form with physical property of PrPSc. J Mol Biol 346, 645-659.
87. Kaneko K, Ball HL, Wille H, Zhang H, Groth D, Torchia M, Tremblay P, Safar J, Prusiner SB, DeArmond SJ et al. (2000) A synthetic peptide initiates Gerstmann-Sträussler-Scheinker (GSS) disease in transgenic mice. J Mol Biol 295, 997-1007.
88. Nazor KE, Kuhn F, Seward T, Green M, Zwald D, Purro M, Schmid J, Biffiger K, Power AM, Oesch B et al. (2005) Immunodetection of disease-associated mutant PrP, which accelerates disease in GSS transgenic mice. EMBO J 24, 2472-2480.
89. Legname G, Nguyen H-OB, Baskakov IV, Cohen FE, DeArmond SJ & Prusiner SB (2005) Strain-specified characteristics of mouse synthetic prions. Proc Natl Acac Sci USA 102, 2168-2173.
90. Bartz JC, Bessen RA, McKenzie D, Marsh RF & Aiken JM (2000) Adaptation and selection of prion protein strain conformations following interspecies transmission of transmissible mink encephalopathy. J Virol 74, 5542-5547.
91. Sc. Prot Sci 14, 1222-1232.
92. Hope J, Multhaup G, Reekie LJD, Kimberlin RH & Beyreuther K (1988) Molecular pathology of scrapie-associated fibril protein (PrP) in mouse brain affected by the ME7 strain of scrapie. Eur J Biochem 172, 271-277.
93. Zou WQ, Capellari S, Parchi P, Sy MS, Gambetti P & Chen SG (2003) Identification of novel proteinase K-resistant C-terminal fragments of PrP in Creutzfeldt-Jakob disease. J Biol Chem 278, 40429-40436.
94. Bocharova OV, Makarava N, Breydo L, Anderson M, Salnikov VV & Baskakov IV (2006) Annealing PrP amyloid firbils at high temperature results in extension of a proteinase K resistant core. J Biol Chem 281, 2373-2379.
95. Weissmann C (1991) A 'unified theory' of prion propagation. Nature 352, 679-683.
96. Gonzalez-Iglesias R, Pajares MA, Espinosa COJC, Oesch B & Gasset M (2002) Prion protein interaction with glycosaminoglycan occurs with the formation of oligomeric complexes stabilized by Cu(II) bridges. J Mol Biol 319, 527-540.
97. Prusiner SB, Scott M, Foster D, Pan K-M, Groth D, Mirenda C, Torchia M, Yang S-L, Serban D, Carlson GA et al. (1990) Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 63, 673-686.
98. Scott M, Groth D, Foster D, Torchia M, Yang S-L, DeArmond SJ & Prusiner SB (1993) Propagation of prions with artificial properties in transgenic mice expressing chimeric PrP genes. Cell 73, 979-988.
99. Pattison IH & Jones KM (1968) Modification of a strain of mouse-adapted scrapie by passage through rats. Res Vet Sci 9, 408-410.
100. Barron RM, Thomson V, King D, Shaw J, Melton DW & Manson JC (2003) Transmission of murine scrapie to P101L transgenic mice. J Gen Virol 84, 3165-3172.
101. Peretz D, Scott M, Groth D, Williamson A, Burton D, Cohen FE & Prusiner SB (2001) Strain-specified relative conformational stability of the scrapie prion protein. Protein Sci 10, 854-863.