Dissociation of infectivity from seeding ability in prions with alternate docking mechanism

PLoS Pathogens

Volumn 7, Issue 7, 2011, Pages

  Miller, Michael B ^a   Geoghegan, James C ^a,b   Supattapone, Surachai ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; CHO CELL; CONTROLLED STUDY; FEMALE; MOLECULAR DOCKING; MOLECULE; MUTAGENESIS; MUTANT; NONHUMAN; PRION DISEASE; PROTEIN INTERACTION; STEREOTYPY; WILD TYPE; ANIMAL; BRAIN; CRICETULUS; GENETICS; HAMSTER; METABOLISM; MOUSE; PATHOLOGY; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE;

CRICETULUS GRISEUS; MAMMALIAN PRION;

ANIMALS; BRAIN; CHO CELLS; CRICETINAE; CRICETULUS; MICE; PRION DISEASES; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PRPC PROTEINS;

EID: 79960934693     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002128     Document Type: Article

References (53)

1. Prusiner SB, (1982) Novel proteinaceous infectious particles cause scrapie. Science 216: 136-144.
2. Prusiner SB, (1998) Prions. Proc Natl Acad Sci U S A 95: 13363-13383.
3. Brandner S, Isenmann S, Raeber A, Fischer M, Sailer A, et al. (1996) Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 379: 339-343.
4. Bueler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, et al. (1993) Mice devoid of PrP are resistant to scrapie. Cell 73: 1339-1347.
5. 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.
6. Manson JC, Clarke AR, McBride PA, McConnell I, Hope J, (1994) PrP gene dosage determines the timing but not the final intensity or distribution of lesions in scrapie pathology. Neurodegeneration 3: 331-340.
7. Kocisko DA, Come JH, Priola SA, Chesebro B, Raymond GJ, et al. (1994) Cell-free formation of protease-resistant prion protein. Nature 370: 471-474.
8. Castilla J, Saa P, Hetz C, Soto C, (2005) In vitro generation of infectious scrapie prions. Cell 121: 195-206.
9. Saa P, Castilla J, Soto C, (2006) Ultra-efficient replication of infectious prions by automated protein misfolding cyclic amplification. J Biol Chem 281: 35245-35252.
10. Murayama Y, Yoshioka M, Horii H, Takata M, Yokoyama T, et al. (2006) Protein misfolding cyclic amplification as a rapid test for assessment of prion inactivation. Biochem Biophys Res Commun 348: 758-762.
11. Deleault NR, Harris BT, Rees JR, Supattapone S, (2007) Formation of native prions from minimal componenets in vitro. Proc Natl Acad Sci U S A 104: 9741-9746.
12. Wang F, Wang X, Yuan CG, Ma J, (2010) Generating a Prion with Bacterially Expressed Recombinant Prion Protein. Science 327: 1132-1135.
13. 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 U S A 97: 5836-5841.
14. Lau AL, Yam AY, Michelitsch MM, Wang X, Gao C, et al. (2007) Characterization of prion protein (PrP)-derived peptides that discriminate full-length PrPSc from PrPC. Proc Natl Acad Sci U S A 104: 11551-11556.
15. Moroncini G, Kanu N, Solforosi L, Abalos G, Telling GC, et al. (2004) Motif-grafted antibodies containing the replicative interface of cellular PrP are specific for PrPSc. Proc Natl Acad Sci U S A 101: 10404-10409.
16. Solforosi L, Bellon A, Schaller M, Cruite JT, Abalos GC, et al. (2007) Toward molecular dissection of PrPC-PrPSc interactions. J Biol Chem 282: 7465-7471.
17. Riek R, Hornemann S, Wider G, Glockshuber R, Wuthrich K, (1997) NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231). FEBS Lett 413: 282-288.
18. Zahn R, (2003) The octapeptide repeats in mammalian prion protein constitute a pH-dependent folding and aggregation site. J Mol Biol 334: 477-488.
19. Peretz D, Williamson RA, Kaneko K, Vergara J, Leclerc E, et al. (2001) Antibodies inhibit prion propagation and clear cell cultures of prion infectivity. Nature 412: 739-743.
20. White AR, Enever P, Tayebi M, Mushens R, Linehan J, et al. (2003) Monoclonal antibodies inhibit prion replication and delay the development of prion disease. Nature 422: 80-83.
21. Wang F, Yin S, Wang X, Zha L, Sy MS, et al. (2010) Role of the highly conserved middle region of prion protein (PrP) in PrP-lipid interaction. Biochemistry 49: 8169-8176.
22. Ostapchenko VG, Makarava N, Savtchenko R, Baskakov IV, (2008) The polybasic N-terminal region of the prion protein controls the physical properties of both the cellular and fibrillar forms of PrP. J Mol Biol 383: 1210-1224.
23. Supattapone S, Muramoto T, Legname G, Mehlhorn I, Cohen FE, et al. (2001) Identification of two prion protein regions that modify scrapie incubation time. J Virol 75: 1408-1413.
24. Baumann F, Tolnay M, Brabeck C, Pahnke J, Kloz U, et al. (2007) Lethal recessive myelin toxicity of prion protein lacking its central domain. EMBO J 26: 538-547.
25. Li A, Christensen HM, Stewart LR, Roth KA, Chiesa R, et al. (2007) Neonatal lethality in transgenic mice expressing prion protein with a deletion of residues 105-125. EMBO J 26: 548-558.
26. Shmerling D, Hegyi I, Fischer M, Blattler T, Brandner S, et al. (1998) Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions. Cell 93: 203-214.
27. Abalos GC, Cruite JT, Bellon A, Hemmers S, Akagi J, et al. (2008) Identifying key components of the PrPC-PrPSc replicative interface. J Biol Chem 283: 34021-34028.
28. Makarava N, Baskakov IV, (2008) Expression and purification of full-length recombinant PrP of high purity. Methods Mol Biol 459: 131-143.
29. Geoghegan JC, Miller MB, Kwak AH, Harris BT, Supattapone S, (2009) Trans-dominant inhibition of prion propagation in vitro is not mediated by an accessory cofactor. PLoS Pathog 5: e1000535.
30. Castilla J, Saa P, Morales R, Abid K, Maundrell K, et al. (2006) Protein misfolding cyclic amplification for diagnosis and prion propagation studies. Methods Enzymol 412: 3-21.
31. Deleault NR, Kascsak R, Geoghegan JC, Supattapone S, (2010) Species-dependent differences in cofactor utilization for formation of the protease-resistant prion protein in vitro. Biochemistry 49: 3928-3934.
32. Castilla J, Morales R, Saa P, Barria M, Gambetti P, et al. (2008) Cell-free propagation of prion strains. Embo J 27: 2557-2566.
33. Saborio GP, Permanne B, Soto C, (2001) Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411: 810-813.
34. Chen B, Morales R, Barria MA, Soto C, (2010) Estimating prion concentration in fluids and tissues by quantitative PMCA. Nat Methods 7: 519-520.
35. Nishina KA, Deleault NR, Mahal SP, Baskakov I, Luhrs T, et al. (2006) The stoichiometry of host PrPC glycoforms modulates the efficiency of PrPSc formation in vitro. Biochemistry 45: 14129-14139.
36. 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.
37. Angers RC, Kang HE, Napier D, Browning S, Seward T, et al. (2010) Prion strain mutation determined by prion protein conformational compatibility and primary structure. Science 328: 1154-1158.
38. Li J, Browning S, Mahal SP, Oelschlegel AM, Weissmann C, (2009) Darwinian Evolution of Prions in Cell Culture. Science 327: 869-872.
39. DePace AH, Santoso A, Hillner P, Weissman JS, (1998) A critical role for amino-terminal glutamine/asparagine repeats in the formation and propagation of a yeast prion. Cell 93: 1241-1252.
40. Brachmann A, Baxa U, Wickner RB, (2005) Prion generation in vitro: amyloid of Ure2p is infectious. Embo J 24: 3082-3092.
41. Glover JR, Kowal AS, Schirmer EC, Patino MM, Liu JJ, et al. (1997) Self-seeded fibers formed by Sup35, the protein determinant of [PSI+], a heritable prion-like factor of S. cerevisiae. Cell 89: 811-819.
42. King CY, Diaz-Avalos R, (2004) Protein-only transmission of three yeast prion strains. Nature 428: 319-323.
43. Tanaka M, Chien P, Naber N, Cooke R, Weissman JS, (2004) Conformational variations in an infectious protein determine prion strain differences. Nature 428: 323-328.
44. Abid K, Morales R, Soto C, (2010) Cellular factors implicated in prion replication. FEBS Lett 584: 2409-2414.
45. Graham JF, Agarwal S, Kurian D, Kirby L, Pinheiro TJ, et al. (2010) Low density subcellular fractions enhance disease-specific prion protein misfolding. J Biol Chem 285: 9868-9880.
46. Fischer M, Rulicke T, Raeber A, Sailer A, Moser M, et al. (1996) Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. Embo J 15: 1255-1264.
47. Supattapone S, Bosque P, Muramoto T, Wille H, Aagaard C, et al. (1999) Prion protein of 106 residues creates an artifical transmission barrier for prion replication in transgenic mice. Cell 96: 869-878.
48. Deleault AM, Deleault NR, Harris BT, Rees JR, Supattapone S, (2008) The effects of prion protein proteolysis and disaggregation on the strain properties of hamster scrapie. J Gen Virol 89: 2642-2650.
49. McKinley MP, Bolton DC, Prusiner SB, (1983) A protease-resistant protein is a structural component of the scrapie prion. Cell 35: 57-62.
50. Aguib Y, Heiseke A, Gilch S, Riemer C, Baier M, et al. (2009) Autophagy induction by trehalose counteracts cellular prion infection. Autophagy 5: 361-369.
51. Enari M, Flechsig E, Weissmann C, (2001) Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a prion protein antibody. Proc Natl Acad Sci U S A 98: 9295-9299.
52. Luhr KM, Nordstrom EK, Low P, Ljunggren HG, Taraboulos A, et al. (2004) Scrapie protein degradation by cysteine proteases in CD11c+ dendritic cells and GT1-1 neuronal cells. J Virol 78: 4776-4782.
53. Mohan J, Hopkins J, Mabbott NA, (2005) Skin-derived dendritic cells acquire and degrade the scrapie agent following in vitro exposure. Immunology 116: 122-133.