A Structural and Functional Comparison Between Infectious and Non-Infectious Autocatalytic Recombinant PrP Conformers

1. Prusiner SB (1998) Prions. Proc Natl Acad Sci U S A 95 : 13363–13383. 9811807

2. 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. 7913989

3. Saborio GP, Permanne B, Soto C (2001) Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411 : 810–813. 11459061

4. Castilla J, Morales R, Saa P, Barria M, Gambetti P, et al. (2008) Cell-free propagation of prion strains. Embo J 27 : 2557–2566. doi: 10.1038/emboj.2008.181 18800058

5. Castilla J, Saa P, Hetz C, Soto C (2005) In vitro generation of infectious scrapie prions. Cell 121 : 195–206. 15851027

6. 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. 17535913

7. Piro JR, Harris BT, Nishina K, Soto C, Morales R, et al. (2009) Prion protein glycosylation is not required for strain-specific neurotropism. J Virol 83 : 5321–5328. doi: 10.1128/JVI.02502-08 19297485

8. Piro JR, Harris BT, Supattapone S (2011) In situ photodegradation of incorporated polyanion does not alter prion infectivity. PLoS Pathog 7: e1002001. doi: 10.1371/journal.ppat.1002001 21304885

9. Colby DW, Wain R, Baskakov IV, Legname G, Palmer CG, et al. (2010) Protease-sensitive synthetic prions. PLoS Pathog 6: e1000736. doi: 10.1371/journal.ppat.1000736 20107515

10. 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. doi: 10.1073/pnas.1206999109 22711839

11. 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. doi: 10.1074/jbc.C110.113464 20304915

12. Legname G, Baskakov IV, Nguyen HO, Riesner D, Cohen FE, et al. (2004) Synthetic mammalian prions. Science 305 : 673–676. 15286374

13. 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. doi: 10.1007/s00401-009-0633-x 20052481

14. Timmes AG, Moore RA, Fischer ER, Priola SA (2013) Recombinant prion protein refolded with lipid and RNA has the biochemical hallmarks of a prion but lacks in vivo infectivity. PLoS One 8: e71081. doi: 10.1371/journal.pone.0071081 23936256

15. Wang F, Wang X, Yuan CG, Ma J (2010) Generating a Prion with Bacterially Expressed Recombinant Prion Protein. Science 327 : 1132–1135. doi: 10.1126/science.1183748 20110469

16. Spinner DS, Kascsak RB, Lafauci G, Meeker HC, Ye X, et al. (2007) CpG oligodeoxynucleotide-enhanced humoral immune response and production of antibodies to prion protein PrPSc in mice immunized with 139A scrapie-associated fibrils. J Leukoc Biol 81 : 1374–1385. 17379700

17. Prusiner SB, Groth DF, Bolton DC, Kent SB, Hood LE (1984) Purification and structural studies of a major scrapie prion protein. Cell 38 : 127–134. 6432339

18. Korth C, Stierli B, Streit P, Moser M, Schaller O, et al. (1997) Prion (PrPSc)-specific epitope defined by a monoclonal antibody. Nature 390 : 74–77. 9363892

19. Bai Y, Milne JS, Mayne L, Englander SW (1993) Primary structure effects on peptide group hydrogen exchange. Proteins 17 : 75–86. 8234246

20. Engen JR (2009) Analysis of protein conformation and dynamics by hydrogen/deuterium exchange MS. Anal Chem 81 : 7870–7875. doi: 10.1021/ac901154s 19788312

21. Riek R, Hornemann S, Wider G, Billeter M, Glockshuber R, et al. (1996) NMR structure of the mouse prion protein domain PrP(121–321). Nature 382 : 180–182. 8700211

22. Siamwiza MN, Lord RC, Chen MC, Takamatsu T, Harada I, et al. (1975) Interpretation of the doublet at 850 and 830 cm-1 in the Raman spectra of tyrosyl residues in proteins and certain model compounds. Biochemistry 14 : 4870–4876. 241390

23. Edwards HG, Hunt DE, Sibley MG (1998) FT-Raman spectroscopic study of keratotic materials: horn, hoof and tortoiseshell. Spectrochim Acta A Mol Biomol Spectrosc 54A: 745–757. 9679318

24. Günzler H, Gremlich H-U (2002) IR spectroscopy: an introduction. Weinheim: Wiley-VCH. xiii, 361 p. p.

25. Caughey B, Raymond GJ, Bessen RA (1998) Strain-dependent differences in beta-sheet conformations of abnormal prion protein. J Biol Chem 273 : 32230–32235. 9822701

26. Caughey BW, Dong A, Bhat KS, Ernst D, Hayes SF, et al. (1991) Secondary structure analysis of the scrapie-associated protein PrP 27–30 in water by infrared spectroscopy. Biochemistry 30 : 7672–7680. 1678278

27. 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. doi: 10.1038/nsmb.2035 21441913

28. Lu X, Wintrode PL, Surewicz WK (2007) Beta-sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange. Proc Natl Acad Sci U S A 104 : 1510–1515. 17242357

29. Nazabal A, Hornemann S, Aguzzi A, Zenobi R (2009) Hydrogen/deuterium exchange mass spectrometry identifies two highly protected regions in recombinant full-length prion protein amyloid fibrils. J Mass Spectrom 44 : 965–977. doi: 10.1002/jms.1572 19283723

30. Smirnovas V, Kim JI, Lu X, Atarashi R, Caughey B, et al. (2009) Distinct structures of scrapie prion protein (PrPSc)-seeded versus spontaneous recombinant prion protein fibrils revealed by hydrogen/deuterium exchange. J Biol Chem 284 : 24233–24241. doi: 10.1074/jbc.M109.036558 19596861

31. Singh J, Udgaonkar JB (2013) Dissection of conformational conversion events during prion amyloid fibril formation using hydrogen exchange and mass spectrometry. J Mol Biol 425 : 3510–3521. doi: 10.1016/j.jmb.2013.06.009 23811055

32. Miller MB, Wang DW, Wang F, Noble GP, Ma J, et al. (2013) Cofactor Molecules Induce Structural Transformation during Infectious Prion Formation. Structure.

33. Kim HJ, Raphael AR, LaDow ES, McGurk L, Weber RA, et al. (2014) Therapeutic modulation of eIF2alpha phosphorylation rescues TDP-43 toxicity in amyotrophic lateral sclerosis disease models. Nat Genet 46 : 152–160. doi: 10.1038/ng.2853 24336168

34. Cobb NJ, Sonnichsen FD, McHaourab H, Surewicz WK (2007) Molecular architecture of human prion protein amyloid: a parallel, in-register beta-structure. Proc Natl Acad Sci U S A 104 : 18946–18951. 18025469

35. Groveman BR, Dolan MA, Taubner LM, Kraus A, Wickner RB, et al. (2014) Parallel In-register Intermolecular beta-Sheet Architectures for Prion-seeded Prion Protein (PrP) Amyloids. J Biol Chem 289 : 24129–24142. doi: 10.1074/jbc.M114.578344 25028516

36. Paramithiotis E, Pinard M, Lawton T, LaBoissiere S, Leathers VL, et al. (2003) A prion protein epitope selective for the pathologically misfolded conformation. Nat Med 9 : 893–899. 12778138

37. Taguchi Y, Mistica AM, Kitamoto T, Schatzl HM (2013) Critical significance of the region between Helix 1 and 2 for efficient dominant-negative inhibition by conversion-incompetent prion protein. PLoS Pathog 9: e1003466. doi: 10.1371/journal.ppat.1003466 23825952

38. Muramoto T, Scott M, Cohen FE, Prusiner SB (1996) Recombinant scrapie-like prion protein of 106 amino acids is soluble. Proc Natl Acad Sci U S A 93 : 15457–15462. 8986833

39. 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. 10102274

40. Kurt TD, Bett C, Fernandez-Borges N, Joshi-Barr S, Hornemann S, et al. (2014) Prion transmission prevented by modifying the beta2-alpha2 loop structure of host PrPC. J Neurosci 34 : 1022–1027. doi: 10.1523/JNEUROSCI.4636-13.2014 24431459

41. Kurt TD, Jiang L, Bett C, Eisenberg D, Sigurdson CJ (2014) A proposed mechanism for the promotion of prion conversion involving a strictly conserved tyrosine residue in the beta2-alpha2 loop of PrPC. J Biol Chem 289 : 10660–10667. doi: 10.1074/jbc.M114.549030 24596090

42. Sigurdson CJ, Nilsson KP, Hornemann S, Heikenwalder M, Manco G, et al. (2009) De novo generation of a transmissible spongiform encephalopathy by mouse transgenesis. Proc Natl Acad Sci U S A 106 : 304–309. doi: 10.1073/pnas.0810680105 19073920

43. Sigurdson CJ, Nilsson KP, Hornemann S, Manco G, Fernandez-Borges N, et al. (2010) A molecular switch controls interspecies prion disease transmission in mice. J Clin Invest 120 : 2590–2599. doi: 10.1172/JCI42051 20551516

44. Hasnain SS, Murphy LM, Strange RW, Grossmann JG, Clarke AR, et al. (2001) XAFS study of the high-affinity copper-binding site of human PrP(91–231) and its low-resolution structure in solution. J Mol Biol 311 : 467–473. 11493001

45. Jackson GS, Murray I, Hosszu LL, Gibbs N, Waltho JP, et al. (2001) Location and properties of metal-binding sites on the human prion protein. Proc Natl Acad Sci U S A 98 : 8531–8535. 11438695

46. Jones CE, Abdelraheim SR, Brown DR, Viles JH (2004) Preferential Cu2+ coordination by His96 and His111 induces beta-sheet formation in the unstructured amyloidogenic region of the prion protein. J Biol Chem 279 : 32018–32027. 15145944

47. Hetz C, Mollereau B (2014) Disturbance of endoplasmic reticulum proteostasis in neurodegenerative diseases. Nat Rev Neurosci 15 : 233–249. doi: 10.1038/nrn3689 24619348

48. Hornemann S, Schorn C, Wuthrich K (2004) NMR structure of the bovine prion protein isolated from healthy calf brains. EMBO Rep 5 : 1159–1164. 15568016

49. Kim JI, Surewicz K, Gambetti P, Surewicz WK (2009) The role of glycophosphatidylinositol anchor in the amplification of the scrapie isoform of prion protein in vitro. FEBS Lett 583 : 3671–3675. doi: 10.1016/j.febslet.2009.10.049 19854187

50. Nishina KA, Supattapone S (2007) Immunodetection of glycophosphatidylinositol-anchored proteins following treatment with phospholipase C. Anal Biochem 363 : 318–320. 17321480

51. Mitra N, Sinha S, Ramya TN, Surolia A (2006) N-linked oligosaccharides as outfitters for glycoprotein folding, form and function. Trends Biochem Sci 31 : 156–163. 16473013

52. Chen PY, Lin CC, Chang YT, Lin SC, Chan SI (2002) One O-linked sugar can affect the coil-to-beta structural transition of the prion peptide. Proc Natl Acad Sci U S A 99 : 12633–12638. 12235358

53. Stohr J, Elfrink K, Weinmann N, Wille H, Willbold D, et al. (2011) In vitro conversion and seeded fibrillization of posttranslationally modified prion protein. Biol Chem 392 : 415–421. doi: 10.1515/BC.2011.048 21476870

54. Cancellotti E, Mahal SP, Somerville R, Diack A, Brown D, et al. (2013) Post-translational changes to PrP alter transmissible spongiform encephalopathy strain properties. EMBO J 32 : 756–769. doi: 10.1038/emboj.2013.6 23395905

55. 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. 15933194

56. Baron GS, Hughson AG, Raymond GJ, Offerdahl DK, Barton KA, et al. (2011) Effect of glycans and the glycophosphatidylinositol anchor on strain dependent conformations of scrapie prion protein: improved purifications and infrared spectra. Biochemistry 50 : 4479–4490. doi: 10.1021/bi2003907 21539311

57. Bett C, Kurt TD, Lucero M, Trejo M, Rozemuller AJ, et al. (2013) Defining the conformational features of anchorless, poorly neuroinvasive prions. PLoS Pathog 9: e1003280. doi: 10.1371/journal.ppat.1003280 23637596

58. 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. doi: 10.1371/journal.ppat.1000800 20221436

59. 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. doi: 10.1128/JVI.01353-12 22915801

60. Marshall KE, Offerdahl DK, Speare JO, Dorward DW, Hasenkrug A, et al. (2014) Glycosylphosphatidylinositol anchoring directs the assembly of Sup35NM protein into non-fibrillar, membrane-bound aggregates. J Biol Chem 289 : 12245–12263. doi: 10.1074/jbc.M114.556639 24627481

61. Pankiewicz J, Prelli F, Sy MS, Kascsak RJ, Kascsak RB, et al. (2006) Clearance and prevention of prion infection in cell culture by anti-PrP antibodies. Eur J Neurosci 23 : 2635–2647. 16817866

62. Williamson RA, Peretz D, Pinilla C, Ball H, Bastidas RB, et al. (1998) Mapping the prion protein using recombinant antibodies. J Virol 72 : 9413–9418. 9765500

63. 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. 17115708

64. 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. doi: 10.1073/pnas.1204498109 22586108