Cofactor molecules induce structural transformation during infectious prion formation

Structure

Volumn 21, Issue 11, 2013, Pages 2061-2068

  Miller, Michael B ^a,d   Wang, Daphne W ^b   Wang, Fei ^c   Noble, Geoffrey P ^a   Ma, Jiyan ^c   Woods Jr , Virgil L ^b   Li, Sheng ^b   Supattapone, Surachai ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEUTERIUM; PRION PROTEIN; RNA; SOLVENT;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; DEUTERIUM HYDROGEN EXCHANGE; IN VITRO STUDY; MASS SPECTROMETRY; MOLECULE; NONHUMAN; PRION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE;

MAMMALIAN PRION;

AMINO ACID SEQUENCE; ANIMALS; DEUTERIUM EXCHANGE MEASUREMENT; MICE; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLGLYCEROLS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PRPSC PROTEINS; RNA;

EID: 84887349000     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.08.025     Document Type: Article

References (55)

1. R.A. Bessen, and R.F. Marsh Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy J. Virol. 68 1994 7859 7868
2. D.C. Bolton, M.P. McKinley, and S.B. Prusiner Identification of a protein that purifies with the scrapie prion Science 218 1982 1309 1311
3. J. Castilla, P. Saá, C. Hetz, and C. Soto In vitro generation of infectious scrapie prions Cell 121 2005 195 206
4. B.W. Caughey, A. Dong, K.S. Bhat, D. Ernst, S.F. Hayes, and W.S. Caughey Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy Biochemistry 30 1991 7672 7680
5. B. Caughey, G.J. Raymond, and R.A. Bessen Strain-dependent differences in beta-sheet conformations of abnormal prion protein J. Biol. Chem. 273 1998 32230 32235
6. M.J. Chalmers, S.A. Busby, B.D. Pascal, G.M. West, and P.R. Griffin Differential hydrogen/deuterium exchange mass spectrometry analysis of protein-ligand interactions Expert Rev. Proteomics 8 2011 43 59
7. J. Chen, and D. Thirumalai Helices 2 and 3 are the initiation sites in the PrP(C) → PrP(SC) transition Biochemistry 52 2013 310 319
8. F. Clavaguera, H. Akatsu, G. Fraser, R.A. Crowther, S. Frank, J. Hench, A. Probst, D.T. Winkler, J. Reichwald, and M. Staufenbiel Brain homogenates from human tauopathies induce tau inclusions in mouse brain Proc. Natl. Acad. Sci. USA 110 2013 9535 9540
9. D.W. Colby, R. Wain, I.V. Baskakov, G. Legname, C.G. Palmer, H.O. Nguyen, A. Lemus, F.E. Cohen, S.J. DeArmond, and S.B. Prusiner Protease-sensitive synthetic prions PLoS Pathog. 6 2010 e1000736
10. S.Y. Dai, M.J. Chalmers, J. Bruning, K.S. Bramlett, H.E. Osborne, C. Montrose-Rafizadeh, R.J. Barr, Y. Wang, M. Wang, and T.P. Burris Prediction of the tissue-specificity of selective estrogen receptor modulators by using a single biochemical method Proc. Natl. Acad. Sci. USA 105 2008 7171 7176
11. N.R. Deleault, B.T. Harris, J.R. Rees, and S. Supattapone Formation of native prions from minimal components in vitro Proc. Natl. Acad. Sci. USA 104 2007 9741 9746
12. N.R. Deleault, J.R. Piro, D.J. Walsh, F. Wang, J. Ma, J.C. Geoghegan, and S. Supattapone Isolation of phosphatidylethanolamine as a solitary cofactor for prion formation in the absence of nucleic acids Proc. Natl. Acad. Sci. USA 109 2012 8546 8551
13. N.R. Deleault, D.J. Walsh, J.R. Piro, F. Wang, X. Wang, J. Ma, J.R. Rees, and S. Supattapone Cofactor molecules maintain infectious conformation and restrict strain properties in purified prions Proc. Natl. Acad. Sci. USA 109 2012 E1938 E1946
14. M.L. DeMarco, and V. Daggett From conversion to aggregation: protofibril formation of the prion protein Proc. Natl. Acad. Sci. USA 101 2004 2293 2298
15. J.R. Engen Analysis of protein conformation and dynamics by hydrogen/deuterium exchange MS Anal. Chem. 81 2009 7870 7875
16. S.W. Englander Hydrogen exchange and mass spectrometry: a historical perspective J. Am. Soc. Mass Spectrom. 17 2006 1481 1489
17. C. Govaerts, H. Wille, S.B. Prusiner, and F.E. Cohen Evidence for assembly of prions with left-handed beta-helices into trimers Proc. Natl. Acad. Sci. USA 101 2004 8342 8347
18. Y. Hamuro, S.J. Coales, M.R. Southern, J.F. Nemeth-Cawley, D.D. Stranz, and P.R. Griffin Rapid analysis of protein structure and dynamics by hydrogen/deuterium exchange mass spectrometry J. Biomol. Tech. 14 2003 171 182
19. C. Hölscher, H. Delius, and A. Bürkle Overexpression of nonconvertible PrPc delta114-121 in scrapie-infected mouse neuroblastoma cells leads to trans-dominant inhibition of wild-type PrP(Sc) accumulation J. Virol. 72 1998 1153 1159
20. S. Hornemann, C. Schorn, and K. Wüthrich NMR structure of the bovine prion protein isolated from healthy calf brains EMBO Rep. 5 2004 1159 1164
21. L.L. Hosszu, N.J. Baxter, G.S. Jackson, A. Power, A.R. Clarke, J.P. Waltho, C.J. Craven, and J. Collinge Structural mobility of the human prion protein probed by backbone hydrogen exchange Nat. Struct. Biol. 6 1999 740 743
22. J. Kazlauskaite, N. Sanghera, I. Sylvester, C. Vénien-Bryan, and T.J. Pinheiro Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization Biochemistry 42 2003 3295 3304
23. J.I. Kim, I. Cali, K. Surewicz, Q. Kong, G.J. Raymond, R. Atarashi, B. Race, L. Qing, P. Gambetti, B. Caughey, and W.K. Surewicz Mammalian prions generated from bacterially expressed prion protein in the absence of any mammalian cofactors J. Biol. Chem. 285 2010 14083 14087
24. C. Kim, T. Haldiman, Y. Cohen, W. Chen, J. Blevins, M.S. Sy, M. Cohen, and J.G. Safar Protease-sensitive conformers in broad spectrum of distinct PrPSc structures in sporadic Creutzfeldt-Jakob disease are indicator of progression rate PLoS Pathog. 7 2011 e1002242
25. L. Konermann, J. Pan, and Y.H. Liu Hydrogen exchange mass spectrometry for studying protein structure and dynamics Chem. Soc. Rev. 40 2011 1224 1234
26. G. Legname, I.V. Baskakov, H.O. Nguyen, D. Riesner, F.E. Cohen, S.J. DeArmond, and S.B. Prusiner Synthetic mammalian prions Science 305 2004 673 676
27. X. Lu, P.L. Wintrode, and W.K. Surewicz Beta-sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange Proc. Natl. Acad. Sci. USA 104 2007 1510 1515
28. K.C. Luk, V. Kehm, J. Carroll, B. Zhang, P. O'Brien, J.Q. Trojanowski, and V.M. Lee Pathological α-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice Science 338 2012 949 953
29. N. Makarava, and I.V. Baskakov Expression and purification of full-length recombinant PrP of high purity Methods Mol. Biol. 459 2008 131 143
30. N. Makarava, G.G. Kovacs, O. Bocharova, R. Savtchenko, I. Alexeeva, H. Budka, R.G. Rohwer, and I.V. Baskakov Recombinant prion protein induces a new transmissible prion disease in wild-type animals Acta Neuropathol. 119 2010 177 187
31. N. Makarava, G.G. Kovacs, R. Savtchenko, I. Alexeeva, H. Budka, R.G. Rohwer, and I.V. Baskakov Stabilization of a prion strain of synthetic origin requires multiple serial passages J. Biol. Chem. 287 2012 30205 30214
32. M.P. McKinley, R.K. Meyer, L. Kenaga, F. Rahbar, R. Cotter, A. Serban, and S.B. Prusiner Scrapie prion rod formation in vitro requires both detergent extraction and limited proteolysis J. Virol. 65 1991 1340 1351
33. M. Meyer-Luehmann, J. Coomaraswamy, T. Bolmont, S. Kaeser, C. Schaefer, E. Kilger, A. Neuenschwander, D. Abramowski, P. Frey, and A.L. Jaton Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host Science 313 2006 1781 1784
34. M.B. Miller, J.C. Geoghegan, and S. Supattapone Dissociation of infectivity from seeding ability in prions with alternate docking mechanism PLoS Pathog. 7 2011 e1002128
35. R.A. Moore, A.G. Timmes, P.A. Wilmarth, D. Safronetz, and S.A. Priola Identification and removal of proteins that co-purify with infectious prion protein improves the analysis of its secondary structure Proteomics 11 2011 3853 3865
36. A. Nazabal, S. Hornemann, A. Aguzzi, and R. Zenobi Hydrogen/deuterium exchange mass spectrometry identifies two highly protected regions in recombinant full-length prion protein amyloid fibrils J. Mass Spectrom. 44 2009 965 977
37. J.V. Olsen, S.E. Ong, and M. Mann Trypsin cleaves exclusively C-terminal to arginine and lysine residues Mol. Cell. Proteomics 3 2004 608 614
38. K.M. Pan, M. Baldwin, J. Nguyen, M. Gasset, A. Serban, D. Groth, I. Mehlhorn, Z. Huang, R.J. Fletterick, F.E. Cohen, and S.B. Prusiner Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins Proc. Natl. Acad. Sci. USA 90 1993 10962 10966
39. M.A. Pastrana, G. Sajnani, B. Onisko, J. Castilla, R. Morales, C. Soto, and J.R. Requena Isolation and characterization of a proteinase K-sensitive PrPSc fraction Biochemistry 45 2006 15710 15717
40. D. Peretz, R.A. Williamson, Y. Matsunaga, H. Serban, C. Pinilla, R.B. Bastidas, R. Rozenshteyn, T.L. James, R.A. Houghten, and F.E. Cohen A conformational transition at the N terminus of the prion protein features in formation of the scrapie isoform J. Mol. Biol. 273 1997 614 622
41. S.B. Prusiner Prions Proc. Natl. Acad. Sci. USA 95 1998 13363 13383
42. R. Riek, S. Hornemann, G. Wider, M. Billeter, R. Glockshuber, and K. Wüthrich NMR structure of the mouse prion protein domain PrP(121-231) Nature 382 1996 180 182
43. R. Riek, S. Hornemann, G. Wider, R. Glockshuber, and K. Wüthrich NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231) FEBS Lett. 413 1997 282 288
44. P. Saá, G.F. Sferrazza, G. Ottenberg, A.M. Oelschlegel, K. Dorsey, and C.I. Lasmézas Strain-specific role of RNAs in prion replication J. Virol. 86 2012 10494 10504
45. G. Sajnani, C.J. Silva, A. Ramos, M.A. Pastrana, B.C. Onisko, M.L. Erickson, E.M. Antaki, I. Dynin, E. Vázquez-Fernández, and C.J. Sigurdson PK-sensitive PrP is infectious and shares basic structural features with PK-resistant PrP PLoS Pathog. 8 2012 e1002547
46. N. Sanghera, and T.J. Pinheiro Binding of prion protein to lipid membranes and implications for prion conversion J. Mol. Biol. 315 2002 1241 1256
47. R.A. Shikiya, and J.C. Bartz In vitro generation of high-titer prions J. Virol. 85 2011 13439 13442
48. V. Smirnovas, J.I. Kim, X. Lu, R. Atarashi, B. Caughey, and W.K. Surewicz Distinct structures of scrapie prion protein (PrPSc)-seeded versus spontaneous recombinant prion protein fibrils revealed by hydrogen/deuterium exchange J. Biol. Chem. 284 2009 24233 24241
49. V. Smirnovas, G.S. Baron, D.K. Offerdahl, G.J. Raymond, B. Caughey, and W.K. Surewicz Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange Nat. Struct. Mol. Biol. 18 2011 504 506
50. J. Stöhr, J.C. Watts, Z.L. Mensinger, A. Oehler, S.K. Grillo, S.J. DeArmond, S.B. Prusiner, and K. Giles Purified and synthetic Alzheimer's amyloid beta (Aβ) prions Proc. Natl. Acad. Sci. USA 109 2012 11025 11030
51. A.G. Timmes, R.A. Moore, E.R. Fischer, and S.A. Priola Recombinant prion protein refolded with lipid and RNA has the biochemical hallmarks of a prion but lacks in vivo infectivity PLoS One 8 2013 e71081
52. F. Wang, F. Yang, Y. Hu, X. Wang, X. Wang, C. Jin, and J. Ma Lipid interaction converts prion protein to a PrPSc-like proteinase K-resistant conformation under physiological conditions Biochemistry 46 2007 7045 7053
53. F. Wang, X. Wang, C.G. Yuan, and J. Ma Generating a prion with bacterially expressed recombinant prion protein Science 327 2010 1132 1135
54. F. Wang, S. Yin, X. Wang, L. Zha, M.S. Sy, and J. Ma Role of the highly conserved middle region of prion protein (PrP) in PrP-lipid interaction Biochemistry 49 2010 8169 8176
55. H.M. Zhang, S.M. McLoughlin, S.D. Frausto, H. Tang, M.R. Emmett, and A.G. Marshall Simultaneous reduction and digestion of proteins with disulfide bonds for hydrogen/deuterium exchange monitored by mass spectrometry Anal. Chem. 82 2010 1450 1454