Introducing a Rigid Loop Structure from Deer into Mouse Prion Protein Increases Its Propensity for Misfolding In Vitro

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Kyle, Leah M ^a   John, Theodore R ^a   Schätzl, Hermann M ^a   Lewis, Randolph V ^b  

^a UNIVERSITY OF WYOMING   (United States)

^b UTAH STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN; PROTEINASE K;

AMINO ACID SUBSTITUTION; ARTICLE; CHRONIC WASTING DISEASE; CIRCULAR DICHROISM; CONTROLLED STUDY; DEER; IN VITRO STUDY; MOLECULAR DYNAMICS; MOOSE; MOUSE; NONHUMAN; PROPENSITY SCORE; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; SURFACE PROPERTY; ULTRACENTRIFUGATION;

AMINO ACID SUBSTITUTION; ANIMALS; CELL-FREE SYSTEM; DEER; ENDOPEPTIDASE K; LIPIDS; MICE; PRIONS; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEOLYSIS; THIAZOLES; WASTING DISEASE, CHRONIC;

CERVIDAE; MAMMALIA; MURINAE;

EID: 84879356527     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066715     Document Type: Article

References (70)

1. Prusiner SB, (1998) Prions. Proceedings of the National Academy of Sciences 95: 13363-13383 doi:10.1073/pnas.95.23.13363.
2. Weissmann C, Li J, Mahal SP, Browning S, (2011) Prions on the move. EMBO Rep 12: 1109-1117.
3. Aguzzi A, Polymenidou M, (2004) Mammalian Prion Biology: One Century of Evolving Concepts. Cell 116: 313-327.
4. Collinge J, (2001) Prion diseases of humans and animals: their causes and molecular basis. Annual review of neuroscience 24: 519-550 doi:10.1146/annurev.neuro.24.1.519.
5. Tatzelt J, Schätzl HM, (2007) Molecular basis of cerebral neurodegeneration in prion diseases. FEBS Journal 274: 606-611 doi:10.1111/j.1742-4658.2007.05633.x.
6. Ma J, (2012) The role of cofactors in prion propagation and infectivity. PLoS pathogens 8: e1002589 doi:10.1371/journal.ppat.1002589.
7. Prusiner SB, (1982) Novel proteinaceous infectious particles cause scrapie. Science (New York, NY) 216: 136-144.
8. Cohen F, Pan K, Huang Z, Baldwin M, Fletterick R, et al. (1994) Structural clues to prion replication. Science 264: 530-531 doi:10.1126/science.7909169.
9. Telling G (2011) Transgenic Mouse Models and Prion Strains. In: Tatzelt J, editor. Prion Proteins SE- 166. Springer Berlin Heidelberg, Vol. 305: 79-99doi:10.1007/128_2011_166.
10. Lasmezas CI, Deslys J-P, Demaimay R, Adjou KT, Lamoury F, et al. (1996) BSE transmission to macaques. Nature 381: 743-744.
11. Priola SA, Vorberg I, (2006) Molecular aspects of disease pathogenesis in the transmissible spongiform encephalopathies. Molecular biotechnology 33: 71-88 doi::10.1385/MB:33:1:71.
12. Angers RC, Browning SR, Seward TS, Sigurdson CJ, Miller MW, et al. (2006) Prions in skeletal muscles of deer with chronic wasting disease. Science (New York, NY) 311: 1117 doi:10.1126/science.1122864.
13. Mathiason CK, Powers JG, Dahmes SJ, Osborn DA, Miller KV, et al. (2006) Infectious prions in the saliva and blood of deer with chronic wasting disease. Science (New York, NY) 314: 133-136 doi:10.1126/science.1132661.
14. Tamgüney G, Giles K, Bouzamondo-Bernstein E, Bosque PJ, Miller MW, et al. (2006) Transmission of elk and deer prions to transgenic mice. Journal of virology 80: 9104-9114 doi:10.1128/JVI.00098-06.
15. Haley NJ, Mathiason CK, Carver S, Zabel M, Telling GC, et al. (2011) Detection of Chronic Wasting Disease Prions in Salivary, Urinary, and Intestinal Tissues of Deer: Potential Mechanisms of Prion Shedding and Transmission. Journal of Virology 85: 6309-6318 doi:10.1128/JVI.00425-11.
16. Tamguney G, Miller MW, Wolfe LL, Sirochman TM, Glidden DV, et al. (2009) Asymptomatic deer excrete infectious prions in faeces. Nature 461: 529-532.
17. Nichols TA, Pulford B, Wyckoff AC, Meyerett C, Michel B, et al. (2009) Detection of protease-resistant cervid prion protein in water from a CWD-endemic area. prion 3: 171-183.
18. Gilch S, Chitoor N, Taguchi Y, Stuart M, Jewell J, et al. (2011) Chronic Wasting Disease. In: Tatzelt J, editor. Prion Proteins SE- 159. Springer Berlin Heidelberg, Vol. 305. pp. 51-77 LA - English.doi:10.1007/128_2011_159.
19. Saunders SE, Bartelt-Hunt SL, Bartz JC, (2012) Occurrence, transmission, and zoonotic potential of chronic wasting disease. Emerging infectious diseases 18: 369-376 doi:10.3201/eid1803.110685.
20. Wopfner F, Weidenhöfer G, Schneider R, Von Brunn A, Gilch S, et al. (1999) Analysis of 27 mammalian and 9 avian PrPs reveals high conservation of flexible regions of the prion protein. Journal of Molecular Biology 289: 1163-1178 doi http://dx.doi.org/10.1006/jmbi.1999.2831.
21. Gossert AD, Bonjour S, Lysek D a, Fiorito F, Wüthrich K, (2005) Prion protein NMR structures of elk and of mouse/elk hybrids. Proceedings of the National Academy of Sciences of the United States of America 102: 646-650 doi:10.1073/pnas.0409008102.
22. Christen B, Hornemann S, Damberger FF, Wüthrich K, (2009) Prion Protein NMR Structure from Tammar Wallaby (Macropus eugenii) Shows that the β2-α2 Loop Is Modulated by Long-Range Sequence Effects. Journal of Molecular Biology 389: 833-845 doi http://dx.doi.org/10.1016/j.jmb.2009.04.040.
23. Vorberg I, Groschup MH, Pfaff E, Priola SA, (2003) Multiple Amino Acid Residues within the Rabbit Prion Protein Inhibit Formation of Its Abnormal Isoform. Journal of Virology 77: 2003-2009 doi:-10.1128/JVI.77.3.2003-2009.2003.
24. Wen Y, Li J, Yao W, Xiong M, Hong J, et al. (2010) Unique structural characteristics of the rabbit prion protein. The Journal of biological chemistry 285: 31682-31693 doi:10.1074/jbc.M110.118844.
25. Khan MQ, Sweeting B, Mulligan VK, Arslan PE, Cashman NR, et al. (2010) Prion disease susceptibility is affected by β-structure folding propensity and local side-chain interactions in PrP. Proceedings of the National Academy of Sciences 107: 19808-19813 doi:10.1073/pnas.1005267107.
26. Pérez DR, Damberger FF, Wüthrich K, (2010) Horse prion protein NMR structure and comparisons with related variants of the mouse prion protein. Journal of molecular biology 400: 121-128 doi:10.1016/j.jmb.2010.04.066.
27. Bett C, Fernández-Borges N, Kurt TD, Lucero M, Nilsson KPR, et al. (2012) Structure of the β2-α2 loop and interspecies prion transmission. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 26: 2868-2876 doi:10.1096/fj.11-200923.
28. Sigurdson CJ, Nilsson KPR, Hornemann S, Heikenwalder M, Manco G, et al. (2009) De novo generation of a transmissible spongiform encephalopathy by mouse transgenesis. Proceedings of the National Academy of Sciences of the United States of America 106: 304-309 doi:10.1073/pnas.0810680105.
29. Sigurdson CJ, Nilsson KPR, Hornemann S, Manco G, Fernández-borges N, et al. (2010) A molecular switch controls interspecies prion disease transmission in mice. Journal of Clinical Investigation 120: 2590-2599 doi:10.1172/JCI42051.2590.
30. Tamgüney G, Giles K, Oehler A, Johnson NL, DeArmond SJ, et al. (2013) Chimeric elk/mouse prion proteins in transgenic mice. Journal of General Virology 94: 443-452 doi:10.1099/vir.0.045989-0.
31. Kurt TD, Telling GC, Zabel MD, Hoover E a, (2009) Trans-species amplification of PrP(CWD) and correlation with rigid loop 170N. Virology 387: 235-243 doi:10.1016/j.virol.2009.02.025.
32. Kirby L, Agarwal S, Graham JF, Goldmann W, Gill AC, (2010) Inverse correlation of thermal lability and conversion efficiency for five prion protein polymorphic variants. Biochemistry 49: 1448-1459 doi:10.1021/bi901855z.
33. Gill AC, Agarwal S, Pinheiro TJT, Graham JF, (2010) Structural requirements for efficient prion protein conversion: cofactors may promote a conversion-competent structure for PrP(C). Prion 4: 235-242 doi:10.4161/pri.4.4.13394.
34. Wilham JM, Orrú CD, Bessen R, Atarashi R, Sano K, et al. (2010) Rapid end-point quantitation of prion seeding activity with sensitivity comparable to bioassays. PLoS pathogens 6: e1001217 doi:10.1371/journal.ppat.1001217.
35. Seelig DM, Mason GL, Telling GC, Hoover EA, (2010) Pathogenesis of chronic wasting disease in cervidized transgenic mice. The American journal of pathology 176: 2785-2797 doi:10.2353/ajpath.2010.090710.
36. Saá P, Castilla J, Soto C, (2006) Ultra-efficient Replication of Infectious Prions by Automated Protein Misfolding Cyclic Amplification. Journal of Biological Chemistry 281: 35245-35252 doi:10.1074/jbc.M603964200.
37. Lührs T, Zahn R, Wüthrich K, (2006) Amyloid formation by recombinant full-length prion proteins in phospholipid bicelle solutions. Journal of molecular biology 357: 833-841 doi:10.1016/j.jmb.2006.01.016.
38. Wang F, Yang F, Hu Y, Wang X, Wang X, et al. (2007) Lipid interaction converts prion protein to a PrPSc-like proteinase K-resistant conformation under physiological conditions. Biochemistry 46: 7045-7053 doi:10.1021/bi700299h.
39. Sanghera N, Pinheiro TJT, (2002) Binding of prion protein to lipid membranes and implications for prion conversion. Journal of molecular biology 315: 1241-1256 doi:10.1006/jmbi.2001.5322.
40. Kazlauskaite J, Sanghera N, (2003) Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization. Biochemistry 42: 3295-3304.
41. 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. Nature methods 4: 645-650 doi:10.1038/nmeth1066.
42. Hornemann S, Korth C, Oesch B, Riek R, Wider G, et al. (1997) Recombinant full-length murine prion protein, mPrP(23-231): purification and spectroscopic characterization. FEBS Letters 413: 277-281 doi:10.1016/S0014-5793(97)00921-6.
43. Gorfe AA, Caflisch A, (2007) Ser170 controls the conformational multiplicity of the loop 166-175 in prion proteins: implication for conversion and species barrier. The FASEB Journal 21: 3279-3287 doi:10.1096/fj.07-8292com.
44. Van der Kamp MW, Daggett V, (2009) The consequences of pathogenic mutations to the human prion protein. Protein engineering, design & selection: PEDS 22: 461-468 doi:10.1093/protein/gzp039.
45. Vanik DL, Surewicz WK, (2002) Disease-associated F198S Mutation Increases the Propensity of the Recombinant Prion Protein for Conformational Conversion to Scrapie-like Form. Journal of Biological Chemistry 277: 49065-49070 doi:10.1074/jbc.M207511200.
46. Hasegawa K, Mohri S, Yokoyama T, (2010) Fragment molecular orbital calculations reveal that the E200K mutation markedly alters local structural stability in the human prion protein. prion 4: 38-44.
47. Liemann S, Glockshuber R, (1999) Influence of amino acid substitutions related to inherited human prion diseases on the thermodynamic stability of the cellular prion protein. Biochemistry 38: 3258-3267 doi:10.1021/bi982714g.
48. Fasano C, Campana V, Zurzolo C, (2006) Protein Only or Something More? Overview of Potential Prion Cofactors. Journal of molecular neuroscience 29: 195-214 doi:10.1385/JMN/29.
49. Hornemann S, Glockshuber R, (1998) A scrapie-like unfolding intermediate of the prion protein domain PrP(121-231) induced by acidic pH. Proceedings of the National Academy of Sciences 95: 6010-6014.
50. Baskakov I, Legname G, (2004) The peculiar nature of unfolding of the human prion protein. Protein Science 13: 586-595 doi:10.1110/ps.03457204.Spontaneous.
51. Morillas M, Swietnicki W, Gambetti P, Surewicz WK, (1999) Membrane Environment Alters the Conformational Structure of the Recombinant Human Prion Protein. Journal of Biological Chemistry 274: 36859-36865 doi:10.1074/jbc.274.52.36859.
52. Surewicz WK, Jones EM, Apetri AC, (2006) The emerging principles of mammalian prion propagation and transmissibility barriers: Insight from studies in vitro. Accounts of chemical research 39: 654-662 doi:10.1021/ar050226c.
53. Apetri A, Maki K, Roder H, Surewicz WK, (2006) Early intermediate in human prion protein folding as evidenced by ultrarapid mixing experiments. Journal of the American 128: 11673-11678 doi:10.1021/ja063880b.Early.
54. Apetri AC, Surewicz WK, (2002) Kinetic Intermediate in the Folding of Human Prion Protein. Journal of Biological Chemistry 277: 44589-44592 doi:10.1074/jbc.C200507200.
55. Swietnicki W, Petersen RB, Gambetti P, Surewicz WK, (1998) Familial Mutations and the Thermodynamic Stability of the Recombinant Human Prion Protein. Journal of Biological Chemistry 273: 31048-31052 doi:10.1074/jbc.273.47.31048.
56. Zhang Y, Swietnicki W, Zagorski MG, Surewicz WK, Sönnichsen FD, (2000) Solution Structure of the E200K Variant of Human Prion Protein: IMPLICATIONS FOR THE MECHANISM OF PATHOGENESIS IN FAMILIAL PRION DISEASES. Journal of Biological Chemistry 275: 33650-33654 doi:10.1074/jbc.C000483200.
57. Apetri AC, Surewicz K, Surewicz WK, (2004) The Effect of Disease-associated Mutations on the Folding Pathway of Human Prion Protein. Journal of Biological Chemistry 279: 18008-18014 doi:10.1074/jbc.M313581200.
58. Riek R, Wider G, Billeter M, Hornemann S, Glockshuber R, et al. (1998) Prion protein NMR structure and familial human spongiform encephalopathies. Proceedings of the National Academy of Sciences 95: 11667-11672 doi:10.1073/pnas.95.20.11667.
59. Paludi D, Thellung S, Chiovitti K, Corsaro A, Villa V, et al. (2007) Different structural stability and toxicity of PrPARR and PrPARQ sheep prion protein variants. Journal of Neurochemistry 103: 2291-2300 doi:10.1111/j.1471-4159.2007.04934.x.
60. Bujdoso R, Burke DF, Thackray AM, (2005) Structural differences between allelic variants of the ovine prion protein revealed by molecular dynamics simulations. Proteins 61: 840-849 doi:10.1002/prot.20755.
61. Fitzmaurice TJ, Burke DF, Hopkins L, Yang S, Yu S, et al. (2008) The stability and aggregation of ovine prion protein associated with classical and atypical scrapie correlates with the ease of unwinding of helix-2. The Biochemical journal 409: 367-375 doi:10.1042/BJ20071122.
62. 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 doi:10.1021/bi100370b.
63. Deleault NNR, Walsh DDJ, Piro JR, Wang F, Wang X, et al. (2012) Cofactor molecules maintain infectious conformation and restrict strain properties in purified prions. Proceedings of the National Academy of Sciences 109: E1938-E1946 doi:10.1073/pnas.1206999109.
64. Supattapone S, (2012) Phosphatidylethanolamine as a prion cofactor. Prion 6: 417-419 doi:10.4161/pri.21826.
65. Deleault NR, Harris BT, Rees JR, Supattapone S, (2007) Formation of native prions from minimal components in vitro. Proceedings of the National Academy of Sciences 104: 9741-9746 doi:10.1073/pnas.0702662104.
66. Wang F, Wang X, Yuan C-G, Ma J, (2010) Generating a prion with bacterially expressed recombinant prion protein. Science. 327: 1132-1135 doi:10.1126/science.1183748.
67. Zhang H, Stockel J, Mehlhorn I, Groth D, Baldwin M, et al. (1997) Physical studies of conformational plasticity in a recombinant prion protein. Biochemistry 36: 3543-3553 doi:10.1021/bi961965r.
68. Kaneko K, Zulianello L, Scott M, Cooper CM, Wallace AC, et al. (1997) Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proceedings of the National Academy of Sciences 94: 10069-10074.
69. Caughey B, Baron G, (2009) Getting a grip on prions: oligomers, amyloids and pathological membrane interactions. Annual review of 78: 177-204 doi:10.1146/annurev.biochem.78.082907.145410.Getting.
70. Zahn R, Liu A, Lührs T, Riek R, Von Schroetter C, et al. (2000) NMR solution structure of the human prion protein. Proceedings of the National Academy of Sciences 97: 145-150 doi:10.1073/pnas.97.1.145.