Development of a new largely scalable in vitro prion propagation method for the production of infectious recombinant prions for high resolution structural studies
Autoři:
Hasier Eraña aff001; Jorge M. Charco aff001; Michele A. Di Bari aff003; Carlos M. Díaz-Domínguez aff001; Rafael López-Moreno aff001; Enric Vidal aff004; Ezequiel González-Miranda aff001; Miguel A. Pérez-Castro aff001; Sandra García-Martínez aff001; Susana Bravo aff005; Natalia Fernández-Borges aff001; Mariví Geijo aff006; Claudia D’Agostino aff003; Joseba Garrido aff006; Jifeng Bian aff007; Anna König aff008; Boran Uluca-Yazgi aff008; Raimon Sabate aff010; Vadim Khaychuk aff007; Ilaria Vanni aff003; Glenn C. Telling aff007; Henrike Heise aff008; Romolo Nonno aff003; Jesús R. Requena aff012; Joaquín Castilla aff001
Působiště autorů:
CIC bioGUNE, Derio (Bizkaia), Spain
aff001; ATLAS Molecular Pharma S. L. Derio (Bizkaia), Spain
aff002; Department of Veterinary Public Health and Food Safety, Istituto Superiore di Sanità, Rome, Italy
aff003; Centre de Recerca en Sanitat Animal (CReSA), UAB-IRTA, Barcelona, Spain
aff004; Proteomics Lab, IDIS, Santiago de Compostela, Spain
aff005; Animal Health Department, NEIKER-Instituto Vasco de Investigación y Desarrollo Agrario, Derio (Bizkaia), Spain
aff006; Prion Research Center (PRC), Colorado State University, Fort Collins, Colorado, United States of America
aff007; Institute of Complex Systems (ICS-6) and Jülich Center for Structural Biology (JuStruct), Forschungszentrum Jülich, Jülich, Germany
aff008; Physikalische Biologie, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany
aff009; Department of Pharmacy and Pharmaceutical Technology and Physical-Chemistry, Faculty of Pharmacy and Food Sciences, University of Barcelona, Spain
aff010; Institute of Nanoscience and Nanotechnology (IN2UB), University of Barcelona, Spain
aff011; CIMUS Biomedical Research Institute, University of Santiago de Compostela-IDIS, Spain
aff012; IKERBasque, Basque Foundation for Science, Bilbao (Bizkaia), Spain
aff013
Vyšlo v časopise:
Development of a new largely scalable in vitro prion propagation method for the production of infectious recombinant prions for high resolution structural studies. PLoS Pathog 15(10): e32767. doi:10.1371/journal.ppat.1008117
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.ppat.1008117
Souhrn
The resolution of the three-dimensional structure of infectious prions at the atomic level is pivotal to understand the pathobiology of Transmissible Spongiform Encephalopathies (TSE), but has been long hindered due to certain particularities of these proteinaceous pathogens. Difficulties related to their purification from brain homogenates of disease-affected animals were resolved almost a decade ago by the development of in vitro recombinant prion propagation systems giving rise to highly infectious recombinant prions. However, lack of knowledge about the molecular mechanisms of the misfolding event and the complexity of systems such as the Protein Misfolding Cyclic Amplification (PMCA), have limited generating the large amounts of homogeneous recombinant prion preparations required for high-resolution techniques such as solid state Nuclear Magnetic Resonance (ssNMR) imaging. Herein, we present a novel recombinant prion propagation system based on PMCA that substitutes sonication with shaking thereby allowing the production of unprecedented amounts of multi-labeled, infectious recombinant prions. The use of specific cofactors, such as dextran sulfate, limit the structural heterogeneity of the in vitro propagated prions and makes possible, for the first time, the generation of infectious and likely homogeneous samples in sufficient quantities for studies with high-resolution structural techniques as demonstrated by the preliminary ssNMR spectrum presented here. Overall, we consider that this new method named Protein Misfolding Shaking Amplification (PMSA), opens new avenues to finally elucidate the three-dimensional structure of infectious prions.
Klíčová slova:
Mouse models – Prion diseases – Proteases – Recombinant proteins – Sulfates – Voles – Dextran – Electrophoretic staining
Zdroje
1. Legname G, Baskakov IV, Nguyen HO, Riesner D, Cohen FE, DeArmond SJ, et al. Synthetic mammalian prions. Science. 2004;305(5684):673–6. Epub 2004/08/03. doi: 10.1126/science.1100195 305/5684/673 [pii]. 15286374.
2. Bocharova OV, Breydo L, Salnikov VV, Gill AC, Baskakov IV. Synthetic prions generated in vitro are similar to a newly identified subpopulation of PrPSc from sporadic Creutzfeldt-Jakob Disease. Protein Sci. 2005;14(5):1222–32. Epub 2005/04/02. ps.041186605 [pii] doi: 10.1110/ps.041186605 15802644; PubMed Central PMCID: PMC2253268.
3. Legname G, Nguyen HO, Baskakov IV, Cohen FE, Dearmond SJ, Prusiner SB. Strain-specified characteristics of mouse synthetic prions. Proc Natl Acad Sci U S A. 2005;102(6):2168–73. Epub 2005/01/27. 0409079102 [pii] doi: 10.1073/pnas.0409079102 15671162; PubMed Central PMCID: PMC548557.
4. Deleault NR, Harris BT, Rees JR, Supattapone S. Formation of native prions from minimal components in vitro. Proc Natl Acad Sci U S A. 2007;104(23):9741–6. Epub 2007/05/31. 0702662104 [pii] doi: 10.1073/pnas.0702662104 17535913; PubMed Central PMCID: PMC1887554.
5. Makarava N, Kovacs GG, Bocharova O, Savtchenko R, Alexeeva I, Budka H, et al. Recombinant prion protein induces a new transmissible prion disease in wild-type animals. Acta Neuropathol. 2010;119(2):177–87. Epub 2010/01/07. doi: 10.1007/s00401-009-0633-x 20052481; PubMed Central PMCID: PMC2808531.
6. Kim JI, Cali I, Surewicz K, Kong Q, Raymond GJ, Atarashi R, et al. Mammalian prions generated from bacterially expressed prion protein in the absence of any mammalian cofactors. J Biol Chem. 2010;285(19):14083–7. Epub 2010/03/23. C110.113464 [pii] doi: 10.1074/jbc.C110.113464 20304915; PubMed Central PMCID: PMC2863186.
7. Colby DW, Wain R, Baskakov IV, Legname G, Palmer CG, Nguyen HO, et al. Protease-sensitive synthetic prions. PLoS Pathog. 6(1):e1000736. Epub 2010/01/29. doi: 10.1371/journal.ppat.1000736 20107515; PubMed Central PMCID: PMC2809756.
8. Wang F, Wang X, Yuan CG, Ma J. Generating a prion with bacterially expressed recombinant prion protein. Science. 2010;327(5969):1132–5. Epub 2010/01/30. science.1183748 [pii] doi: 10.1126/science.1183748 20110469; PubMed Central PMCID: PMC2893558.
9. Elezgarai SR, Fernández-Borges N, Erana H, Sevillano A, Moreno J, Harrathi C, et al. Generation of a new infectious recombinant prion: a model to understand Gerstmann–Sträussler–Scheinker syndrome. Sci Rep. 2017. doi: 10.1038/s41598-017-09489-3 28851967
10. Fernández-Borges N, Di Bari MA, Erana H, Sanchez-Martin M, Pirisinu L, Parra B, et al. Cofactors influence the biological properties of infectious recombinant prions. Acta Neuropathol. 2017. doi: 10.1007/s00401-017-1782-y 29094186.
11. Charco JM, Erana H, Venegas V, Garcia-Martinez S, Lopez-Moreno R, Gonzalez-Miranda E, et al. Recombinant PrP and Its Contribution to Research on Transmissible Spongiform Encephalopathies. Pathogens. 2017;6(4). doi: 10.3390/pathogens6040067 29240682; PubMed Central PMCID: PMC5750591.
12. Wang F, Wang X, Orru CD, Groveman BR, Surewicz K, Abskharon R, et al. Self-propagating, protease-resistant, recombinant prion protein conformers with or without in vivo pathogenicity. PLoS Pathog. 2017;13(7):e1006491. doi: 10.1371/journal.ppat.1006491 28704563; PubMed Central PMCID: PMC5524416.
13. Zhang Y, Wang F, Wang X, Zhang Z, Xu Y, Yu G, et al. Comparison of 2 synthetically generated recombinant prions. Prion. 2014;8(2):215–20. doi: 10.4161/pri.28669 24721728
14. Deleault NR, Piro JR, Walsh DJ, Wang F, Ma J, Geoghegan JC, et al. Isolation of phosphatidylethanolamine as a solitary cofactor for prion formation in the absence of nucleic acids. Proc Natl Acad Sci U S A. 2012;109(22):8546–51. Epub 2012/05/16. doi: 10.1073/pnas.1204498109 22586108; PubMed Central PMCID: PMC3365173.
15. Deleault NR, Walsh DJ, Piro JR, Wang F, Wang X, Ma J, et al. Cofactor molecules maintain infectious conformation and restrict strain properties in purified prions. Proc Natl Acad Sci U S A. 2012;109(28):E1938–46. Epub 2012/06/20. doi: 10.1073/pnas.1206999109 22711839; PubMed Central PMCID: PMC3396481.
16. Watts JC, Giles K, Stohr J, Oehler A, Bhardwaj S, Grillo SK, et al. Spontaneous generation of rapidly transmissible prions in transgenic mice expressing wild-type bank vole prion protein. Proc Natl Acad Sci U S A. 2012;109(9):3498–503. Epub 2012/02/15. doi: 10.1073/pnas.1121556109 22331873; PubMed Central PMCID: PMC3295307.
17. Watts JC, Giles K, Patel S, Oehler A, DeArmond SJ, Prusiner SB. Evidence that bank vole PrP is a universal acceptor for prions. PLoS Pathog. 2014;10(4):e1003990. doi: 10.1371/journal.ppat.1003990 24699458; PubMed Central PMCID: PMC3974871.
18. Di Bari MA, Nonno R, Castilla J, D'Agostino C, Pirisinu L, Riccardi G, et al. Chronic wasting disease in bank voles: characterisation of the shortest incubation time model for prion diseases. PLoS Pathog. 2013;9(3):e1003219. Epub 2013/03/19. doi: 10.1371/journal.ppat.1003219 23505374; PubMed Central PMCID: PMC3591354.
19. Deleault NR, Kascsak R, Geoghegan JC, Supattapone S. Species-dependent differences in cofactor utilization for formation of the protease-resistant prion protein in vitro. Biochemistry. 2010;49(18):3928–34. Epub 2010/04/10. doi: 10.1021/bi100370b 20377181; PubMed Central PMCID: PMC3021175.
20. Lawson VA, Lumicisi B, Welton J, Machalek D, Gouramanis K, Klemm HM, et al. Glycosaminoglycan sulphation affects the seeded misfolding of a mutant prion protein. PLoS One. 2010;5(8):e12351. Epub 2010/09/03. doi: 10.1371/journal.pone.0012351 20808809; PubMed Central PMCID: PMC2925953.
21. Supattapone S. Synthesis of high titer infectious prions with cofactor molecules. J Biol Chem. 2014;289(29):19850–4. doi: 10.1074/jbc.R113.511329 24860097; PubMed Central PMCID: PMC4106305.
22. Bruce ME. TSE strain variation. Br Med Bull. 2003;66:99–108. Epub 2003/10/03. doi: 10.1093/bmb/66.1.99 14522852.
23. Weissmann C, Li J, Mahal SP, Browning S. Prions on the move. EMBO Rep. 2011;12(11):1109–17. Epub 2011/10/15. doi: 10.1038/embor.2011.192 21997298; PubMed Central PMCID: PMC3207107.
24. Collinge J. Medicine. Prion strain mutation and selection. Science. 2010;328(5982):1111–2. Epub 2010/05/29. doi: 10.1126/science.1190815 20508117.
25. Erana H, Castilla J. The architecture of prions: how understanding would provide new therapeutic insights. Swiss Med Wkly. 2016;146:w14354. doi: 10.4414/smw.2016.14354 27684312.
26. Lu X, Wintrode PL, Surewicz WK. Beta-sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange. Proc Natl Acad Sci U S A. 2007;104(5):1510–5. Epub 2007/01/24. 0608447104 [pii] doi: 10.1073/pnas.0608447104 17242357; PubMed Central PMCID: PMC1785245.
27. Nazabal A, Hornemann S, Aguzzi A, Zenobi R. Hydrogen/deuterium exchange mass spectrometry identifies two highly protected regions in recombinant full-length prion protein amyloid fibrils. J Mass Spectrom. 2009;44(6):965–77. Epub 2009/03/14. doi: 10.1002/jms.1572 19283723.
28. Smirnovas V, Kim JI, Lu X, Atarashi R, Caughey B, Surewicz WK. Distinct structures of scrapie prion protein (PrPSc)-seeded versus spontaneous recombinant prion protein fibrils revealed by hydrogen/deuterium exchange. J Biol Chem. 2009;284(36):24233–41. Epub 2009/07/15. M109.036558 [pii] doi: 10.1074/jbc.M109.036558 19596861; PubMed Central PMCID: PMC2782017.
29. Eberl H, Tittmann P, Glockshuber R. Characterization of recombinant, membrane-attached full-length prion protein. J Biol Chem. 2004;279(24):25058–65. Epub 2004/03/20. doi: 10.1074/jbc.M400952200 [pii]. 15031284.
30. Sajnani G, Pastrana MA, Dynin I, Onisko B, Requena JR. Scrapie prion protein structural constraints obtained by limited proteolysis and mass spectrometry. J Mol Biol. 2008;382(1):88–98. Epub 2008/07/16. S0022-2836(08)00797-3 [pii] doi: 10.1016/j.jmb.2008.06.070 18621059.
31. Sajnani G, Silva CJ, Ramos A, Pastrana MA, Onisko BC, Erickson ML, et al. PK-sensitive PrP is infectious and shares basic structural features with PK-resistant PrP. PLoS Pathog. 2012;8(3):e1002547. Epub 2012/03/08. doi: 10.1371/journal.ppat.1002547 22396643; PubMed Central PMCID: PMC3291653.
32. Vazquez-Fernandez E, Alonso J, Pastrana MA, Ramos A, Stitz L, Vidal E, et al. Structural organization of mammalian prions as probed by limited proteolysis. PLoS One. 2012;7(11):e50111. Epub 2012/11/28. doi: 10.1371/journal.pone.0050111 23185550; PubMed Central PMCID: PMC3502352.
33. Sevillano AM, Fernandez-Borges N, Younas N, Wang F, S RE, Bravo S, et al. Recombinant PrPSc shares structural features with brain-derived PrPSc: Insights from limited proteolysis. PLoS Pathog. 2018;14(1):e1006797. doi: 10.1371/journal.ppat.1006797 29385212; PubMed Central PMCID: PMC5809102.
34. Vazquez-Fernandez E, Vos MR, Afanasyev P, Cebey L, Sevillano AM, Vidal E, et al. The Structural Architecture of an Infectious Mammalian Prion Using Electron Cryomicroscopy. PLoS Pathog. 2016;12(9):e1005835. doi: 10.1371/journal.ppat.1005835 27606840; PubMed Central PMCID: PMC5015997.
35. Wan W, Wille H, Stohr J, Kendall A, Bian W, McDonald M, et al. Structural studies of truncated forms of the prion protein PrP. Biophys J. 2015;108(6):1548–54. doi: 10.1016/j.bpj.2015.01.008 25809267; PubMed Central PMCID: PMC4375555.
36. Groveman BR, Dolan MA, Taubner LM, Kraus A, Wickner RB, Caughey B. Parallel in-register intermolecular beta-sheet architectures for prion-seeded prion protein (PrP) amyloids. J Biol Chem. 2014;289(35):24129–42. doi: 10.1074/jbc.M114.578344 25028516; PubMed Central PMCID: PMC4148845.
37. Baskakov IV, Caughey B, Requena JR, Sevillano AM, Surewicz WK, Wille H. The prion 2018 round tables (I): the structure of PrP(Sc). Prion. 2019;13(1):46–52. doi: 10.1080/19336896.2019.1569450 30646817.
38. Laws DD, Bitter HM, Liu K, Ball HL, Kaneko K, Wille H, et al. Solid-state NMR studies of the secondary structure of a mutant prion protein fragment of 55 residues that induces neurodegeneration. Proc Natl Acad Sci U S A. 2001;98(20):11686–90. Epub 2001/09/20. doi: 10.1073/pnas.201404298 [pii]. 11562491; PubMed Central PMCID: PMC58790.
39. Siemer AB, Ritter C, Ernst M, Riek R, Meier BH. High-resolution solid-state NMR spectroscopy of the prion protein HET-s in its amyloid conformation. Angew Chem Int Ed Engl. 2005;44(16):2441–4. Epub 2005/03/17. doi: 10.1002/anie.200462952 15770629.
40. Gremer L, Schölzel D, Schenk C, Reinartz E, Labahn J, Ravell RBG, et al. Fibril structure of amyloid-β(1–42) by cryo–electron microscopy. Science. 2017;358(6359):116–9. doi: 10.1126/science.aao2825 28882996
41. Theint T, Nadaud PS, Aucoin D, Helmus JJ, Pondaven SP, Surewicz K, et al. Species-dependent structural polymorphism of Y145Stop prion protein amyloid revealed by solid-state NMR spectroscopy. Nat Commun. 2017;8(1):753. doi: 10.1038/s41467-017-00794-z 28963458; PubMed Central PMCID: PMC5622040.
42. Aucoin D, Xia Y, Theint T, Nadaud PS, Surewicz K, Surewicz WK, et al. Protein-solvent interfaces in human Y145Stop prion protein amyloid fibrils probed by paramagnetic solid-state NMR spectroscopy. J Struct Biol. 2018. doi: 10.1016/j.jsb.2018.04.002 29679649.
43. Ladner-Keay CL, Griffith BJ, Wishart DS. Shaking alone induces de novo conversion of recombinant prion proteins to beta-sheet rich oligomers and fibrils. PLoS One. 2014;9(6):e98753. doi: 10.1371/journal.pone.0098753 24892647; PubMed Central PMCID: PMC4043794.
44. Darros‐Barbosa R, Balaban MO, Teixeira AA. Temperature and Concentration Dependence of Density of Model Liquid Foods. International Journal of Food Properties. 2003;6(2):195–214. doi: 10.1081/jfp-120017815
45. Makarava N, Kovacs GG, Savtchenko R, Alexeeva I, Budka H, Rohwer RG, et al. Genesis of mammalian prions: from non-infectious amyloid fibrils to a transmissible prion disease. PLoS Pathog. 2011;7(12):e1002419. Epub 2011/12/07. doi: 10.1371/journal.ppat.1002419 22144901; PubMed Central PMCID: PMC3228811.
46. Ramakrishnan MA. Determination of 50% endpoint titer using a simple formula. World J Virol. 2016;5(2):85–6. doi: 10.5501/wjv.v5.i2.85 27175354; PubMed Central PMCID: PMC4861875.
47. Andronesi OC, Becker S, Seidel K, Heise H, Young HS, Baldus M. Determination of Membrane Protein Structure and Dynamics by Magic-Angle-Spinning Solid-State NMR Spectroscopy. Journal of the American Chemical Society. 2005;127(37):12965–74. doi: 10.1021/ja0530164 16159291
48. Vazquez-Fernandez E, Young HS, Requena JR, Wille H. The Structure of Mammalian Prions and Their Aggregates. Int Rev Cell Mol Biol. 2017;329:277–301. doi: 10.1016/bs.ircmb.2016.08.013 28109330.
49. Burke C, Walsh D, Steele A, Agrimi U, Di Bari MA, Watts JC, et al. Full restoration of specific infectivity and strain properties from pure mammalian prion protein. PLoS Pathog. 2019;15(3):e1007662. doi: 10.1371/journal.ppat.1007662 30908557.
50. Timmes AG, Moore RA, Fischer ER, Priola SA. Recombinant prion protein refolded with lipid and RNA has the biochemical hallmarks of a prion but lacks in vivo infectivity. PLoS One. 2013;8(7):e71081. doi: 10.1371/journal.pone.0071081 23936256; PubMed Central PMCID: PMC3728029.
51. Fernandez-Borges N, Castilla J. PMCA. A Decade of In Vitro Prion Replication. Current Chemical Biology. 2010;4(3):200–7. doi: 10.2174/187231310792062693
52. Baskakov IV. Autocatalytic conversion of recombinant prion proteins displays a species barrier. J Biol Chem. 2004;279(9):7671–7. Epub 2003/12/12. doi: 10.1074/jbc.M310594200 [pii]. 14668351.
53. Piening N, Weber P, Giese A, Kretzschmar H. Breakage of PrP aggregates is essential for efficient autocatalytic propagation of misfolded prion protein. Biochem Biophys Res Commun. 2005;326(2):339–43. Epub 2004/12/08. S0006-291X(04)02608-7 [pii] doi: 10.1016/j.bbrc.2004.11.039 15582583.
54. Silva CJ, Vazquez-Fernandez E, Onisko B, Requena JR. Proteinase K and the structure of PrPSc: The good, the bad and the ugly. Virus Res. 2015;207:120–6. doi: 10.1016/j.virusres.2015.03.008 25816779.
55. Tixador P, Herzog L, Reine F, Jaumain E, Chapuis J, Le Dur A, et al. The physical relationship between infectivity and prion protein aggregates is strain-dependent. PLoS Pathog. 2010;6(4):e1000859. Epub 2010/04/27. doi: 10.1371/journal.ppat.1000859 20419156; PubMed Central PMCID: PMC2855332.
56. Igel-Egalon A, Bohl J, Moudjou M, Herzog L, Reine F, Rezaei H, et al. Heterogeneity and Architecture of Pathological Prion Protein Assemblies: Time to Revisit the Molecular Basis of the Prion Replication Process? Viruses. 2019;11(5). doi: 10.3390/v11050429 31083283.
57. Igel-Egalon A, Beringue V, Rezaei H, Sibille P. Prion Strains and Transmission Barrier Phenomena. Pathogens. 2018;7(1). doi: 10.3390/pathogens7010005 29301257; PubMed Central PMCID: PMC5874731.
58. Van Melckebeke H, Wasmer C, Lange A, Ab E, Loquet A, Bockmann A, et al. Atomic-resolution three-dimensional structure of HET-s(218–289) amyloid fibrils by solid-state NMR spectroscopy. J Am Chem Soc. 2010;132(39):13765–75. Epub 2010/09/11. doi: 10.1021/ja104213j 20828131.
59. Heise H, Hoyer W, Becker S, Andronesi OC, Riedel D, Baldus M. Molecular-level secondary structure, polymorphism, and dynamics of full-length alpha-synuclein fibrils studied by solid-state NMR. Proc Natl Acad Sci U S A. 2005;102(44):15871–6. doi: 10.1073/pnas.0506109102 16247008; PubMed Central PMCID: PMC1276071.
60. Seuring C, Verasdonck J, Ringler P, Cadalbert R, Stahlberg H, Bockmann A, et al. Amyloid Fibril Polymorphism: Almost Identical on the Atomic Level, Mesoscopically Very Different. J Phys Chem B. 2017;121(8):1783–92. doi: 10.1021/acs.jpcb.6b10624 28075583.
61. Bartz JC, McKenzie DI, Bessen RA, Marsh RF, Aiken JM. Transmissible mink encephalopathy species barrier effect between ferret and mink: PrP gene and protein analysis. J Gen Virol. 1994;75 (Pt 11):2947–53. Epub 1994/11/01. doi: 10.1099/0022-1317-75-11-2947 7964604.
62. Tycko R. Symmetry-based constant-time homonuclear dipolar recoupling in solid state NMR. J Chem Phys. 2007;126(6):064506. doi: 10.1063/1.2437194 17313228.
63. Shewmaker F, Kryndushkin D, Chen B, Tycko R, Wickner RB. Two prion variants of Sup35p have in-register parallel beta-sheet structures, independent of hydration. Biochemistry. 2009;48(23):5074–82. Epub 2009/05/05. doi: 10.1021/bi900345q 19408895; PubMed Central PMCID: PMC2744896.
64. Ohhashi Y, Yamaguchi Y, Kurahashi H, Kamatari YO, Sugiyama S, Uluca B, et al. Molecular basis for diversification of yeast prion strain conformation. Proc Natl Acad Sci U S A. 2018;115(10):2389–94. doi: 10.1073/pnas.1715483115 29467288; PubMed Central PMCID: PMC5877990.
65. Wang X, McGovern G, Zhang Y, Wang F, Zha L, Jeffrey M, et al. Intraperitoneal Infection of Wild-Type Mice with Synthetically Generated Mammalian Prion. PLoS Pathog. 2015;11(7):e1004958. doi: 10.1371/journal.ppat.1004958 26136122; PubMed Central PMCID: PMC4489884.
66. Wang F, Wang X, Abskharon R, Ma J. Prion infectivity is encoded exclusively within the structure of proteinase K-resistant fragments of synthetically generated recombinant PrP(Sc). Acta Neuropathol Commun. 2018;6(1):30. doi: 10.1186/s40478-018-0534-0 29699569; PubMed Central PMCID: PMC5921397.
67. Walsh DJ, Tuttle MD, Burke CM, Zilm KW, Supattapone S, editors. Large-scale production of phospholipid cofactor recombinant prions with high specific infectivity. Prion 2019; 2019 May 2019; Edmonton, Canada: Taylor & Francis Online (Prion).
68. Bessen RA, Marsh RF. Identification of two biologically distinct strains of transmissible mink encephalopathy in hamsters. J Gen Virol. 1992;73 (Pt 2):329–34. Epub 1992/02/01. doi: 10.1099/0022-1317-73-2-329 1531675.
69. Laferriere F, Tixador P, Moudjou M, Chapuis J, Sibille P, Herzog L, et al. Quaternary structure of pathological prion protein as a determining factor of strain-specific prion replication dynamics. PLoS Pathog. 2013;9(10):e1003702. doi: 10.1371/journal.ppat.1003702 24130496; PubMed Central PMCID: PMC3795044.
70. Katorcha E, Makarava N, Savtchenko R, D'Azzo A, Baskakov IV. Sialylation of prion protein controls the rate of prion amplification, the cross-species barrier, the ratio of PrPSc glycoform and prion infectivity. PLoS Pathog. 2014;10(9):e1004366. doi: 10.1371/journal.ppat.1004366 25211026; PubMed Central PMCID: PMC4161476.
71. Fernandez-Borges N, Erana H, Elezgarai SR, Harrathi C, Venegas V, Castilla J. A Quick Method to Evaluate the Effect of the Amino Acid Sequence in the Misfolding Proneness of the Prion Protein. Methods Mol Biol. 2017;1658:205–16. doi: 10.1007/978-1-4939-7244-9_15 28861792.
72. Erana H, Fernandez-Borges N, Elezgarai SR, Harrathi C, Charco JM, Chianini F, et al. In Vitro Approach To Identify Key Amino Acids in Low Susceptibility of Rabbit Prion Protein to Misfolding. J Virol. 2017;91(24). doi: 10.1128/JVI.01543-17 28978705; PubMed Central PMCID: PMC5709604.
73. Otero A, Hedman C, Fernandez-Borges N, Erana H, Marin B, Monzon M, et al. A Single Amino Acid Substitution, Found in Mammals with Low Susceptibility to Prion Diseases, Delays Propagation of Two Prion Strains in Highly Susceptible Transgenic Mouse Models. Mol Neurobiol. 2019. doi: 10.1007/s12035-019-1535-0 30847740.
74. Castilla J, Saa P, Hetz C, Soto C. In vitro generation of infectious scrapie prions. Cell. 2005;121(2):195–206. Epub 2005/04/27. S0092-8674(05)00156-X [pii] doi: 10.1016/j.cell.2005.02.011 15851027.
75. Saa P, Castilla J, Soto C. Ultra-efficient replication of infectious prions by automated protein misfolding cyclic amplification. J Biol Chem. 2006;281(46):35245–52. Epub 2006/09/20. M603964200 [pii] doi: 10.1074/jbc.M603964200 16982620.
76. Saborio GP, Permanne B, Soto C. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature. 2001;411(6839):810–3. Epub 2001/07/19. doi: 10.1038/35081095 11459061.
77. Fernandez-Borges N, de Castro J, Castilla J. In vitro studies of the transmission barrier. Prion. 2009;3(4):220–3. Epub 2009/12/17. 10500 [pii]. doi: 10.4161/pri.3.4.10500 20009509; PubMed Central PMCID: PMC2807695.
78. Harrathi C, Fernandez-Borges N, Erana H, Elezgarai SR, Venegas V, Charco JM, et al. Insights into the Bidirectional Properties of the Sheep-Deer Prion Transmission Barrier. Mol Neurobiol. 2018. doi: 10.1007/s12035-018-1443-8 30592012.
79. Bocharova OV, Breydo L, Parfenov AS, Salnikov VV, Baskakov IV. In vitro conversion of full-length mammalian prion protein produces amyloid form with physical properties of PrP(Sc). J Mol Biol. 2005;346(2):645–59. Epub 2005/01/27. S0022-2836(04)01539-6 [pii] doi: 10.1016/j.jmb.2004.11.068 15670611.
80. Nonno R, Di Bari MA, Cardone F, Vaccari G, Fazzi P, Dell'Omo G, et al. Efficient transmission and characterization of Creutzfeldt-Jakob disease strains in bank voles. PLoS Pathog. 2006;2(2):e12. Epub 2006/03/07. doi: 10.1371/journal.ppat.0020012 16518470; PubMed Central PMCID: PMC1383487.
81. Pirisinu L, Marcon S, Di Bari MA, D'Agostino C, Agrimi U, Nonno R. Biochemical characterization of prion strains in bank voles. Pathogens. 2013;2(3):446–56. doi: 10.3390/pathogens2030446 25437201; PubMed Central PMCID: PMC4235696.
82. Muller H, Brener O, Andreoletti O, Piechatzek T, Willbold D, Legname G, et al. Progress towards structural understanding of infectious sheep PrP-amyloid. Prion. 2014;8(5):344–58. doi: 10.4161/19336896.2014.983754 25482596; PubMed Central PMCID: PMC4601355.
83. Fung BM, Kithrin AK, Ermolaev K. An improved broadband decoupling sequence for liquid crystals and solids. Journal of Magnetic Resonance. 2000;142(1):97–101. doi: 10.1006/jmre.1999.1896 10617439
84. Gonzalez-Montalban N, Makarava N, Ostapchenko VG, Savtchenk R, Alexeeva I, Rohwer RG, et al. Highly efficient protein misfolding cyclic amplification. PLoS Pathog. 2011;7(2):e1001277. Epub 2011/02/25. doi: 10.1371/journal.ppat.1001277 21347353; PubMed Central PMCID: PMC3037363.
85. Johnson CJ, Aiken JM, McKenzie D, Samuel MD, Pedersen JA. Highly efficient amplification of chronic wasting disease agent by protein misfolding cyclic amplification with beads (PMCAb). PLoS One. 2012;7(4):e35383. Epub 2012/04/20. doi: 10.1371/journal.pone.0035383 22514738; PubMed Central PMCID: PMC3325955.
Štítky
Hygiena a epidemiologie Infekční lékařství LaboratořČlánek vyšel v časopise
PLOS Pathogens
2019 Číslo 10
- Perorální antivirotika jako vysoce efektivní nástroj prevence hospitalizací kvůli COVID-19 − otázky a odpovědi pro praxi
- Stillova choroba: vzácné a závažné systémové onemocnění
- Jak souvisí postcovidový syndrom s poškozením mozku?
- Diagnostický algoritmus při podezření na syndrom periodické horečky
- Měli bychom postcovidový syndrom léčit antidepresivy?
Nejčtenější v tomto čísle
- Alterations in cellular expression in EBV infected epithelial cell lines and tumors
- Correction: A specific sequence in the genome of respiratory syncytial virus regulates the generation of copy-back defective viral genomes
- Influenza virus polymerase subunits co-evolve to ensure proper levels of dimerization of the heterotrimer
- Induction of PGRN by influenza virus inhibits the antiviral immune responses through downregulation of type I interferons signaling
Zvyšte si kvalifikaci online z pohodlí domova
Kardiologické projevy hypereozinofilií
nový kurzVšechny kurzy