Genesis of Mammalian Prions: From Non-infectious Amyloid Fibrils to a Transmissible Prion Disease
The transmissible agent of prion disease consists of a prion protein in its abnormal, β-sheet rich state (PrPSc), which is capable of replicating itself according to the template-assisted mechanism. This mechanism postulates that the folding pattern of a newly recruited polypeptide chain accurately reproduces that of a PrPSc template. Here we report that authentic PrPSc and transmissible prion disease can be generated de novo in wild type animals by recombinant PrP (rPrP) amyloid fibrils, which are structurally different from PrPSc and lack any detectable PrPSc particles. When induced by rPrP fibrils, a long silent stage that involved two serial passages preceded development of the clinical disease. Once emerged, the prion disease was characterized by unique clinical, neuropathological, and biochemical features. The long silent stage to the disease was accompanied by significant transformation in neuropathological properties and biochemical features of the proteinase K-resistant PrP material (PrPres) before authentic PrPSc evolved. The current work illustrates that transmissible prion diseases can be induced by PrP structures different from that of authentic PrPSc and suggests that a new mechanism different from the classical templating exists. This new mechanism designated as “deformed templating” postulates that a change in the PrP folding pattern from the one present in rPrP fibrils to an alternative specific for PrPSc can occur. The current work provides important new insight into the mechanisms underlying genesis of the transmissible protein states and has numerous implications for understanding the etiology of neurodegenerative diseases.
Vyšlo v časopise:
Genesis of Mammalian Prions: From Non-infectious Amyloid Fibrils to a Transmissible Prion Disease. PLoS Pathog 7(12): e32767. doi:10.1371/journal.ppat.1002419
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002419
Souhrn
The transmissible agent of prion disease consists of a prion protein in its abnormal, β-sheet rich state (PrPSc), which is capable of replicating itself according to the template-assisted mechanism. This mechanism postulates that the folding pattern of a newly recruited polypeptide chain accurately reproduces that of a PrPSc template. Here we report that authentic PrPSc and transmissible prion disease can be generated de novo in wild type animals by recombinant PrP (rPrP) amyloid fibrils, which are structurally different from PrPSc and lack any detectable PrPSc particles. When induced by rPrP fibrils, a long silent stage that involved two serial passages preceded development of the clinical disease. Once emerged, the prion disease was characterized by unique clinical, neuropathological, and biochemical features. The long silent stage to the disease was accompanied by significant transformation in neuropathological properties and biochemical features of the proteinase K-resistant PrP material (PrPres) before authentic PrPSc evolved. The current work illustrates that transmissible prion diseases can be induced by PrP structures different from that of authentic PrPSc and suggests that a new mechanism different from the classical templating exists. This new mechanism designated as “deformed templating” postulates that a change in the PrP folding pattern from the one present in rPrP fibrils to an alternative specific for PrPSc can occur. The current work provides important new insight into the mechanisms underlying genesis of the transmissible protein states and has numerous implications for understanding the etiology of neurodegenerative diseases.
Zdroje
1. PrusinerSB 1996 Prion diseases. NathansonNAhmedRGonzalez-ScaranoFGriffinDHolmesK Viral Pathogenesis New York Raven Press 855 911
2. PrusinerSB 1982 Novel proteinaceous infectious particles cause scrapie. Science 216 136 144
3. GriffithJS 1967 Self-replication and scrapie. Nature 215 1043 1044
4. LegnameGBaskakovIVNguyenH-OBRiesnerDCohenFE 2004 Synthetic mammalian prions. Science 305 673 676
5. ColbyDWGilesKLegnameGWilleHBaskakovIV 2009 Design and construction of diverse mammalian prion strains. Proc Acad Natl Sci U S A 106 20417 20422
6. MakaravaNKovacsGGBocharovaOVSavtchenkoRAlexeevaI 2010 Recombinant prion protein induces a new transmissible prion disease in wild type animals. Acta Neuropathol 119 177 187
7. ColbyDWWainRBaskakovIVLegnameGPAlmerCG 2010 Protease-sensitive synthetic prions. PLoS Pathog 6 e1000736
8. BarriaMAMukherjeeAGonzalez-RomeroDMoralesRSotoC 2009 De Novo Generation of Infectious Prions In Vitro Produces a New Disease Phenotype. PLOS Pathog 5 e1000421
9. DeleaultNRHarrisBTReesJRSupattaponeS 2007 Formation of native prions from minimal components in vitro. Proc Acad Natl Sci U S A 104 9741 9746
10. WangFWangXYuanC-GMaJ 2010 Generating a Prion Bacterially Expressed Recombinant Prion Protein. Science 327 1132 1135
11. CaugheyBBaronGSChesebroBJeffreyM 2009 Getting a grip on prions: oligomers, amyloids, and pathological membrane interactions. Annu Rev Biochem 78 177 204
12. CaugheyBBaronGS 2006 Prions and their partners in crime. Nature 443 803 810
13. SotoC 2011 Prion hypothesis: the end of the controversy? Trends Biochem Sci 36 151 158
14. WilleHBianWMcDonaldMKendallAColbyDW 2009 Natural and synthetic prion structure from X-ray fiber diffraction. Proc Acad Natl Sci U S A 106 16990 16995
15. WilleHZhangG-FBaldwinMACohenFEPrusinerSB 1996 Separation of scrapie prion infectivity from PrP amyloid polymers. J Mol Biol 259 608 621
16. PiroJRWangFWalshDJReesJRMaJ 2011 Seeding Specificity and Ultrastructural Characteristics of Infectious Recombinant Prions. Biochemistry 50 7111 7116
17. OstapchenkoVGSawayaMRMakaravaNSavtchenkoRNilssonKP 2010 Two amyloid states of the prion protein display significantly different folding patterns. J Mol Biol 400 908 921
18. BocharovaOVMakaravaNBreydoLAndersonMSalnikovVV 2006 Annealing PrP amyloid firbils at high temperature results in extension of a proteinase K resistant core. J Biol Chem 281 2373 2379
19. Gonzalez-MontalbanNMakaravaNOstapchenkoVGSavtchenkoRAlexeevaI 2011 Highly Efficient Protein Misfolding Cyclic Amplification. PLoS Pathog 7 e1001277
20. KovacsGGPreusserMStrohschneiderMBudkaH 2005 Subcellular Localization of Disease-Associated Prion Protein in the Human Brain. Am J Pathol 166 287 294
21. PeretzDScottMGrothDWilliamsonABurtonD 2001 Strain-specified relative conformational stability of the scrapie prion protein. Protein Sci 10 854 863
22. DeleaultNRLucassenRWSupattaponeS 2003 RNA molecules stimulate prion protein conversion. Nature 425 717 720
23. DeleaultNRKascsakRGeogheganJCSupattaponeS 2010 Species-dependent differences in cofactor utilization for formation of the protease-resistant prion protein in vitro. Biochemistry 49 3928 3934
24. SaaPCastillaJSotoC 2006 Ultra-efficient Replication of Infectious Prions by Automated Protein Misfolding Cyclic Amplification. J Biol Chem 281 35245 35252
25. BocharovaOVBreydoLSalnikovVVGillACBaskakovIV 2005 Synthetic prions generated in vitro are similar to a newly identified subpopulation of PrPSc from sporadic Creutzfeldt-Jakob Disease PrPSc . Prot Science 14 1222 1232
26. SpassovSBeekesMNaumannD 2006 Structural differences between TSEs strains investigated by FT-IR spectroscopy. Biochim Biophys Acta 1760 1138 1149
27. MakaravaNBaskakovIV 2008 The same primary structure of the prion protein yields two distinct self-propagating states. J Biol Chem 283 15988 15996
28. SunYBreydoLMakaravaNYangQBocharovaOV 2007 Site-specific conformational studies of PrP amyloid fibrils revealed two cooperative folding domain within amyloid structure. J Biol Chem 282 9090 9097
29. LegnameGNguyenH-OBBaskakovIVCohenFEDeArmondSJ 2005 Strain-specified characteristics of mouse synthetic prions. Proc Natl Aca Sci U S A 102 2168 2173
30. KimuraKKuboMYokoyamaT 2000 Characteristics of prion protein (PrP(Sc)) in the brains of hamsters inoculated serially with a mouse-passaged scrapie strain. J Comp Pathol 122 123 130
31. MakaravaNOstapchenkoVGSavtchenkoRBaskakovIV 2009 Conformational switching within individual amyloid fibrils. J Biol Chem 284 14386 14395
32. BaskakovIV 2009 Switching in amyloid structure within individual fibrils: implication for strain adaptation, species barrier and strain classification. FEBS Lett 583 2618 2622
33. ColbyDWZhangQWangSGrothDLegnameG 2007 Prion detection by an amyloid seeding assay. Proc Acad Natl Sci U S A 104 20914 20919
34. AtarashiRMooreRASimVLHughsonAGDorwardDW 2007 Ultrasensitive detection of scrapie prion protein using seeded conversion of recombinant prion protein. Nature Methods 4 645 650
35. KimJICaliISurewiczKKongQRaymondGJ 2010 Mammalian prions generated from bacterially expressed prion protein in the absence of any mammalian cofactors. J Biol Chem 285 14083 14087
36. HillAFJoinerSLinehanJDesbruslaisMLantosPL 2000 Species-barrier-independent prion replication in apparently resistant species. Proc Natl Acad Sci U S A 97 10248 10253
37. RaceRRainseARaymondGCaugheyBChesebroB 2001 Long-Term Subclinical Carrier State Preceedes Scrapie Replication and Adaptation in a Resistant Species: Analogies to Bovine Spongiform Encephalopathy and Varian Creutzfeldt-Jakob Disease in Humans. J Virol 2001 10106 10112
38. WilleHMcDonaldMBianWKendallABorovinskiyA 2008 X-ray fiber diffraction reveals major structural differences between brain-derived prions and recombinant prion protein amyloid. Abstracts, International Conference "Prion-2008"; 8-10 October 2008; Madrid, Spain
39. LasmézasCIDeslysJ-PRobainOJaeglyABeringueV 1997 Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein. Science 275 402 405
40. BarronRMCampbellSLKingDBellonAChapmanKE 2007 High titer of transmissible spongiform encephalopathy infectivity associated with extremely low levels of PrPSc in vitro. J Biol Chem 35878 35886
41. SandbergMKAl-DoujailyHSharpsBClarkeARCollingeJ 2011 Prion propagation and toxicity in vitro occur in two distinct mechanistic phases. Nature 470 540 542
42. ComoyEECasaloneCLescoutra-EtchegarayNZanussoGFreireS 2008 Atypical BSE (BASE) transmitted from asymptomatic aging cattle to a primate. Plos ONE 3 e3017
43. PedenAHHeadMWRitchieDLBellJEIronsideJW 2004 Preclinical vCJD after blood transfusion in a PRNP codon 129 heterozygous patient. Lancet 364 527 529
44. ZouWQCapellariSParchiPSyMSGambettiP 2003 Identification of Novel Proteinase K-resistant C-terminal Fragments of PrP in Creutzfeldt-Jakob Disease. J Biol Chem 278 40429 40436
45. MillerG 2009 Could they all be prion diseases? Science 326 1337 1339
46. FrostBDiamondMI 2010 Prion-like mechanisms on neurodegenerative diseases. Nat Rev Neuroscience 11 155 159
47. AguzziARajendranL 2009 The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64 783 790
48. EiseleYSObermullerUHeilbronnerGBaumannFKaeserSA 2010 Peripherally applied Abeta-containing inoculates induce cerebral beta-amyloidosis. Science 330 980 982
49. JeanLThomasBTahiri-AlaouiAShawMVauxDJ 2007 Heterologous amyloid seeding: revisiting the role of acetylcholinesterase in Alzheimer' disease. Plos ONE 2 e652
50. YanJFuXGeFZhangBYaoJ 2007 Cross-seeding and cross-competition in mouse apolipoprotein A-II amyloid fibrils and protein A amyloid fibrils. Am J Pathol 171 172 180
51. MoralesREstradaLDDiaz-EspinozaRMorales-ScheihingDJaraMC 2010 Molecular cross talk between misfolded proteins in animal models of Alzheimer's and prion diseases. J Neurosci 30 4528 4535
52. DerkatchILBradleyMEZhouPChernoffYOLiebmanSW 1997 Genetic and environmental factors affecting the de novo appearance of the [PSI+] prion in Saccharomyces cerevisiae. Genetics 147 507 519
53. DerkatchILBradleyMEHongJYLiebmanSW 2001 Prions affect the appearance of other prions: the story of [PIN(+)]. Cell 106 171 182
54. DerkatchILUptainSMQuteiroTFKrishnanRLindquistSL 2004 Effects of Q/N-rich, polyQ, and non-polyQ, amyloids on the de novo formation of the [PSI+] prion in yeast and aggregation of Sup35 in vitro. Proc Acad Natl Sci U S A 101 12934 12939
55. HaikSPrivatNAdjouKTSazdovitchVDormontD 2002 Alpha-synuclein-immunoreactive deposits in human and animal prion diseases. Acta Neuropath (Berlin) 103 516 520
56. AdjouKTAllixSOuidjaMOBackerSCouquetC 2007 Alpha-synuclein accumulates in the brain of scrapie-affected sheep and goats. J Comp Pathol 137 78 81
57. TakahashiMHoshiiYKawanoHGondoTIshiharaT 1996 Ulstrastructural evidence for collocalization of kappa light chain- and beta 2-microglobulin -derived amyloid using double labelling immunogold electron microscopy. Virchows Arch 429 383 388
58. MiyazonoMKitamotoTDoh-uraKIwakiTTateishiJ 1992 Creutzfeldt-Jakob disease with codon 129 polymorphism (Valine): a comparative study of patients with codon 102 point mutation or without mutations. Acta Neuropathol 84 349 354
59. GaluskeRADrachLMNichtweissMMarquardtGFranzK 2004 Colocalization of different types of amyloid in the walls of cerebral blood vessels of patients from cerebral amyloid angiopathy and spontaneous intracranial hemorrhage: a report of 5 cases. Clin Neuropathol 23 113 119
60. BocharovaOVBreydoLParfenovASSalnikovVVBaskakovIV 2005 In vitro conversion of full length mammalian prion protein produces amyloid form with physical property of PrPSc. J Mol Biol 346 645 659
61. DeleaultAMDeleaultNRHarrisBTReesJRSupattaponeS 2008 The effects of prion protein proteolysis and disaggregation on the strain properties of hamster scrapie. J Gen Virol 89 2642 2650
62. CastillaJSaaPHetzCSotoC 2005 In vitro generation of infectious scrapie prions. Cell 121 195 206
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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