Evidence That Bank Vole PrP Is a Universal Acceptor for Prions

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Prions are infectious proteins that cause devastating neurodegenerative diseases in both humans and animals. Unlike other rodents, bank voles are highly susceptible to prions from many different species, suggesting that bank voles do not impose a “species barrier,” which normally restricts the transmission of prions from one species to another. We were curious as to whether the unprecedented promiscuity of bank voles for prions is due to the specific prion protein sequence expressed, or to some other factor inherent to bank vole physiology. To answer this question, we inoculated transgenic mice that express bank vole prion protein [Tg(BVPrP) mice] with a diverse set of prions deriving from eight different species. Like bank voles, Tg(BVPrP) mice were highly susceptible to prions from all species tested, demonstrating that the BVPrP sequence mediates the enhanced susceptibility of bank voles to prions. Because the amino acid sequences of mouse and BVPrP differ at only eight positions, our results demonstrate that alterations to a small subset of residues within PrP can have a profound effect on the susceptibility of an organism to prions from another species.

Vyšlo v časopise: Evidence That Bank Vole PrP Is a Universal Acceptor for Prions. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1003990
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003990

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Zdroje

1. WattsJC, BalachandranA, WestawayD (2006) The expanding universe of prion diseases. PLoS Pathog 2: e26.

2. ColbyDW, PrusinerSB (2011) Prions. Cold Spring Harb Perspect Biol 3: a006833.

3. AguzziA, RajendranL (2009) The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64: 783–790.

4. PrusinerSB (1982) Novel proteinaceous infectious particles cause scrapie. Science 216: 136–144.

5. PrusinerSB (1998) Prions. Proc Natl Acad Sci USA 95: 13363–13383.

6. McKinleyMP, BoltonDC, PrusinerSB (1983) A protease-resistant protein is a structural component of the scrapie prion. Cell 35: 57–62.

7. DeArmondSJ, SánchezH, YehielyF, QiuY, Ninchak-CaseyA, et al. (1997) Selective neuronal targeting in prion disease. Neuron 19: 1337–1348.

8. ParchiP, GieseA, CapellariS, BrownP, Schulz-SchaefferW, et al. (1999) Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects. Ann Neurol 46: 224–233.

9. BessenRA, MarshRF (1994) Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy. J Virol 68: 7859–7868.

10. TellingGC, ParchiP, DeArmondSJ, CortelliP, MontagnaP, et al. (1996) Evidence for the conformation of the pathologic isoform of the prion protein enciphering and propagating prion diversity. Science 274: 2079–2082.

11. Dickinson AG (1976) Scrapie in sheep and goats. In: Kimberlin RH, editor. Slow Virus Diseases of Animals and Man. Amsterdam: North-Holland Publishing Company. pp. 209–241.

12. TateishiJ, KitamotoT, HoqueMZ, FurukawaH (1996) Experimental transmission of Creutzfeldt-Jakob disease and related diseases to rodents. Neurology 46: 532–537.

13. PeretzD, WilliamsonRA, LegnameG, MatsunagaY, VergaraJ, et al. (2002) A change in the conformation of prions accompanies the emergence of a new prion strain. Neuron 34: 921–932.

14. Pattison IH (1965) Experiments with scrapie with special reference to the nature of the agent and the pathology of the disease. In: Gajdusek DC, Gibbs CJ, Jr., Alpers MP, editors. Slow, Latent and Temperate Virus Infections, NINDB Monograph 2. Washington, D.C.: U.S. Government Printing. pp. 249–257.

15. ScottM, FosterD, MirendaC, SerbanD, CoufalF, et al. (1989) Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell 59: 847–857.

16. PrusinerSB, ScottM, FosterD, PanK-M, GrothD, et al. (1990) Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 63: 673–686.

17. TellingGC, ScottM, MastrianniJ, GabizonR, TorchiaM, et al. (1995) Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell 83: 79–90.

18. AsanteEA, LinehanJM, DesbruslaisM, JoinerS, GowlandI, et al. (2002) BSE prions propagate as either variant CJD-like or sporadic CJD-like prion strains in transgenic mice expressing human prion protein. EMBO J 21: 6358–6366.

19. ScottMR, WillR, IronsideJ, NguyenH-OB, TremblayP, et al. (1999) Compelling transgenetic evidence for transmission of bovine spongiform encephalopathy prions to humans. Proc Natl Acad Sci USA 96: 15137–15142.

20. ScottMR, PeretzD, NguyenH-OB, DeArmondSJ, PrusinerSB (2005) Transmission barriers for bovine, ovine, and human prions in transgenic mice. J Virol 79: 5259–5271.

21. GilesK, GliddenDV, PatelS, KorthC, GrothD, et al. (2010) Human prion strain selection in transgenic mice. Ann Neurol 68: 151–161.

22. CollingeJ, ClarkeAR (2007) A general model of prion strains and their pathogenicity. Science 318: 930–936.

23. ChandlerRL, TurfreyBA (1972) Inoculation of voles, Chinese hamsters, gerbils and guinea-pigs with scrapie brain material. Res Vet Sci 13: 219–224.

24. NonnoR, Di BariMA, CardoneF, VaccariG, FazziP, et al. (2006) Efficient transmission and characterization of Creutzfeldt-Jakob disease strains in bank voles. PLoS Pathog 2: e12.

25. AgrimiU, NonnoR, Dell'OmoG, Di BariMA, ConteM, et al. (2008) Prion protein amino acid determinants of differential susceptibility and molecular feature of prion strains in mice and voles. PLoS Pathog 4: e1000113.

26. Di BariMA, ChianiniF, VaccariG, EspositoE, ConteM, et al. (2008) The bank vole (Myodes glareolus) as a sensitive bioassay for sheep scrapie. J Gen Virol 89: 2975–2885.

27. Di BariMA, NonnoR, CastillaJ, D'AgostinoC, PirisinuL, et al. (2013) Chronic wasting disease in bank voles: characterisation of the shortest incubation time model for prion diseases. PLoS Pathog 9: e1003219.

28. CossedduGM, NonnoR, VaccariG, BucalossiC, Fernandez-BorgesN, et al. (2011) Ultra-efficient PrPSc amplification highlights potentialities and pitfalls of PMCA technology. PLoS Pathog 7: e1002370.

29. KanekoK, ZulianelloL, ScottM, CooperCM, WallaceAC, et al. (1997) Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proc Natl Acad Sci USA 94: 10069–10074.

30. DeleaultNR, LucassenRW, SupattaponeS (2003) RNA molecules stimulate prion protein conversion. Nature 425: 717–720.

31. CaugheyB, BaronGS (2006) Prions and their partners in crime. Nature 443: 803–810.

32. DeleaultNR, PiroJR, WalshDJ, WangF, MaJ, et al. (2012) Isolation of phosphatidylethanolamine as a solitary cofactor for prion formation in the absence of nucleic acids. Proc Natl Acad Sci USA 109: 8546–8551.

33. WattsJC, GilesK, StöhrJ, OehlerA, BhardwajS, et al. (2012) Spontaneous generation of rapidly transmissible prions in transgenic mice expressing wild-type bank vole prion protein. Proc Natl Acad Sci USA 109: 3498–3503.

34. ChristenB, PerezDR, HornemannS, WüthrichK (2008) NMR structure of the bank vole prion protein at 20 degrees C contains a structured loop of residues 165–171. J Mol Biol 383: 306–312.

35. CartoniC, SchininaME, MarasB, NonnoR, VaccariG, et al. (2005) Identification of the pathological prion protein allotypes in scrapie-infected heterozygous bank voles (Clethrionomys glareolus) by high-performance liquid chromatography-mass spectrometry. J Chromatogr A 1081: 122–126.

36. WillRG, IronsideJW, ZeidlerM, CousensSN, EstibeiroK, et al. (1996) A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347: 921–925.

37. CrozetC, BencsikA, FlamantF, LezmiS, SamarutJ, et al. (2001) Florid plaques in ovine PrP transgenic mice infected with an experimental ovine BSE. EMBO Rep 2: 952–956.

38. BruceME, WillRG, IronsideJW, McConnellI, DrummondD, et al. (1997) Transmissions to mice indicate that ‘new variant’ CJD is caused by the BSE agent. Nature 389: 498–501.

39. TamgüneyG, GilesK, Bouzamondo-BernsteinE, BosquePJ, MillerMW, et al. (2006) Transmission of elk and deer prions to transgenic mice. J Virol 80: 9104–9114.

40. PeretzD, ScottM, GrothD, WilliamsonA, BurtonD, et al. (2001) Strain-specified relative conformational stability of the scrapie prion protein. Protein Sci 10: 854–863.

41. WemheuerWM, BenestadSL, WredeA, Schulze-SturmU, WemheuerWE, et al. (2009) Similarities between forms of sheep scrapie and Creutzfeldt-Jakob disease are encoded by distinct prion types. Am J Pathol 175: 2566–2573.

42. HillAF, JoinerS, LinehanJ, DesbruslaisM, LantosPL, et al. (2000) Species-barrier-independent prion replication in apparently resistant species. Proc Natl Acad Sci USA 97: 10248–10253.

43. KobayashiA, SakumaN, MatsuuraY, MohriS, AguzziA, et al. (2010) Experimental verification of a traceback phenomenon in prion infection. J Virol 84: 3230–3238.

44. LiJ, BrowningS, MahalSP, OelschlegelAM, WeissmannC (2010) Darwinian evolution of prions in cell culture. Science 327: 869–872.

45. KorthC, KanekoK, GrothD, HeyeN, TellingG, et al. (2003) Abbreviated incubation times for human prions in mice expressing a chimeric mouse—human prion protein transgene. Proc Natl Acad Sci USA 100: 4784–4789.

46. BishopMT, WillRG, MansonJC (2010) Defining sporadic Creutzfeldt-Jakob disease strains and their transmission properties. Proc Natl Acad Sci USA 107: 12005–12010.

47. GilesK, De NicolaGF, PatelS, GliddenDV, KorthC, et al. (2012) Identification of I137M and other mutations that modulate incubation periods for two human prion strains. J Virol 86: 6033–6041.

48. LegnameG, NguyenH-OB, PeretzD, CohenFE, DeArmondSJ, et al. (2006) Continuum of prion protein structures enciphers a multitude of prion isolate-specified phenotypes. Proc Natl Acad Sci USA 103: 19105–19110.

49. BettC, KurtTD, LuceroM, TrejoM, RozemullerAJ, et al. (2013) Defining the conformational features of anchorless, poorly neuroinvasive prions. PLoS Pathog 9: e1003280.

50. AyersJI, SchuttCR, ShikiyaRA, AguzziA, KincaidAE, et al. (2011) The strain-encoded relationship between PrP replication, stability and processing in neurons is predictive of the incubation period of disease. PLoS Pathog 7: e1001317.

51. ColbyDW, GilesK, LegnameG, WilleH, BaskakovIV, et al. (2009) Design and construction of diverse mammalian prion strains. Proc Natl Acad Sci USA 106: 20417–20422.

52. GhaemmaghamiS, WattsJC, NguyenH-O, HayashiS, DeArmondSJ, et al. (2011) Conformational transformation and selection of synthetic prion strains. J Mol Biol 413: 527–542.

53. KimberlinRH, HallSM, WalkerCA (1983) Pathogenesis of mouse scrapie: evidence for direct neural spread of infection to the CNS after injection of sciatic nerve. J Neurol Sci 61: 315–325.

54. KimberlinRH, WalkerCA (1986) Pathogenesis of scrapie (strain 263K) in hamsters infected intracerebrally, intraperitoneally or intraocularly. J Gen Virol 67: 255–263.

55. SafarJG, GeschwindMD, DeeringC, DidorenkoS, SattavatM, et al. (2005) Diagnosis of human prion disease. Proc Natl Acad Sci USA 102: 3501–3506.

56. SandbergMK, Al-DoujailyH, SharpsB, ClarkeAR, CollingeJ (2011) Prion propagation and toxicity in vivo occur in two distinct mechanistic phases. Nature 470: 540–542.

57. GibbsCJJr, GajdusekDC (1973) Experimental subacute spongiform virus encephalopathies in primates and other laboratory animals. Science 182: 67–68.

58. RaymondGJ, RaymondLD, Meade-WhiteKD, HughsonAG, FavaraC, et al. (2007) Transmission and adaptation of chronic wasting disease to hamsters and transgenic mice: evidence for strains. J Virol 81: 4305–4314.

59. TaylorDR, ParkinET, CocklinSL, AultJR, AshcroftAE, et al. (2009) Role of ADAMs in the ectodomain shedding and conformational conversion of the prion protein. J Biol Chem 284: 22590–22600.

60. WattsJC, HuoH, BaiY, EhsaniS, JeonAH, et al. (2009) Interactome analyses identify ties of PrP and its mammalian paralogs to oligomannosidic N-glycans and endoplasmic reticulum-derived chaperones. PLoS Pathog 5: e1000608.

61. TaylorDR, WhitehouseIJ, HooperNM (2009) Glypican-1 mediates both prion protein lipid raft association and disease isoform formation. PLoS Pathog 5: e1000666.

62. SigurdsonCJ, NilssonKP, HornemannS, HeikenwalderM, MancoG, et al. (2009) De novo generation of a transmissible spongiform encephalopathy by mouse transgenesis. Proc Natl Acad Sci USA 106: 304–309.

63. SigurdsonCJ, Joshi-BarrS, BettC, WinsonO, MancoG, et al. (2011) Spongiform encephalopathy in transgenic mice expressing a point mutation in the beta2-alpha2 loop of the prion protein. J Neurosci 31: 13840–13847.

64. SigurdsonCJ, NilssonKP, HornemannS, MancoG, Fernandez-BorgesN, et al. (2010) A molecular switch controls interspecies prion disease transmission in mice. J Clin Invest 120: 2590–2599.

65. BettC, Fernandez-BorgesN, KurtTD, LuceroM, NilssonKP, et al. (2012) Structure of the beta2-alpha2 loop and interspecies prion transmission. FASEB J 26: 2868–2876.

66. HornemannS, GlockshuberR (1998) A scrapie-like unfolding intermediate of the prion protein domain PrP(121–231) induced by acidic pH. Proc Natl Acad Sci USA 95: 6010–6014.

67. KuwataK, LiH, YamadaH, LegnameG, PrusinerSB, et al. (2002) Locally disordered conformer of the hamster prion protein: a crucial intermediate to PrPSc? Biochemistry 41: 12277–12283.

68. PolymenidouM, StoeckK, GlatzelM, VeyM, BellonA, et al. (2005) Coexistence of multiple PrPSc types in individuals with Creutzfeldt-Jakob disease. Lancet Neurol 4: 805–814.

69. CaliI, CastellaniR, AlshekhleeA, CohenY, BlevinsJ, et al. (2009) Co-existence of scrapie prion protein types 1 and 2 in sporadic Creutzfeldt-Jakob disease: its effect on the phenotype and prion-type characteristics. Brain 132: 2643–2658.

70. AngersRC, KangHE, NapierD, BrowningS, SewardT, et al. (2010) Prion strain mutation determined by prion protein conformational compatibility and primary structure. Science 328: 1154–1158.

71. KimberlinRH, WalkerCA (1985) Competition between strains of scrapie depends on the blocking agent being infectious. Intervirology 23: 74–81.

72. BartzJC, KramerML, SheehanMH, HutterJA, AyersJI, et al. (2007) Prion interference is due to a reduction in strain-specific PrPSc levels. J Virol 81: 689–697.

73. WeissmannC, LiJ, MahalSP, BrowningS (2012) Prions on the move. EMBO Rep 12: 1109–1117.

74. JuckerM, WalkerLC (2013) Self-propagation of pathogenic protein aggregates in neurodegenerative diseases. Nature 501: 45–51.

75. PrusinerSB (2012) A unifying role for prions in neurodegenerative diseases. Science 336: 1511–1513.

76. BüelerH, FisherM, LangY, BluethmannH, LippH-P, et al. (1992) Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356: 577–582.

77. BerryDB, LuD, GevaM, WattsJC, BhardwajS, et al. (2013) Drug resistance confounding prion therapeutics. Proc Natl Acad Sci USA 110: E4160–E4169.

78. CarlsonGA, EbelingC, YangS-L, TellingG, TorchiaM, et al. (1994) Prion isolate specified allotypic interactions between the cellular and scrapie prion proteins in congenic and transgenic mice. Proc Natl Acad Sci USA 91: 5690–5694.

79. WattsJC, StöhrJ, BhardwajS, WilleH, OehlerA, et al. (2011) Protease-resistant prions selectively decrease shadoo protein. PLoS Pathog 7: e1002382.

80. SafarJG, GilesK, LessardP, LetessierF, PatelS, et al. (2011) Conserved properties of human and bovine prion strains on transmission to guinea pigs. Lab Invest 91: 1326–1336.

81. CarlsonGA, GoodmanPA, LovettM, TaylorBA, MarshallST, et al. (1988) Genetics and polymorphism of the mouse prion gene complex: control of scrapie incubation time. Mol Cell Biol 8: 5528–5540.

82. SafarJG, ScottM, MonaghanJ, DeeringC, DidorenkoS, et al. (2002) Measuring prions causing bovine spongiform encephalopathy or chronic wasting disease by immunoassays and transgenic mice. Nat Biotechnol 20: 1147–1150.

83. KascsakRJ, RubensteinR, MerzPA, Tonna-DeMasiM, FerskoR, et al. (1987) Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J Virol 61: 3688–3693.

84. WilliamsonRA, PeretzD, PinillaC, BallH, BastidasRB, et al. (1998) Mapping the prion protein using recombinant antibodies. J Virol 72: 9413–9418.