Spontaneous generation of infectious prion disease in transgenic mice

Emerging Infectious Diseases

Volumn 19, Issue 12, 2013, Pages 1938-1947

  Torres, Juan María ^a   Castilla, Joaquín ^a,b   Pintado, Belén ^a   Gutiérrez Adan, Alfonso ^a   Andréoletti, Olivier ^c   Aguilar Calvo, Patricia ^a   Arroba, Ana Isabel ^a   Parra Arrondo, Beatriz ^a   Ferrer, Isidro ^d   Manzanares, Jorge ^e   Espinosa, Juan Carlos ^a  

^a INIA   (Spain)

^b BASQUE FOUNDATION FOR SCIENCE   (Spain)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^e MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; GLIAL FIBRILLARY ACIDIC PROTEIN; MUTANT PROTEIN; PRION PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BOVINE SPONGIFORM ENCEPHALOPATHY; CELL PROLIFERATION; CONTROLLED STUDY; CREUTZFELDT JAKOB DISEASE; GERSTMANN STRAUSSLER SCHEINKER SYNDROME; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MICROGLIA; MOUSE; NONHUMAN; PHENOTYPE; PRION DISEASE; PROTEIN EXPRESSION; SPONTANEOUS MUTATION; TRANSGENIC MOUSE; VIRUS INFECTIVITY; VIRUS TRANSMISSION; WESTERN BLOTTING;

BOVINE PRION PROTEIN; BOVINE PRP; BOVINE SPONGIFORM ENCEPHALOPATHY; BSE; GERSTMANN-STRÄUSSLER-SCHEINKER SYNDROME; PRIONS AND RELATED DISEASES; SPONTANEOUS GENERATION; TRANSGENIC MICE; TRANSMISSIBLE SPONGIFORM ENCEPHALOPATHY; TSE;

ANIMALS; BRAIN; CATTLE; ENCEPHALOPATHY, BOVINE SPONGIFORM; GENE EXPRESSION; GENOTYPE; HIPPOCAMPUS; HUMANS; MICE; MICE, TRANSGENIC; MUTATION; OPEN READING FRAMES; PRION DISEASES; PRPSC PROTEINS;

EID: 84888124449     PISSN: 10806040     EISSN: 10806059     Source Type: Journal    
DOI: 10.3201/eid1912.130106     Document Type: Article

References (40)

1. Griffith JS. Self-replication and scrapie. Nature. 1967;215:1043-4. http://dx.doi.org/10.1038/2151043a0
2. McKinley MP, Bolton DC, Prusiner SB. A protease-resistant protein is a structural component of the scrapie prion. Cell. 1983;35:57-62. http://dx.doi.org/10.1016/0092-8674(83)90207-6
3. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science. 1982;216:136-44. http://dx.doi.org/10.1126/ science.6801762
4. Prusiner SB. Molecular biology of prion diseases. Science. 1991;252:1515-22. http://dx.doi.org/10.1126/science.1675487
5. Brown P, Gibbs CJ Jr, Rodgers-Johnson P, Asher DM, Sulima MP, Bacote A, et al. Human spongiform encephalopathy: the National Institutes of Health series of 300 cases of experimentally transmitted disease. Ann Neurol. 1994;35:513-29. http://dx.doi.org/10.1002/ ana.410350504
6. Tateishi J, Kitamoto T, Hoque MZ, Furukawa H. Experimental transmission of Creutzfeldt-Jakob disease and related diseases to rodents. Neurology. 1996;46:532-7. http://dx.doi.org/10.1212/WNL.46.2.532
7. Mastrianni JA, Capellari S, Telling GC, Han D, Bosque P, Prusiner SB, et al. Inherited prion disease caused by the V210I mutation: transmission to transgenic mice. Neurology. 2001;57:2198-205. http://dx.doi.org/10.1212/WNL.57.12.2198
8. Nonno R, Bari MA, Cardone F, l transmission and characterization of Creutzfeldt-Jakob disease strains in bank voles. PLoS Pathog. 2006;2:e12. http:// dx.doi.org/10.1371/journal.ppat.0020012
9. Collinge J, Palmer MS. Prion diseases. Curr Opin Genet Dev. 1992;2:448-54. http://dx.doi.org/10.1016/S0959-437X(05)80156-X
10. Collinge J. Molecular neurology of prion disease. J Neurol Neurosurg Psychiatry. 2005;76:906-19. http://dx.doi.org/10.1136/ jnnp.2004.048660
11. Collinge J, Clarke AR. A general model of prion strains and their pathogenicity. Science. 2007;318:930-6. http://dx.doi.org/10.1126/ science.1138718
12. Chiesa R, Drisaldi B, Quaglio E, Migheli A, Piccardo P, Ghetti B, et al. Accumulation of protease-resistant prion protein (PrP) and apoptosis of cerebellar granule cells in transgenic mice expressing a PrP insertional mutation. Proc Natl Acad Sci U S A. 2000;97:5574-9. http://dx.doi.org/10.1073/pnas.97.10.5574
13. Castilla J, Gutierrez-Adan A, Brun A, Pintado B, Salguero FJ, Parra B, et al. Transgenic mice expressing bovine PrP with a four extra repeat octapeptide insert mutation show a spontaneous, non-transmissible, neurodegenerative disease and an expedited course of BSE infection. FEBS Lett. 2005;579:6237-46. http://dx.doi.org/10.1016/j.febslet.2005.09.099
14. Chiesa R, Piccardo P, Quaglio E, Drisaldi B, Si-Hoe SL, Takao M, et al. Molecular distinction between pathogenic and infectious properties of the prion protein. J Virol. 2003;77:7611-22. http:// dx.doi.org/10.1128/JVI.77.13.7611-7622.2003
15. Hsiao KK, Scott M, Foster D, Groth DF, DeArmond SJ, Prusiner SB. Spontaneous neurodegeneration in transgenic mice with mutant prion protein. Science. 1990;250:1587-90. http://dx.doi. org/10.1126/science.1980379
16. Jackson WS, Borkowski AW, Faas H, Steele AD, King OD, Watson N, et al. Spontaneous generation of prion infectivity in fatal familial insomnia knockin mice. Neuron. 2009;63:438-50. http://dx.doi. org/10.1016/j.neuron.2009.07.026
17. Sigurdson CJ, Nilsson KP, Hornemann S, Heikenwalder M, Manco G, Schwarz P, et al. De novo generation of a transmissible spongiform encephalopathy by mouse transgenesis. Proc Natl Acad Sci U S A. 2009;106:304-9. http://dx.doi.org/10.1073/pnas.0810680105
18. Hsiao K, Baker HF, Crow TJ, Poulter M, Owen F, Terwilliger JD, et al. Linkage of a prion protein missense variant to Gerstmann-Sträussler syndrome. Nature. 1989;338:342-5. http://dx.doi. org/10.1038/338342a0
19. Ikeda SI, Yanagisawa N, Glenner GG, Allsop D. Gerstmann-Sträussler-Scheinker disease showing protein amyloid deposits in the peripheral regions of PrP immunoreactive amyloid plaques. Neurodegeneration. 1992;1:281-8.
20. Castilla J, Gutierrez Adan A, Brun A, Pintado B, Ramirez MA, Parra B, et al. Early detection of PrP(res) in BSE-infected bovine PrP transgenic mice. Arch Virol. 2003;148:677-91. http://dx.doi. org/10.1007/s00705-002-0958-4
21. Borchelt DR, Davis J, Fischer M, Lee MK, Slunt HH, Ratovitsky T, et al. A vector for expressing foreign genes in the brains and hearts of transgenic mice. Genet Anal. 1996;13:159-63. http://dx.doi. org/10.1016/S1050-3862(96)00167-2
22. Castilla J, Gutierrez-Adan A, Brun A, Pintado B, Parra B, Ramirez MA, et al. Different behavior toward bovine spongiform encephalopathy infection of bovine prion protein transgenic mice with one extra repeat octapeptide insert mutation. J Neurosci. 2004;24:2156-64. http://dx.doi.org/10.1523/JNEUROSCI.3811-03.2004
23. Sisó S, Puig B, Varea R, Vidal E, Acin C, Prinz M, et al. Abnormal synaptic protein expression and cell death in murine scrapie. Acta Neuropathol. 2002;103:615-26. http://dx.doi.org/10.1007/s00401-001-0512-6
24. Padilla D, Béringue V, Espinosa JC, Andreoletti O, Jaumain E, Reine F, et al. Sheep and goat BSE propagate more efficiently than cattle BSE in human PrP transgenic mice. PLoS Pathog. 2011;7:e1001319. http://dx.doi.org/10.1371/journal.ppat.1001319
25. Féraudet C, Morel N, Simon S, Volland H, Frobert Y, Creminon C, et al. Screening of 145 anti-PrP monoclonal antibodies for their capacity to inhibit PrPSc replication in infected cells. J Biol Chem. 2005;280:11247-58. http://dx.doi.org/10.1074/jbc.M407006200
26. Yull HM, Ritchie DL, Langeveld JP, van Zijderveld FG, Bruce ME, Ironside JW, et al. Detection of type 1 prion protein in variant Creutzfeldt-Jakob disease. Am J Pathol. 2006;168:151-7. http://dx.doi.org/10.2353/ajpath.2006.050766
27. Andréoletti O, Lacroux C, Chabert A, Monnereau L, Tabouret G, Lantier F, et al. PrP(Sc) accumulation in placentas of ewes exposed to natural scrapie: influence of foetal PrP genotype and effect on ewe-to-lamb transmission. J Gen Virol. 2002;83:2607-16.
28. Fraser H, Dickinson AG. The sequential development of the brain lesion of scrapie in three strains of mice. J Comp Pathol. 1968;78:301-11. http://dx.doi.org/10.1016/0021-9975(68)90006-6
29. Andréoletti O, Simon S, Lacroux C, Morel N, Tabouret G, Chabert A, et al. PrP(Sc) accumulation in myocytes from sheep incubating natural scrapie. Nat Med. 2004;10:591-3. http://dx.doi.org/10.1038/ nm1055
30. Brun A, Castilla J, Ramirez MA, Prager K, Parra B, Salguero FJ, et al. Proteinase K enhanced immunoreactivity of the prion proteinspecific monoclonal antibody 2A11. Neurosci Res. 2004;48:75-83. http://dx.doi.org/10.1016/j.neures.2003.09.004
31. Torres JM, Andreoletti O, Lacroux C, Prieto I, Lorenzo P, Larska M, et al. Classical bovine spongiform encephalopathy by transmission of H-type prion in homologous prion protein context. Emerg Infect Dis. 2011;17:1636-44. http://dx.doi.org/10.3201/eid1709.101403
32. Espinosa JC, Andreoletti O, Castilla J, Herva ME, Morales M, Alamillo E, et al. Sheep-passaged bovine spongiform encephalopathy agent exhibits altered pathobiological properties in bovine-PrP transgenic mice. J Virol. 2007;81:835-43. http://dx.doi.org/10.1128/ JVI.01356-06
33. Bruce ME, McConnell I, Fraser H, Dickinson AG. The disease characteristics of different strains of scrapie in Sinc congenic mouse lines: implications for the nature of the agent and host control of pathogenesis. J Gen Virol. 1991;72:595-603. http://dx.doi.org/10.1099/0022-1317-72-3-595
34. Priola SA, Chesebro B. Abnormal properties of prion protein with insertional mutations in different cell types. J Biol Chem. 1998;273:11980-5. http://dx.doi.org/10.1074/jbc.273.19.11980
35. Hsiao KK, Groth D, Scott M, Yang SL, Serban H, Rapp D, et al. Serial transmission in rodents of neurodegeneration from transgenic mice expressing mutant prion protein. Proc Natl Acad Sci U S A. 1994;91:9126-30. http://dx.doi.org/10.1073/pnas.91.19.9126
36. Telling GC, Haga T, Torchia M, Tremblay P, DeArmond SJ, Prusiner SB. Interactions between wild-type and mutant prion proteins modulate neurodegeneration in transgenic mice. Genes Dev. 1996;10:1736-50. http://dx.doi.org/10.1101/gad.10.14.1736
37. Manson JC, Jamieson E, Baybutt H, Tuzi NL, Barron R, McConnell I, et al. A single amino acid alteration (101L) introduced into murine PrP dramatically alters incubation time of transmissible spongiform encephalopathy. EMBO J. 1999;18:6855-64. http:// dx.doi.org/10.1093/emboj/18.23.6855
38. Asante EA, Gowland I, Grimshaw A, Linehan JM, Smidak M, Houghton R, et al. Absence of spontaneous disease and comparative prion susceptibility of transgenic mice expressing mutant human prion proteins. J Gen Virol. 2009;90:546-58. http://dx.doi. org/10.1099/vir.0.007930-0
39. Nicholson EM, Brunelle BW, Richt JA, Kehrli ME Jr, Greenlee JJ. Identification of a heritable polymorphism in bovine PRNP associated with genetic transmissible spongiform encephalopathy: evidence of heritable BSE. PLoS ONE. 2008;3:e2912. http://dx.doi. org/10.1371/journal.pone.0002912
40. Stöhr J, Watts JC, Legname G, Oehler A, Lemus A, Nguyen HO, et al. Spontaneous generation of anchorless prions in transgenic mice. Proc Natl Acad Sci U S A. 2011;108:21223-8. http://dx.doi. org/10.1073/pnas.1117827108