Enhanced virulence of sheep-passaged bovine spongiform encephalopathy agent is revealed by decreased polymorphism barriers in prion protein conversion studies

Journal of Virology

Volumn 88, Issue 5, 2014, Pages 2903-2912

  Priem, Jan ^a   Langeveld, Jan P M ^a   van Keulen, Lucien J M ^a   van Zijderveld, Fred G ^a   Andreoletti, Olivier ^b   Bossers, Alex ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN;

ANIMAL TISSUE; ARTICLE; BOVINE SPONGIFORM ENCEPHALOPATHY AGENT; CATTLE; CONTROLLED STUDY; GENOTYPE; HOST SUSCEPTIBILITY; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MISFOLDING CYCLIC AMPLIFICATION; PROTEIN POLYMORPHISM; SHEEP; SPECIES IDENTIFICATION; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS TRANSMISSION; VIRUS VIRULENCE;

ANIMALS; BRAIN; CATTLE; ENCEPHALOPATHY, BOVINE SPONGIFORM; GENOTYPE; PRIONS; PROTEIN FOLDING; SCRAPIE; SHEEP; SPECIES SPECIFICITY; VIRULENCE;

EID: 84896718376     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02446-13     Document Type: Article

References (71)

1. Andréoletti O, Berthon P, Marc D, Sarradin P, Grosclaude J, van Keulen L, Schelcher F, Elsen JM, Lantier F. 2000. Early accumulation of PrP(Sc) in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J. Gen. Virol. 81:3115-3126. http://vir.sgmjournals.org/content/81/12/3115.
2. van Keulen LJ, Bossers A, van Zijderveld F. 2008. TSE pathogenesis in cattle and sheep. Vet. Res. 39:24. http://dx.doi.org/10.1051/vetres:2007061.
3. van Keulen LJ, Schreuder BE, Vromans ME, Langeveld JP, Smits MA. 2000. Pathogenesis of natural scrapie in sheep. Arch. Virol. Suppl. 2000(16):57-71.
4. Caughey B, Baron GS, Chesebro B, Jeffrey M. 2009. Getting a grip on prions: oligomers, amyloids, and pathological membrane interactions. Annu. Rev. Biochem. 78:177-204. http://dx.doi.org/10.1146/annurev .biochem.78.082907.145410.
5. Deleault NR, Walsh DJ, Piro JR, Wang F, Wang X, Ma J, Rees JR, Supattapone S. 2012. Cofactor molecules maintain infectious conformation and restrict strain properties in purified prions. Proc. Natl. Acad. Sci. U. S. A. 109:E1938-E1946. http://dx.doi.org/10.1073/pnas.1206999109.
6. Supattapone S. 2004. Prion protein conversion in vitro. J. Mol. Med. 82:348-356. http://dx.doi.org/10.1007/s00109-004-0534-3.
7. Hunter N, Bossers A. 2006. The PrP genotype as a marker for scrapie susceptibility in sheep, p 640-647. In Hörnlimann B, Riesner D, Kretzschmar H (ed), Prions in humans and animals. de Gruyter, Berlin, Germany.
8. Bossers A, Schreuder BE, Muileman IH, Belt PB, Smits MA. 1996. PrP genotype contributes to determining survival times of sheep with natural scrapie. J. Gen. Virol. 77(Part 10):2669-2673.
9. Goldmann W, Hunter N, Smith G, Foster J, Hope J. 1994. PrP genotype and agent effects in scrapie: change in allelic interaction with different isolates of agent in sheep, a natural host of scrapie. J. Gen. Virol. 75(Part 5):989-995.
10. Hunter N. 2003. Scrapie and experimental BSE in sheep. Br. Med. Bull. 66:171-183. http://dx.doi.org/10.1093/bmb/66.1.171.
11. Foster JD, Hope J, Fraser H. 1993. Transmission of bovine spongiform encephalopathy to sheep and goats. Vet. Rec. 133:339-341. http://dx.doi .org/10.1136/vr.133.14.339.
12. Bossers A, Belt P, Raymond GJ, Caughey B, de Vries R, Smits MA. 1997. Scrapie susceptibility-linked polymorphisms modulate the in vitro conversion of sheep prion protein to protease-resistant forms. Proc. Natl. Acad. Sci. U.S.A. 94:4931-4936. http://dx.doi.org/10.1073/pnas.94.10 .4931.
13. Bossers A, de Vries R, Smits MA. 2000. Susceptibility of sheep for scrapie as assessed by in vitro conversion of nine naturally occurring variants of PrP. J. Virol. 74:1407-1414. http://dx.doi.org/10.1128/JVI.74.3.1407 -1414.2000.
14. Rigter A, Langeveld JP, Timmers-Parohi D, Jacobs JG, Moonen PL, Bossers A. 2007. Mapping of possible prion protein self-interaction domains using peptide arrays. BMC Biochem. 8:6. http://dx.doi.org/10.1186 /1471-2091-8-6.
15. Sigurdson CJ, Nilsson KP, Hornemann S, Manco G, Fernandez-Borges N, Schwarz P, Castilla J, Wuthrich K, Aguzzi A. 2010. A molecular switch controls interspecies prion disease transmission in mice. J. Clin. Invest. 120:2590-2599. http://dx.doi.org/10.1172/JCI42051.
16. Rigter A, Bossers A. 2005. Sheep scrapie susceptibility-linked polymorphisms do not modulate the initial binding of cellular to diseaseassociated prion protein prior to conversion. J. Gen. Virol. 86:2627-2634. http://dx.doi.org/10.1099/vir.0.80901-0.
17. Horiuchi M, Priola SA, Chabry J, Caughey B. 2000. Interactions between heterologous forms of prion protein: binding, inhibition of conversion, and species barriers. Proc. Natl. Acad. Sci. U.S.A. 97:5836-5841. http: //dx.doi.org/10.1073/pnas.110523897.
18. Bellworthy SJ, Dexter G, Stack M, Chaplin M, Hawkins SA, Simmons MM, Jeffrey M, Martin S, Gonzalez L, Hill P. 2008. Oral transmission of BSE to VRQ/VRQ sheep in an experimental flock. Vet. Rec. 162:130-131. http://dx.doi.org/10.1136/vr.162.4.130.
19. Ridley RM, Baker HF. 1996. Oral transmission of BSE to primates. Lancet 348: 1174. http://dx.doi.org/10.1016/S0140-6736(05)65312-3.
20. Béringue V, Andreoletti O, Le Dur A, Essalmani R, Vilotte JL, Lacroux C, Reine F, Herzog L, Biacabe AG, Baron T, Caramelli M, Casalone C, Laude H. 2007. A bovine prion acquires an epidemic bovine spongiform encephalopathy strain-like phenotype on interspecies transmission. J. Neurosci. 27:6965-6971. http://dx.doi.org/10.1523/JNEUROSCI.0693 -07.2007.
21. Stack M, Gonzalez L, Jeffrey M, Martin S, Macaldowie C, Chaplin M, Thorne J, Sayers R, Davis L, Bramwell J, Grimmer S, Bellworthy S. 2009. Three serial passages of bovine spongiform encephalopathy in sheep do not significantly affect discriminatory test results. J. Gen. Virol. 90: 764-768. http://dx.doi.org/10.1099/vir.0.005983-0.
22. Hill AF, Desbruslais M, Joiner S, Sidle KC, Gowland I, Collinge J, Doey LJ, Lantos P. 1997. The same prion strain causes vCJD and BSE. Nature 389:448-450, 526.
23. Spiropoulos J, Lockey R, Sallis RE, Terry LA, Thorne L, Holder TM, Beck KE, Simmons MM. 2011. Isolation of prion with BSE properties from farmed goat. Emerg. Infect. Dis. 17:2253-2261. http://dx.doi.org/10 .3201/eid1712.110333.
24. Eloit M, Adjou K, Coulpier M, Fontaine JJ, Hamel R, Lilin T, Messiaen S, Andreoletti O, Baron T, Bencsik A, Biacabe AG, Beringue V, Laude H, Le Dur A, Vilotte JL, Comoy E, Deslys JP, Grassi J, Simon S, Lantier F, Sarradin P. 2005. BSE agent signatures in a goat. Vet. Rec. 156:523-524.
25. Jeffrey M, Martin S, Gonzalez L, Foster J, Langeveld JP, van Zijderveld FG, Grassi J, Hunter N. 2006. Immunohistochemical features of PrP(d) accumulation in natural and experimental goat transmissible spongiform encephalopathies. J. Comp. Pathol. 134:171-181. http://dx.doi.org/10 .1016/j.jcpa.2005.10.003.
26. Wells GA, Hawkins SA, Green RB, Austin AR, Dexter I, Spencer YI, Chaplin MJ, Stack MJ, Dawson M. 1998. Preliminary observations on the pathogenesis of experimental bovine spongiform encephalopathy (BSE): an update. Vet. Rec. 142:103-106. http://dx.doi.org/10.1136/vr.142.5.103.
27. Buschmann A, Groschup MH. 2005. Highly bovine spongiform encephalopathy-sensitive transgenic mice confirm the essential restriction of infectivity to the nervous system in clinically diseased cattle. J. Infect. Dis. 192:934-942. http://dx.doi.org/10.1086/431602.
28. Bellworthy SJ, Hawkins SA, Green RB, Blamire I, Dexter G, Dexter I, Lockey R, Jeffrey M, Ryder S, Berthelin-Baker C, Simmons MM. 2005. Tissue distribution of bovine spongiform encephalopathy infectivity in Romney sheep up to the onset of clinical disease after oral challenge. Vet. Rec. 156:197-202. http://dx.doi.org/10.1136/vr.156.7.197.
29. van Keulen LJ, Schreuder BE, Vromans ME, Langeveld JP, Smits MA. 1999. Scrapie-associated prion protein in the gastrointestinal tract of sheep with natural scrapie. J. Comp. Pathol. 121:55-63. http://dx.doi.org/10.1053/jcpa.1998.0300.
30. Bruce ME, McConnell I, Will RG, Ironside JW. 2001. Detection of variant Creutzfeldt-Jakob disease infectivity in extraneural tissues. Lancet 358:208-209. http://dx.doi.org/10.1016/S0140-6736(01)05411-3.
31. Espinosa JC, Andreoletti O, Castilla J, Herva ME, Morales M, Alamillo E, San-Segundo FD, Lacroux C, Lugan S, Salguero FJ, Langeveld J, Torres JM. 2007. Sheep-passaged bovine spongiform encephalopathy agent exhibits altered pathobiological properties in bovine-PrP transgenic mice. J. Virol. 81:835-843. http://dx.doi.org/10.1128/JVI.01356-06.
32. Plinston C, Hart P, Chong A, Hunter N, Foster J, Piccardo P, Manson JC, Barron RM. 2011. Increased susceptibility of human-PrP transgenic mice to bovine spongiform encephalopathy infection following passage in sheep. J. Virol. 85:1174-1181. http://dx.doi.org/10.1128/JVI.01578-10.
33. Tamgüney G, Miller MW, Giles K, Lemus A, Glidden DV, DeArmond SJ, Prusiner SB. 2009. Transmission of scrapie and sheep-passaged bovine spongiform encephalopathy prions to transgenic mice expressing elk prion protein. J. Gen. Virol. 90:1035-1047. http://dx.doi.org/10.1099/vir .0.007500-0.
34. Saborío GP, Soto C, Kascsak RJ, Levy E, Kascsak R, Harris DA, Frangione B. 1999. Cell-lysate conversion of prion protein into its protease-resistant isoform suggests the participation of a cellular chaperone. Biochem. Biophys. Res. Commun. 258:470-475. http://dx.doi.org/10 .1006/bbrc.1999.0660.
35. Lucassen R, Nishina K, Supattapone S. 2003. In vitro amplification of protease-resistant prion protein requires free sulfhydryl groups. Biochemistry 42:4127-4135. http://dx.doi.org/10.1021/bi027218d.
36. Kocisko DA, Priola SA, Raymond GJ, Chesebro B, Lansbury PT, Jr, Caughey B. 1995. Species specificity in the cell-free conversion of prion protein to protease-resistant forms: a model for the scrapie species barrier. Proc. Natl. Acad. Sci. U.S.A. 92:3923-3927. http://dx.doi.org/10.1073/pnas.92.9.3923.
37. Eiden M, Palm GJ, Hinrichs W, Matthey U, Zahn R, Groschup MH. 2006. Synergistic and strain-specific effects of bovine spongiform encephalopathy and scrapie prions in the cell-free conversion of recombinant prion protein. J. Gen. Virol. 87:3753-3761. http://dx.doi.org/10.1099/vir .0.81590-0.
38. Atarashi R, Wilham JM, Christensen L, Hughson AG, Moore RA, Johnson LM, Onwubiko HA, Priola SA, Caughey B. 2008. Simplified ultrasensitive prion detection by recombinant PrP conversion with shaking. Nat. Methods 5:211-212. http://dx.doi.org/10.1038/nmeth0308-211.
39. Kirby L, Birkett CR, Rudyk H, Gilbert IH, Hope J. 2003. In vitro cell-free conversion of bacterial recombinant PrP to PrPres as a model for conversion. J. Gen. Virol. 84:1013-1020. http://dx.doi.org/10.1099/vir.0 .18903-0.
40. Raymond GJ, Bossers A, Raymond LD, O'Rourke KI, McHolland LE, Bryant PK, III, Miller MW, Williams ES, Smits M, Caughey B. 2000. Evidence of a molecular barrier limiting susceptibility of humans, cattle and sheep to chronic wasting disease. EMBO J. 19:4425-4430. http://dx.doi.org/10.1093/emboj/19.17.4425.
41. Raymond GJ, Hope J, Kocisko DA, Priola SA, Raymond LD, Bossers A, Ironside J, Will RG, Chen SG, Petersen RB, Gambetti P, Rubenstein R, Smits MA, Lansbury PT, Jr, Caughey B. 1997. Molecular assessment of the potential transmissibilities of BSE and scrapie to humans. Nature 388: 285-288. http://dx.doi.org/10.1038/40876.
42. Castilla J, Morales R, Saa P, Barria M, Gambetti P, Soto C. 2008. Cell-free propagation of prion strains. EMBO J. 27:2557-2566. http://dx .doi.org/10.1038/emboj.2008.181.
43. Castilla J, Saa P, Hetz C, Soto C. 2005. In vitro generation of infectious scrapie prions. Cell 121:195-206. http://dx.doi.org/10.1016/j.cell.2005.02 .011.
44. Orrú CD, Wilham JM, Hughson AG, Raymond LD, McNally KL, Bossers A, Ligios C, Caughey B. 2009. Human variant Creutzfeldt-Jakob disease and sheep scrapie PrP(res) detection using seeded conversion of recombinant prion protein. Protein Eng. Des. Sel. 22:515-521. http://dx .doi.org/10.1093/protein/gzp031.
45. Thorne L, Terry LA. 2008. In vitro amplification of PrPSc derived from the brain and blood of sheep infected with scrapie. J. Gen. Virol. 89:3177-3184. http://dx.doi.org/10.1099/vir.0.2008/004226-0.
46. Orrú CD, Wilham JM, Raymond LD, Kuhn F, Schroeder B, Raeber AJ, Caughey B. 2011. Prion disease blood test using immunoprecipitation and improved quaking-induced conversion. mBio 2(3):e00078 -11. http://dx.doi.org/10.1128/mBio.00078-11.
47. Saborio GP, Permanne B, Soto C. 2001. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411:810-813. http://dx.doi.org/10.1038/35081095.
48. Jones M, Peden AH, Head MW, Ironside JW. 2011. The application of in vitro cell-free conversion systems to human prion diseases. Acta Neuropathol. 121:135-143. http://dx.doi.org/10.1007/s00401-010-0708-8.
49. Fernández-Borges N, de Castro J, Castilla J. 2009. In vitro studies of the transmission barrier. Prion 3:220-223. http://dx.doi.org/10.4161/pri.3.4 .10500.
50. Kurt TD, Telling GC, Zabel MD, Hoover EA. 2009. Trans-species amplification of PrP(CWD) and correlation with rigid loop 170N. Virology 387:235-243. http://dx.doi.org/10.1016/j.virol.2009.02.025.
51. Meyerett C, Michel B, Pulford B, Spraker TR, Nichols TA, Johnson T, Kurt T, Hoover EA, Telling GC, Zabel MD. 2008. In vitro strain adaptation of CWD prions by serial protein misfolding cyclic amplification. Virology 382:267-276. http://dx.doi.org/10.1016/j.virol.2008.09.023.
52. Castilla J, Gonzalez-Romero D, Saa P, Morales R, De Castro J, Soto C. 2008. Crossing the species barrier by PrP(Sc) replication in vitro generates unique infectious prions. Cell 134:757-768. http://dx.doi.org/10.1016/j .cell.2008.07.030.
53. Thuring CM, van Keulen LJ, Langeveld JP, Vromans ME, van Zijderveld FG, Sweeney T. 2005. Immunohistochemical distinction between preclinical bovine spongiform encephalopathy and scrapie infection in sheep. J. Comp. Pathol. 132:59-69. http://dx.doi.org/10.1016/j.jcpa.2004 .06.004.
54. Andreoletti O. 2003. European FP5 project QLK3-CT-2002-01309 to study BSE strain in sheep. http://cordis.europa.eu/projects/rcn/67194_en .html.
55. Morales R, Duran-Aniotz C, Diaz-Espinoza R, Camacho MV, Soto C. 2012. Protein misfolding cyclic amplification of infectious prions. Nat. Protoc. 7:1397-1409. http://dx.doi.org/10.1038/nprot.2012.067.
56. Langeveld JP, Jacobs JG, Erkens JH, Bossers A, van Zijderveld FG, van Keulen LJ. 2006. Rapid and discriminatory diagnosis of scrapie and BSE in retro-pharyngeal lymph nodes of sheep.BMCVet. Res. 2:19. http://dx.doi .org/10.1186/1746-6148-2-19.
57. Padilla D, Beringue V, Espinosa JC, Andreoletti O, Jaumain E, Reine F, Herzog L, Gutierrez-Adan A, Pintado B, Laude H, Torres JM. 2011. Sheep and goat BSE propagate more efficiently than cattle BSE in human PrP transgenic mice. PLoS Pathog. 7:e1001319. http://dx.doi.org/10.1371/journal.ppat.1001319.
58. Espinosa JC, Herva ME, Andreoletti O, Padilla D, Lacroux C, Cassard H, Lantier I, Castilla J, Torres JM. 2009. Transgenic mice expressing porcine prion protein resistant to classical scrapie but susceptible to sheep bovine spongiform encephalopathy and atypical scrapie. Emerg. Infect. Dis. 15:1214-1221. http://dx.doi.org/10.3201/eid1508.081218.
59. Béringue V, Herzog L, Jaumain E, Reine F, Sibille P, Le Dur A, Vilotte JL, Laude H. 2012. Facilitated cross-species transmission of prions in extraneural tissue. Science 335:472-475. http://dx.doi.org/10.1126/science.1215659.
60. González L, Chianini F, Martin S, Siso S, Gibbard L, Reid HW, Jeffrey M. 2007. Comparative titration of experimental ovine BSE infectivity in sheep and mice. J. Gen. Virol. 88:714-717. http://dx.doi.org/10.1099/vir .0.82426-0.
61. Beck KE, Thorne L, Lockey R, Vickery CM, Terry LA, Bujdoso R, Spiropoulos J. 2013. Strain typing of classical scrapie by transgenic mouse bioassay using protein misfolding cyclic amplification to replace primary passage. PLoS One 8:e57851. http://dx.doi.org/10.1371/journal.pone .0057851.
62. Thorne L, Holder T, Ramsay A, Edwards J, Taema MM, Windl O, Maddison BC, Gough KC, Terry LA. 2012. In vitro amplification of ovine prions from scrapie-infected sheep from Great Britain reveals distinct patterns of propagation. BMC Vet. Res. 8:223. http://dx.doi.org/10 .1186/1746-6148-8-223.
63. Everest SJ, Ramsay AM, Chaplin MJ, Everitt S, Stack MJ, Neale MH, Jeffrey M, Moore SJ, Bellworthy SJ, Terry LA. 2011. Detection and localisation of PrP(Sc) in the liver of sheep infected with scrapie and bovine spongiform encephalopathy. PLoS One 6:e19737. http://dx.doi.org/10.1371/journal.pone.0019737.
64. Bossers A, Rigter A, de Vries R, Smits MA. 2003. In vitro conversion of normal prion protein into pathologic isoforms. Clin. Lab. Med. 23:227-247. http://dx.doi.org/10.1016/S0272-2712(02)00063-X.
65. Bucalossi C, Cosseddu G, D'Agostino C, Di Bari MA, Chiappini B, Conte M, Rosone F, De Grossi L, Scavia G, Agrimi U, Nonno R, Vaccari G. 2011. Assessment of the genetic susceptibility of sheep to scrapie by protein misfolding cyclic amplification and comparison with experimental scrapie transmission studies. J. Virol. 85:8386-8392. http://dx.doi.org/10.1128/JVI.00241-11.
66. Priola SA, Caughey B, Race RE, Chesebro B. 1994. Heterologous PrP molecules interfere with accumulation of protease-resistant PrP in scrapie-infected murine neuroblastoma cells. J. Virol. 68:4873-4878.
67. Gnzález L, Jeffrey M, Dagleish MP, Goldmann W, Siso S, Eaton SL, Martin S, Finlayson J, Stewart P, Steele P, Pang Y, Hamilton S, Reid HW, Chianini F. 2012. Susceptibility to scrapie and disease phenotype in sheep: cross-Prnp genotype experimental transmissions with natural sources. Vet. Res. 43:55. http://dx.doi.org/10.1186/1297-9716-43-55.
68. Jacobs JG, Bossers A, Rezaei H, van Keulen LJ, McCutcheon S, Sklaviadis T, Lantier I, Berthon P, Lantier F, van Zijderveld FG, Langeveld JP. 2011. Proteinase K-resistant material in ARR/VRQ sheep brain affected with classical scrapie is composed mainly of VRQ prion protein. J. Virol. 85:12537-12546. http://dx.doi.org/10.1128/JVI.00448-11.
69. Saá P, Castilla J, Soto C. 2006. Ultra-efficient replication of infectious prions by automated protein misfolding cyclic amplification. J. Biol. Chem. 281:35245-35252. http://dx.doi.org/10.1074/jbc.M603964200.
70. Green KM, Castilla J, Seward TS, Napier DL, Jewell JE, Soto C, Telling GC. 2008. Accelerated high fidelity prion amplification within and across prion species barriers. PLoS Pathog. 4:e1000139. http://dx.doi.org/10 .1371/journal.ppat.1000139.
71. Thuring CM, Erkens JH, Jacobs JG, Bossers A, Van Keulen LJ, Garssen GJ, Van Zijderveld FG, Ryder SJ, Groschup MH, Sweeney T, Langeveld JP. 2004. Discrimination between scrapie and bovine spongiform encephalopathy in sheep by molecular size, immunoreactivity, and glycoprofile of prion protein. J. Clin. Microbiol. 42:972-980. http://dx.doi.org/10.1128/JCM.42.3.972-980.2004.