Transgenic Mouse Bioassay: Evidence That Rabbits Are Susceptible to a Variety of Prion Isolates
Prions, the infectious agents responsible for causing mad cow disease, amongst other diseases, can transmit from one species to another. For example, Bovine Spongiform Encephalopathy can transmit to humans resulting in invariably fatal variant Creutzfeldt-Jakob Disease. We wanted to study the susceptibility of rabbits as, until recently, they were considered a prion resistant species. Once proven otherwise, we wanted to know which particular prions rabbits were susceptible to. With this aim, a transgenic mouse was designed expressing the rabbit prion protein gene instead of the corresponding mouse gene to model the transmission barrier between rabbits and other species. The resultant mice where challenged with several field prion isolates including classical and atypical strains of Bovine Spongiform Encephalopathy, sheep Scrapie and cervid Chronic Wasting disease. The transgenic mice were susceptible to classical and atypical Bovine Spongiform Encephalopathy prions and also to mouse-adapted Scrapie prions. This information must be taken into account when assessing the risk of using ruminant derived protein as a protein source to feed rabbits.
Vyšlo v časopise:
Transgenic Mouse Bioassay: Evidence That Rabbits Are Susceptible to a Variety of Prion Isolates. PLoS Pathog 11(8): e32767. doi:10.1371/journal.ppat.1004977
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004977
Souhrn
Prions, the infectious agents responsible for causing mad cow disease, amongst other diseases, can transmit from one species to another. For example, Bovine Spongiform Encephalopathy can transmit to humans resulting in invariably fatal variant Creutzfeldt-Jakob Disease. We wanted to study the susceptibility of rabbits as, until recently, they were considered a prion resistant species. Once proven otherwise, we wanted to know which particular prions rabbits were susceptible to. With this aim, a transgenic mouse was designed expressing the rabbit prion protein gene instead of the corresponding mouse gene to model the transmission barrier between rabbits and other species. The resultant mice where challenged with several field prion isolates including classical and atypical strains of Bovine Spongiform Encephalopathy, sheep Scrapie and cervid Chronic Wasting disease. The transgenic mice were susceptible to classical and atypical Bovine Spongiform Encephalopathy prions and also to mouse-adapted Scrapie prions. This information must be taken into account when assessing the risk of using ruminant derived protein as a protein source to feed rabbits.
Zdroje
1. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science (80-). 1982;216: 136–144. 6801762
2. Prusiner SB. Prions. Proc Natl Acad Sci U S A. 1998;95: 13363–13383. 9811807
3. Bruce ME, Will RG, Ironside JW, McConnell I, Drummond D, Suttie A, et al. Transmissions to mice indicate that “new variant” CJD is caused by the BSE agent. Nature. 1997;389: 498–501. 9333239
4. Eloit M, Adjou K, Coulpier M, Fontaine JJ, Hamel R, Lilin T, et al. BSE agent signatures in a goat. Vet Rec. 2005;156: 523–524.
5. Pearson GR, Gruffydd-Jones TJ, Wyatt JM, Hope J, Chong A, Scott AC, et al. Feline spongiform encephalopathy. Vet Rec. 1991;128: 532.
6. Stack MJ, Chaplin MJ, Clark J. Differentiation of prion protein glycoforms from naturally occurring sheep scrapie, sheep-passaged scrapie strains (CH1641 and SSBP1), bovine spongiform encephalopathy (BSE) cases and Romney and Cheviot breed sheep experimentally inoculated with BSE using. Acta Neuropathol. 2002;104: 279–286. 12172914
7. Bellworthy SJ, Dexter G, Stack M, Chaplin M, Hawkins SA, Simmons MM, et al. Oral transmission of BSE to VRQ/VRQ sheep in an experimental flock. Vet Rec. 2008;162: 130–131. 18223273
8. Pearson GR, Wyatt JM, Gruffydd-Jones TJ, Hope J, Chong A, Higgins RJ, et al. Feline spongiform encephalopathy: fibril and PrP studies. Vet Rec. 1992;131: 307–310. 1279883
9. Bartz JC, Marsh RF, McKenzie DI, Aiken JM. The host range of chronic wasting disease is altered on passage in ferrets. Virology. 1998;251: 297–301. doi: 10.1006/viro.1998.9427 9837794
10. Lezmi S, Bencsik A, Monks E, Petit T, Baron T. First case of feline spongiform encephalopathy in a captive cheetah born in France: PrP(sc) analysis in various tissues revealed unexpected targeting of kidney and adrenal gland. Histochem Cell Biol. 2003;119: 415–422. 12783238
11. Poser CM. Notes on the history of the prion diseases. Part I. Clin Neurol Neurosurg. 2002;104: 1–9. 11792469
12. Wells GA, Wilesmith JW. The neuropathology and epidemiology of bovine spongiform encephalopathy. Brain Pathol. 1995;5: 91–103. 7767494
13. Wyatt JM, Pearson GR, Smerdon TN, Gruffydd-Jones TJ, Wells GA, Wilesmith JW. Naturally occurring scrapie-like spongiform encephalopathy in five domestic cats. Vet Rec. 1991;129: 233–236. 1957458
14. Barlow RM. Transmissible mink encephalopathy: pathogenesis and nature of the aetiological agent. J Clin Pathol Suppl (R Coll Pathol). 1972;6: 102–109.
15. Gajdusek DC. Unconventional viruses and the origin and disappearance of kuru. Science (80-). 1977;197: 943–960. 142303
16. Williams ES. Chronic wasting disease. Vet Pathol. 2005;42: 530–549. 16145200
17. Biacabe A-G, Laplanche J-L, Ryder S, Baron T. Distinct molecular phenotypes in bovine prion diseases. EMBO Rep. 2004;5: 110–5. 14710195
18. Casalone C, Zanusso G, Acutis P, Ferrari S, Capucci L, Tagliavini F, et al. Identification of a second bovine amyloidotic spongiform encephalopathy: Molecular similarities with sporadic Creutzfeldt-Jakob disease. PNAS. 2004;101:3065–3070. 14970340
19. Le Dur A, Beringue V, Andreoletti O, Reine F, Lai TL, Baron T, et al. A newly identified type of scrapie agent can naturally infect sheep with resistant PrP genotypes. Proc Natl Acad Sci U S A. 2005;102: 16031–16036. 16239348
20. Benestad SL, Sarradin P, Thu B, Schönheit J, Tranulis M a, Bratberg B. Cases of scrapie with unusual features in Norway and designation of a new type, Nor98. Vet Rec. 2003;153: 202–8. 12956297
21. Fernández-Borges N, Chianini F, Eraña H, Vidal E, Eaton SL, Pintado B, et al. Naturally prion resistant mammals: a utopia? Prion. 2012;6: 425–9. doi: 10.4161/pri.22057 22954650
22. Chianini F, Fernández-Borges N, Eraña H, Pang Y, Vidal E, Eaton SL, et al. Prion-resistant or prion-susceptible species, this is the question. Virulence. Landes Bioscience; 2013;4: 333–334. doi: 10.4161/viru.24456
23. Chianini F, Fernandez-Borges N, Vidal E, Gibbard L, Pintado B, de Castro J, et al. Rabbits are not resistant to prion infection. Proceedings of the National Academy of Sciences. 2012;109;5080–5085.
24. Di Bari MA, Chianini F, Vaccari G, Esposito E, Conte M, Eaton SL, et al. The bank vole (Myodes glareolus) as a sensitive bioassay for sheep scrapie. J Gen Virol. 2008;89: 2975–2985. doi: 10.1099/vir.0.2008/005520-0 19008382
25. Espinosa JC, Herva ME, Andréoletti O, Padilla D, Lacroux C, Cassard H, et al. Transgenic mice expressing porcine prion protein resistant to classical scrapie but susceptible to sheep bovine spongiform encephalopathy and atypical scrapie. Emerg Infect Dis. 2009;15: 1214–21. doi: 10.3201/eid1508.081218 19751582
26. Fernández-Borges N, de Castro J, Castilla J. In vitro studies of the transmission barrier. Prion. 2009;3: 220–3. 20009509
27. Kurt TD, Seelig DM, Schneider JR, Johnson CJ, Telling GC, Heisey DM, et al. Alteration of the chronic wasting disease species barrier by in vitro prion amplification. J Virol. 2011;85: 8528–37. doi: 10.1128/JVI.00809-11 21697475
28. Le Dur A, Béringue V, Andréoletti O, Reine F, Laï TL, Baron T, et al. A newly identified type of scrapie agent can naturally infect sheep with resistant PrP genotypes. Proc Natl Acad Sci U S A. 2005;102: 16031–6. 16239348
29. 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: 835–843. 17079295
30. 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. doi: 10.1371/journal.ppat.1001319 21445238
31. Stewart P, Campbell L, Skogtvedt S, Griffin K a, Arnemo JM, Tryland M, et al. Genetic predictions of prion disease susceptibility in carnivore species based on variability of the prion gene coding region. PLoS One. 2012;7: e50623. doi: 10.1371/journal.pone.0050623 23236380
32. Vorberg I, Groschup MH, Pfaff E, Priola SA. Multiple amino acid residues within the rabbit prion protein inhibit formation of its abnormal isoform. J Virol. 2003;77: 2003–2009. 12525634
33. Zhang J. The Structural Stability of Wild-type Horse Prion Protein. J Biomol Struct Dyn. 2011;29: 369–377. 21875155
34. Barlow RM, Rennie JC. The fate of ME7 scrapie infection in rats, guinea-pigs and rabbits. Res Vet Sci. 1976;21: 110–111. 821118
35. Gibbs CJ, Gajdusek DC. Experimental subacute spongiform virus encephalopathies in primates and other laboratory animals. Science. 1973;182: 67–68. 4199733
36. Vidal E, Fernández-Borges N, Pintado B, Ordóñez M, Márquez M, Fondevila D, et al. Bovine spongiform encephalopathy induces misfolding of alleged prion-resistant species cellular prion protein without altering its pathobiological features. J Neurosci. 2013;33: 7778–86. doi: 10.1523/JNEUROSCI.0244-13.2013 23637170
37. Sarradin P, Viglietta C, Limouzin C, Andreoletti O, Daniel-Carlier N, Barc C, et al. Transgenic rabbits expressing ovine PrP are susceptible to scrapie. PLoS Pathog. 2015;11:e1005077.
38. Lombardi G, Casalone C, A DA, Gelmetti D, Torcoli G, Barbieri I, et al. Intraspecies transmission of BASE induces clinical dullness and amyotrophic changes. PLoS Pathog. 2008;4: e1000075. doi: 10.1371/journal.ppat.1000075 18497860
39. Westaway D, DeArmond SJ, Cayetano-Canlas J, Groth D, Foster D, Yang SL, et al. Degeneration of skeletal muscle, peripheral nerves, and the central nervous system in transgenic mice overexpressing wild-type prion proteins. Cell. 1994;76: 117–29. 8287472
40. Castilla J, Gutierrez Adan A, Brun A, Pintado B, Ramirez MA, Parra B, et al. Early detection of PrPres in BSE-infected bovine PrP transgenic mice. Arch Virol. 2003;148: 677–691. 12664293
41. Fischer M, Rülicke T, Raeber A, Sailer A, Moser M, Oesch B, et al. Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 1996;15: 1255–64f. 8635458
42. Castilla J, Saa P, Morales R, Abid K, Maundrell K, Soto C. Protein misfolding cyclic amplification for diagnosis and prion propagation studies. Methods Enzym. 2006;412: 3–21.
43. Saa P, Castilla J, Soto C. Cyclic amplification of protein misfolding and aggregation. Methods Mol Biol. 2005;299: 53–65. 15980595
44. Castilla J, Saá P, Hetz C, Soto C. In vitro generation of infectious scrapie prions. Cell. 2005;121: 195–206. 15851027
45. 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: 159–163. 9117892
46. Castilla J, Gutiérrez Adán a, Brun a, Pintado B, Ramírez M a, Parra B, et al. Early detection of PrPres in BSE-infected bovine PrP transgenic mice. Arch Virol. 2003;148: 677–91. 12664293
47. Scott M, Foster D, Mirenda C, Serban D, Coufal F, Walchli M, et al. Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell. 1989;59: 847–857. 2574076
48. Siso S, Ordoñez M, Cordón I, Vidal E, Pumarola M. Distribution of PrPres in the brains of BSE-affected cows detected by active surveillance in Catalonia, Spain. Vet Rec. 2004;155: 524–525. 15551927
49. Vidal E, Marquez M, Ordonez M, Raeber AJ, Struckmeyer T, Oesch B, et al. Comparative study of the PrPBSE distribution in brains from BSE field cases using rapid tests. J Virol Methods. 2005;127: 24–32. 15893562
50. Douet J-Y, Lacroux C, Corbière F, Litaise C, Simmons H, Lugan S, et al. PrP expression level and sensitivity to Prion infection. J Virol. 2014; 88:5870–5872. doi: 10.1128/JVI.00369-14 24574409
51. 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. doi: 10.1371/journal.ppat.1001319 21445238
52. Pirisinu L, Marcon S, Bari M, D’Agostino C, Agrimi U, Nonno R. Biochemical Characterization of Prion Strains in Bank Voles. Pathogens. Multidisciplinary Digital Publishing Institute; 2013;2: 446–456. doi: 10.3390/pathogens2030446 25437201
53. 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. Westaway D, editor. PLoS Pathog. Public Library of Science; 2006;2: e12. 16518470
54. CHANDLER RL. Encephalopathy in mice produced by inoculation with scrapie brain material. Lancet. 1961;1: 1378–9. 13692303
55. Dickinson AG, Meikle VM. A comparison of some biological characteristics of the mouse-passaged scrapie agents, 22A and ME7. Genet Res. 1969;13: 213–25. 4978935
56. Saunders SE, Bartelt-Hunt SL, Bartz JC. Occurrence, transmission, and zoonotic potential of chronic wasting disease. Emerg Infect Dis. 2012;18: 369–76. doi: 10.3201/eid1803.110685 22377159
57. Hamir AN, Kehrli ME, Kunkle RA, Greenlee JJ, Nicholson EM, Richt JA, et al. Experimental interspecies transmission studies of the transmissible spongiform encephalopathies to cattle: comparison to bovine spongiform encephalopathy in cattle. J Vet Diagn Invest. 2011;23: 407–20. doi: 10.1177/1040638711403404 21908269
58. Race B, Meade-White KD, Miller MW, Barbian KD, Rubenstein R, LaFauci G, et al. Susceptibilities of nonhuman primates to chronic wasting disease. Emerg Infect Dis. 2009;15: 1366–76. doi: 10.3201/eid1509.090253 19788803
59. Mathiason CK, Nalls A V, Seelig DM, Kraft SL, Carnes K, Anderson KR, et al. Susceptibility of domestic cats to chronic wasting disease. J Virol. 2013;87: 1947–56. doi: 10.1128/JVI.02592-12 23236066
60. Raymond GJ, Raymond LD, Meade-White KD, Hughson AG, Favara C, Gardner D, et al. Transmission and adaptation of chronic wasting disease to hamsters and transgenic mice: evidence for strains. J Virol. 2007;81: 4305–14. 17287284
61. Harrington RD, Baszler T V, O’Rourke KI, Schneider DA, Spraker TR, Liggitt HD, et al. A species barrier limits transmission of chronic wasting disease to mink (Mustela vison). J Gen Virol. 2008;89: 1086–96. doi: 10.1099/vir.0.83422-0 18343853
62. Heisey DM, Mickelsen NA, Schneider JR, Johnson CJ, Johnson CJ, Langenberg JA, et al. Chronic wasting disease (CWD) susceptibility of several North American rodents that are sympatric with cervid CWD epidemics. J Virol. 2010;84: 210–5. doi: 10.1128/JVI.00560-09 19828611
63. Sigurdson CJ, Manco G, Schwarz P, Liberski P, Hoover EA, Hornemann S, et al. Strain fidelity of chronic wasting disease upon murine adaptation. J Virol. 2006;80: 12303–11. 17020952
64. Lee Y-H, Sohn H-J, Kim M-J, Kim H-J, Park K-J, Lee W-Y, et al. Experimental chronic wasting disease in wild type VM mice. J Vet Med Sci. 2013;75: 1107–10. 23708962
65. Baron T, Biacabe AG, Arsac JN, Benestad S, Groschup MH. Atypical transmissible spongiform encephalopathies (TSEs) in ruminants. Vaccine. 2006; 22(6):823–42.
66. Benestad SL, Sarradin P, Thu B, Schonheit J, Tranulis MA, Bratberg B. Cases of scrapie with unusual features in Norway and designation of a new type, Nor98. Vet Rec. 2003;153: 202–208. 12956297
67. Green R, Horrocks C, Wilkinson A, Hawkins SA, Ryder SJ. Primary Isolation of the Bovine Spongiform Encephalopathy Agent in Mice: Agent Definition based on a Review of 150 Transmissions. J Comp Pathol. 2005;132: 117–131. 15737338
68. Lloyd SE, Linehan JM, Desbruslais M, Joiner S, Buckell J, Brandner S, et al. Characterization of two distinct prion strains derived from bovine spongiform encephalopathy transmissions to inbred mice. J Gen Virol. 2004;85: 2471–8. 15269389
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2015 Číslo 8
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Human Non-neutralizing HIV-1 Envelope Monoclonal Antibodies Limit the Number of Founder Viruses during SHIV Mucosal Infection in Rhesus Macaques
- Type VI Secretion System Toxins Horizontally Shared between Marine Bacteria
- Are Human Intestinal Eukaryotes Beneficial or Commensals?
- Illuminating Targets of Bacterial Secretion