1887

Journal of General Virology header logo

Volume 90, Issue 1

Alteration of the biological and biochemical characteristics of bovine spongiform encephalopathy prions during interspecies transmission in transgenic mice models Free

Abstract

In the interspecies transmission of prions, the species barrier influences the susceptibility of the host. Bovine spongiform encephalopathy (BSE) prions affect a wide range of host species but do not affect hamsters. In order to study this species barrier, this study analysed the transmissibility of BSE prions to several lines of transgenic (Tg) mice, including those expressing mouse and hamster chimeric prion proteins (MH2M and MHM2 mice). BSE prions were transmitted to tga20, MHM2 and ICR mice, and the incubation period was approximately 400 days. Thus, these mice were classified as ‘susceptible mice’. However, BSE prions were not transmitted to MH2M and TgHaNSE mice, and these mice were classified as ‘resistant mice’. After the BSE prions were passaged once in wild-type mice, they could be transmitted to resistant mice. The characteristics of the accumulated abnormal isoform of PrP (PrP) in susceptible and resistant mice were determined using Western blotting. A BSE-like glycoform pattern of PrP was detected in all of the susceptible mice using two different antibodies that recognized either the N- or the C-terminal end of the 27–30 kDa protease-resistant fragment of PrP (PrP) as the epitope. In contrast, proteinase digestion followed by deglycosylation analysis showed that, in addition to PrP, truncated PrP fragments existed in resistant mice. These mixed PrP fragments may have resulted from the adaptation of resistant mice to BSE prions.

  • Received:
  • Accepted:
  • Published Online:
© SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.004754-0
2009-01-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/1/261.html?itemId=/content/journal/jgv/10.1099/vir.0.004754-0&mimeType=html&fmt=ahah

References

  1. Baker, H. F., Ridley, R. M., Wells, G. A. & Ironside, J. W.(1998). Prion protein immunohistochemical staining in the brains of monkeys with transmissible spongiform encephalopathy. Neuropathol Appl Neurobiol 24, 476–486.[CrossRef] [Google Scholar]
  2. Biacabe, A. G., Laplanche, J. L., Ryder, S. & Baron, T.(2004). Distinct molecular phenotypes in bovine prion diseases. EMBO Rep 5, 110–114.[CrossRef] [Google Scholar]
  3. Bons, N., Mestre-Frances, N., Belli, P., Cathala, F., Gajdusek, D. C. & Brown, P.(1999). Natural and experimental oral infection of nonhuman primates by bovine spongiform encephalopathy agents. Proc Natl Acad Sci U S A 96, 4046–4051.[CrossRef] [Google Scholar]
  4. Buschmann, A., Gretzschel, A., Biacabe, A. G., Schiebel, K., Corona, C., Hoffmann, C., Eiden, M., Baron, T., Casalone, C. & Groschup, M. H.(2006). Atypical BSE in Germany – proof of transmissibility and biochemical characterization. Vet Microbiol 117, 103–116.[CrossRef] [Google Scholar]
  5. Casalone, C., Zanusso, G., Acutis, P., Ferrari, S., Capucci, L., Tagliavini, F., Monaco, S. & Caramelli, M.(2004). Identification of a second bovine amyloidotic spongiform encephalopathy: molecular similarities with sporadic Creutzfeldt–Jakob disease. Proc Natl Acad Sci U S A 101, 3065–3070.[CrossRef] [Google Scholar]
  6. Collinge, J., Sidle, K. C. L., Meads, J., Ironside, J. & Hill, A. F.(1996). Molecular analysis of prion strain variation and the aetiology of ‘new variant’ CJD. Nature 383, 685–690.[CrossRef] [Google Scholar]
  7. Espinosa, J. C., Andréoletti, O., Castilla, J., Herva, M. E., Morales, M., Alamillo, E., San-Segundo, F. D., Lacroux, C., Lugan, S. & other authors(2007). Sheep-passaged bovine spongiform encephalopathy agent exhibits altered pathobiological properties in bovine-PrP transgenic mice. J Virol 81, 835–843.[CrossRef] [Google Scholar]
  8. Fischer, M., Rülicke, T., Raeber, A., Sailer, A., Moser, M., Oesch, B., Brandner, S., Aguzzi, A. & Weissmann, C.(1996). Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J 15, 1255–1264. [Google Scholar]
  9. Foster, J. D., Hope, J. & Fraser, H.(1993). Transmission of bovine spongiform encephalopathy to sheep and goats. Vet Rec 133, 339–341.[CrossRef] [Google Scholar]
  10. Fraser, H., Bruce, M. E., Chree, A., McConnell, I. & Wells, G. A. H.(1992). Transmission of bovine spongiform encephalopathy and scrapie to mice. J Gen Virol 73, 1891–1897.[CrossRef] [Google Scholar]
  11. Goldmann, W., Martin, T., Foster, J., Hughes, S., Smith, G., Hughes, K., Dawson, M. & Hunter, N.(1996). Novel polymorphisms in the caprine PrP gene: a codon 142 mutation associated with scrapie incubation period. J Gen Virol 77, 2885–2891.[CrossRef] [Google Scholar]
  12. Hayashi, H. K., Yokoyama, T., Takata, M., Iwamaru, Y., Imamura, M., Ushiki, Y. K. & Shinagawa, M.(2005). The N-terminal cleavage site of PrPSc from BSE differs from that of PrPSc from scrapie. Biochem Biophys Res Commun 328, 1024–1027.[CrossRef] [Google Scholar]
  13. Hill, A. F., Desbruslais, M., Joiner, S., Sidle, K. C. L., Gowland, I., Collinge, J., Doey, L. J. & Lantos, P.(1997). The same prion strain causes vCJD and BSE. Nature 389, 448–450.[CrossRef] [Google Scholar]
  14. Hill, A. F., Joiner, S., Linehan, J., Desbruslais, M., Lantos, P. L. & Collinge, J.(2000). Species-barrier-independent prion replication in apparently resistant species. Proc Natl Acad Sci U S A 97, 10248–10253.[CrossRef] [Google Scholar]
  15. Horiuchi, M., Yamazaki, N., Ikeda, T., Ishiguro, N. & Shinagawa, M.(1995). A cellular form of prion protein (PrPC) exists in many non-neuronal tissues of sheep. J Gen Virol 76, 2583–2587.[CrossRef] [Google Scholar]
  16. Hunter, N., Moore, L., Hosie, B. D., Dingwall, W. S. & Greig, A.(1997). Association between natural scrapie and PrP genotype in a flock of Suffolk sheep in Scotland. Vet Rec 140, 59–63.[CrossRef] [Google Scholar]
  17. Jacobs, J. G., Langeveld, J. P. M., Biacabe, A. G., Acutis, P. L., Polak, M. P., Gavier-Widen, D., Buschmann, A., Caramelli, M., Casalone, C. & other authors(2007). Molecular discrimination of atypical bovine spongiform encephalopathy strains from a geographical region spanning a wide area in Europe. J Clin Microbiol 45, 1821–1829.[CrossRef] [Google Scholar]
  18. Kim, C. L., Umetani, A., Matsui, T., Ishiguro, N., Shinagawa, M. & Horiuchi, M.(2004). Antigenic characterization of an abnormal isoform of prion protein using a new diverse panel of monoclonal antibodies. Virology 320, 40–51.[CrossRef] [Google Scholar]
  19. Kimberlin, R. H.(1991). Agent host interactions and pathogenesis. In Sub-acute Spongiform Encephalopathies, pp. 137–147. Edited by R. Bradley, M. Savey & B. Marchant. Dordrecht: Kluwer Academic Publishers.
  20. Kirkwood, J. K. & Cunningham, A. A.(1994). Epidemiological observations on spongiform encephalopathies in captive wild animals in the British Isles. Vet Rec 135, 296–303.[CrossRef] [Google Scholar]
  21. Kobayashi, A., Asano, M., Mohri, S. & Kitamoto, T.(2007). Cross-sequence transmission of sporadic Creutzfeldt–Jakob disease creates a new prion strain. J Biol Chem 282, 30022–30028.[CrossRef] [Google Scholar]
  22. Lasmézas, C. I., Deslys, J. P., Demaimay, R., Adjou, K. T., Lamoury, F., Dormont, D., Robain, O., Ironside, J. & Hauw, J. J.(1996). BSE transmission to macaques. Nature 381, 743–744.[CrossRef] [Google Scholar]
  23. Moore, R. A., Vorberg, I. & Priola, S. A.(2005). Species barriers in prion diseases – brief review. Arch Virol Suppl 19, 187–202. [Google Scholar]
  24. Priola, S. A., Chabry, J. & Chan, K.(2001). Efficient conversion of normal prion protein (PrP) by abnormal hamster PrP is determined by homology at amino acid residue 155. J Virol 75, 4673–4680.[CrossRef] [Google Scholar]
  25. Prusiner, S. B.(1991). Molecular biology of prion diseases. Science 252, 1515–1522.[CrossRef] [Google Scholar]
  26. Race, R. E., Priola, S. A., Bessen, R. A., Ernst, D., Dockter, J., Rall, G. F., Mucke, L., Chesebro, B. & Oldstone, M. B.(1995). Neuron-specific expression of a hamster prion protein minigene in transgenic mice induces susceptibility to hamster scrapie agent. Neuron 15, 1183–1191.[CrossRef] [Google Scholar]
  27. Robinson, M. M., Hadlow, W. J., Huff, T. P., Wells, G. A. H., Dawson, M., Marsh, R. F. & Gorham, J. R.(1994). Experimental infection of mink with bovine spongiform encephalopathy. J Gen Virol 75, 2151–2155.[CrossRef] [Google Scholar]
  28. Scott, M., Foster, D., Mirenda, C., Serban, D., Coufal, F., Wälchli, M., Torchia, M., Groth, D., Carlson, G. & other authors(1989). Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell 59, 847–857.[CrossRef] [Google Scholar]
  29. Scott, M., Groth, D., Foster, D., Torchia, M., Yang, S. L., DeArmond, S. J. & Prusiner, S. B.(1993). Propagation of prions with artificial properties in transgenic mice expressing chimeric PrP genes. Cell 73, 979–988.[CrossRef] [Google Scholar]
  30. Scott, M. R., Safar, J., Telling, G., Nguyen, O., Groth, D., Torchia, M., Koehler, R., Tremblay, P., Walther, D. & other authors(1997). Identification of a prion protein epitope modulating transmission of bovine spongiform encephalopathy prions to transgenic mice. Proc Natl Acad Sci U S A 94, 14279–14284.[CrossRef] [Google Scholar]
  31. Wells, G. A. H. & Wilesmith, J. W.(1995). The neuropathology and epidemiology of bovine spongiform encephalopathy. Brain Pathol 5, 91–103.[CrossRef] [Google Scholar]
  32. Westaway, D., Goodman, P. A., Mirenda, C. A., McKinley, M. P., Carlson, G. A. & Prusiner, S. B.(1987). Distinct prion proteins in short and long scrapie incubation period mice. Cell 51, 651–662.[CrossRef] [Google Scholar]
  33. Wyatt, J. M., Pearson, G. R., Smerdon, T. N., Gruffydd-Jones, T. J. & Wells, G. A. H.(1990). Spongiform encephalopathy in cat. Vet Rec 126, 513 [Google Scholar]
  34. Wyatt, J. M., Pearson, G. R., Smerdon, T. N., Gruffydd-Jones, T. J., Wells, G. A. H. & Wilesmith, J. W.(1991). Naturally occurring scrapie-like spongiform encephalopathy in five domestic cats. Vet Rec 129, 233–236.[CrossRef] [Google Scholar]
  35. Yamakawa, Y., Hagiwara, K., Nohtomi, K., Nakamura, Y., Nishijima, M., Higuchi, Y., Sato, Y., Sata, T. & The Expert Committee for BSE diagnosis, Ministry of Health, Labour and Welfare of Japan(2003). Atypical proteinase K-resistant prion protein (PrPres) observed in an apparently healthy 23-month-old Holstein steer. Jpn J Infect Dis 56, 221–222. [Google Scholar]
  36. Yokoyama, T., Kimura, K., Tagawa, Y. & Yuasa, N.(1995). Preparation and characterization of antibodies against mouse prion protein (PrP) peptides. Clin Diagn Lab Immunol 2, 172–176. [Google Scholar]
  37. Yokoyama, T., Kimura, K. M., Ushiki, Y., Yamada, S., Morooka, A., Nakashiba, T., Sassa, T. & Itohara, S.(2001).In vivo conversion of cellular prion protein to pathogenic isoforms, as monitored by conformation-specific antibodies. J Biol Chem 276, 11265–11271.[CrossRef] [Google Scholar]
  38. Yokoyama, T., Msujin, K., Yamakawa, Y., Sata, T., Murayama, Y., Shu, Y., Okada, H., Mohri, S. & Shinagawa, M.(2007a). Experimental transmission of two young and one suspended bovine spongiform encephalopathy (BSE) cases to bovinized transgenic mice. Jpn J Infect Dis 60, 317–320. [Google Scholar]
  39. Yokoyama, T., Shimada, K., Masujin, K., Iwamaru, Y., Imamura, M., Ushiki, Y. K., Kimura, K. M., Itohara, S. & Shinagawa, M.(2007b). Both host prion protein 131–188 subregion and prion strain characteristics regulate glycoform of PrPSc. Arch Virol 152, 603–609.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.004754-0
Loading
Alteration of the biological and biochemical characteristics of bovine spongiform encephalopathy prions during interspecies transmission in transgenic mice models
J. Gen. Virol. 90, 261 (2009); https://doi.org/10.1099/vir.0.004754-0
/content/journal/jgv/10.1099/vir.0.004754-0
/content/journal/jgv/10.1099/vir.0.004754-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error