1887

Abstract

Sheep with an ARQ/ARQ genotype at codon positions 136/154/171 are highly susceptible to experimental infection with bovine spongiform encephalopathy (BSE). However, a number of sheep challenged orally or intracerebrally with BSE were clinically asymptomatic and found to survive or were diagnosed as BSE-negative when culled. Sequencing of the full gene open reading frame of BSE-susceptible and -resistant sheep indicated that, in the majority of Suffolk sheep, resistance was associated with an M112T variant (TARQ allele). A high proportion (47 of 49; 96 %) of BSE-challenged wild-type (MARQ/MARQ) Suffolk sheep were BSE-infected, whereas none of the 20 sheep with at least one TARQ allele succumbed to BSE. Thirteen TARQ-carrying sheep challenged with BSE are still alive and some have survival periods equivalent to, or greater than, reported incubation periods of BSE in ARR/ARR and VRQ/VRQ sheep.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.012724-0
2009-10-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/10/2569.html?itemId=/content/journal/jgv/10.1099/vir.0.012724-0&mimeType=html&fmt=ahah

References

  1. Andréoletti O., Morel N., Lacroux C., Rouillon V., Barc C., Tabouret G., Sarradin P., Berthon P., Bernardet P. other authors 2006; Bovine spongiform encephalopathy agent in spleen from an ARR/ARR orally exposed sheep. J Gen Virol 87:1043–1046 [CrossRef]
    [Google Scholar]
  2. Babar M. E., Farid A., Benkel B. F., Ahmad J., Nadeem A., Imran M. 2009; Frequencies of PrP genotypes and their implication for breeding against scrapie susceptibility in nine Pakistani sheep breeds. Mol Biol Rep 36:561–565 [CrossRef]
    [Google Scholar]
  3. Baylis M. 2002; The BSE-susceptible proportion of UK sheep. Vet Rec 151:481–482 [CrossRef]
    [Google Scholar]
  4. Bellworthy S. J., Hawkins S. A., Green R. B., Blamire I., Dexter G., Dexter I., Lockey R., Jeffrey M., Ryder S. & other authors (2005a). 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 [CrossRef]
    [Google Scholar]
  5. Bellworthy S. J., Dexter G., Stack M., Chaplin M., Hawkins S. A., Simmons M. M., Jeffrey M., Martin S., Gonzalez L. other authors 2005b; Natural transmission of BSE between sheep within an experimental flock. Vet Rec 157:206 [CrossRef]
    [Google Scholar]
  6. Bellworthy S. J., Dexter G., Stack M., Chaplin M., Hawkins S. A., Simmons M. M., Jeffrey M., Martin S., Gonzalez L. other authors 2008; Oral transmission of BSE to VRQ/VRQ sheep in an experimental flock. Vet Rec 162:130–131
    [Google Scholar]
  7. Bossers A., de Vries R., Smits M. A. 2000; Susceptibility of sheep for scrapie as assessed by in vitro conversion of nine naturally occurring variants of PrP. J Virol 74:1407–1414 [CrossRef]
    [Google Scholar]
  8. Bruce M. E., Will R. G., Ironside J. W., McConnell I., Drummond D., Suttie A., McCardle L., Chree A., Hope J. other authors 1997; Transmissions to mice indicate that ‘new variant’ CJD is caused by the BSE agent. Nature 389:498–501 [CrossRef]
    [Google Scholar]
  9. Collinge J., Sidle K. C., 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]
  10. Eloit M., Adjou K., Coulpier M., Fontaine J. J., Hamel R., Lilin T., Messiaen S., Andréoletti O., Baron T. other authors 2005; BSE agent signatures in a goat. Vet Rec 156:523–524
    [Google Scholar]
  11. Ferguson N. M., Ghani A. C., Donnelly C. A., Hagenaars T. J., Anderson R. M. 2002; Estimating the human health risk from possible BSE infection of the British sheep flock. Nature 415:420–424 [CrossRef]
    [Google Scholar]
  12. Foster J. D., Parnham D. W., Hunter N., Bruce M. 2001a; Distribution of the prion protein in sheep terminally affected with BSE following experimental oral transmission. J Gen Virol 82:2319–2326
    [Google Scholar]
  13. Foster J. D., Parnham D., Chong A., Goldmann W., Hunter N. 2001b; Clinical signs, histopathology and genetics of experimental transmission of BSE and natural scrapie to sheep and goats. Vet Rec 148:165–171 [CrossRef]
    [Google Scholar]
  14. Fryer H. R., Baylis M., Sivam K., McLean A. R. 2007; Quantifying the risk from ovine BSE and the impact of control strategies. Proc Biol Sci 274:1497–1503 [CrossRef]
    [Google Scholar]
  15. Gavier-Widén D., Stack M. J., Baron T., Balachandran A., Simmons M. 2005; Diagnosis of transmissible spongiform encephalopathies in animals: a review. J Vet Diagn Invest 17:509–527 [CrossRef]
    [Google Scholar]
  16. 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 75:989–995 [CrossRef]
    [Google Scholar]
  17. Goldmann W., Baylis M., Chihota C., Stevenson E., Hunter N. 2005; Frequencies of PrP gene haplotypes in British sheep flocks and the implications for breeding programmes. J Appl Microbiol 98:1294–1302 [CrossRef]
    [Google Scholar]
  18. Goldmann W., Houston F., Stewart P., Perucchini M., Foster J., Hunter N. 2006; Ovine prion protein variant A136R154L168Q171 increases resistance to experimental challenge with bovine spongiform encephalopathy agent. J Gen Virol 87:3741–3745 [CrossRef]
    [Google Scholar]
  19. Gombojav A., Ishiguro N., Horiuchi M., Shinagawa M. 2004; Unique amino acid polymorphisms of PrP genes in Mongolian sheep breeds. J Vet Med Sci 66:1293–1295 [CrossRef]
    [Google Scholar]
  20. Heaton M. P., Leymaster K. A., Freking B. A., Hawk D. A., Smith T. P., Keele J. W., Snelling W. M., Fox J. M., Chitko-McKown C. G. other authors 2003; Prion gene sequence variation within diverse groups of U.S. sheep, beef cattle, and deer. Mamm Genome 14:765–777 [CrossRef]
    [Google Scholar]
  21. Hill A. F., Desbruslais M., Joiner S., Sidle K. C., 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]
  22. Houston F., Foster J. D., Chong A., Hunter N., Bostock C. J. 2000; Transmission of BSE by blood transfusion in sheep. Lancet 356:999–1000 [CrossRef]
    [Google Scholar]
  23. Houston F., Goldmann W., Chong A., Jeffrey M., González L., Foster J., Parnham D., Hunter N. 2003; Prion diseases: BSE in sheep bred for resistance to infection. Nature 423:498 [CrossRef]
    [Google Scholar]
  24. Hunter N. 2003; Scrapie and experimental BSE in sheep. Br Med Bull 66:171–183 [CrossRef]
    [Google Scholar]
  25. Ikeda T., Horiuchi M., Ishiguro N., Muramatsu Y., Kai-Uwe G. D., Shinagawa M. 1995; Amino acid polymorphisms of PrP with reference to onset of scrapie in Suffolk and Corriedale sheep in Japan. J Gen Virol 76:2577–2581 [CrossRef]
    [Google Scholar]
  26. Jeffrey M., Ryder S., Martin S., Hawkins S. A., Terry L., Berthelin-Baker C., Bellworthy S. J. 2001; Oral inoculation of sheep with the agent of bovine spongiform encephalopathy (BSE). 1. Onset and distribution of disease-specific PrP accumulation in brain and viscera. J Comp Pathol 124:280–289 [CrossRef]
    [Google Scholar]
  27. Jeffrey M., Martin S., González L., Foster J., Langeveld J. P., van Zijderveld F. G., Grassi J., Hunter N. 2006; Immunohistochemical features of PrPd accumulation in natural and experimental goat transmissible spongiform encephalopathies. J Comp Pathol 134:171–181 [CrossRef]
    [Google Scholar]
  28. Kao R. R., Gravenor M. B., Baylis M., Bostock C. J., Chihota C. M., Evans J. C., Goldmann W., Smith A. J., McLean A. R. 2002; The potential size and duration of an epidemic of bovine spongiform encephalopathy in British sheep. Science 295:332–335 [CrossRef]
    [Google Scholar]
  29. Kao R. R., Houston F., Baylis M., Chihota C. M., Goldmann W., Gravenor M. B., Hunter N., McLean A. R. 2003; Epidemiological implications of the susceptibility to BSE of putatively resistant sheep. J Gen Virol 84:3503–3512 [CrossRef]
    [Google Scholar]
  30. Laegreid W. W., Clawson M. L., Heaton M. P., Green B. T., O'Rourke K. I., Knowles D. P. 2008; Scrapie resistance in ARQ sheep. J Virol 82:10318–10320 [CrossRef]
    [Google Scholar]
  31. Lan Z., Wang Z. L., Liu Y., Zhang X. 2006; Prion protein gene (PRNP) polymorphisms in Xinjiang local sheep breeds in China. Arch Virol 151:2095–2101 [CrossRef]
    [Google Scholar]
  32. Laplanche J. L., Chatelain J., Westaway D., Thomas S., Dussaucy M., Brugere-Picoux J., Launay J. M. 1993; PrP polymorphisms associated with natural scrapie discovered by denaturing gradient gel electrophoresis. Genomics 15:30–37 [CrossRef]
    [Google Scholar]
  33. Moum T., Olsaker I., Hopp P., Moldal T., Valheim M., Moum T., Benestad S. L. 2005; Polymorphisms at codons 141 and 154 in the ovine prion protein gene are associated with scrapie Nor98 cases. J Gen Virol 86:231–235 [CrossRef]
    [Google Scholar]
  34. Ohara J., Togari T., Kurokawa A., Maeda J., Ishiguro N., Furuoka H., Horiuchi M. 2007; Frequencies of PrP genotypes in meat breeds of Japanese sheep and trail of selective breeding in experimental sheep flock. J Vet Med Sci 69:1325–1329 [CrossRef]
    [Google Scholar]
  35. Prusiner S. B. 1982; Novel proteinaceous particles cause scrapie. Science 216:136–144 [CrossRef]
    [Google Scholar]
  36. Ronzon F., Bencsik A., Lezmi S., Vulin J., Kodjo A., Baron T. 2006; BSE inoculation to prion diseases-resistant sheep reveals tricky silent carriers. Biochem Biophys Res Commun 350:872–877 [CrossRef]
    [Google Scholar]
  37. Saunders G. C., Cawthraw S., Mountjoy S., Hope J., Windl O. 2006; PrP genotypes of atypical scrapie cases in Great Britain. J Gen Virol 87:3141–3149 [CrossRef]
    [Google Scholar]
  38. Saunders G. C., Cawthraw S., Mountjoy S. J., Tout A. C., Sayers A. R., Hope J., Windl O. 2009; Ovine PRNP untranslated region and promoter haplotype diversity. J Gen Virol 90:1289–1293 [CrossRef]
    [Google Scholar]
  39. Serrano C., Martín-Burriel I., Lyahyai J., Monzón M., El Hamidi M., Acín C., Badiola J. J., Tligui N., Zaragoza P. 2007; Polymorphisms of the PRNP gene in Moroccan sheep breeds. Vet Rec 161:524–525 [CrossRef]
    [Google Scholar]
  40. Sharpe A., McElroy M., Langeveld J. P., Bassett H., O'Donoghue A. M., Sweeney T. 2005; Immunohistochemical studies of scrapie archival material from Irish ARQ/ARQ sheep for evidence of bovine spongiform encephalopathy-derived disease. Res Vet Sci 79:29–35 [CrossRef]
    [Google Scholar]
  41. Simmons M. M., Konold T., Simmons H. A., Spencer Y. I., Lockey R., Spiropoulos J., Everitt S., Clifford D. 2007; Experimental transmission of atypical scrapie to sheep. BMC Vet Res 3:20 [CrossRef]
    [Google Scholar]
  42. Simmons H. A., Simmons M. M., Spencer Y. I., Chaplin M. J., Povey G., Davis A., Ortiz-Pelaez A., Hunter N., Matthews D. other authors 2009; Atypical scrapie in sheep from a UK research flock which is free from classical scrapie. BMC Vet Res 5:8 [CrossRef]
    [Google Scholar]
  43. Stack M., Jeffrey M., Gubbins S., Grimmer S., González L., Martin S., Chaplin M., Webb P., Simmons M. other authors 2006; Monitoring for bovine spongiform encephalopathy in sheep in Great Britain, 1998–2004. J Gen Virol 87:2099–2107 [CrossRef]
    [Google Scholar]
  44. Thuring C. M., Erkens J. H., Jacobs J. G., Bossers A., Van Keulen L. J., Garssen G. J., Van Zijderveld F. G., Ryder S. J., Groschup M. H. other authors 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 [CrossRef]
    [Google Scholar]
  45. Vaccari G., D'Agostino C., Nonno R., Rosone F., Conte M., Di Bari M. A., Chiappini B., Esposito E., De Grossi L. other authors 2007; Prion protein alleles showing a protective effect on the susceptibility of sheep to scrapie and bovine spongiform encephalopathy. J Virol 81:7306–7309 [CrossRef]
    [Google Scholar]
  46. van Keulen L. J., Vromans M. E., Dolstra C. H., Bossers A., van Zijderveld F. G. 2008; Pathogenesis of bovine spongiform encephalopathy in sheep. Arch Virol 153:445–453 [CrossRef]
    [Google Scholar]
  47. Ward H. J., Everington D., Cousens S. N., Smith-Bathgate B., Leitch M., Cooper S., Heath C., Knight R. S., Smith P. G. other authors 2006; Risk factors for variant Creutzfeldt–Jakob disease: a case–control study. Ann Neurol 59:111–120 [CrossRef]
    [Google Scholar]
  48. Wells G. A. H., Scott A. C., Johnson C. T., Gunning R. F., Hancock R. D., Jeffrey M., Dawson M., Bradley R. 1987; A novel progressive spongiform encephalopathy in cattle. Vet Rec 121:419–420 [CrossRef]
    [Google Scholar]
  49. Wells G. A. H., Konold T., Arnold M. E., Austin A. R., Hawkins S. A. C., Stack M., Simmons M. M., Lee Y. H., Gavier-Widén D. other authors 2007; Bovine spongiform encephalopathy: the effect of oral exposure dose on attack rate and incubation period in cattle. J Gen Virol 88:1363–1373 [CrossRef]
    [Google Scholar]
  50. Wilesmith J. W., Ryan J. B., Hueston W. D. 1992; Bovine spongiform encephalopathy: case–control studies of calf feeding practices and meat and bonemeal inclusion in proprietary concentrates. Res Vet Sci 52:325–331 [CrossRef]
    [Google Scholar]
  51. Will R. G., Ironside J. W., Zeidler M., Cousens S. N., Estibeiro K., Alperovitch A., Poser S., Pocchiari M., Hofman A. other authors 1996; A new variant of Creutzfeldt–Jakob disease in the UK. Lancet 347:921–925 [CrossRef]
    [Google Scholar]
  52. Yang S., Thackray A. M., Fitzmaurice T. J., Bujdoso R. 2008; Copper-induced structural changes in the ovine prion protein are influenced by a polymorphism at codon 112. Biochim Biophys Acta 1784683–692 [CrossRef]
    [Google Scholar]
  53. Zhang L., Li N., Fan B., Fang M., Xu W. 2004; PRNP polymorphisms in Chinese ovine, caprine and bovine breeds. Anim Genet 35:457–461 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.012724-0
Loading
/content/journal/jgv/10.1099/vir.0.012724-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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