Chronic wasting disease prions are not transmissible to transgenic mice overexpressing human prion protein

Journal of General Virology

Volumn 91, Issue 10, 2010, Pages 2651-2657

  Sandberg, Malin K ^a   Al Doujaily, Huda ^a   Sigurdson, Christina J ^b   Glatzel, Markus ^c   O'Malley, Catherine ^a   Powell, Caroline ^a   Asante, Emmanuel A ^a   Linehan, Jacqueline M ^a   Brandner, Sebastian ^a   Wadsworth, Jonathan D F ^a   Collinge, John ^a  

^a NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

METHIONINE; PRION PROTEIN; VALINE; PRION;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CHRONIC WASTING DISEASE; CHRONIC WASTING DISEASE AGENT; CONTROLLED STUDY; DEER; DISEASE TRANSMISSION; IMMUNOBLOTTING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD; TRANSGENIC MOUSE; ANIMAL; BIOSYNTHESIS; BOVIDS; DISEASE MODEL; GENETICS; HUMAN; INNATE IMMUNITY; PRION; SPECIES DIFFERENCE; TRANSMISSION; WILD ANIMAL; ZOONOSIS;

ANIMALS; ANIMALS, WILD; DISEASE MODELS, ANIMAL; HUMANS; IMMUNITY, INNATE; MICE; MICE, TRANSGENIC; PRIONS; RUMINANTS; SPECIES SPECIFICITY; WASTING DISEASE, CHRONIC; ZOONOSES;

ANIMALIA; CERVIDAE; MUS; MUS MUSCULUS; ODOCOILEUS HEMIONUS; ODOCOILEUS VIRGINIANUS;

EID: 77956867705     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.024380-0     Document Type: Article

References (65)

1. Anderson, C. A., Bosque, P., Filley, C. M., Arciniegas, D. B., Kleinschmidt-Demasters, B. K., Pape, W. J. & Tyler, K. L. (2007). Colorado surveillance programfor chronic wasting disease transmission to humans: lessons from 2 highly suspicious but negative cases. Arch Neurol 64, 439-441.
2. Angers, R. C., Browning, S. R., Seward, T. S., Sigurdson, C. J., Miller, M. W., Hoover, E. A. & Telling, G. C. (2006). Prions in skeletal muscles of deer with chronic wasting disease. Science 311, 1117.
3. Angers, R. C., Kang, H. E., Napier, D., Browning, S., Seward, T., Mathiason, C., Balachandran, A., McKenzie, D., Castilla, J. & other authors (2010). Prion strain mutation determined by prion protein conformational compatibility and primary structure. Science 328, 1154-1158.
4. Asante, E. A., Linehan, J. M., Desbruslais, M., Joiner, S., Gowland, I., Wood, A. L., Welch, J., Hill, A. F., Lloyd, S. E. & other authors (2002). BSE prions propagate as either variant CJD-like or sporadic CJD-like prion strains in transgenic mice expressing human prion protein. EMBO J 21, 6358-6366.
5. Asante, E. A., Linehan, J. M., Gowland, I., Joiner, S., Fox, K., Cooper, S., Osiguwa, O., Gorry, M., Welch, J. & other authors (2006). Dissociation of pathological and molecular phenotype of variant Creutzfeldt-Jakob disease in transgenic human prion protein 129 heterozygous mice. Proc Natl Acad Sci U S A 103, 10759-10764.
6. Baeten, L. A., Powers, B. E., Jewell, J. E., Spraker, T. R. & Miller, M. W. (2007). A natural case of chronic wasting disease in a free-ranging moose (Alces alces shirasi). J Wildl Dis 43, 309-314.
7. Belay, E. D. (2004). Chronic wasting disease and potential transmission to humans. Emerg Infect Dis 10, 977-984.
8. Belay, E. D., Gambetti, P., Schonberger, L. B., Parchi, P., Lyon, D. R., Capellari, S., McQuiston, J. H., Bradley, K., Dowdle, G. & other authors (2001). Creutzfeldt-Jakob disease in unusually young patients who consumed venison. Arch Neurol 58, 1673-1678.
9. Beringue, V., Vilotte, J. L. & Laude, H. (2008). Prion agents diversity and species barrier. Vet Res 39, 47.
10. Browning, S. R., Mason, G. L., Seward, T., Green, M., Eliason, G. A., Mathiason, C., Miller, M. W., Williams, E. S., Hoover, E. & other authors (2004). Transmission of prions from mule deer and elk with chronic wasting disease to transgenic mice expressing cervid PrP. J Virol 78, 13345-13350.
11. 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.
12. Sc replication in vitro generates unique infectious prions. Cell 134, 757-768.
13. Collinge, J. (1999). Variant Creutzfeldt-Jakob disease. Lancet 354, 317-323.
14. Collinge, J. (2010). Prion strain mutation and selection. Science 328, 1111-1112.
15. Collinge, J. & Clarke, A. R. (2007). A general model of prion strains and their pathogenicity. Science 318, 930-936.
16. Collinge, J., Palmer, M. S., Sidle, K. C. L., Gowland, I., Medori, R., Ironside, J. & Lantos, P. L. (1995a). Transmission of fatal familial insomnia to laboratory animals. Lancet 346, 569-570.
17. Collinge, J., Palmer, M. S., Sidle, K. C. L., Hill, A. F., Gowland, I., Meads, J., Asante, E., Bradley, R., Doey, L. J. & other authors (1995b). Unaltered susceptibility to BSE in transgenic mice expressing human prion protein. Nature 378, 779-783. (Pubitemid 26004409)
18. 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.
19. Collinge, J., Whitfield, J., McKintosh, E., Beck, J., Mead, S., Thomas, D. J. & Alpers, M. P. (2006). Kuru in the 21st century - an acquired human prion disease with very long incubation periods. Lancet 367, 2068-2074.
20. Collinge, J., Whitfield, J., McKintosh, E., Frosh, A., Mead, S., Hill, A. F., Brandner, S., Thomas, D. & Alpers, M. P. (2008). A clinical study of kuru patients with long incubation periods at the end of the epidemic in Papua New Guinea. Philos Trans R Soc Lond B Biol Sci 363, 3725-3739.
21. Fox, K. A., Jewell, J. E., Williams, E. S. & Miller, M. W. (2006). Patterns of PrPCWD accumulation during the course of chronic wasting disease infection in orally inoculated mule deer (Odocoileus hemionus). J Gen Virol 87, 3451-3461.
22. Green, K. M., Browning, S. R., Seward, T. S., Jewell, J. E., Ross, D. L., Green, M. A., Williams, E. S., Hoover, E. A. & Telling, G. C. (2008). The elk PRNP codon 132 polymorphism controls cervid and scrapie prion propagation. J Gen Virol 89, 598-608.
23. Guiroy, D. C., Williams, E. S., Song, K.-J., Yanagihara, R. & Gajdusek, D. C. (1993). Fibrils in brains of Rocky Mountain elk with chronic wasting disease contain scrapie amyloid. Acta Neuropathol 86, 77-80.
24. Haley, N. J., Seelig, D. M., Zabel, M. D., Telling, G. C. & Hoover, E. A. (2009). Detection of CWD prions in urine and saliva of deer by transgenic mouse bioassay. PLoS ONE 4, e4848.
25. Hamir, A. N., Gidlewski, T., Spraker, T. R., Miller, J. M., Creekmore, L., Crocheck, M., Cline, T. & O'Rourke, K. I. (2006). Preliminary observations of genetic susceptibility of elk (Cervus elaphus nelsoni) to chronic wasting disease by experimental oral inoculation. J Vet Diagn Invest 18, 110-114.
26. Heisey, D. M., Mickelsen, N. A., Schneider, J. R., Johnson, C. J., Johnson, C. J., Langenberg, J. A., Bochsler, P. N., Keane, D. P. & Barr, D. J. (2010). Chronic wasting disease (CWD) susceptibility of several North American rodents that are sympatric with cervid CWD epidemics. J Virol 84, 210-215.
27. Hill, A. F., Desbruslais, M., Joiner, S., Sidle, K. C. L., Gowland, I. & Collinge, J. (1997). The same prion strain causes vCJD and BSE. Nature 389, 448-450.
28. Jennelle, C. S., Samuel, M. D., Nolden, C. A., Keane, D. P., Barr, D. J., Johnson, C., Vanderloo, J. P., Aiken, J. M., Hamir, A. N. & other authors (2009). Surveillance for transmissible spongiform encephalopathy in scavengers of white-tailed deer carcasses in the chronic wasting disease area of Wisconsin. J Toxicol Environ Health A 72, 1018-1024.
29. Kascsak, R. J., Rubenstein, R., Merz, P. A., Tonna DeMasi, M., Fersko, R., Carp, R. I., Wisniewski, H. M. & Diringer, H. (1987). Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J Virol 61, 3688-3693.
30. Kim, T. Y., Shon, H. J., Joo, Y. S., Mun, U. K., Kang, K. S. & Lee, Y. S. (2005). Additional cases of chronic wasting disease in imported deer in Korea. J Vet Med Sci 67, 753-759.
31. Kong, Q., Huang, S., Zou, W., Vanegas, D., Wang, M., Wu, D., Yuan, J., Zheng, M., Bai, H. & other authors (2005). Chronic wasting disease of elk: transmissibility to humans examined by transgenic mouse models. J Neurosci 25, 7944-7949.
32. Kong, Q., Zheng, M., Casalone, C., Qing, L., Huang, S., Chakraborty, B., Wang, P., Chen, F., Cali, I. & other authors (2008). Evaluation of the human transmission risk of an atypical bovine spongiform encephalopathy prion strain. J Virol 82, 3697-3701.
33. Kurt, T. D., Telling, G. C., Zabel, M. D. & Hoover, E. A. (2009). Transspecies amplification of PrPCWD and correlation with rigid loop 170N. Virology 387, 235-243.
34. Lloyd, S. E., Linehan, J. M., Desbruslais, M., Joiner, S., Buckell, J., Brandner, S., Wadsworth, J. D. & Collinge, J. (2004). Characterization of two distinct prion strains derived from bovine spongiform encephalopathy transmissions to inbred mice. J Gen Virol 85, 2471-2478.
35. Lloyd, S. E., Maytham, E. G., Pota, H., Grizenkova, J., Molou, E., Uphill, J., Hummerich, H., Whitfield, J., Alpers, M. P. & other authors (2009). HECTD2 is associated with susceptibility to mouse and human prion disease. PLoS Genet 5, e1000383.
36. Marsh, R. F., Kincaid, A. E., Bessen, R. A. & Bartz, J. C. (2005). Interspecies transmission of chronic wasting disease prions to squirrel monkeys (Saimiri sciureus). J Virol 79, 13794-13796.
37. Mathiason, C. K., Powers, J. G., Dahmes, S. J., Osborn, D. A., Miller, K. V., Warren, R. J., Mason, G. L., Hays, S. A., Hayes-Klug, J. & other authors (2006). Infectious prions in the saliva and blood of deer with chronic wasting disease. Science 314, 133-136.
38. Mathiason, C. K., Hays, S. A., Powers, J., Hayes-Klug, J., Langenberg, J., Dahmes, S. J., Osborn, D. A., Miller, K. V., Warren, R. J. & other authors (2009). Infectious prions in pre-clinical deer and transmission of chronic wasting disease solely by environmental exposure. PLoS ONE 4, e5916.
39. Mawhinney, S., Pape, W. J., Forster, J. E., Anderson, C. A., Bosque, P. & Miller, M. W. (2006). Human prion disease and relative risk associated with chronic wasting disease. Emerg Infect Dis 12, 1527-1535.
40. Mead, S., Poulter, M., Uphill, J., Beck, J., Whitfield, J., Webb, T. E., Campbell, T., Adamson, G., Deriziotis, P. & other authors (2009). Genetic risk factors for variant Creutzfeldt-Jakob disease: a genomewide association study. Lancet Neurol 8, 57-66.
41. Meade-White, K., Race, B., Trifilo, M., Bossers, A., Favara, C., LaCasse, R., Miller, M., Williams, E., Oldstone, M. & other authors (2007). Resistance to chronic wasting disease (CWD) in transgenic mice expressing a naturally occurring allelic variant of deer prion protein. J Virol 81, 4533-4539.
42. Nichols, T. A., Pulford, B., Wyckoff, A. C., Meyerett, C., Michel, B., Gertig, K., Hoover, E. A., Jewell, J. E., Telling, G. C. & other authors (2009). Detection of protease-resistant cervid prion protein in water from a CWD-endemic area. Prion 3, 171-183.
43. O'Rourke, K. I., Spraker, T. R., Hamburg, L. K., Besser, T. E., Brayton, K. A. & Knowles, D. P. (2004). Polymorphisms in the prion precursor functional gene but not the pseudogene are associated with susceptibility to chronic wasting disease in white-tailed deer. J Gen Virol 85, 1339-1346.
44. Prusiner, S. B. (1998). Prions. Proc Natl Acad Sci U S A 95, 13363-13383.
45. Race, R. E., Raines, A., Baron, T. G., Miller, M. W., Jenny, A. & Williams, E. S. (2002). Comparison of abnormal prion protein glycoform patterns from transmissible spongiform encephalopathy agent-infected deer, elk, sheep, and cattle. J Virol 76, 12365-12368.
46. Race, B., Meade-White, K., Race, R. & Chesebro, B. (2009a). Prion infectivity in fat of deer with chronic wasting disease. J Virol 83, 9608-9610.
47. Race, B., Meade-White, K. D., Miller, M. W., Barbian, K. D., Rubenstein, R., LaFauci, G., Cervenakova, L., Favara, C., Gardner, D. & other authors (2009b). Susceptibilities of nonhuman primates to chronic wasting disease. Emerg Infect Dis 15, 1366-1376.
48. Raymond, G. J., Bossers, A., Raymond, L. D., O'Rourke, K. I., McHolland, L. E., Bryant, P. K., III, Miller, M. W., Williams, E. S., Smits, M. & other authors (2000). Evidence of a molecular barrier limiting susceptibility of humans, cattle and sheep to chronic wasting disease. EMBO J 19, 4425-4430.
49. Raymond, G. J., Raymond, L. D., Meade-White, K. D., Hughson, A. G., Favara, C., Gardner, D., Williams, E. S., Miller, M. W., Race, R. E. & other authors (2007). Transmission and adaptation of chronic wasting disease to hamsters and transgenic mice: evidence for strains. J Virol 81, 4305-4314.
50. Safar, J., Wille, H., Itri, V., Groth, D., Serban, H., Torchia, M., Cohen, F. E. & Prusiner, S. B. (1998). Eight prion strains have PrPSc molecules with different conformations. Nat Med 4, 1157-1165.
51. Sigurdson, C. J. (2008). A prion disease of cervids: chronic wasting disease. Vet Res 39, 41.
52. Sigurdson, C. J. & Aguzzi, A. (2007). Chronic wasting disease. Biochim Biophys Acta 1772, 610-618.
53. Sigurdson, C. J., Mathiason, C. K., Perrott, M. R., Eliason, G. A., Spraker, T. R., Glatzel, M., Manco, G., Bartz, J. C., Miller, M. W. & other authors (2008). Experimental chronic wasting disease (CWD) in the ferret. J Comp Pathol 138, 189-196.
54. Tamguney, G., Giles, K., Bouzamondo-Bernstein, E., Bosque, P. J., Miller, M. W., Safar, J., DeArmond, S. J. & Prusiner, S. B. (2006). Transmission of elk and deer prions to transgenic mice. J Virol 80, 9104-9114.
55. Tamguney, G., Miller, M. W., Wolfe, L. L., Sirochman, T. M., Glidden, D. V., Palmer, C., Lemus, A., DeArmond, S. J. & Prusiner, S. B. (2009). Asymptomatic deer excrete infectious prions in faeces. Nature 461, 529-532.
56. Trifilo, M. J., Ying, G., Teng, C. & Oldstone, M. B. (2007). Chronic wasting disease of deer and elk in transgenic mice: oral transmission and pathobiology. Virology 365, 136-143.
57. Wadsworth, J. D. & Collinge, J. (2007). Update on human prion disease. Biochim Biophys Acta 1772, 598-609.
58. Wadsworth, J. D., Joiner, S., Hill, A. F., Campbell, T. A., Desbruslais, M., Luthert, P. J. & Collinge, J. (2001). Tissue distribution of protease resistant prion protein in variant CJD using a highly sensitive immunoblotting assay. Lancet 358, 171-180.
59. Wadsworth, J. D., Asante, E., Desbruslais, M., Linehan, J., Joiner, S., Gowland, I., Welch, J., Stone, L., Lloyd, S. & other authors (2004). Human prion protein with valine 129 prevents expression of variant CJD phenotype. Science 306, 1793-1796.
60. Wadsworth, J. D., Joiner, S., Fox, K., Linehan, J., Desbruslais, M., Brandner, S., Asante, E. & Collinge, J. (2007). Prion infectivity in variant Creutzfeldt-Jakob disease rectum. Gut 56, 90-94.
61. Wadsworth, J. D., Joiner, S., Linehan, J. M., Desbruslais, M., Fox, K., Cooper, S., Cronier, S., Asante, E. A., Mead, S. & other authors (2008a). Kuru prions and sporadic Creutzfeldt-Jakob disease prions have equivalent transmission properties in transgenic and wild-type mice. Proc Natl Acad Sci U S A 105, 3885-3890.
62. Wadsworth, J. D., Powell, C., Beck, J. A., Joiner, S., Linehan, J. M., Brandner, S., Mead, S. & Collinge, J. (2008b). Molecular diagnosis of human prion disease. Methods Mol Biol 459, 197-227.
63. Williams, E. S. (2005). Chronic wasting disease. Vet Pathol 42, 530-549.
64. Williams, E. S. & Young, S. (1980). Chronic wasting disease of captive mule deer: a spongiform encephalopathy. J Wildl Dis 16, 89-98.
65. Williams, E. S. & Young, S. (1982). Spongiform encephalopathy of Rocky Mountain elk. J Wildl Dis 18, 465-471.