1887

Abstract

Prions, the aetiological agents of transmissible spongiform encephalopathies, exhibit extreme resistance to degradation. Soil can retain prion infectivity in the environment for years. Reactive soil components may, however, contribute to the inactivation of prions in soil. Members of the birnessite family of manganese oxides (MnO) rank among the strongest natural oxidants in soils. Here, we report the abiotic degradation of pathogenic prion protein (PrP) by a synthetic analogue of naturally occurring birnessite minerals. Aqueous MnO suspensions degraded the PrP as evidenced by decreased immunoreactivity and diminished ability to seed protein misfolding cyclic amplification reactions. Birnessite-mediated PrP degradation increased as a solution's pH decreased, consistent with the pH-dependence of the redox potential of MnO. Exposure to 5.6 mg MnO ml (PrP : MnO=1 : 110) decreased PrP levels by ≥4 orders of magnitude. Manganese oxides may contribute to prion degradation in soil environments rich in these minerals.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.003251-0
2009-01-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/1/275.html?itemId=/content/journal/jgv/10.1099/vir.0.003251-0&mimeType=html&fmt=ahah

References

  1. Barrett, K. A. & McBride, M. B.(2005). Oxidative degradation of glyphosate and aminomethylphosphonate by manganese oxide. Environ Sci Technol 39, 9223–9228.[CrossRef] [Google Scholar]
  2. Bolton, D. C., McKinley, M. P. & Prusiner, S. B.(1982). Identification of a protein that purifies with the scrapie prion. Science 218, 1309–1311.[CrossRef] [Google Scholar]
  3. Bricker, O.(1965). Some stability relations in system Mn-O2-H2O at 25 °C and 1 atmosphere total pressure. Am Mineral 50, 1296–1354. [Google Scholar]
  4. Brown, P. & Gajdusek, D. C.(1991). Survival of scrapie virus after 3 years' interment. Lancet 337, 269–270.[CrossRef] [Google Scholar]
  5. Chihota, C. M., Gravenor, M. B. & Baylis, M.(2004). Investigation of trace elements in soil as risk factors in the epidemiology of scrapie. Vet Rec 154, 809–813.[CrossRef] [Google Scholar]
  6. Cooke, C. M., Rodger, J., Smith, A., Fernie, K., Shaw, G. & Somerville, R. A.(2007). Fate of prions in soil: detergent extraction of PrP from soils. Environ Sci Technol 41, 811–817.[CrossRef] [Google Scholar]
  7. Gao, J.(2007). Ph.D. dissertation. University of Wisconsin – Madison.
  8. Georgsson, G., Sigurdarson, S. & Brown, P.(2006). Infectious agent of sheep scrapie may persist in the environment for at least 16 years. J Gen Virol 87, 3737–3740.[CrossRef] [Google Scholar]
  9. Greig, J. R.(1940). Scrapie, observations on the transmission of the disease by mediate contact. Vet J 96, 203–206. [Google Scholar]
  10. Gudmundsdottir, K. B., Sigurdarson, S., Kristinsson, J., Eiriksson, T. & Johannesson, T.(2006). Iron and iron/manganese ratio in forage from Icelandic sheep farms, relation to scrapie. Acta Vet Scand48 (16).. [Google Scholar]
  11. Hinkley, G. T., Johnson, C. J., Jacobson, K. H., Bartholomay, C., McMahon, K. D., McKenzie, D., Aiken, J. M. & Pedersen, J. A.(2008). Persistence of pathogenic prion protein during simulated wastewater treatment processes. Environ Sci Technol 42, 5254–5259.[CrossRef] [Google Scholar]
  12. Hoinville, L. J.(1996). A review of the epidemiology of scrapie in sheep. Rev Sci Tech 15, 827–852. [Google Scholar]
  13. Johnson, C. J., Phillips, K. E., Schramm, P. T., McKenzie, D., Aiken, J. M. & Pedersen, J. A.(2006). Prions adhere to soil minerals and remain infectious. PLoS Pathog 2, e32[CrossRef] [Google Scholar]
  14. Johnson, C. J., Pedersen, J. A., Chappell, R. J., McKenzie, D. & Aiken, J. M.(2007). Oral transmissibility of prion disease is enhanced by binding to soil particles. PLoS Pathog 3, e93[CrossRef] [Google Scholar]
  15. Klausen, J., Haderlein, S. B. & Schwarzenbach, R. P.(1997). Oxidation of substituted anilines by aqueous MnO2: effect of co-solutes on initial and quasi-steady-state kinetics. Environ Sci Technol 31, 2642–2649.[CrossRef] [Google Scholar]
  16. Ma, X., Benson, C. H., McKenzie, D., Aiken, J. M. & Pedersen, J. A.(2007). Adsorption of pathogenic prion protein to quartz sand. Environ Sci Technol 41, 2324–2330.[CrossRef] [Google Scholar]
  17. 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.[CrossRef] [Google Scholar]
  18. McBride, M. B.(2007). Trace metals and sulfur in soils and forage of a chronic wasting disease locus. Environ Chem 4, 134–139.[CrossRef] [Google Scholar]
  19. McKenzie, R. M.(1989). Manganese oxides and hydroxides. In Minerals in Soil Environments, 2nd edn, pp. 439–465. Edited by J. B. Dixon, S. B. Weed & R. C. Dinauer. Madison, WI: Soil Science Society of America.
  20. Miller, M. W. & Williams, E. S.(2003). Prion disease, horizontal prion transmission in mule deer. Nature 425, 35–36.[CrossRef] [Google Scholar]
  21. Miller, M. W., Williams, E. S., Hobbs, N. T. & Wolfe, L. L.(2004). Environmental sources of prion transmission in mule deer. Emerg Infect Dis 10, 1003–1006.[CrossRef] [Google Scholar]
  22. Murray, J. W.(1974). Surface chemistry of hydrous manganese dioxide. J Colloid Interface Sci 46, 357–371.[CrossRef] [Google Scholar]
  23. Naidja, A., Liu, C. & Huang, P. M.(2002). Formation of protein-birnessite complex, XRD, FTIR, and AFM analysis. J Colloid Interface Sci 251, 46–56.[CrossRef] [Google Scholar]
  24. Pálsson, P. A.(1979). Rida (scrapie) in Iceland and its epidemiology. In Slow Transmissible Diseases of the Nervous System. 1st edn, pp. 357–366. Edited by S. B. Prusiner & W. J. Hadlow. New York: Academic Press.
  25. Post, J. E.(1999). Manganese oxide minerals, crystal structures and economic and environmental significance. Proc Natl Acad Sci U S A 96, 3447–3454.[CrossRef] [Google Scholar]
  26. Quiquampoix, H., Servagent-Noinville, S. & Baron, M.-H.(2002). Enzyme adsorption on soil mineral surfaces and consequences for the catalytic activity. In Enzymes in the Environment: Activity, Ecology, and Applications, pp. 285–306. Edited by R. G. Burns & R. P. Dick. New York: Marcell Dekker.
  27. Ragnarsdottir, K. V. & Hawkins, D. P.(2006). Bioavailable copper and manganese in soils from Iceland and their relationship with scrapie occurrence in sheep. J Geochem Explor 88, 228–234.[CrossRef] [Google Scholar]
  28. Rao, M. A., Russo, F., Granata, V., Berisio, R., Zagari, A. & Gianfreda, L.(2007). Fate of prions in soil: interaction of a recombinant ovine prion protein with synthetic humic-like mineral complexes. Soil Biol Biochem 39, 493–504.[CrossRef] [Google Scholar]
  29. Rubert, K. F. & Pedersen, J. A.(2006). Kinetics of oxytetracycline reaction with a hydrous manganese oxide. Environ Sci Technol 40, 7216–7221.[CrossRef] [Google Scholar]
  30. 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.[CrossRef] [Google Scholar]
  31. 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.[CrossRef] [Google Scholar]
  32. Safar, J. G., Lessard, P., Tamgüney, G., Freyman, Y., Deering, C., Letessier, F., DeArmond, S. J. & Prusiner, S. B.(2008). Transmission and detection of prions in feces. J Infect Dis 198, 81–89.[CrossRef] [Google Scholar]
  33. Schramm, P. T., Johnson, C. J., Mathews, N. E., McKenzie, D., Aiken, J. M. & Pedersen, J. A.(2006). Potential role of soil in the transmission of prion disease. Rev Mineral Geochem 64, 135–152.[CrossRef] [Google Scholar]
  34. Seidel, B., Thomzig, A., Buschmann, A., Groschup, M. H., Peters, R., Beekes, M. & Terytze, K.(2007). Scrapie agent (Strain 263K) can transmit disease via the oral route after persistence in soil over years. PLoS ONE 2, e435[CrossRef] [Google Scholar]
  35. Stone, A. T.(1987). Reductive dissolution of manganese(III/IV) oxides by substituted phenols. Environ Sci Technol 21, 979–988.[CrossRef] [Google Scholar]
  36. Stone, A. T. & Morgan, J. J.(1984). Reduction and dissolution of manganese(III) and manganese(IV) oxides by organics. 2. Survey of the reactivity of organics. Environ Sci Technol 18, 617–624.[CrossRef] [Google Scholar]
  37. Taylor, D. M.(2000). Inactivation of transmissible degenerative encephalopathy agents. A review. Vet J 159, 10–17.[CrossRef] [Google Scholar]
  38. Tebo, B. M., Bargar, J. R., Clement, B. G., Dick, G. J., Murray, K. J., Parker, D., Verity, R. & Webb, S. M.(2004). Biogenic manganese oxides: properties and mechanisms of formation. Annu Rev Earth Planet Sci 32, 287–328.[CrossRef] [Google Scholar]
  39. Villalobos, M., Toner, B., Bargar, J. & Sposito, G.(2003). Characterization of the manganese oxide produced by Pseudomonas putida strain MnB1. Geochim Cosmochim Acta 67, 2649–2662.[CrossRef] [Google Scholar]
  40. Zhang, H. C. & Huang, C. H.(2005). Oxidative transformation of fluoroquinolone antibacterial agents and structurally related amines by manganese oxide. Environ Sci Technol 39, 4474–4483.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.003251-0
Loading
/content/journal/jgv/10.1099/vir.0.003251-0
Loading

Data & Media loading...

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