Humic substances interfere with detection of pathogenic prion protein

Soil Biology and Biochemistry

Volumn 68, Issue , 2014, Pages 309-316

  Smith, Christen B ^a   Booth, Clarissa J ^b   Wadzinski, Tyler J ^a   Legname, Giuseppe ^c   Chappell, Rick ^d   Johnson, Christopher J ^e   Pedersen, Joel A ^a,b  

^a Wisconsin Electric Machines and Power Electronics Consortium   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c SISSA   (Italy)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^e NATIONAL WILDLIFE HEALTH CENTER   (United States)

Author keywords

Humic substances; Immunoblotting; Natural organic matter; Prion; Protein detection; Transmissible spongiform encephalopathy

Indexed keywords

BIOGEOCHEMISTRY; NEURODEGENERATIVE DISEASES; ORGANIC ACIDS; ORGANIC COMPOUNDS; PROTEINS; SOILS;

HUMIC SUBSTANCES; IMMUNOBLOTTING; NATURAL ORGANIC MATTERS; PRION; PROTEIN DETECTION; TRANSMISSIBLE SPONGIFORM ENCEPHALOPATHIES;

BIOLOGICAL MATERIALS;

CONCENTRATION (COMPOSITION); DEER; DISEASE TRANSMISSION; HUMIC SUBSTANCE; INOCULATION; ORGANIC MATTER; PARTICULATE MATTER; PATHOGEN; PRION DISEASE; PROTEIN; RODENT; SOIL TYPE;

CERVIDAE; CRICETINAE;

EID: 84903269281     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2013.10.005     Document Type: Article

References (50)

1. Bessen, R.A., Marsh, R.F., 1992. Identification of two biologically distinct strains of transmissible mink encephalopathy in hamsters. J. Gen. Virol. 73, 329-334.
2. Bolton, D.C., Bendheim, P.E., Marmorstein, A.D., Potempska, A., 1987. Isolation and structural studies of the intact scrapie agent protein. Arch. Biochem. Biophys. 258, 579-590.
3. Booth, C.J., Johnson, C.J., Pedersen, J.A., 2013. Microbial and enzymatic inactivation of prions in soil environments. Soil Biol. Biochem. 59, 1-15.
4. Boyd, S.A., Mortland, M.M., 1990. Enzyme interactions with clays and clay-organic matter complexes. In: Bollag, J.-M., Stotzky, G. (Eds.), Soil Biochemistry, vol. 6. Marcel Dekker Inc., New York, pp. 1-28.
5. Brown, P., Gajdusek, D.C., 1991. Survival of scrapie virus after 3 years' interment. Lancet 337, 269-270.
6. Colby, D.W., Prusiner, S.B., 2011. Prions. Cold Spring Harbor Perspect. Biol. 3, 6833-6855.
7. Colby, D.W., Zhang, Q., Wang, S., Groth, D., Legname, G., Riesner, D., Prusiner, S.B., 2007. Prion detection by an amyloid seeding assay. Proc. Natl. Acad. Sci. U S A 104, 20914-20919.
8. 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.
9. Genovesi, S., Leita, L., Sequi, P., Andrighetto, I., Sorgato, M.C., Bertoli, A., 2007. Direct detection of soil-bound prions. PLoS One 2, e1069.
10. Hsu, P.-H., Hatcher, P.G., 2005. New evidence for covalent coupling of peptides to humic acids based on 2D NMR spectroscopy: a means for preservation. Geochim. Cosmochim. Acta 69, 4521-4533.
11. Huang, H., Spencer, J.L., Soutyrine, A., Guan, J., Rendulich, J., Balachandran, A., 2007. Evidence for degradation of abnormal prion protein in tissues from sheep with scrapie during composting. Can. J. Vet. Res. 71, 34-40.
12. Jacobson, K.H., Lee, S., McKenzie, D., Benson, C.H., Pedersen, J.A., 2009. Transport of the pathogenic prion protein through landfill materials. Environ. Sci. Technol. 43, 2022-2028.
13. Jacobson, K.H., Lee, S., Somerville, R.A., McKenzie, D., Benson, C.H., Pedersen, J.A., 2010. Transport of pathogenic prion protein through soils. J. Environ. Qual. 39, 1145-1152.
14. 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 Pathogens 2, e32.
15. 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 Pathogens 3, e93.
16. Johnson, C.J., McKenzie, D., Pedersen, J.A., Aiken, J.M., 2011a. Meat and bone meal and mineral feed additives may increase the risk of oral prion disease transmission. J. Toxicol. Environ. Health. A. 74, 161-166.
17. Johnson, C.J., Herbst, A., Duque-Velasquez, C., Vanderloo, J.P., Bochsler, P., Chappell, R., McKenzie, D., 2011b. Prion protein polymorphisms affect chronic wasting disease progression. PLoS One 6, e17450.
18. Kocisko, D.A., Baron, G.S., Rubenstein, R., Chen, J., Kuizon, S., Caughey, B., 2003. New inhibitors of scrapie-associated prion protein formation in a library of 2, 000 drugs and natural products. J. Virol. 77, 10288-10294.
19. Leita, L., Fornasier, F., De Nobili, M., Bertoli, A., Genovesi, S., Sequi, P., 2006. Interactions of prion proteins with soil. Soil. Biol. Biochem. 38, 1638-1644.
20. 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.
21. Sc with soils is influenced by prion source and soil type. Environ. Sci. Technol. 44, 8503-8508.
22. McKenzie, D., Bartz, J., Mirwald, J., Olander, D., Marsh, R., Aiken, J., 1998. Reversibility of scrapie inactivation is enhanced by copper. J. Biol. Chem. 273, 25545-5547.
23. Murase, A., Yoneda, M., Ueno, R., Yonebayashi, K., 2003. Isolation of extracellular protein from greenhouse soil. Soil. Biol. Biochem. 35, 733-736.
24. Nagaoka, K., Yoshioka, M., Shimozaki, N., Yamamura, T., Murayama, Y., Yokoyama, T., Mohri, S., 2010. Sensitive detection of scrapie prion protein in soil. Biochem. Biophys. Res. Commun. 397, 626-630.
25. Nichols, T.A., Pulford, B., Wyckoff, A.C., Meyerett, C., Michel, B., Gertig, K., Hoover, E.A., Jewell, J.E., Telling, G.C., Zabel, M.D., 2009. Detection of proteaseresistant cervid prion protein in water from a CWD-endemic area. Prion 3, 171-183.
26. Pedersen, J.A., Somerville, R., 2011. Why and how are TSEs sometimes spread via environmental routes? In: Deslys, J.-P., Pocchiari, M., Reisner, D., Somerville, R. (Eds.), Decontamination of Prions. Düsseldorf University Press, Düsseldorf, Germany (in press). Q2.
27. Polano, M., Anselmi, C., Leita, L., Negro, A., De Nobili, M., 2008. Organic polyanions act as complexants of prion protein in soil. Biochem. Biophys. Res. Commun. 367, 323-329.
28. Prusiner, S.B., Cochran, S.P., Groth, D.F., Downey, D.E., Bowman, K.A., Martinez, H.M., 1982. Measurement of the scrapie agent using an incubation-time interval assay. Ann. Neurol. 11, 353-358.
29. Prusiner, S.B., Cochran, S.P., Alpers, M.P., 1985. Transmission of scrapie in hamsters. J. Infect. Dis. 152, 971-978.
30. Pucci, A., D'Acqui, L.P., Calamai, L., 2008. Fate of prions in soil: interactions of RecPrP with organic matter of soil aggregates as revealed by LTA-PAS. Environ. Sci. Technol. 42, 728-733.
31. 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.
32. Ritchie, J.D., Perdue, E.M., 2003. Proton-binding study of standard and reference fulvic acids, humic acids, and natural organic matter. Geochim. Cosmochim. Acta 67, 85-96.
33. Roberts, P., Jones, D.L., 2008. Critical evaluation of methods for determining total protein in soil solution. Soil Biol. Biochem. 40, 1485-1495.
34. Rosier, C.L., Hoye, A.T., Rillig, M.C., 2006. Glomalin-related soil protein: assessment of current detection and quantification tools. Soil Biol. Biochem. 38, 2205-2211.
35. Russo, F., Johnson, C.J., Johnson, C.J., McKenzie, D., Aiken, J.M., Pedersen, J.A., 2009. Pathogenic prion protein is degraded by a manganese oxide mineral found in soils. J. Gen. Virol. 90, 275-280.
36. 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.
37. Saunders, S.E., Bartz, J.C., Bartelt-Hunt, S.L., 2009. Prion protein adsorption to soil in a competitive matrix is slow and reduced. Environ. Sci. Technol. 43, 7728-7733.
38. Saunders, S.E., Bartz, J.C., Vercauteren, K.C., Bartelt-Hunt, S.L., 2010. Enzymatic digestion of chronic wasting disease prions bound to soil. Environ. Sci. Technol. 44, 4129-4135.
39. Saunders, S.E., Shikiya, R.A., Langenfeld, K., Bartelt-Hunt, S.L., Bartz, J.C., 2011a. Replication efficiency of soil-bound prions varies with soil type. J. Virol. 85, 5476-5482.
40. Saunders, S.E., Bartz, J.C., Vercauteren, K.C., Bartelt-Hunt, S.L., 2011b. An enzymatic treatment of soil-bound prions effectively inhibits replication. Appl. Environ. Microbiol. 77, 4313-4317.
41. Saunders, S.E., Yuan, Q., Bartz, J.C., Bartelt-Hunt, S.L., 2011c. Effects of solution chemistry and aging time on prion protein adsorption and replication of soilbound prions. PLoS One 6, e18752.
42. Schindler, F.V., Mercer, E.J., Rice, J.A., 2007. Chemical characteristics of glomalinrelated soil protein (GRSP) extracted from soils of varying organic matter content. Soil. Biol. Biochem. 39, 320-329.
43. 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.
44. Scott, M., Foster, D., Mirenda, C., Serban, D., Coufal, F., Wälchli, M., Torchia, M., Groth, D., Carlson, G., DeArmond, S.J., Westaway, D., Prusiner, S.B., 1989. Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell 59, 847-857.
45. 263K) can transmit disease via the oral route after persistence in soil over years. PLoS One 2, e435.
46. Silveira, J.R., Raymond, G.J., Hughson, A.G., Race, R.E., Sim, V.L., Hayes, S.F., Caughey, B., 2005. The most infectious prion protein particles. Nature 437, 257-261.
47. Smith, C.B., Booth, C.J., Pedersen, J.A., 2011. Fate of prions in soil: a review. J. Environ. Qual. 40, 449-461.
48. Tan, W.F., Koopal, L.K., Norde, W., 2009. Interaction between humic acid and lysozyme, studied by dynamic light scattering and isothermal titration calorimetry. Environ. Sci. Technol. 43, 591-596.
49. 1H) Nuclear Magnetic Resonance Spectrometry. U.S. Geological Survey, Denver, CO. Water-Resources Investigations Report 89-4196.
50. Zang, X., van Heemst, J.D.H., Dria, K.J., Hatcher, P.G., 2000. Encapsulation of protein in humic acid from a histosol as an explanation for the occurrence of organic nitrogen in soil and sediment. Org. Geochem. 31, 679-695.