Attachment of pathogenic prion protein to model oxide surfaces

Environmental Science and Technology

Volumn 47, Issue 13, 2013, Pages 6925-6934

  Jacobson, Kurt H ^a   Kuech, Thomas R ^a   Pedersen, Joel A ^a,b  

^a University of Wisconsin Madison   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM OXIDES; INFECTIOUS AGENTS; MINERAL SURFACES; OPTICAL WAVEGUIDE LIGHT MODE SPECTROSCOPY; POSITIVELY CHARGED; QUARTZ CRYSTAL MICROBALANCE WITH DISSIPATION MONITORING; SOIL ENVIRONMENT; TRANSMISSIBLE SPONGIFORM ENCEPHALOPATHIES;

ALUMINUM; BIOCHEMISTRY; IONIC STRENGTH; NEURODEGENERATIVE DISEASES; SOILS;

RECOMBINANT PROTEINS;

ALUMINUM OXIDE; OXIDE; PRION PROTEIN; SILICON DERIVATIVE;

BIOAVAILABILITY; DISEASE PREVALENCE; DISEASE TRANSMISSION; HOST-PATHOGEN INTERACTION; MINERAL; NEUROLOGY; OXIDE; RECOMBINATION; RUMINANT; SOIL TYPE;

ARTICLE; CONTROLLED STUDY; IONIC STRENGTH; PH; PRION; QUARTZ CRYSTAL MICROBALANCE; SPECTROSCOPY; STATIC ELECTRICITY; SURFACE PROPERTY;

ADSORPTION; ALUMINUM OXIDE; PRIONS; SILICON DIOXIDE; SOIL;

EID: 84880112909     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es3045899     Document Type: Article

References (73)

1. Miller, M. W.; Williams, E. S.; Hobbs, N. T.; Wolfe, L. L. Environmental sources of prion transmission in mule deer Emerg. Infect. Dis. 2004, 10, 1003-1006
2. Schramm, P. T.; Johnson, C. J.; Mathews, N. E.; McKenzie, D.; Aiken, J. M.; Pedersen, J. A. Potential role of soil in the transmission of prion disease. Medical Mineralogy and Geochemistry Rev. Mineral. Geochem. 2006, 64, 135-152
3. Pedersen, J. A.; Somerville, R. Why and how are TSEs sometimes spread via environmental routes? In Decontamination of Prions; Deslys, J.-P.; Pocchiari, M.; Reisner, D.; Somerville, R., Eds.; Düsseldorf University Press: Düsseldorf, Germany, 2012; pp 19-37.
4. Pruisner, S. B. P. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 13363-13383
5. C) expression in bovine somatic tissues Prion 2009, 3, 161-170
6. Brown, P.; Cervenakova, L. A prion lexicon (out of control) Lancet 2005, 365, 122
7. Safar, J.; Roller, P. P.; Gajdusek, D. C.; Gibbs, C. J., Jr. Scrapie amyloid (prion) protein has the conformational characteristics of an aggregated molten globule folding intermediate Biochem. 1994, 33, 8375-8383
8. Smirnovas, V.; Baron, G. S.; Offerdahl, D. K.; Raymond, G. J.; Caughey, B.; Surewicz, W. K. Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange Nat. Struct. Mol. Biol. 2011, 18, 504-506
9. Gossert, A. D.; Bonjour, S.; Lysek, D. A.; Fiorito, F.; Wüthrich, K. Prion protein NMR structures of elk and of mouse/elk hybrids Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 646-650
10. Lysek, D. A.; Schorn, C.; Nivon, L. G.; Esteve-Moya, V.; Christen, B.; Calzolai, L.; von Schroetter, C.; Fiorito, F.; Herrmann, T.; Guntert, P.; Wüthrich, K. Prion protein NMR structures of cats, dogs, pigs, and sheep Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 640-645
11. Riek, R.; Hornemann, S.; Wider, G.; Glockshuber, R.; Wüthrich, K. NMR characterization of the full-length recombinant muring prion protein, m PrP(23-231) FEBS Lett. 1997, 413, 282-288
12. Zahn, R.; Liu, A.; Lührs, T.; Riek, R.; von Schroetter, C.; López Garcia, F.; Billeter, M.; Calzolai, L.; Wider, G.; Wüthrich NMR solution structure of the human prion protein Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 145-150
13. Colby, D. W.; Prusiner, S. B. Prions Cold Spring Harbor Perspect. Biol. 2011, 3, a006833
14. DeMarco, M. L.; Silveira, J.; Caughey, B.; Dagget, V. Structural properties of prion protein protofibrils and fibrils: An experimental assessment of atomic models Biochem. 2006, 45, 15573-15582
15. Diaz-Espinoza, R.; Soto, C. High-resolution structure of infectious prion proteins: The final frontier Nature Struct. Molec. Biol. 2012, 19, 370-377
16. Tamgüney, G.; Miller, M. W.; Wolfe, L. L.; Sirochman, T. M.; Glidden, D. V.; Palmer, C.; Lemus, A.; DeArmond, S. J.; Prusiner, S. B. Asymptomatic deer excrete infectious prions in faeces Nature 2009, 461, 529-532
17. Tamgüney, G.; Miller, M. W.; Wolfe, L. L.; Sirochman, T. M.; Glidden, D. V.; Palmer, C.; Lemus, A.; DeArmond, S. J.; Prusiner, S. B. Asymptomatic deer excrete infectious prions in faeces Nature 2010, 466, 652
18. Gregori, L.; Kovacs, G. G.; Alexeeva, I.; Budka, H.; Rohwer, R. G. Excretion of transmissible spongiform encephalopathy infectivity in urine Emg. Infect. Dis. 2008, 14, 1406-1412
19. 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.; Seelig, D. M.; Wild, M. A.; Wolfe, L. L.; Spraker, T. R.; Miller, M. W.; Sigurdson, C. J.; Tellings, G. C.; Hoover, E. A. Infectious prions in the saliva and blood of deer with chronic wasting disease Science 2006, 314, 133-136
20. Brown, P.; Gajdusek, D. C. Survival of scrapie virus after 3 years' interment Lancet 1991, 337, 269-270
21. Seidel, B.; Thomzig, A.; Buschmann, A.; Groschup, M. H.; Peters, R.; Beekes, M.; Terytze, K. Scrapie agent (strain 263K) can transmit disease via the oral route after persistence in soil over years PLoS ONE 2007, 5, e435
22. Arthur, W. J., III; Alldredge, A. W. Soil ingestion by mule deer in northcentral Colorado J. Range Manage. 1979, 32, 67-71
23. Beyer, W. N.; Conner, E. E.; Gerould, S. Estimates of soil ingestion by wildlife J. Wildl. Manage. 1994, 58, 375-382
24. Hui, C. A. Geophagy and potential contaminant exposure for terrestrial vertebrates Rev. Environ. Contam. Toxicol. 2004, 183, 115-134
25. Johnson, C. J.; Pedersen, J. A.; Chappell, R. J.; McKenzie, D.; Aiken, J. M. Oral transmissibility of prion disease is enhanced by binding to soil particles PLoS Path. 2007, 3, e93
26. Johnson, C. J.; McKenzie, D.; Pedersen, J. A.; Aiken, J. M. Meat and bone meal and mineral feed additives may increase the risk of oral prion disease transmission J. Toxicol. Environ. Health, Part A 2011, 74, 161-166
27. Johnson, C. J.; Phillips, K. E.; Schramm, P. T.; McKenzie, D.; Aiken, J. M.; Pedersen, J. A. Prions adhere to soil minerals and remain infectious PLoS Path. 2006, 2, e32
28. Cooke, C. M.; Shaw, G. Fate of prions in soil: Longevity and migration of recPrP in soil columns Soil Biol. Biochem. 2007, 39, 1181-1191
29. Ma, X.; Benson, C. H.; McKenzie, D.; Aiken, J. M.; Pedersen, J. A. Adsorption of pathogenic prion protein to quartz sand Environ. Sci. Technol. 2007, 41, 2324-2330
30. Hinckley, G. T.; Johnson, C. J.; Jacobson, K. H.; Bartholomay, C.; McMahon, K. D.; McKenzie, D.; Aiken, J. M.; Pedersen, J. A. Persistance of pathogenic prion protein during simulated wastewater treatment processes Environ. Sci. Technol. 2008, 42, 5254-5259
31. Jacobson, K. H.; Lee, S.; McKenzie, D.; Benson, C. H.; Pedersen, J. A. Transport of the pathogenic prion protein through landfill materials Environ. Sci. Technol. 2009, 43, 2022-2028
32. Saunders, S. E.; Bartz, J. C.; Bartelt-Hunt, S. L. PrP adsorption to soil in a competitive matrix is slow and reduced Environ. Sci. Technol. 2009, 43, 7728-7733
33. Jacobson, K. H.; Lee, S.; Sommerville, R. A.; McKenzie, D.; Benson, C. H.; Pedersen, J. A. Transport of the pathogenic prion protein through soils J. Environ. Qual. 2010, 39, 1145-1152
34. Sc with soils is influenced by prion source and soil type Environ. Sci. Technol. 2010, 44, 8503-8508
35. Saunders, S. E.; Bartz, J. C.; Telling, G. C.; Bartelt-Hunt, S. L. Environmentally relevant forms of the prion protein Environ. Sci. Technol. 2008, 42, 6573-6579
36. Bessen, R. A.; Marsh, R. F. Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy J. Virol. 1994, 68, 7859-7868
37. res) from transmissible spongiform encephalopathy-affected brain tissue. In Techniques in Prion Research; Lehmann, S.; Grassi, J., Eds.; Birkhäuser Verlag: Basel, 2004; pp 16-26.
38. Cronier, S.; Gros, N.; Tattum, M. H.; Jackson, G. S.; Clarke, A. R.; Collinge, J.; Wadsworth, J. D. F. Detection and characterization of proteinase K-sensitive disease- related prion protein with thermolysin Biochem. J. 2008, 416, 297-305
39. Prusiner, S. B.; McKinley, M. P.; Bowman, K. A.; Bolton, D. C.; Bendheim, P. E.; Groth, D. F.; Glenner, G. G. Scrapie prions aggregate to form amyloid-like birefringent rods Cell 1983, 35, 349-358
40. Sahai, N.; Sverjensky, D. A. Evaluation of internally consistent parameters for the triple-layer model by the systematic analysis of oxide surface titration data Geochim. Cosmochim. Acta 1997, 61, 2801-2826
41. Lundblad, R. L.; MacDonald, F. Handbook of Biochemistry and Molecular Biology; CRC Press; Boca Raton, FL, 2010.
42. Rodahl, M.; Höök, F.; Krozer, A.; Brzezinski, P.; Kasemo, B. Quartz crystal microbalance setup for frequency and Q-factor measurements in gaseous and liquid environments Rev. Sci. Instrum. 1995, 66, 3924-3930
43. Reviakine, I.; Johannsmann, D.; Richter, R. P. Hearing what you cannot see and visualizing what you hear: Interpreting quartz crystal microbalance data from solvated interfaces Anal. Chem. 2011, 83, 8838-8848
44. Sauerbrey, G. Verwendung von Schwingquarzen zur Wägung dünner Schichten und zur Mikrowägung Z. Phys. 1959, 155, 206-222
45. Voinova, M. V.; Rodahl, M.; Jonson, M.; Kasemo, B. Viscoelastic acoustic response of layered polymer films at fluid-solid interfaces: Continuum mechanics approach Phys. Scr. 1999, 59, 391-396
46. Cleveland, W. S.; Devlin, S. T. Locally weighted regression: An approach to regression analysis by local fitting J. Am. Stat. Assoc. 1988, 83, 596-610
47. Eisele, N. B.; Andersson, F. I.; Frey, S.; Richter, R. P. Viscoelasticity of thin biomolecular films: A case study on nucleoporin phenylalanine-glycine repeats grated to a histidine-tag capturing QCM-D sensor Biomacromolec. 2010, 13, 2322-2332
48. Vörös, J.; Ramsden, J. J.; Csúcs, G.; Szendro, I.; De Paul, S. M.; Textor, M.; Spencer, N. D. Optical grating coupler biosensors Biomaterials 2002, 23, 3699-3710
49. Tiefenthaler, K.; Lukosz, W. Sensitivity of grating couplers as integrated-optical chemical sensors J. Opt. Soc. Am. B. 1989, 6, 209-220
50. de Feijter, J. A.; Benjamins, J.; Veer, F. A. Ellipsometry as a tool to study the adsorption of synthetic and biopolymers at the air-water interface Biopolymers 1978, 17, 1759-1772
51. Ball, V.; Ramsden, J. J. Buffer dependence of refractive index increments of protein solutions Biopolymers 1998, 46, 489-492
52. Vörös, J. The density and refractive index of adsorbing protein layers Biophys. J. 2004, 87, 553-561
53. 2. 1. Forces driving adsorption Environ. Sci. Technol. 2010, 44, 8870-8876
54. Hansma, H. G.; Kim, K. J.; Laney, D. E.; Garcia, R. A.; Argaman, M.; Allen, M. J.; Parson, S. M. Properties of biomolecules measured from atomic force microscope images: A review J. Struct. Biol. 1997, 119, 99-108
55. Scheinthal, B. M.; Bettelheim, F. A. Multiple forms of sialic acids Carbohyd. Res. 1968, 6, 257-265
56. Rudd, P. M.; Endo, T.; Colominas, C.; Groth, D.; Wheeler, S. F.; Harvey, S. F.; Wormald, M. R.; Serban, H.; Prusiner, S. B.; Kobata, A.; Raymond, D. A. Glycosylation differences between the normal and pathogenic prion protein isoforms Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 13044-13049
57. Stahl, N.; Baldwin, M. A.; Teplow, D. B.; Hood, L.; Gibson, B. W.; Burlingame, A. L.; Prusiner, S. B. Structural studies of the scrapie prion protein using mass spectrometry and amino acid sequencing Biochem. 1993, 32, 1991-2002
58. Bergström, L. Hamaker constants of inorganic materials Adv. Colloid. Interfac. 1997, 70, 125-169
59. Bhattacharjee, S.; Ko, C.-H.; Elimelech, M. DLVO interaction between rough surfaces Langmuir 1998, 14, 3365-3375
60. Madliger, M.; Gasser, C. A.; Schwarzenbach, R. P.; Sander, M. Adsorption of transgenic insecticidal Cry1Ab protein to silica particles. Effects on transport and bioactivity Environ. Sci. Technol. 2011, 45, 4377-4384
61. Saunders, S. E.; Yuan, Q.; Bartz, J. C.; Bartelt-Hunt, S. Effects of solution chemistry and aging time on prion protein adsorption and replication of soil-bound prions PLoS ONE 2011, 6, e18752
62. Vasina, E. N.; Déjardin, P.; Rezaei, H.; Grosclaude, J.; Quiquampoix, H. Fate of prions of soil: Adsorption kinetics of recombinant unglycosylated ovine prion protein onton mica in laminar flow conditions and subsequent desorption Biomacromolec. 2005, 6, 3425-3432
63. Rigou, P.; Rezaei, H.; Grosclaude, J.; Staunton, S.; Quiquampoix, H. Fate of prions in soil: Adsorption and extraction by electroelution of recombinant ovine prion protein from montmorillonite and natural soils Environ. Sci. Technol. 2006, 40, 1497-1503
64. Cooke, C. M.; Shaw, G. Fate of prions in soil: Longevity and migration of recPrP in soil columns Soil Biol. Biochem. 2007, 39, 1181-1191
65. Rao, M. A.; Russo, F.; Granata, V.; Berisio, R.; Zagari, A.; Gianfreda, L. Fate of prions in soil: Interaction of a recombinant ovine prion protein with synthetic humic-like complexes Soil Biol. Biochem. 2007, 39, 493-504
66. Wopfner, F.; Weidenhöfer, G.; Schneider, R.; von Brunn, A.; Gilch, S.; Schwarz, T. F.; Wener, T.; Schätzl, H. M. Analysis of 27 mammalian and 9 avian PrPs reveals high conservation of flexible regions of the prion protein J. Mol. Biol. 1999, 1163-1178
67. Hiemstra, T.; Yong, H.; Van Riemsdijk, W. H. Interfacial charging phenomena of aluminum (hydr)oxides Langmuir 1999, 15, 5942-5955
68. Appel, C.; Ma, L. Q.; Rhue, R. D.; Kennelley, E. Point of zero charge determination in soils and minerals via traditional methods and detection of electoracoustic mobility Geoderma 2003, 113, 77-93
69. Brinza, L.; Benning, L. G.; Statham, P. J. Adsorption studies of Mo and V onto ferrihydrite Mineral. Mag. 2008, 72, 385-388
70. 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. Detection of protease-resistant cervid prion protein in water from a CWD-endemic area Prion 2009, 3, 171-183
71. Tomaszewski, J. E.; Madliger, M.; Pedersen, J. A.; Schwarzenbach, R. P.; Sander, M. Adsorption of insecticidal Cry1Ab protein to humic substances. 2. Influence of humic and fulvic acid charge and polarity characteristics Environ. Sci. Technol. 2012, 46, 9932-9940
72. Ohshima, H. Henry's function for electrophoresis of a cylindrical colloidal particle J. Coll. Interface Sci. 1996, 180, 299-301
73. Lemmon, E. W.; McLinden, M. O.; Friend, D. G.; Thermophysical Properties of Fluid Systems in NIST Chemistry WebBook, NIST Standard Reference Database Number 69, Eds. Linstrom, P.J.; Mallard, W.G., National Institute of Standards and Technology, Gaithersburg MD, 20899. http://webbook.nist.gov (accessed October 28, 2012)