Prion protein polymerisation triggered by manganese-generated prion protein seeds

Journal of Neurochemistry

Volumn 120, Issue 1, 2012, Pages 177-189

  Hesketh, Shirley ^a   Thompsett, Andrew R ^a,b   Brown, David R ^a  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF EAST LONDON   (United Kingdom)

Author keywords

aggregation; bovine spongiform encephalopathy; CJD; manganese; prion; scrapie

Indexed keywords

MANGANESE; OLIGOMER; PRION PROTEIN; RECOMBINANT PROTEIN;

ALLELE; ARTICLE; CATALYSIS; CHICKEN; DISEASE RESISTANCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN POLYMERIZATION; SCRAPIE; SHEEP;

ALLELES; ANIMALS; BLOTTING, WESTERN; CATALYSIS; CHICKENS; HYDROGEN-ION CONCENTRATION; MANGANESE; MICROSCOPY, ELECTRON; MUTATION; POLYMERIZATION; POLYMORPHISM, GENETIC; PRIONS; RECOMBINANT PROTEINS; SCRAPIE; SHEEP; THIAZOLES;

BOVINAE; OVIS ARIES;

EID: 83855162745     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07540.x     Document Type: Article

References (43)

1. Baskakov I. V., Legname G., Prusiner S. B., and, Cohen F. E., (2001) Folding of prion protein to its native alpha-helical conformation is under kinetic control. J. Biol. Chem. 276, 19687-19690.
2. Bocharova O. V., Breydo L., Parfenov A. S., Salnikov V. V., and, Baskakov I. V., (2005a) In vitro conversion of full-length mammalian prion protein produces amyloid form with physical properties of PrP(Sc). J. Mol. Biol. 346, 645-659.
3. Bocharova O. V., Breydo L., Salnikov V. V., and, Baskakov I. V., (2005b) Copper(II) inhibits in vitro conversion of prion protein into amyloid fibrils. Biochemistry 44, 6776-6787. (Pubitemid 40637231)
4. Brazier M. W., Davies P., Player E., Marken F., Viles J. H., and, Brown D. R., (2008) Manganese binding to the prion protein. J. Biol. Chem. 283, 12831-12839.
5. Brazier M. W., Volitakis I., and, Kvasnicka M., et al. (2010) Manganese chelation therapy extends survival in a mouse model of M1000 prion disease. J. Neurochem. 114, 440-451.
6. Brown D. R., (2011) Prions and manganese: a maddening beast. Metallomics 3, 229-238.
7. Brown D. R., Hafiz F., Glasssmith L. L., Wong B. S., Jones I. M., Clive C., and, Haswell S. J., (2000) Consequences of manganese replacement of copper for prion protein function and proteinase resistance. EMBO J. 19, 1180-1186. (Pubitemid 30151014)
8. Bruce M. E., Will R. G., and, Ironside J. W., et al. (1997) Transmissions to mice indicate that 'new variant' CJD is caused by the BSE agent. Nature 389, 498-501. (Pubitemid 27435325)
9. Chakroun N., Prigent S., Dreiss C. A., Noinville S., Chapuis C., Fraternali F., and, Rezaei H., (2010) The oligomerization properties of prion protein are restricted to the H2H3 domain. FASEB J. 24, 3222-3231.
10. Cohen F. E., and, Prusiner S. B., (1998) Pathologic conformations of prion proteins. Annu. Rev. Biochem. 67, 793-819. (Pubitemid 28411145)
11. Cui T., Daniels M., Wong B. S., Li R., Sy M. S., Sassoon J., and, Brown D. R., (2003) Mapping the functional domain of the prion protein. Eur. J. Biochem. 270, 3368-3376. (Pubitemid 37020923)
12. Davies P., and, Brown D. R., (2008) The chemistry of copper binding to PrP: is there sufficient evidence to elucidate a role for copper in protein function? Biochem. J. 410, 237-244. (Pubitemid 351346181)
13. Davies P., and, Brown D. R., (2009) Manganese enhances prion protein survival in model soils and increases prion infectivity to cells. PLoS ONE 4, e7518.
14. Davies P., Marken F., Salter S., and, Brown D. R., (2009) Thermodynamic and voltammetric characterization of the metal binding to the prion protein: insights into pH dependence and redox chemistry. Biochemistry 48, 2610-2619.
15. Fitzmaurice T. J., Burke D. F., Hopkins L., Yang S., Yu S., Sy M. S., Thackray A. M., and, Bujdoso R., (2008) The stability and aggregation of ovine prion protein associated with classical and atypical scrapie correlates with the ease of unwinding of helix-2. Biochem. J. 409, 367-375. (Pubitemid 351184955)
16. Hesketh S., Sassoon J., Knight R., Hopkins J., and, Brown D. R., (2007) Elevated manganese levels in blood and central nervous system occur before onset of clinical signs in scrapie and bovine spongiform encephalopathy. J. Anim. Sci. 85, 1596-1609. (Pubitemid 46861507)
17. Hesketh S., Sassoon J., Knight R., and, Brown D. R., (2008) Elevated manganese levels in blood and CNS in human prion disease. Mol. Cell. Neurosci. 37, 590-598.
18. Kaneko K., Zulianello L., Scott M., Cooper C. M., Wallace A. C., James T. L., Cohen F. E., and, Prusiner S. B., (1997) Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proc. Natl. Acad. Sci. U S A 94, 10069-10074.
19. Kocisko D. A., Come J. H., Priola S. A., Chesebro B., Raymond G. J., Lansbury P. T., and, Caughey B., (1994) Cell-free formation of protease-resistant prion protein. Nature 370, 471-474. (Pubitemid 24263553)
20. Le Dur A., Beringue V., and, Andreoletti O., et al. (2005) A newly identified type of scrapie agent can naturally infect sheep with resistant PrP genotypes. Proc. Natl. Acad. Sci. U S A 102, 16031-16036. (Pubitemid 41552862)
21. Leffers K. W., Wille H., Stohr J., Junger E., Prusiner S. B., and, Riesner D., (2005) Assembly of natural and recombinant prion protein into fibrils. Biol. Chem. 386, 569-580. (Pubitemid 41447578)
22. Legleiter L. R., Liu H. C., Lloyd K. E., Hansen S. L., Fry R. S., and, Spears J. W., (2007) Exposure to low dietary copper or low copper coupled with high dietary manganese for one year does not alter brain prion protein characteristics in the mature cow. J. Anim. Sci. 85, 2895-2903. (Pubitemid 350105653)
23. Mallucci G., Dickinson A., Linehan J., Klohn P. C., Brandner S., and, Collinge J., (2003) Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302, 871-874. (Pubitemid 37339628)
24. Masel J., and, Jansen V. A., (1999) The kinetics of proteinase K digestion of linear prion polymers. Proc. Biol. Sci. 266, 1927-1931. (Pubitemid 29457078)
25. Masel J., Genoud N., and, Aguzzi A., (2005) Efficient inhibition of prion replication by PrP-Fc(2) suggests that the prion is a PrP(Sc) oligomer. J. Mol. Biol. 345, 1243-1251. (Pubitemid 40092237)
26. May B. C., Govaerts C., Prusiner S. B., and, Cohen F. E., (2004) Prions: so many fibers, so little infectivity. Trends Biochem. Sci. 29, 162-165. (Pubitemid 38472018)
27. Prusiner S. B., (1998) Prions. Proc. Natl. Acad. Sci. U S A 95, 13363-13383. (Pubitemid 28525623)
28. Riesner D., Kellings K., Post K., Wille H., Serban H., Groth D., Baldwin M. A., and, Prusiner S. B., (1996) Disruption of prion rods generates 10-nm spherical particles having high alpha-helical content and lacking scrapie infectivity. J. Virol. 70, 1714-1722. (Pubitemid 26062931)
29. Saborio G. P., Permanne B., and, Soto C., (2001) Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411, 810-813. (Pubitemid 32588105)
30. Silveira J. R., Raymond G. J., Hughson A. G., Race R. E., Sim V. L., Hayes S. F., and, Caughey B., (2005) The most infectious prion protein particles. Nature 437, 257-261. (Pubitemid 41294488)
31. Supattapone S., Bosque P., and, Muramoto T., et al. (1999) Prion protein of 106 residues creates an artifical transmission barrier for prion replication in transgenic mice. Cell 96, 869-878. (Pubitemid 29165089)
32. Supattapone S., Bouzamondo E., Ball H. L., Wille H., Nguyen H. O., Cohen F. E., DeArmond S. J., Prusiner S. B., and, Scott M., (2001) A protease-resistant 61-residue prion peptide causes neurodegeneration in transgenic mice. Mol. Cell. Biol. 21, 2608-2616. (Pubitemid 32222110)
33. Thackray A. M., Klein M. A., Aguzzi A., and, Bujdoso R., (2002a) Chronic subclinical prion disease induced by low-dose inoculum. J. Virol. 76, 2510-2517. (Pubitemid 34150719)
34. Thackray A. M., Knight R., Haswell S. J., Bujdoso R., and, Brown D. R., (2002b) Metal imbalance and compromised antioxidant function are early changes in prion disease. Biochem. J. 362, 253-258. (Pubitemid 34174483)
35. Thackray A. M., Klein M. A., and, Bujdoso R., (2003) Subclinical prion disease induced by oral inoculation. J. Virol. 77, 7991-7998. (Pubitemid 36792795)
36. Tsenkova R. N., Iordanova I. K., Toyoda K., and, Brown D. R., (2004) Prion protein fate governed by metal binding. Biochem. Biophys. Res. Commun. 325, 1005-1012. (Pubitemid 39487971)
37. Tzaban S., Friedlander G., Schonberger O., Horonchik L., Yedidia Y., Shaked G., Gabizon R., and, Taraboulos A., (2002) Protease-sensitive scrapie prion protein in aggregates of heterogeneous sizes. Biochemistry 41, 12868-12875. (Pubitemid 35192516)
38. Uppington K. M., and, Brown D. R., (2008) Resistance of cell lines to prion toxicity aided by phospho-ERK expression. J. Neurochem. 105, 842-852. (Pubitemid 351562734)
39. Will R. G., Ironside J. W., and, Zeidler M., et al. (1996) A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347, 921-925. (Pubitemid 26102546)
40. Wong B. S., Wang H., Brown D. R., and, Jones I. M., (1999) Selective oxidation of methionine residues in prion proteins. Biochem. Biophys. Res. Commun. 259, 352-355. (Pubitemid 29281236)
41. Wong B. S., Venien-Bryan C., Williamson R. A., Burton D. R., Gambetti P., Sy M. S., Brown D. R., and, Jones I. M., (2000) Copper refolding of prion protein. Biochem. Biophys. Res. Commun. 276, 1217-1224.
42. Wong B. S., Chen S. G., and, Colucci M., et al. (2001) Aberrant metal binding by prion protein in human prion disease. J. Neurochem. 78, 1400-1408. (Pubitemid 32899771)
43. Zhu F., Davies P., Thompsett A. R., Kelly S. M., Tranter G. E., Hecht L., Isaacs N. W., Brown D. R., and, Barron L. D., (2008) Raman optical activity and circular dichroism reveal dramatic differences in the influence of divalent copper and manganese ions on prion protein folding. Biochemistry 47, 2510-2517. (Pubitemid 351304556)