Amyloidogenic metal-binding proteins: New investigative pathways

Biochemical Society Transactions

Volumn 36, Issue 6, 2008, Pages 1299-1303

  Davies, Paul ^a   Fontaine, Sarah N ^a   Moualla, Dima ^a   Wang, Xiaoyan ^a   Wright, Josephine A ^a   Brown, David R ^a  

^a University of Bath   (United Kingdom)

Author keywords

Alzheimer's disease; Amyloid precursor protein; Neurodegeneration; Parkinson's disease; Prion; Synuclein; Transmissible spongiform encephalopathy (TSE)

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BINDING PROTEIN; COPPER ION; METAL BINDING PROTEIN; PRION PROTEIN; UNCLASSIFIED DRUG; AMYLOID; METAL; PROTEIN;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; BINDING AFFINITY; DEGENERATIVE DISEASE; DISEASE MODEL; ELECTROCHEMISTRY; GENE EXPRESSION; HUMAN; INFECTION; METAL BINDING; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRION DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN FUNCTION; REVIEW; ANIMAL; CHEMISTRY; COMMUNICABLE DISEASE; GENETICS; METABOLISM;

AMYLOID; ANIMALS; COMMUNICABLE DISEASES; ELECTROCHEMISTRY; HUMANS; METALS; PROTEIN BINDING; PROTEINS;

EID: 59149103558     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0361299     Document Type: Review

References (50)

1. Roher, A.E., Lowenson, J.D., Clarke, S., Woods, A.S., Cotter, R.J., Gowing, E. and Ball, M.J. (1993) β-Amyloid-(1-42) is a major component of cerebrovascular amyloid deposits: implications for the pathology of Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 90, 10836-10840
2. Xia, W., Zhang, J., Perez, R., Koo, E.H. and Selkoe, D.J. (1997) Interaction between amyloid precursor protein and presenilins in mammalian cells: implications for the pathogenesis of Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 94, 8208-8213
3. Spillantini, M.G., Schmidt, M.L., Lee, V.M., Trojanowski, J.Q., Jakes, R. and Goedert, M. (1997) α-Synuclein in Lewy bodies. Nature 388, 839-840
4. Prusiner, S.B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383
5. Hesse, L., Beher, D., Masters, C.L. and Multhaup, G. (1994) The βA4 amyloid precursor protein binding to copper. FEBS Lett. 349, 109-116
6. Schmechel, A., Zentgraf, H., Scheuermann, S., Fritz, G., Pipkorn, R., Reed, J., Beyreuther, K., Bayer, T.A. and Multhaup, G. (2003) Alzheimer β-amyloid homodimers facilitate Aβ fibrillization and the generation of conformational antibodies. J. Biol. Chem. 278, 35317-35324
7. Bush, A.I., Multhaup, G., Moir, R.D., Williamson, T.G., Small, D.H., Rumble, B., Pollwein, P., Beyreuther, K. and Masters, C.L. (1993) A novel zinc(II) binding site modulates the function of the βA4 amyloid protein precursor of Alzheimer's disease. J. Biol. Chem. 268, 16109-16112
8. Atwood, C.S., Moir, R.D., Huang, X., Scarpa, R.C., Bacarra, M.E., Romano, D.M., Hartshorn, M.A., Tanzi, R.E. and Bush, A.I. (1998) Dramatic aggregation of Alzheimer Aβ by Cu(II) is induced by conditions representing physiological acidosis. J. Biol. Chem. 273, 12817-12826
9. 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
10. Brown, D.R. (1999) Prion protein expression aids cellular uptake and veratridine-induced release of copper. J. Neurosci. Res. 58, 717-725
11. Brown, D.R., Wong, B.S., Hatiz, F., Clive, C., Haswell, S. and Jones, I.M. (1999) Normal prion protein has an activity like that of superoxide dismutase. Biochem. J. 344, 1-5
12. Bocharova, O.V., Breydo, L., Salnikov, V.V. and Baskakov, I.V. (2005) Copper(II) inhibits in vitro conversion of prion protein into amyloid fibrils. Biochemistry 44, 6776-6787
13. Sigurdsson, E.M., Brown, D.R., Alim, M.A., Scholtzova, H., Carp, R., Meeker, H.C., Prelli, F., Frangione, B. and Wisniewski, T. (2003) Copper chelation delays the onset of prion disease. J. Biol. Chem. 278, 46199-46202
14. Zhu, F., Davies, P., Thomsett, A.R., Kelly, S.M., Tranter, G.E., Hecht, L., Isaacs, N.E., 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
15. 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
16. Rasia, R.M., Bertoncini, C.W., Marsh, D., Hoyer, W., Cherny, D., Zweckstetter, M., Griesinger, C., Jovin, T.M. and Fernández, C.O. (2005) Structural characterization of copper(II) binding to α-synuclein: insights into the bioinorganic chemistry of Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 102, 4294-4299
17. Bharathi and Rao, K.S. (2007) Thermodynamics imprinting reveals differential binding of metals to α-synuclein: relevance to Parkinson's disease. Biochem. Biophys. Res. Commun. 359, 115-120
18. Hornshaw, M.P., McDermott, J.R. and Candy, J.M. (1995) Copper binding to the N-terminal tandem repeat regions of mammalian and avian prion protein. Biochem. Biophys. Res. Commun. 207, 621-629
19. Brown, D.R., Qin, K., Herms, J.W., Madlung, A., Manson, J., Strome, R., Fraser, P.E., Kruck, T., von Bohlen, A., Schulz-Schaeffer, W. et al. (1997) The cellular prion protein binds copper in vivo. Nature 390, 684-687
20. Jackson, G.S., Murray, I., Hosszu, L.L., Gibbs, N., Waltho, J.P., Clarke, A.R. and Collinge, J. (2001) Location and properties of metal-binding sites on the human prion protein. Proc. Natl. Acad. Sci. U.S.A. 98, 8531-8535
21. Thompsett, A.R., Abdelraheim, S.R., Daniels, M. and Brown, D.R. (2005) High affinity binding between copper and full-length prion protein identified by two different techniques. J. Biol. Chem. 280, 42750-42758
22. Brown, D.R., Clive, C. and Haswell, S.J. (2001) Anti-oxidant activity related to copper binding of native prion protein. J. Neurochem. 76, 69-76
23. Wong, B.-S., Chen, S.G., Colucci, M., Xie, Z., Pan, T., Liu, T., Li, R., Gambetti, P., Sy, M.-S. and Brown, D.R. (2001) Aberrant metal binding by prion protein in human prion disease. J. Neurochem. 78, 1400-1408
24. Thackray, A.M., Knight, R., Haswell, S.J., Bujdoso, R. and Brown, D.R. (2002) Metal imbalance and compromised antioxidant function are early changes in prion disease. Biochem. J. 362, 253-258
25. 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
26. Multhaup, G., Schlicksupp, A., Hesse, L., Beher, D., Ruppert, T., Masters, C.L. and Beyreuther, K. (1996) The amyloid precursor protein of Alzheimer's disease in the reduction of copper(II) to copper(I). Science 271, 1406-1409
27. Multhaup, G., Ruppert, T., Schlicksupp, A., Hesse, L., Bill, E., Pipkorn, R., Masters, C.L. and Beyreuther, K. (1998) Copper-binding amyloid precursor protein undergoes a site-specific fragmentation in the reduction of hydrogen peroxide. Biochemistry 37, 7224-7230
28. Valensin, D., Mancini, F.M., Luczkowski, M., Janicka, A., Wisniewska, K., Gaggelli, E., Valensin, G., Lankiewicz, L. and Kozlowski, H. (2004) Identi.cation of a novel high af.nity copper binding site in the APP(145-155) fragment of amyloid precursor protein. Dalton Trans., 16-22
29. Bush, A.I. (2000) Metals and neuroscience. Curr. Opin. Chem. Biol. 4, 184-191
30. Atwood, C.S., Huang, X., Moir, R.D., Tanzi, R.E. and Bush, A.I. (1999) Role of free radicals and metal ions in the pathogenesis of Alzheimer's disease. Met. Ions Biol. Syst. 36, 309-364
31. Bush, A.I., Pettingell, W.H., Multhaup, G., de Paradis, M., Vonsattel, J.P., Gusella, J.F., Beyreuther, K., Masters, C.L. and Tanzi, R.E. (1994) Rapid induction of Alzheimer Aβ amyloid formation by zinc. Science 265, 1464-1467
32. 1-42. J. Neurochem. 75, 1219-1233
33. Paik, S.R., Shin, H.J., Lee, J.H., Chang, C.S. and Kim, J. (1999) Copper(II)-induced self-oligomerization of α-synuclein. Biochem. J. 340, 821-828
34. Binolfi, A., Rasia, R.M., Bertoncini, C.W., Ceolin, M., Zweckstetter, M., Griesinger, C., Jovin, T.M. and Fernández, C.O. (2006) Interaction of α-synuclein with divalent metal ions reveals key differences: a link between structure, binding specificity and fibrillation enhancement. J. Am. Chem. Soc. 128, 9893-9901
35. Hutter, G., Heppner, F.L. and Aguzzi, A. (2003) No superoxide dismutase activity of cellular prion protein in vivo. Biol. Chem. 384, 1279-1285
36. Jones, S., Batchelor, M., Bhelt, D., Clarke, A.R., Collinge, J. and Jackson, G.S. (2005) Recombinant prion protein does not possess SOD-1 activity. Biochem. J. 392, 309-312
37. White, A.R., Reyes, R., Mercer, J.F., Camakaris, J., Zheng, H., Bush, A.I,, Multhaup, G., Beyreuther, K., Masters, C.L. and Cappai, R. (1999) Copper levels are increased in the cerebral cortex and liver of APP and APLP2 knockout mice. Brain Res. 842, 439-444
38. Jiang, D., Men, L., Wang, J., Zhang, Y., Chickenyen, S., Wang, Y. and Zhou, F. (2007) Redox reactions of copper complexes formed with different β-amyloid peptides and their neuropathological relevance. Biochemistry 46, 9270-9282
39. Paik, S.R., Shin, H.J. and Lee, J.H. (2000) Metal-catalyzed oxidation of α-synuclein in the presence of copper(II) and hydrogen peroxide. Arch. Biochem. Biophys. 378, 269-277
40. Uversky, V.N., Li, J. and Fink, A.L. (2001) Metal-triggered structural transformations, aggregation, and fibrillation of human α-synuclein: a possible molecular NK between Parkinson's disease and heavy metal exposure. J. Biol. Chem. 276, 44284-44296
41. Quaglio, E., Chiesa, R. and Harris, D.A. (2001) Copper converts the cellular prion protein into a protease-resistant species that is distinct from the scrapie isoform. J. Biol. Chem. 276, 11432-11438
42. McKenzie, D., Bartz, J., Mirwald, J., Olander, D., Marsh, R. and Aiken, J. (1998) Reversibility of scrapie inactivation is enhanced by copper. J. Biol. Chem. 273, 25545-25547
43. Büeler, H., Aguzzi, A., Sailer, A., Greiner, R.A., Autenried, P., Aguet, M. and Weissmann, C. (1993) Mice devoid of PrP are resistant to scrapie. Cell 73, 1339-1347
44. Fischer, M., Rülicke, T., Raeber, A., Sailer, A., Moser, M., Oesch, B., Brandner, S., Aguzzi, A. and Weissmann, C. (1996) Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 15, 1255-1264
45. Singleton, A.B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R. et al. (2003) α-Synuclein locus triplication causes Parkinson's disease. Science 302, 841
46. Ohtake, H., Limprasert, P., Fan, Y., Onodera, O., Kakita, A., Takahashi, H., Bonner, L.T., Tsuang, D.W., Murray, I.V., Lee, V.M. et al. (2004) β-Synuclein gene alterations in dementia with Lewy bodies. Neurology 63, 805-811
47. Dingwall, C. (2007) A copper-binding site in the cytoplasmic domain of BACE1 identifies a possible link to metal homoeostasis and oxidative stress in Alzheimer's disease. Biochem. Soc. Trans. 35, 571-573
48. Varela-Nallar, L., Toledo, E.M., Larrondo, L.F., Cabral, A.L., Martins, V.R. and Inestrosa, N.C. (2006) Induction of cellular prion protein gene expression by copper in neurons. Am. J. Physiol. Cell Physiol. 290, C271-C281
49. Haigh, C.L., Wright, J.A. and Brown, D.R. (2007) Regulation of prion protein expression by non coding regions of the Prnp gene. J. Mol. Biol. 368, 915-927
50. 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