Copper(II) inhibits in vitro conversion of prion protein into amyloid fibrils

Biochemistry

Volumn 44, Issue 18, 2005, Pages 6776-6787

  Bocharova, Olga V ^a   Breydo, Leonid ^a   Salnikov, Vadim V ^a   Baskakov, Ilia V ^a,b,c  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CONCENTRATION (PROCESS); COPPER COMPOUNDS; DISEASES; DNA; GENETIC ENGINEERING; PATHOLOGY;

COPPER-INDUCED EFFECT; INCUBATION; MICROMOLAR CONCENTRATION; TRANSGENIC MICE;

PROTEINS;

AMYLOID; COPPER ION; MANGANESE; PRION PROTEIN; RECOMBINANT PROTEIN; ZINC;

ALPHA HELIX; ARTICLE; IN VITRO STUDY; PH; PRION DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE;

AMYLOID; ANIMALS; BINDING SITES; CATIONS, DIVALENT; COPPER; DRUG RESISTANCE; ENDOPEPTIDASE K; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; MACROMOLECULAR SUBSTANCES; MANGANESE; MICE; PEPTIDE FRAGMENTS; PRIONS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; ZINC;

MUS MUSCULUS;

EID: 18344391235     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050251q     Document Type: Article

References (76)

1. Prusiner, S. B. (1997) Prion diseases and the BSE crisis, Science 278, 245-251.
2. Pan, K.-M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., Cohen, F. E., and Prusiner, S. B. (1993) Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins, Proc. Natl. Acad. Sci. U.S.A. 90, 10962-10966.
3. Caughey, B. W., Dong, A., Bhat, K. S., Ernst, D., Hayes, S. F., and Caughey, W. S. (1991) Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy, Biochemistry 30, 7672-7680.
4. Prusiner, S. B. (1982) Novel proteinaceous infectious particles cause scrapie, Science 216, 136-144.
5. Hornemann, S., Schorn, C., and Wuthrich, K. (2004) NMR structure of bovine prion protein isolated from healthy calf brain, EMBO Rep., 5, 1159-1164.
6. Riek, R., Hornemann, S., Wider, G., Glockshuber, R., and Wüthrich, K. (1997) NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231,. FEBS Lett, 413, 282-288.
7. Donne, D. G., Viles, J. H., Groth, D., Mehlhorn, I., James, T. L., Cohen, F. E., Prusiner, S. B., Wright, P. E., and Dyson, H. J. (1997) Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible, Proc. Natl. Acad. Sci. U.S.A. 94, 13452-13457.
8. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R., and Wüthrich, K. (1996) NMR structure of the mouse prion protein domain PrP(121-231), Nature 382, 180-182.
9. James, T. L., Liu, H., Ulyanov, N. B., Farr-Jones, S., Zhang, H., Donne, D. G., Kaneko, K., Groth, D., Mehlhorn, I., Prusiner, S. B., and Cohen, F. E. (1997) Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform, Proc. Natl. Acad. Sci. U.S.A. 94, 10086-10091.
10. Jackson, G. S., Hosszu, L. L. P., Power, A., Hill, A. F., Kenney, J., Saibil, H., Craven, C. J., Waltho, J. P., Clarke, A. R., and Collinge, J. (1999) Reversible conversion of monomeric human prion protein between native and fibrilogenic conformations, Science, 283, 1935-1937.
11. Baskakov, I. V., Legname, G., Prusiner, S. B., and Cohen, F. E. (2001) Folding of prion protein to its native α-helical conformation is under kinetic control, J. Biol. Chem., 276, 19687-19690.
12. Rezaei, H., Choiset, Y., Eghiaian, F., Treguer, E., Mentre, P., Debey, P., Grosclaude, J., and Haertle, T. (2002) Amyloidogenic unfolding intermediates differentiate sheep prion protein variants, J. Mol. Biol., 322, 799-814.
13. Lee, S., and Eisenberg, D. (2003) Seeded conversion of recombinant prion protein to a disulfide-bonded oligomer by a reduction-oxidation process, Nat. Struct. Biol., 10, 725-730.
14. Kazlauskaite, J., Sanghera, N., Sylvester, I., Venien-Bryan, C., and Pinheiro, T. J. (2003) Structural changesof the prion protein in lipid membranes leading to aggregation and fibrillization, Biochemistry, 42, 3295-3304.
15. Sokolowski, F., Modler, A. J., Masuch, R., Zirwer, D., Baier, M., Lutsch, G., M. D. A., Gast, K., and Naumann, D. (2003) Formation of critical oligomers is a key event during conformational transition of recombinant syrian hamster prion protein, J. Biol. Chem. 278, 40481-40492.
16. Torrent, J., Alvarez-Martinez, M. T., Heitz, F., Liautard, J. P., Balny, C., and Lange, R. (2003) Alternative prion structural changes revealed by high pressure, Biochemistry 42, 1318-1325.
17. Cordeiro, Y., Machado, F., Juliano, L., Juliano, M. A., Brentani, R. R., Foguel, D., and Silva, J. L. (2001) DNA converts cellular prion protein into the beta-sheet conformation and inhibits prion peptide aggregation, J. Biol. Chem. 276, 49400-49409.
18. Swietnicki, W., Morillas, M., Chen, S. G., Gambetti, P., and Surewicz, W. K. (2000) Aggregation and fibrillization of the recombinant human prion protein huPrP90-231, Biochemistry 39, 424-431.
19. Baskakov, I. V., Legname, G., Gryczynski, Z., and Prusiner, S. B. (2004) The peculiar nature of unfolding of human prion protein, Protein Sci. 13, 586-595.
20. Baskakov, I.V., Legname, G., Baldwin, M. A., Prusiner, S. B., and Cohen, F. E. (2002) Pathway complexity of prion protein assembly into amyloid, J. Biol. Chem. 277, 21140-21148.
21. Baskakov, I. V. (2004) Autocatalytic conversion of recombinant prion proteins displays a species barrier, J. Biol. Chem. 279, 586-595.
22. Legname, G., Baskakov, I. V., Nguyen, H.-O. B., Riesner, D., Cohen, F.E., DeArmond, S. J., and Prusiner, S. B. (2004) Synthetic mammalian prions, Science 305, 673-676.
23. Gabus, C., Derrington, E., Leblanc, P., Chnaiderman, J., Dormont, D., Swietnicki, W., Morillas, M., Surewicz, W. K., Marc, D., Nandi, P., and Darlix, J. L. (2004) The prion protein has RNA binding chaperoning properties characteristic of nucleocasid protein NCP7 of HIV-1, J. Biol. Chem. 276, 19301-19309.
24. Warner, R. G., Hundt, C., Weiss, S., and Turnbull, J. E. (2002) Identification of the heparan sulfate binding sites in the cellular prion protein, J. Biol. Chem. 277, 18421-18430.
25. Gonzalez-Iglesias, R., Pajares, M. A., Espinosa, C. O. J. C., Oesch, B., and Gasset, M. (2002) Prion protein interaction with glycosaminoglycan occurs with the formation of oligomeric complexes stabilized by Cu(II) bridges, J. Mol. Biol. 319, 527-540.
26. Prusiner, S. B., McKinley, M. P., Bowman, K. A., Bolton, D. C., Bendheim, P. E., Groth, D. F., and Glenner, G. G. (1983) Scrapie prions aggregate to form amyloid-like birefringent rods, Cell 35, 349-358.
27. 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.
28. Lawson, V. A., Priola, S. A., Meade-White, K., Lawton, M., and Chesebro, B. (2004) Flexible N-terminal region of prion protein influences conformation of protease resistant prion protein isoforms associated with cross-species scrapie infection in vivo and in vitro, J. Biol. Chem. 279, 13689-13695.
29. 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., Giese, A., Westaway, D., and Kretzschmar, H. (1997) The cellular prion protein binds copper in vivo, Nature 390, 684-687.
30. Pattison, I. H., and Jebbett, J. N. (1971) Histopathological similarities between scrapie and cuprizone toxocity in mice, Nature 230, 115-117.
31. Hijazi, N., Shaked, Y., Rosenmann, H., Ben-Hur, T., and Gabizon, R. (2003) Copper binding to PrPC may inhibit prion disease propagation, Brain Res. 993, 192-200.
32. Sigurdsson, E. M., Brown, D. R., Alim, M. A., Scholtzove, H., Carp, R., Meeker, H. C., Prelli, F., Frangione, B., and Wisniewski, T. (2003) Copper chelation delayes the onset of prion disease, J. Biol. Chem. 278, 46199-46202.
33. Millhauser, G. L. (2004) Copper binding in the prion protein, Acc. Chem. Res. 37, 79-85.
34. Qin, K., Yang, D. S., Yang, Y., Chishti, M. A., Meng, L. J., Kretzchmar, H. A., Yip, C. M., Fraser, P. E., and Westaway, D. (2000) Copper(II)-induced conformational changes and proteasae resistance in recombinant and cellular PrP, J. Biol. Chem. 275, 19131.
35. Quaglio, E., Chiesa, B., and Harris, D. (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.
36. Goldfarb, L. G., Brown, P., McCombie, W. R., Goldgaber, D., Swergold, G. D., Wills, P. R., Cervenakova, L., Baron, H., Gibbs, C. J., Jr., and Gajdusek, D. C. (1991) Transmissible familial Creutzfeldt-Jakob disease associated with five, seven, and eight extra octapeptide coding repeats in the PRNP gene, Proc. Natl. Acad. Sci. U.S.A. 88, 10926-10930.
37. 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.
38. Hornshaw, M. P., McDermott, J. R., Candy, J. M., and Lakey, J. H. (1995) Copper binding to the N-terminal tandem repeat region of mammalian and avian prion protein: structural studies using synthetic peptides, Biochem. Biophys. Res. Commun. 214, 993-999.
39. 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.
40. Stöckel, J., Safar, J., Wallace, A. C., Cohen, F. E., and Prusiner, S. B. (1998) Prion protein selectively binds copper(II) ions, Biochemistry 37, 7185-7193.
41. Whittal, R. M., Ball, H. L., Cohen, F. E., Burlingame, A. L., Prusiner, S. B., and Baldwin, M. A. (2000) Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry, Protein Sci. 9, 332-343.
42. 2+ binding sites in the N-terminal domain of the prion protein by EPR and CD spectroscopy, Biochemistry 39, 13760-13771.
43. Viles, J. H., Cohen, F. E., Prusiner, S. B., Goodin, D. B., Wright, P. E., and Dyson, H. J. (1999) Copper binding to the prion protein: structural implications of four identical cooperative binding sites, Proc. Natl. Acad. Sci. U.S.A. 96, 2042-2047.
44. Garnett, A. P., and Viles, J. H. (2003) Copper binding to the octarepeats of the prion protein, J. Biol. Chem. 278, 6795-6802.
45. 2+ coordination by His96 and His111 induces b-sheet formation in the unstructured amyloidogenic region of the prion protein, J. Biol. Chem. 279, 32018-32027.
46. Burns, C. S., Aronoff-Spencer, E., Legname, G., Prusiner, S. B., Antholine, W. E., Gerfen, G. J., Peisach, J., and Millhauser, G. L. (2003) Copper coordination in the full-length, recombinant prion protein, Biochemistry 42, 6794-6803.
47. Jackson, G. S., Murray, I., Hosszu, 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.
48. Cohlberg, J. A., Li, J., Uversky, V. N., and Fink, A. L. (2002) Heparin and other glycosaminoglycans stimulate the formation of amyloid fibrils from a-synuclein in vitro, Biochemistry 41, 1502-1511.
49. 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.
50. Qin, K., Yang, Y., Mastrangelo, P., and Westaway, D. (2002) Mapping Cu(II) binding sites in prion proteins by diethyl pyrocarbonate modification and matrix assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometric foot-printing, J. Biol. Chem. 277, 1981-1990.
51. Bocharova, O. V., Breydo, L., Parfenov, A. S., Salnikov, V. V., and Baskakov, I. V. (2005) In vitro conversion of full length mammalian prion protein produces amyloid form with physical property of PrPSc, J. Mol. Biol. 346, 645-659.
52. Flechsig, E., Shmerling, D., Hegyi, I., Raeber, A. J., Fischer, M., Cozzio, A., von Mering, C., Aguzzi, A., and Weissmann, C. (2000) Prion protein devoid of the octapeptide repeat region restores susceptibility to scrapie in PrP knockout mice, Neuron 27, 399-408.
53. Zahn, R. (2003) The octapeptide repeats in mammalian prion protein constitue a pH-dependent folding and aggregqtion site, J. Mol. Biol. 334, 477-488.
54. Gonzalez-Iglesias, R., Elvira, G., Rodriguez-Navarro, J. A., Velez, M., Calero, M., Pajares, M. A., and Gasset, M. (2004) Cu2+ binding triggers aBoPrP assembly into insoluble laminar polymers, FEBS Lett. 556, 161-166.
55. Nishina, K., Jenks, S., and Supattapone, S. (2004) Ionic strength and transition metals control PrPSc protease resistance and conversion-inducing activity, J. Biol Chem. 279, 40788-40794.
56. Chiesa, R., Piccardo, P., Quaglio, E., Drisaldi, B., Si-Hoe, S. L., Takao, M., Ghetti, B., and Harris, D. A. (2003) Molecular distinction between pathogenic and infectious properties of the prion protein, J. Virol. 77, 7622.
57. Wadsworth, J. D. F., Hill, A. F., Joiner, S., Jackson, G. S., Clarke, A. R., and Collinge, J. (1999) Strain-specific prion-protein conformation determined by metal ions, Nat. Cell Biol. 1, 55-59.
58. Notari, S., Capellari, S., Giese, A., Westner, I., Baruzzi, A., Ghetti, B., Gambetti, P., Kretzschmar, H. A., and Parchi, P. (2004) Effects of different experimental conditions on the PrPSc core generated by protease digestion, J. Biol. Chem. 279, 16797-16804.
59. Jimenez, J. L., Guijarro, J. I., Orlova, E., Zurdo, J., Dobson, C. M., Sunde, M., and Saibil, H. (1999) Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing, EMBO J. 18, 815-821.
60. Jimenez, J. L., Nettleton, E. J., Bouchard, M., Robinson, C. V., Dobson, C. M., and Saibil, H. (2002) The protofilament structure of insulin amyloid fibrils, Proc. Nat. Acad. Sci. U.S.A. 99, 9196-9201.
61. Lashuel, H. A., LaBrenz, S. R., Woo, L., Serpell, L. C., and Kelly, J. W. (2000) Protofilaments, filaments, ribbons, and fibrils from peptidomimetic self-assembly: implications for amyloid fibril formation and materials science, J. Am. Chem. Soc. 122, 5262-5277.
62. Jansen, R., Dzwolak, W., and Winter, R. (2005) Amyloidogenic self-assembly of insulin aggregates probed by high-resolution atomic force microscopy, Biophys. J. 88, 1344-1353.
63. Khurana, R., and Fink, A. L. (2000) Do parallel β-helix proteins have a unique Fourier transform infrared spectrum?, Biophys. J. 78, 994-1000.
64. Rachidi, W., Mange, A., Senator, A., Guiraud, P., Riondel, J., Benboubetral, M., Favier, A., and Lehmann, S. (2003) Prion infection impairs copper binding of cultured cells, J. Biol. Chem. 278, 14595-14598.
65. Vassallo, N., and Herms, J. (2003) Cellular prion protein function in copper homeostasis and redox signaling at the synaps, J. Neurochem. 86, 544.
66. Giese, A., Levin, J., Bertsch, U., and Kretzchmar, H. A. (2004) Effect of metal ions on de novo aggregation of full-length prion protein, Biochem. Biophys. Res. Commun. 320, 1240-1246.
67. Levin, J., Bertsch, U., Kretzchmar, H. A., and Giese, A. (2005) Single particle analysis of manganese-induced prion protein aggregates, Biochem. Biophys. Res. Commun. 329, 1200-1207.
68. Cereghetti, G. M., Schweiger, A., Glockshuber, R., and Doorslaer, S. V. (2001) Electron paramagnetic resonance evidance for binding of Cu2+ to the C-terminal domain of the murine prion protein, Biophys. J. 81, 516-525.
69. Cereghetti, G. M., Schweiger, A., Glockshuber, R., and Doorslaer, S. V. (2003) Stability and Cu(II) binding of prion protein variants related to inherited human prion diseases, Biophys. J. 84, 1985-1997.
70. Hasnain, S. S., Murphy, L. M., Strange, R. W., Grossmann, J. G., Clarke, A. R., Jackson, G. S., and Collinge, J. (2001) XAFS study of the high-affinity copper-binding site of human PrP90-231 and its low-resolution structure in solution, J. Mol. Biol 311, 467-473.
71. Burns, C. S., Aronoff-Spencer, E., Dunham, C. M., Lario, P., Avdievich, N. I., Antholine, W. E., Olmstead, M.M., Vrielink, A., Gerfen, G. J., Peisach, J., Scott, W. G., and Millhauser, G. L. (2002) Molecular features of the copper binding sites in the octarepeat domain of the prion protien, Biochemistry 41, 4001.
72. Morante, S., Gonzalez-Iglesias, R., Potrich, C., Meneghini, C., Meyer-Klaucke, W., Menestrina, G., and Gasset, M. (2004) Inter-and intra-octarepeat Cu(II) site geometries in the prion protein: implications in Cu(II) binding cooperativity and Cu(II)-mediated assemblies, J. Biol. Chem. 279, 11753-11759.
73. DeArmond, S. J., Ironside, J. W., Bouzamondo, E., Peretz, D., and Fraser, J. R. (2004) Neuropathology of prion diseases, in Prion Biology and Diseases (Prusiner, S.B., ed), pp 777-856, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
74. DeArmond, S. J., McKinley, M. P., Barry, R. A., Braunfeld, M. B., McColloch, J. R., and Prusiner, S. B. (1985) Identification of prion amyloid filaments in scrapie-infected brain, Cell 41, 221-235.
75. Weissmann, C. (2004) The state of the prion, Nat. Rev. Microbiol. 2, 861-871.
76. Baskakov, I. V., and Bocharova, O. V. (2005) In Vitro conversion of mammalian prion protein into amyloid fibrils displays unusual features, Biochemistry 44, 2339-2348.