The affinity of copper binding to the prion protein octarepeat domain: Evidence for negative cooperativity

Biochemistry

Volumn 45, Issue 43, 2006, Pages 13083-13092

  Walter, Eric D ^a   Chattopadhyay, Madhuri ^a   Millhauser, Glenn L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; COORDINATION REACTIONS; COPPER; DISSOCIATION; FLUORESCENCE; PARAMAGNETIC RESONANCE; POSITIVE IONS; QUENCHING;

CONCENTRATION RANGES; COORDINATION SPECIES; OCTAREPEAT DOMAINS;

PROTEINS;

COPPER ION; METAL ION; PRION PROTEIN;

ARTICLE; BINDING AFFINITY; DISSOCIATION CONSTANT; ELECTRON SPIN RESONANCE; FLUORESCENCE SPECTROSCOPY; METAL BINDING; NONHUMAN; OXIDATION REDUCTION REACTION; PEPTIDE SYNTHESIS; PRION DISEASE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN;

ALGORITHMS; AMINO ACID SEQUENCE; BINDING SITES; BINDING, COMPETITIVE; CIRCULAR DICHROISM; COPPER; ELECTRON SPIN RESONANCE SPECTROSCOPY; HISTIDINE; KINETICS; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; PRIONS; PROTEIN BINDING; REPETITIVE SEQUENCES, AMINO ACID; SPECTROMETRY, FLUORESCENCE;

EID: 33751108289     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060948r     Document Type: Article

References (34)

1. Prusiner, S. B. (1997) Prion diseases and the BSE crisis, Science 278, 245-251.
2. Prusiner, S. B. (1998) Prions, Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383.
3. Prusiner, S. B. (2003) Prion Biology and Diseases, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Herms, J., Tings, T., Gall, S., Madlung, A., Giese, A., Siebert, H., Schürmann, P., Windl, O., Brose, N., and Kretzschmar, H. (1999) Evidence of presynaptic location and function of the prion protein, J. Neurosci. 19, 8866-8875.
5. Vassallo, N., and Herms, J. (2003) Cellular prion protein function in copper homeostasis and redox signalling at the synapse, J. Neurochem. 86, 538-544.
6. 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, 13452-13456.
7. Inestrosa, N. C., Cerpa, W., and Varela-Nallar, L. (2005) Copper brain homeostasis: Role of amyloid precursor protein and prion protein, IUBMB Life 57, 645-650.
8. 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., Westway, D., and Kretzschmar, H. (1997) The cellular prion protein binds copper in vivo, Nature 390, 684-687.
9. Millhauser, G. L. (2004) Copper binding in the prion protein, Acc. Chem. Res. 37, 79-85.
10. 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.
11. Pauly, P. C., and Harris, D. A. (1998) Copper stimulates endocytosis of the prion protein, J. Biol. Chem. 273, 33107-33119.
12. Drisaldi, B., Coomaraswamy, J., Mastrangelo, P., Strome, B., Yang, J., Watts, J. C., Chishti, M. A., Marvi, M., Windl, O., Ahrens, R., Major, F., Sy, M. S., Kretzschmar, H., Fraser, P. E., Mount, H. T., and Westaway, D. (2004) Genetic mapping of activity determinants within cellular prion proteins: N-Terminal modules in PrPC offset pro-apoptotic activity of the Doppel helix B/B' region, J. Biol. Chem. 279, 55443-55454.
13. Roucou, X., Gains, M., and LeBlanc, A. C. (2004) Neuroprotective functions of prion protein, J. Neurosci. Res. 75, 153-161.
14. Brown, D. R., Schmidt, B., and Kretzschmar, H. A. (1998) Effects of copper on survival of prion protein knockout neurons and glia, J. Neurochem. 70, 1686-1693.
15. Kanaani, J., Prusiner, S. B., Diacovo, J., Baekkeskov, S., and Legname, G. (2005) Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hippocampal neurons in vitro, J. Neurochem. 95, 1373-1386.
16. Brown, D. R., Wong, B.-S., Hafiz, F., Clive, C., Haswell, S. J., and Jones, I. M. (1999) Normal prion protein has an activity like that of superoxide dismutase, Biochem. J. 344, 1-5.
17. Challopadhyay, M., Walter, E. D., Newell, D. J., Jackson, P. J., Aronoff-Spencer, E., Peisach, J., Gerfen, G. J., Bennett, B., Amholine, W. E., and Millhauser, G. L. (2005) The octarepeat domain of the prion protein binds Cu(II) with three distinct coordination modes at pH 7.4, J. Am. Chem. Soc. 127, 12647-12656.
18. 2+ binding sites in the N-terminal domain of the prion protein by EPR and CD spectroscopy, Biochemistry 39, 13760-13771.
19. 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 protein, Biochemistry 41, 3991-4001.
20. 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.
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. Kramer, M. L., Kratzin, H. D., Schmidt, B., Romer, A., Windl, O., Liemann, S., Hornemann, S., and Kretzschmar, H. (2001) Prion prolein binds copper within the physiological concentration range, J. Biol. Chem. 276, 16711-16719.
23. Garnett, A. P., and Viles, J. H. (2003) Copper binding to the octarepeals of the prion protein. Afffinity, specificity, folding and cooperativity: Insights from circular dichroism, J. Biol. Chem. 278, 6795-6802.
24. Jackson, G. S., Murray, I., Hosszu, L. L. P., 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.
25. 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.
26. Cantor, C. R., and Schimmel, P. R. (1980) Biophysical Chemistry, W. H. Freeman, San Francisco, CA.
27. Shields, S. B., and Franklin, S. J. (2004) De novo design of a copper(II)-binding helix-turn-helix chimera: The prion octarepeat motif in a new context, Biochemistry 43, 16086-16091.
28. Qin, K., Yang, Y., Mastrangelo, P., and Westaway, D. (2002) Mapping Cu(II) bindings sites in prion proteins by diethylpyrocarbonate modification and MALDI-TOF mass spectrometric "footprinting", J. Biol. Chem. 277, 1981-1990.
29. Koshland, D. E., Jr., and Hamadani, K. (2002) Proteomics and models for enzyme cooperativity, J. Biol. Chem. 277, 46841-46844.
30. Klamt, F., Dal-Pizzol, F., Conte D. A., Frota, M. L., Jr., Walz, R.. Andrades, M. E., Gomes, D. A., Silva, E., Brentani, R. R., Izquierdo, I., and Moreira, J. C. F. (2001) Imbalance of antioxidant defense in mice lacking cellular priori protein, Free Radical Biol. Med. 30, 1137-1144.
31. Hopt, A., Korte, S., Fink, H., Panne, U., Niessner, R., Jahn, R., Kretzschmar, H., and Herms, J. (2003) Methods for studying synaptosomal copper release, J. Neurosci. Methods 128, 159-172.
32. Kardos, J., Kovacs, I., Hajos, F., Kalman, M., and Simonyi, M. (1989) Nerve endings from rat brain tissue release copper upon depolarization. A possible role in regulating neuronal excitability, Neurosci. Lett. 103, 139-144.
33. May, P. M., Linder, P. W., and Williams, D. R. (1977) Computer simulation of metal-ion equilibria in biofluids: Models for the low-molecular-weight complex distribution of calcium(II), magnesium(II), manganese(II), iron(III), copper(II), zinc(II), and lead(II) ions in human blood plasma, J. Chem. Soc., Dalton Trans. 588-595.
34. Dawson, R. M. C., Elliot, D. C., Elliot, D. H., and Jones, K. M. (1986) Data for Biochemical Research, 3rd ed., pp 408-410, Oxford University Press, Oxford, U.K.