Prion protein reduces both oxidative and non-oxidative copper toxicity

Journal of Neurochemistry

Volumn 98, Issue 3, 2006, Pages 677-689

  Haigh, Cathryn L ^a   Brown, David R ^a  

^a University of Bath   (United Kingdom)

Author keywords

Copper; Glycine; Oxidative Stress; Prion; PrP

Indexed keywords

COPPER; GLYCINE; PRION PROTEIN;

ARTICLE; LIPID PEROXIDATION; METAL BINDING; MUTATIONAL ANALYSIS; NEUROPROTECTION; NEUROTOXICITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION;

ANIMALS; CELLS, CULTURED; COPPER; FREE RADICALS; MICE; MUTATION; OXIDATIVE STRESS; PRIONS;

EID: 33745918650     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03906.x     Document Type: Article

References (56)

1. Armendariz A. D., Gonzalez M., Loguinov A. V. and Vulpe C. D. (2004) Gene expression profiling in chronic copper overload reveals upregulation of Prnp and App. Physiol Genomics 20 (1), 45-5.
2. Brown D. R. (1999) Prion protein expression aids cellular uptake and veratridine-induced release of copper. J. Neurosci. Res. 58, 717-725.
3. Brown D. R. (2001) Prion and prejudice: normal protein at the synapse. Trends Neurosci. 24, 85-90.
4. 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.
5. Brown D. R., Schmidt B. and Kretzschmar H. A. (1998) Effects of copper on survival of prion protein knockout neurones and glia. J. Neurochem. 70, 1686-1693.
6. Brown D. R., Qin K., Herms J. W et al. (1997a) The cellular prion protein binds copper in vivo. Nature 390, 684-687.
7. Brown D. R., Schulz-Schaeffer W. J., Schmidt B. and Kretzschmar H. A. (1997b) Prion protein-deficient cells show altered response to oxidative stress due to decreased SOD-1 activity. Exp Neurol. 146, 104-112.
8. Brown D. R., St. Nicholas R.J. and Canevari L. (2002) Lack of prion protein expression results in a neuronal phenotype sensitive to stress. J. Neurosci. Res. 67, 211-224.
9. Brown D. R., Wong B. S., Hafiz. 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.
10. 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.
11. Chacon M. A., Barria M. I., Lorca R., Huidobro-Toro J. P. and Inestrosa N. C. (2003) A human prion protein peptide (PrP(59-91)) protects against copper neurotoxicity. Mol. Psychiatry. 8, 853-862.
12. Cohen F. E. and Prusiner S. B. (1998) Pathologic conformations of prion proteins. Annu. Rev. Biochem. 67, 793-819.
13. Collinge J. (2001) Prion diseases of humans and animals. their causes and molecular basis. Annu. Rev. Neurosci. 24, 519-550.
14. 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.
15. Cuthbert J. A. (1995) Wilson's disease: a new gene and an animal model for an old disease. J. Invest Med. 43, 323-336.
16. Dupuis L., Mbebi C., Gonzalez, de Aguilar J. L., Rene F., Muller A., de Tapia M. and Loeffler J. P. (2002) Loss of prion protein in a transgenic model of amyotrophic lateral sclerosis. Mol Cell Neurosci. 19, 216-224.
17. Esterbauer H., Schaur R. J. and Zollner H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol. Med. 11, 81-128.
18. Frederikse P. H., Zigler Jr S. J., Farnsworth P. N. and Carper D. A. (2000) Prion protein expression in mammalian lenses. Curr. Eye. Res. 20, 137-143.
19. Guentchev M., Siedlak S. L., Jarius C., Tagliavini F., Castellani R. J., Perry G., Smith M. A. and Budka H. (2002) Oxidative damage to nucleic acids in human prion disease. Neurobiol. Dis. 9, 275-281.
20. Guentchev M., Voigtlander T., Haberler C., Groschup M. H. and Budka H. (2000) Evidence for oxidative stress in experimental prion disease. Neurobiol. Dis. 7, 270-273.
21. Haigh C. L., Edwards K. and Brown D. R. (2005) Copper binding is the governing determinant of prion protein turnover. Mol. Cell. Neuro. 30, 186-196.
22. Hartter D. E. and Barnea A. (1988) Brain tissue accumulates 67copper by two ligand-dependent saturable processes. A high affinity, low capacity and a low affinity, high capacity process. J. Biol. Chem. 263, 799-805.
23. Holme A., Daniels M., Sassoon J. and Brown D. R. (2003) A novel method of generating neuronal cell lines from gene-knockout mice to study prion protein membrane orientation. Eur. J. Neurosci. 18, 571-579.
24. Hutter G., Heppner F. L. and Aguzzi A. (2003) No superoxide dismutase activity of cellular prion protein in vivo. Biol. Chem. 384, 1279-1285.
25. Jagetia G. C., Ganapathi N. G. and Unnikrishnan M. K. (1993) Copperglycinate protects mice exposed to various doses of gamma radiation. Strahlenther Onkol. 169, 323-328.
26. Johnson R. E. and Campbell R. J. (1982) Wilson's disease. Electron microscopic, x-ray energy spectroscopic, and atomic absorption spectroscopic studies of corneal copper deposition and distribution. Laboratory Invest. 46, 564-569.
27. Kim B. H., Lee H. G., Choi J. K., Kim J. I., Choi E. K., Carp R. I. and Kim Y. S. (2004) The cellular prion protein (PrPC) prevents apoptotic neuronal cell death and mitochondrial dysfunction induced by serum deprivation. Mol Brain Res. 124, 40-50.
28. Klamt R, Dal-Pizzol F., Da Fronte Jr, M. L. C., Walz. R., Andrades M. E., Da Silva E. G., Brentani R. R., Izquierdo I. and Moreira J. C. F. (2001) Imbalance of antioxidant defense in mice lacking cellular prion protein. Free Rad Biol. Med. 30, 1137-1144.
29. Kuwahara C., Takeuchi A. M., Nishimura T. et al. (1999) Prions prevent neuronal cell-line death. Nature. 400, 225-226.
30. Lai J. C. K. and Blass J. P. (1984) Neurotoxic effects of copper. Neurochem. Res. 9, 1699-1711.
31. McLennan N. F., Brennan P. M., McNeill A. et al. (2004) Prion protein accumulation and neuroprotection in hypoxic brain damage. Am. J. Pathol. 165, 227-235.
32. Milhavet O., Mcmahon H. E., Rachidi W. et al. (2000) Prion infection impairs the cellular response to oxidative stress. Proc. Natl Acad. Sci. U S A 97, 13 937-13 942.
33. Mouillet-Richard S., Ermonval M., Chebassier C., Laplanche J. L., Lehmann S., Launay J. M. and Kellermann O. (2000) Signal transduction through prion protein. Science 289, 1925-1928
34. Nishimura T., Sakudo A., Nakamura I. et al. (2004) Cellular prion protein regulates intracellular hydrogen peroxide level and prevents copper-induced apoptosis. Biochem. Biophys. Res. Commun. 323, 218-222.
35. Pauly P. C. and Harris D. A. (1998) Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 273, 33 107-33 110.
36. Petersen R. B., Siedlak S. L., Lee H. G. et al. (2005) Redox metals and oxidative abnormalities in human prion diseases. Acta Neuropathol (Berl). 110, 232-238.
37. Predki P. F. and Sarkar B. (1992) Effect of replacement of 'zinc finger' zinc on estrogen receptor DNA interactions. J. Biol. Chem. 267, 5842-5846.
38. Prusiner S. B. (1982) Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144.
39. Prusiner S. B. (1998) Prions. Proc. Natl. Acad. Sci. USA 95, 13 363-13 383.
40. Rae T. D., Schmidt P. J., Pufahl R. A., Culotta V. C. and O'Halloran T. V. (1999) Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284, 805-808.
41. Roucou X. and Leblanc A. C. (2005) Cellular prion protein neuroprotective function: implications in prion diseases. J. Mol Med. 83, 3-11.
42. Salès N., Rodolfo K., Hässig R., Faucheux B., Di Giamberdino L. and Moya K. L. (1998) Cellular prion protein localization in rodent and primate brain. Eur. J. Neurosci. 10, 2464-2471.
43. Schmitt-Ulms G., Legname G., Baldwin M. A. et al. (2001) Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein. J. Mol. Biol. 314, 1209-1225.
44. Senator A., Rachidi W., Lehmann S., Favier A. and Benboubetra M. (2004) Prion protein protects against DNA damage induced by paraquat in cultured cells. Free Radic Biol. Med. 37, 1224-1230.
45. Shaked Y., Rosenmann H., Talmor G. and Gabizon R. (1999) A C-terminal-truncated PrP isoform is present in mature sperm. J. Biol. Chem. 274, 32 153-32 158.
46. Sunyach C., Jen A., Deng J., Fitzgerald K., Frobert Y., Grassi J., Mccaffrey M. W. and Morris R. (2003) The mechanism of internalisation of glycosylphosphatidylinositol-anchored prion protein. EMBO J. 22, 3591-3601.
47. Voigtlander T., Kloppel S., Birner P., Jarius C., Flicker H., Verghese-Nitolakaki S., Sklaviadis T., Guentchev M. and Budka H. (2001) Marked increase of neuronal prion protein immunoreactivity in Alzheimer's disease and human prion diseases. Acta Neuropathol (Berl). 101, 417-423.
48. Voskoboinik I., Greenough M., La Fontaine S., Mercer J. F. and Camakaris J. (2001) Functional studies on the Wilson copper P-type ATPase and toxic milk mouse mutant. Biochem. Biophys. Res. Commun. 281, 966-970.
49. WalZ. R., Amaral O. B., Rockenbach I. C., Roesler R., Izquierdo I., Cavalieiro E. A., Martins V. R. and Brentani R. R. (1999) Increased sensitivity to seizures in mice lacking cellular prion protein. Epilepsia 40, 1679-1682.
50. Watt N. T., Taylor D. R., Gillott A., Thomas D. A., Perera W. S. and Hooper N. M. (2005) Reactive oxygen species-mediated beta-cleavage of the prion protein in the cellular response to oxidative stress. J. Biol. Chem. in press.
51. Weise J., Crome O., Sandau R., Schulz-Schaeffer W, Bahr M. and Zerr I. (2004) Upregulation of cellular prion protein (PrPc) after focal cerebral ischemia and influence of lesion severity. Neurosci. Lett. 372, 146-150.
52. White A. R., Collins S. J., Maher F., Jobling M. F., Stewart L. R., Thyer J. M., Beyreuther K., Masters C. L. and Cappai R. (1999) Prion protein-deficient neurons reveal lower glutathione reductase activity and increased susceptibility to hydrogen peroxide toxicity. Am. J. Pathol. 155, 1723-1730.
53. Williams W. M., Stadtman E. R. and Moskovitz. J. (2004) Ageing and exposure to oxidative stress in vivo differentially affect cellular levels of PrP in mouse cerebral microvessels and brain parenchyma. Neuropathol Appl. Neurobiol. 30, 161-168.
54. Wong B. S., Brown D. R., Pan T. et al. (2001) Oxidative impairment in scrapie-infected mice is associated with brain metals perturbations and altered antioxidant activities. J. Neurochem. 79, 689-698.
55. Wopfher F., Weidenhofer G., Schneider R., von Brunn A., Gilch S., Schwarz. T. F., Werner T. and Schatzl H. M. (1999) Analysis of 27 mammalian and 9 avian PrPs reveals high conservation of flexible regions of the prion protein. J. Mol Biol. 289, 1163-1178.
56. Zeng F., Watt N. T., Walmsley A. R. and Hooper N. M. (2003) Tethering the N-terminus of the prion protein compromises the cellular response to oxidative stress. J. Neurochem. 84, 480-490.