Cellular prion protein function in copper homeostasis and redox signalling at the synapse

Journal of Neurochemistry

Volumn 86, Issue 3, 2003, Pages 538-544

  Vassallo, Neville ^a   Herms, Jochen W ^b  

^a UNIVERSITY OF MALTA   (Malta)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Calcium signalling; Cellular prion protein; Copper homeostasis; Oxidative stress; Redox reaction

Indexed keywords

CALCIUM ION; COPPER; FREE RADICAL; PRION PROTEIN;

CALCIUM SIGNALING; COPPER METABOLISM; HUMAN; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; SHORT SURVEY; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM; COPPER; HOMEOSTASIS; HUMANS; OXIDATION-REDUCTION; PRPC PROTEINS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 0041302374     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.01882.x     Document Type: Short Survey

References (57)

1. Atabay C., Cagnoli C. M., Kharlamov E., Ikonomovic M. D. and Manev H. (1996) Removal of serum from primary cultures of cerebellar granule neurones induces oxidative stress and DNA fragmentation. protection with antioxidants and glutamate receptor antagonists. J. Neurosci. Res. 43, 465-475.
2. Avery S. V. (2001) Metal toxicity in yeasts and the role of oxidative stress. Adv. Appl. Microbiol. 49, 111-142.
3. Bounhar Y., Zhang Y., Goodyer C. G. and LeBlanc A. (2001) Prion protein protects human neurones against Bax-mediated apoptosis. J. Biol. Chem. 276, 39145-39149.
4. Brown D. R., Qin K., Herms J. W., Madlung A., Manson J., Strome R., Fraser P. E., Kruck T., von Bohlen A., Schulz-Schaffer W., Giese A., Westaway D. and Kretzschmar H. (1997a) The cellular prion protein binds copper in vivo. Nature 390, 684-687.
5. 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.
6. 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.
7. Brown D. R., Clive C. and Haswell S. J. (2001) Antioxidant activity related to copper binding of native prion protein. J. Neurochem. 76, 69-76.
8. Budka H. (1997) Transmissible spongiform encephalopathies (prion diseases). In: Neuropathology The Diagnostic Approach., (Garcia, J. H., ed.), pp. 449-474. Mosby, St. Louis.
9. Chiarini L. B., Freitas A. R., Zanata S. M., Brentani R. R., Martins V. R. and Linden R. (2002) Cellular prion protein transduces neuroprotective signals. EMBO J. 21, 3317-3326.
10. + currents. Neurosci. Lett. 209, 49-52.
11. Collinge J., Whittington M. A., Sidle K. C., Smith C. J., Palmer M. S., Clarke A. R. and Jefferys J. G. (1994) Prion protein is necessary for normal synaptic function. Nature 370, 295-297.
12. C) in extracerebral tissues. Cell Tissue Res. 22, 77-84.
13. Fournier J. G., Escaig-Haye F. and Grigoriev V. (2000) Ultrastructural localization of prion proteins: physiological and pathological implications. Microscopy Res. Technol. 50, 76-88.
14. Garnett A. P. and Viles J. H. (2003) Copper binding to the octarepeats of the prion protein. Affinity, specificity, folding and cooperativity; insights from circular dichroism. J. Biol. Chem. 278, 6795-6802.
15. Halliwell B. and Gutteridge J. M. C. (1984) Oxygen toxicity, oxygen radicals, transition metals and diseases. Biochem. J. 219, 1-4.
16. 67copper. Synapse 2, 412-415.
17. Herms J., Tings T., Gall S., Madlung A., Giese A., Siebert H., Schurmann P., Windl O., Brose N. and Kretzschmar H. (1999) Evidence of pre-synaptic localization and function of the prion protein. J. Neurosci. 19, 8866-8875.
18. Herms J. W., Korte S., Gall S., Schneider I., Dunker S. and Kretzschmar H. (2000) Altered intracellular calcium homeostasis in cerebellar granule cells of prion protein-deficient mice. J. Neurochem. 75, 1487-1492.
19. + currents in cerebellar Purkinje cells. Neurobiol. Dis. 8, 324-330.
20. C exists in many nonneuronal tissues of sheep. J. Gen. Virol. 76, 2583-2587.
21. 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.
22. 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. USA 98, 8531-8535.
23. 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. 28, 139-144.
24. Kirkland R. A., Windelborn J. A., Kasprzak J. M. and Franklin J. L. (2002) A Bax-induced pro-oxidant state is critical for cytochrome c release during programmed neuronal death. J. Neurosci. 22, 6480-6490.
25. Klamt F., Dal-Pizzol F., Conte da Frota M. L., Walz R., Andrades M. E., da Silva E. G., Brentani R. R., Izquierdo I. and Fonseca Moreira J. C. (2001) Imbalance of antioxidant defense in mice lacking cellular prion protein. Free Radic. Biol. Med. 30, 1137-1144.
26. Kramer M. L., Kratzin H. D., Schmidt B., Romer A., Windl O., Liemann S., Homemann S. and Kretzschmar H. (2001) Prion protein binds copper within the physiological concentration range. J. Biol. Chem. 276, 16711-16719.
27. Kretzschmar H. A., Ironside J. W., DeArmond S. J. and Tateishi J. (1996) Diagnostic criteria for sporadic Creutzfeldt-Jakob disease. Arch. Neurol. 53, 913-920.
28. C as a copper-binding protein at the synapse. Arch. Virol. 16, 239-249.
29. Kristensson K., Feuerstein B., Taraboulos A., Hyun W. C., Prusiner S. B. and DeArmond S. J. (1993) Scrapie prions alter receptor-mediated calcium responses in cultured cells. Neurology 43, 2335-2341.
30. Kuwahara C., Takeuchi A. M., Nishimura T., Haraguchi K., Kubosaki A., Matsumoto Y., Saeki K., Matsumoto Y., Yokoyama T., Itohara S. and Onodera T. (1999) Prions prevent neuronal cell-line death. Nature 400, 225-226.
31. Lee K. S., Magalhaes A. C., Zanata S. M., Brentani R. R., Martins V. R. and Prado M. A. (2001) Internalization of mammalian fluorescent cellular prion protein and N-terminal deletion mutants in living cells. J. Neurochem. 79, 79-87.
32. Martins V. R., Mercadante A. F., Cabral A. L., Freitas A. R. and Castro R. M. (2001) Insights into the physiological function of cellular prion protein. Braz. J. Med. Biol. Res. 34, 585-595.
33. McKinley M. P., Bolton D. C. and Prusiner S. B. (1983) A protease-resistant protein is a structural component of the scrapie prion. Cell 35, 57-62.
34. McMahon H. E., Mange A., Nishida N., Creminon C., Casanova D. and Lehmann S. (2001) Cleavage of the amino terminus of the prion protein by reactive oxygen species. J. Biol. Chem. 276, 2286-2291.
35. Milhavet O., McMahon H. E., Rachidi W., Nishida N., Katamine S., Mange A., Arlotto M., Casanova D., Riondel J., Favier A. and Lehmann S. (2000) Prion infection impairs the cellular response to oxidative stress. Proc. Natl Acad. Sci. USA 97, 13937-13942.
36. Miura T., Hori I. A., Mototani H. and Takeuchi H. (1999) Raman spectroscopic study on the copper (II) binding mode of prion octapeptide and its pH dependence. Biochemistry 38, 11560-11569.
37. Nam S. C. and Hockberger P. E. (1992) Divalent ions released from stainless steel hypodermic needles reduce neuronal calcium currents. Pflugers Arch. 420, 106-108.
38. Pan K. M., Baldwin M., Nguyen J., Gasset M., Serban A., Groth D., Melhorn I., Ziwei H., Fletterick R. J., Cohen F. E. and Prusiner S. B. (1993) Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc. Natl Acad. Sci. USA 90, 10962-10966.
39. Pauly P. C. and Harris D. A. (1998) Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 273, 33107-33110.
40. Prusiner S. B. (1991) Molecular biology of prion diseases. Science 252, 1515-1522.
41. Prusiner S. B. (1998) Prions. Proc. Natl Acad. Sci. USA 95, 13363-13383.
42. Rachidi W., Vilette D., Guiraud P., Arlotto M., Riondel J., Laude H., Lehmann S. and Favier A. (2003) Expression of prion protein increases cellular copper binding and antioxidant enzyme activities but not copper delivery. J. Biol. Chem. 278, 9064-9072.
43. 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.
44. Stahl N., Borchelt D. R. and Prusiner S. B. (1990) Differential release of cellular and scrapie prion proteins from cellular membranes by phosphatidylinositol-specific phospholipase C. Biochemistry 29, 5405-5412.
45. Stockel 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.
46. Sumudhu W., Perera S. and Hooper N. M. (2001) Ablation of the metal ion-induced endocytosis of the prion protein by disease-associated mutation of the octarepeat region. Curr. Biol. 11, 519-523.
47. Thellung S., Florio T., Villa V., Corsaro A., Arena S., Amico C., Robello M., Salmona M., Forloni G., Bugiani O., Tagliavini F. and Schettini G. (2000) Apoptotic cell death and impairment of L-type voltage-sensitive calcium channel activity in rat cerebellar granule cells treated with the prion protein fragment 106-126. Neurobiol. Dis. 7, 299-309.
48. 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. USA 96, 2042-2047.
49. Waggoner D. J., Drisaldi B., Bartnikas T. B., Casareno R. L., Prohaska J. R., Gitlin J. and Harris D. A. (2000) Brain copper content and cuproenzyme activity do not vary with prion protein expression level. J Biol. Chem. 275, 7455-7458.
50. Wei J., Srinivasan C., Han H., Valentine J.S. and Gralla E.B. (2001) Evidence for a novel role of copper-zinc superoxide dismutase in zinc metabolism. J. Biol. Chem. 276, 44798-44803.
51. 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 neurones reveal lower glutathione reductase activity and increased susceptibility to hydrogen peroxide toxicity. Am. J. Pathol. 155, 1723-1730.
52. Wong B. S., Pan T., Liu T., Li R., Gambetti P. and Sy M. S. (2000) Differential contribution of superoxide dismutase activity by prion protein in vivo. Biochem. Biophys. Res. Commun. 273, 136-139.
53. Wong B. S., Brown D. R., Pan T., Whiteman M., Liu T., Bu X., Li R., Gambetti P., Olesik J., Rubenstein R. and Sy M. S. (2001a) Oxidative impairment in scrapie-infected mice is associated with brain metals perturbations and altered antioxidant activities. J. Neurochem. 79, 689-698.
54. 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. (2001b) Aberrant metal binding by prion protein in human prion disease. J. Neurochem. 78, 1400-1408.
55. Wong B. S., Liu T., Li R., Pan T., Petersen R. B., Smith M. A., Gambetti P., Perry G., Manson J. C., Brown D. R. and Sy M. S. (2001c) Increased levels of oxidative stress markers detected in the brains of mice devoid of prion protein. J. Neurochem. 76, 565-572.
56. Wong K., Qiu Y., Hyun W., Nixon R., VanCleff J., Sanchez-Salazar J., Prusiner S. B. and DeArmond S. J. (1996) Decreased receptor-mediated calcium response in prion-infected cells correlates with decreased membrane fluidity and IP3 release. Neurology 47, 741-750.
57. Zanata S. M., Lopes M. H., Mercadante A. F., Hajj G. N., Chiarini L. B., Nomizo R., Freitas A. R., Cabral A. L., Lee K. S., Juliano M. A., de Oliveira E., Jachieri S. G., Burlingame A., Huang L., Linden R., Brentani R. R. and Martins V. R. (2002) Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J. 21, 3307-3316.