Copper is toxic to PrP-ablated mice and exacerbates disease in a mouse model of E200K genetic prion disease

Neurobiology of Disease

Volumn 45, Issue 3, 2012, Pages 1010-1017

  Canello, Tamar ^a   Friedman Levi, Yael ^a   Mizrahi, Michal ^a   Binyamin, Orli ^a   Cohen, Eran ^a   Frid, Kati ^a   Gabizon, Ruth ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

Copper; Fibroblasts; Genetic; Oxidation; Prion; Transgenic

Indexed keywords

COPPER; PRION PROTEIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE EXACERBATION; EMBRYO; FIBROBLAST; HEAVY METAL POISONING; IRRITABILITY; LONG TERM EXPOSURE; MOUSE; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; ONSET AGE; PRION DISEASE; PRIORITY JOURNAL; PROTEIN FUNCTION; WALKING; WILD TYPE;

AGE FACTORS; ANIMALS; CELLS, CULTURED; CEREBELLUM; CHROMATOGRAPHY, AFFINITY; COPPER; COPPER SULFATE; CREUTZFELDT-JAKOB SYNDROME; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; FIBROBLASTS; GENE EXPRESSION REGULATION; GLUTAMIC ACID; HUMANS; IMIDAZOLES; LYSINE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PRIONS; PROTEIN BINDING;

EID: 84856573192     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.12.020     Document Type: Article

References (47)

1. Aguzzi A., et al. Molecular mechanisms of prion pathogenesis. Annu. Rev. Pathol. 2008, 3:11-40.
2. Armendariz A.D., et al. Gene expression profiling in chronic copper overload reveals upregulation of Prnp and App. Physiol. Genomics 2004, 20:45-54.
3. Bastianelli E. Distribution of calcium-binding proteins in the cerebellum. Cerebellum 2003, 2:242-262.
4. Bellingham S.A., et al. Regulation of prion gene expression by transcription factors SP1 and metal transcription factor-1. J. Biol. Chem. 2009, 284:1291-1301.
5. Ben-Hur T., et al. Transplanted multipotential neural precursor cells migrate into the inflamed white matter in response to experimental autoimmune encephalomyelitis. Glia 2003, 41:73-80.
6. Brown P., et al. Human spongiform encephalopathy: the National Institutes of Health series of 300 cases of experimentally transmitted disease. Ann. Neurol. 1994, 35:513-529.
7. Brown D.R., et al. The cellular prion protein binds copper in vivo. Nature 1997, 390:684-687.
8. Brown D.R., et al. Prion protein-deficient cells show altered response to oxidative stress due to decreased SOD-1 activity. Exp. Neurol. 1997, 146:104-112.
9. Bueler H., et al. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 1992, 356:577-582.
10. Canello T., et al. Methionine sulfoxides on PrPSc: a prion-specific covalent signature. Biochemistry 2008, 47:8866-8873.
11. Canello T., et al. Oxidation of Helix-3 methionines precedes the formation of PK resistant PrP. PLoS Pathog. 2010, 6:e1000977.
12. Chapman J., et al. The risk of developing Creutzfeldt-Jakob disease in subjects with the PRNP gene codon 200 point mutation. Neurology 1994, 44:1683-1686.
13. Diarra-Mehrpour M., et al. Prion protein prevents human breast carcinoma cell line from tumor necrosis factor alpha-induced cell death. Cancer Res. 2004, 64:719-727.
14. Ferrer I. Synaptic pathology and cell death in the cerebellum in Creutzfeldt-Jakob disease. Cerebellum 2002, 1:213-222.
15. Friedman-Levi Y., et al. Fatal and transmissible disease in a mouse model of genetic E200K Creutzfeldt-Jakob disease. Plos Phatog. 2011, 7(11):e1002350.
16. Gabizon R., et al. Purified prion proteins and scrapie infectivity copartition into liposomes. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:4017-4021.
17. Goldfarb L.G., et al. Creutzfeldt-Jacob disease associated with the PRNP codon 200Lys mutation: an analysis of 45 families. Eur. J. Epidemiol. 1991, 7:477-486.
18. Haviv Y., et al. Induced neuroprotection independently from PrPSc accumulation in a mouse model for prion disease treated with simvastatin. Arch. Neurol. 2008, 65:762-775.
19. Hebert C.D., et al. Subchronic toxicity of cupric sulfate administered in drinking water and feed to rats and mice. Fundam. Appl. Toxicol. 1993, 21:461-475.
20. Hijazi N., et al. Copper binding to PrPC may inhibit prion disease propagation. Brain Res. 2003, 993:192-200.
21. Hsiao K., Meiner Z., Kahana E., Cass C., Kahana I., Avrahami D., Scarlato G., Abramsky O., Prusiner S.B., Gabizon R. Mutation of the prion protein in Libyan Jews with Creutzfeldt-Jakob disease. N. Engl. J. Med. 1991, 324:1091-1097.
22. Jomova K., Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology 2011, 283:65-87.
23. Kim B.H., et al. The cellular prion protein (PrPC) prevents apoptotic neuronal cell death and mitochondrial dysfunction induced by serum deprivation. Brain Res. Mol. Brain Res. 2004, 124:40-50.
24. Kovacs G.G., et al. Genetic Creutzfeldt-Jakob disease associated with the E200K mutation: characterization of a complex proteinopathy. Acta Neuropathol. 2010, 121:39-57.
25. Lasmezas C.I., et al. Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein. Science 1997, 275:402-405.
26. Mallucci G.R., et al. Post-natal knockout of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration. EMBO J. 2002, 21:202-210.
27. Manson J.C., et al. 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol. Neurobiol. 1994, 8:121-127.
28. McKinley M.P., et al. Ultrastructural localization of scrapie prion proteins in cytoplasmic vesicles of infected cultured cells. Lab Invest. 1991, 65:622-630.
29. Meiner Z., et al. Familial Creutzfeldt-Jakob disease. Codon 200 prion disease in Libyan Jews. Medicine (Baltimore) 1997, 76:227-237.
30. Meiner Z., et al. Tau and 14-3-3 of genetic and sporadic Creutzfeldt-Jakob disease patients in Israel. J. Neurol. 2011, 258:255-262.
31. Meli M., et al. Dynamic diagnosis of familial prion diseases supports the beta2-alpha2 loop as a universal interference target. PLoS One 2011, 6:e19093.
32. Meyer R.K., et al. Separation and properties of cellular and scrapie prion proteins. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:2310-2314.
33. Moskovitz J., et al. Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12920-12925.
34. Muras A.G., et al. Prion protein ablation increases cellular aggregation and embolization contributing to mechanisms of metastasis. Int. J. Cancer 2009, 125:1523-1531.
35. Parkin E.T., et al. Cellular prion protein regulates beta-secretase cleavage of the Alzheimer's amyloid precursor protein. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11062-11067.
36. Prusiner S.B. Novel proteinaceous infectious particles cause scrapie. Science 1982, 216:136-144.
37. Prusiner S.B., Hsiao K.K. Human prion diseases. Ann. Neurol. 1994, 35:385-395.
38. Quaglio E., et al. Copper converts the cellular prion protein into a protease-resistant species that is distinct from the scrapie isoform. J. Biol. Chem. 2001, 276:11432-11438.
39. Roberts T.K., et al. PrPC, the cellular isoform of the human prion protein, is a novel biomarker of HIV-associated neurocognitive impairment and mediates neuroinflammation. Am. J. Pathol. 2010, 177:1848-1860.
40. Sakaguchi S., et al. Loss of cerebellar Purkinje cells in aged mice homozygous for a disrupted PrP gene. Nature 1996, 380:528-531.
41. Shaked Y., et al. A C-terminal-truncated PrP isoform is present in mature sperm. J. Biol. Chem. 1999, 274:32153-32158.
42. Shaked Y., et al. Copper binding to the PrP isoforms: a putative marker of their conformation and function. J. Virol. 2001, 75:7872-7874.
43. Shmerling D., et al. Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions. Cell 1998, 93:203-214.
44. Spudich S., et al. Complete penetrance of Creutzfeldt-Jakob disease in Libyan Jews carrying the E200K mutation in the prion protein gene. Mol. Med. 1995, 1:607-613.
45. Westergard L., et al. The cellular prion protein (PrP(C)): its physiological function and role in disease. Biochim. Biophys. Acta 2007, 1772:629-644.
46. Williams W.M., et al. Ageing and exposure to oxidative stress in vivo differentially affect cellular levels of PrP in mouse cerebral microvessels and brain parenchyma. Neuropathol. Appl. Neurobiol. 2004, 30:161-168.
47. Xu J. Preparation, culture, and immortalization of mouse embryonic fibroblasts. Curr. Protoc. Mol. Biol. 2005, Chapter 28.1.1-28.1.8.