Copper pathology in vulnerable brain regions in Parkinson's disease

Neurobiology of Aging

Volumn 35, Issue 4, 2014, Pages 858-866

  Davies, Katherine M ^a,b   Bohic, Sylvain ^c,d,e   Carmona, Asunción ^f,g   Ortega, Richard ^f,g   Cottam, Veronica ^a   Hare, Dominic J ^h,i   Finberg, John P M ^j   Reyes, Stefanie ^a,b   Halliday, Glenda M ^a,b   Mercer, Julian F B ^k   Double, Kay L ^a,b,l  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^d EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^e UNIV GRENOBLE ALPES   (France)

^f UNIVERSITÉ DE BORDEAUX   (France)

^g CENTRE DE CALCUL DE L INSTITUT NATIONAL DE PHYSIQUE NUCLEAIRE ET DE PHYSIQUE DES PARTICULES   (France)

^h UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

ⁱ UNIVERSITY OF MELBOURNE   (Australia)

^j TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^k DEAKIN UNIVERSITY   (Australia)

^l UNIVERSITY OF SYDNEY   (Australia)

more..

Author keywords

Copper; Copper transporter 1 (Ctr1); Human brain; Parkinson's disease; Substantia nigra; Superoxide dismutase 1 (SOD1)

Indexed keywords

COPPER; COPPER TRANSPORTER PROTEIN 1; COPPER ZINC SUPEROXIDE DISMUTASE; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANATOMICAL VARIATION; ANTERIOR CINGULATE; ARTICLE; CELL SURVIVAL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIFFUSE LEWY BODY DISEASE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; LOCUS CERULEUS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SUBSTANTIA NIGRA; WESTERN BLOTTING;

COPPER; COPPER TRANSPORTER 1 (CTR1); HUMAN BRAIN; PARKINSON'S DISEASE; SUBSTANTIA NIGRA; SUPEROXIDE DISMUTASE 1 (SOD1);

ALPHA-SYNUCLEIN; CATION TRANSPORT PROTEINS; COPPER; GYRUS CINGULI; HUMANS; LOCUS COERULEUS; MOLECULAR TARGETED THERAPY; NEURONS; PARKINSON DISEASE; SUBSTANTIA NIGRA; SUPEROXIDE DISMUTASE;

EID: 84891373057     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.09.034     Document Type: Article

References (45)

1. Antharam V., Collingwood J.F., Bullivant J.P., Davidson M.R., Chandra S., Mikhaylova A., Finnegan M.E., Batich C., Forder J.R., Dobson J. High field magnetic resonance microscopy of the human hippocampus in Alzheimer's disease: quantitative imaging and correlation with iron. Neuroimage 2012, 59:1249-1260.
2. Ayton S., Lei P., Duce J.A., Wong B.X., Sedjahtera A., Adlard P.A., Bush A.I., Finkelstein D.I. Ceruloplasmin dysfunction and therapeutic potential for Parkinson disease. Ann. Neurol. 2012, 73:554-559.
3. Battaglia G., Fornai F., Busceti C.L., Aloisi G., Cerrito F., De Blasi A., Melchiorri D., Nicoletti F. Selective blockade of mGlu5 metabotropic glutamate receptors is protective against methamphetamine neurotoxicity. J.Neurosci. 2002, 22:2135-2141.
4. Bertinato J., Swist E., Plouffe L.J., Brooks S.P., L'Abbe M.R. Ctr2 is partially localized to the plasma membrane and stimulates copper uptake in COS-7 cells. Biochem. J. 2008, 409:731-740.
5. Binolfi A., Rodriguez E.E., Valensin D., D'Amelio N., Ippoliti E., Obal G., Duran R., Magistrato A., Pritsch O., Zweckstetter M., Valensin G., Carloni P., Quintanar L., Griesinger C., Fernandez C.O. Bioinorganic chemistry of Parkinson's disease: structural determinants for the copper-mediated amyloid formation of alpha-synuclein. Inorg. Chem. 2010, 49:10668-10679.
6. Bohic S., Murphy K., Paulus W., Cloetens P., Salome M., Susini J., Double K. Intracellular chemical imaging of the developmental phases of human neuromelanin using synchrotron X-ray microspectroscopy. Anal. Chem. 2008, 80:9557-9566.
7. Botella J.A., Bayersdorfer F., Schneuwly S. Superoxide dismutase overexpression protects dopaminergic neurons in a Drosophila model of Parkinson's disease. Neurobiol. Dis. 2008, 30:65-73.
8. Braak H., Del Tredici K., Rub U., de Vos R.A., Jansen Steur E.N., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 2003, 24:197-211.
9. Brown N.M., Torres A.S., Doan P.E., O'Halloran T.V. Oxygen and the copper chaperone CCS regulate posttranslational activation of Cu, Zn superoxide dismutase. Proc. Natl. Acad. Sci. U.S.A 2004, 101:5518-5523.
10. Carmona A., Deves G., Ortega R. Quantitative micro-analysis of metal ions in subcellular compartments of cultured dopaminergic cells by combination of three ion beam techniques. Anal. Bioanal. Chem. 2008, 390:1585-1594.
11. Cater M.A., La Fontaine S., Mercer J.F. Copper binding to the N-terminal metal-binding sites or the CPC motif is not essential for copper-induced trafficking of the human Wilson protein (ATP7B). Biochem. J. 2007, 401:143-153.
12. Dancis A., Haile D., Yuan D.S., Klausner R.D. The Saccharomyces cerevisiae copper transport protein (Ctr1p). Biochemical characterization, regulation by copper, and physiologic role in copper uptake. J.Biol. Chem. 1994, 269:25660-25667.
13. Davies K.M., Hare D.J., Cottam V., Chen N., Hilgers L., Halliday G., Mercer J.F., Double K.L. Localization of copper and copper transporters in the human brain. Metallomics 2013, 5:43-51.
14. de Bie P., Muller P., Wijmenga C., Klomp L.W. Molecular pathogenesis of Wilson and Menkes disease: correlation of mutations with molecular defects and disease phenotypes. J.Med. Genet. 2007, 44:673-688.
15. De Freitas J.M., Liba A., Meneghini R., Valentine J.S., Gralla E.B. Yeast lacking Cu-Zn superoxide dismutase show altered iron homeostasis. Role of oxidative stress in iron metabolism. J.Biol. Chem. 2000, 275:11645-11649.
16. Dexter D.T., Wells F.R., Lees A.J., Agid F., Agid Y., Jenner P., Marsden C.D. Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson's disease. J.Neurochem. 1989, 52:1830-1836.
17. Dickson D.W., Braak H., Duda J.E., Duyckaerts C., Gasser T., Halliday G.M., Hardy J., Leverenz J.B., Del Tredici K., Wszolek Z.K., Litvan I. Neuropathological assessment of Parkinson's disease: refining the diagnostic criteria. Lancet Neurol. 2009, 8:1150-1157.
18. Gray L.W., Peng F., Molloy S.A., Pendyala V.S., Muchenditsi A., Muzik O., Lee J., Kaplan J.H., Lutsenko S. Urinary copper elevation in a mouse model of Wilson's disease is a regulated process to specifically decrease the hepatic copper load. PloS One 2012, 7:e38327.
19. Halliday G.M., Ophof A., Broe M., Jensen P.H., Kettle E., Fedorow H., Cartwright M.I., Griffiths F.M., Shepherd C.E., Double K.L. Alpha-synuclein redistributes to neuromelanin lipid in the substantia nigra early in Parkinson's disease. Brain 2005, 128:2654-2664.
20. Harding A.J., Stimson E., Henderson J.M., Halliday G.M. Clinical correlates of selective pathology in the amygdala of patients with Parkinson's disease. Brain 2002, 125:2431-2445.
21. Henchcliffe C., Beal M.F. Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis. Nat. Clin. Pract. Neurol. 2008, 4:600-609.
22. Hirsch E., Graybiel A.M., Agid Y.A. Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 1988, 334:345-348.
23. Kaler S.G. ATP7A-related copper transport diseases-emerging concepts and future trends. Nat. Rev. Neurol. 2011, 7:15-29.
24. Ke B.X., Llanos R.M., Wright M., Deal Y., Mercer J.F. Alteration of copper physiology in mice overexpressing the human Menkes protein ATP7A. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290:R1460-R1467.
25. Knight S.A., Labbe S., Kwon L.F., Kosman D.J., Thiele D.J. Awidespread transposable element masks expression of a yeast copper transport gene. Genes Dev. 1996, 10:1917-1929.
26. Larner F., Sampson B., Rehkamper M., Weiss D.J., Dainty J.R., O'Riordan S., Panetta T., Bain P.G. High precision isotope measurements reveal poor control of copper metabolism in Parkinsonism. Metallomics 2013, 5:125-132.
27. Loeffler D.A., LeWitt P.A., Juneau P.L., Sima A.A., Nguyen H.U., DeMaggio A.J., Brickman C.M., Brewer G.J., Dick R.D., Troyer M.D., Kanaley L. Increased regional brain concentrations of ceruloplasmin in neurodegenerative disorders. Brain Res. 1996, 738:265-274.
28. Lombardo M.F., Ciriolo M.R., Rotilio G., Rossi L. Prolonged copper depletion induces expression of antioxidants and triggers apoptosis in SH-SY5Y neuroblastoma cells. Cell Mol. Life Sci. 2003, 60:1733-1743.
29. McCord J.M., Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J.Biol. Chem. 1969, 244:6049-6055.
30. Meloni G., Vasak M. Redox activity of alpha-synuclein-Cu is silenced by Zn(7)-metallothionein-3. Free Radic. Biol. Med. 2011, 50:1471-1479.
31. Montine T.J., Phelps C.H., Beach T.G., Bigio E.H., Cairns N.J., Dickson D.W., Duyckaerts C., Frosch M.P., Masliah E., Mirra S.S., Nelson P.T., Schneider J.A., Thal D.R., Trojanowski J.Q., Vinters H.V., Hyman B.T. National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease: a practical approach. Acta Neuropathol. 2012, 123:1-11.
32. Nose Y., Kim B.E., Thiele D.J. Ctr1 drives intestinal copper absorption and is essential for growth, iron metabolism, and neonatal cardiac function. Cell Metab. 2006, 4:235-244.
33. Popescu B.F., Robinson C.A., Rajput A., Rajput A.H., Harder S.L., Nichol H. Iron, copper, and zinc distribution of the cerebellum. Cerebellum 2009, 8:74-79.
34. Prohaska J.R. Comparison of copper metabolism between brindled mice and dietary copper-deficient mice using 67Cu. J.Nutr. 1983, 113:1212-1220.
35. Rees E.M., Thiele D.J. Identification of a vacuole-associated metalloreductase and its role in Ctr2-mediated intracellular copper mobilization. J.Biol. Chem. 2007, 282:21629-21638.
36. Rose F., Hodak M., Bernholc J. Mechanism of copper(II)-induced misfolding of Parkinson's disease protein. Sci. Rep. 2011, 1:11.
37. Santner A., Uversky V.N. Metalloproteomics and metal toxicology of alpha-synuclein. Metallomics 2010, 2:378-392.
38. Schaefer M., Gitlin J.D. Genetic disorders of membrane transport. IV. Wilson's disease and Menkes disease. Am. J. Physiol. 1999, 276:G311-G314.
39. Strausak D., Mercer J.F., Dieter H.H., Stremmel W., Multhaup G. Copper in disorders with neurological symptoms: Alzheimer's, Menkes, and Wilson diseases. Brain Res. Bull. 2001, 55:175-185.
40. Takahata K., Shimazu S., Katsuki H., Yoneda F., Akaike A. Effects of selegiline on antioxidant systems in the nigrostriatum in rat. J.Neural. Transm. 2006, 113:151-158.
41. Torsdottir G., Sveinbjornsdottir S., Kristinsson J., Snaedal J., Johannesson T. Ceruloplasmin and superoxide dismutase (SOD1) in Parkinson's disease: a follow-up study. J.Neurol. Sci. 2006, 241:53-58.
42. Tripanichkul W., Sripanichkulchai K., Duce J.A., Finkelstein D.I. 17Beta-estradiol reduces nitrotyrosine immunoreactivity and increases SOD1 and SOD2 immunoreactivity in nigral neurons in male mice following MPTP insult. Brain Res. 2007, 1164:24-31.
43. Uitti R.J., Rajput A.H., Rozdilsky B., Bickis M., Wollin T., Yuen W.K. Regional metal concentrations in Parkinson's disease, other chronic neurological diseases, and control brains. Can. J. Neurol. Sci. 1989, 16:310-314.
44. Wang X., Moualla D., Wright J.A., Brown D.R. Copper binding regulates intracellular alpha-synuclein localisation, aggregation and toxicity. J.Neurochem. 2010, 113:704-714.
45. Wright J.A., Wang X., Brown D.R. Unique copper-induced oligomers mediate alpha-synuclein toxicity. FASEB. J. 2009, 23:2384-2393.