Role of the P-Type ATPases, ATP7A and ATP7B in brain copper homeostasis

Frontiers in Aging Neuroscience

Volumn 5, Issue AUG, 2013, Pages

  Telianidis, Jonathon ^a,d   Hung, Ya Hui ^b,c   Materia, Stephanie ^a   Fontaine, Sharon La ^a  

^a DEAKIN UNIVERSITY   (Australia)

^b FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d MONASH UNIVERSITY   (Australia)

Author keywords

ATP7A; ATP7A related motor neuropathy; ATP7B; Copper; Copper homeostasis; Menkes disease; Occipital horn syndrome; Wilson disease

Indexed keywords

COPPER; COPPER EXPORTING ADENOSINE TRIPHOSPHATASE; MENKES PROTEIN; WILSON DISEASE PROTEIN;

ALZHEIMER DISEASE; ASTROCYTE; BRAIN CAPILLARY; BRAIN CELL; BRAIN LEVEL; BRAIN METABOLISM; CAPILLARY ENDOTHELIUM; CELL TYPE; CENTRAL NERVOUS SYSTEM; CHOROID; ENDOTHELIUM CELL; ENZYME DEFECT; ENZYME REGULATION; EPITHELIUM CELL; HOMEOSTASIS; HUMAN; MENKES SYNDROME; MICROGLIA; MOTONEURON; MOTOR NEUROPATHY; NERVE CELL; NERVE DEGENERATION; NEUROBLASTOMA CELL; NEUROLOGIC DISEASE; NONHUMAN; PIGMENT EPITHELIUM; PINEAL BODY; PRION DISEASE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; WILSON DISEASE;

EID: 84897366042     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2013.00044     Document Type: Review

References (213)

1. Acevedo, K. M., Hung, Y. H., Dalziel, A. H., Li, Q. X., Laughton, K., Wikhe, K., et al. (2011). Copper promotes the trafficking of the amyloid precursor protein. J. Biol. Chem. 286, 8252-8262. doi: 10.1074/jbc.M110.128512
2. Achila, D., Banci, L., Bertini, I., Bunce, J., Ciofi-Baffoni, S., and Huffman, D. L. (2006). Structure of human Wilson protein domains 5 and 6 and their interplay with domain 4 and the copper chaperone HAH1 in copper uptake. Proc. Natl. Acad. Sci. U.S.A. 103, 5729-5734. doi: 10.1073/pnas.0504472103
3. Ackland, M. L., Cornish, E. J., Paynter, J. A., Grimes, A., Michalczyk, A., and Mercer, J. F. B. (1997). Expression of Menkes disease gene in mammary carcinoma cells. Biochem. J. 328, 237-243. Pubmed Abstract | Pubmed Full Text
4. Albrecht, P., Müller, A.-K., Ringelstein, M., Finis, D., Geerling, G., Cohn, E., et al. (2012). Retinal neurodegeneration in Wilson's disease revealed by spectral domain optical coherence tomography. PLoS ONE 7:e49825. doi: 10.1371/journal.pone.0049825
5. Allen, K., Buck, N., Cheah, D., Gazeas, S., Bhathal, P., and Mercer, J. (2006). Chronological changes in tissue copper, zinc and iron in the toxic milk mouse and effects of copper loading. Biometals 19, 555-564. doi: 10.1007/s10534-005-5918-5
6. Aon-Bertolino, M. L., Romero, J. I., Galeano, P., Holubiec, M., Badorrey, M. S., Saraceno, G. E., et al. (2011). Thioredoxin and glutaredoxin system proteinsimmunolocalization in the rat central nervous system. Biochim. Biophys. Acta 1810, 93-110. doi: 10.1016/j.bbagen.2010.06.011
7. Balijepalli, S., Tirumalai, P. S., Swamy, K. V., Boyd, M. R., Mieyal, J. J., and Ravindranath, V. (1999). Rat brain thioltransferase: regional distribution, immunological characterization, and localization by fluorescent in situ hybridization. J. Neurochem. 72, 1170-1178. doi: 10.1046/j.1471-4159.1999.0721170.x
8. Barnea, A., Hartter, D., Cho, G., Bhasker, K., Katz, B., and Edwards, M. (1990). Further characterization of the process of in vitro uptake of radiolabeled copper by the rat brain. J. Inorg. Biochem. 40, 103-110. doi: 10.1016/0162-0134(90)80043-W
9. Barnes, N., Tsivkovskii, R., Tsivkovskaia, N., and Lutsenko, S. (2005). The copper-transporting ATPases, Menkes and Wilson disease proteins, have distinct roles in adult and developing cerebellum. J. Biol. Chem. 280, 9640-9645. doi: 10.1074/jbc.M413840200
10. Barnes, N. L., Bartee, M., Y., Braiterman, L., Gupta, A., Ustiyan, V., Zuzel, V., et al. (2009). Cell-specific trafficking suggests a new role for renal ATP7B in the intracellular copper storage. Traffic 10, 767-779. doi: 10.1111/j.1600-0854.2009.00901.x
11. Bertram, L., Mcqueen, M. B., Mullin, K., Blacker, D., and Tanzi, R. E. (2007). Systematic meta-analyses of Alzheimer disease genetic association studies: the AlzGene database. Nat. Genet. 39, 17-23. doi: 10.1038/ng1934
12. Bohlken, A., Cheung, B. B., Bell, J. L., Koach, J., Smith, S., Sekyere, E., et al. (2009). ATP7A is a novel target of retinoic acid receptor [beta]2 in neuroblastoma cells. Br. J. Cancer 100, 96-105. doi: 10.1038/sj.bjc.6604833
13. Borjigin, J., Payne, A. S., Deng, J., Li, X., Wang, M. W., Ovodenko, B., et al. (1999). A novel pineal night-specific ATPase encoded by the Wilson disease gene. J. Neurosci. 19, 1018-1026. Pubmed Abstract | Pubmed Full Text
14. Borm, B., Moller, L. B., Hausser, I., Emeis, M., Baerlocher, K., Horn, N., et al. (2004). Variable clinical expression of an identical mutation in the ATP7A gene for Menkes disease/occipital horn syndrome in three affected males in a single family. J. Pediatr. 145, 119-121. doi: 10.1016/j.jpeds.2004.04.033
15. Braiterman, L., Nyasae, L., Guo, Y., Bustos, R., Lutsenko, S., and Hubbard, A. (2009). Apical targeting and Golgi retention signals reside within a 9-amino acid sequence in the copper-ATPase, ATP7B. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G433-G444. doi: 10.1152/ajpgi.90489.2008
16. Braiterman, L., Nyasae, L., Leves, F., and Hubbard, A. L. (2011). Critical roles for the COOH terminus of the Cu-ATPase ATP7B in protein stability, trans-Golgi network retention, copper sensing, and retrograde trafficking. Am. J. Physiol. Gastrointest. Liver Physiol. 301, G69-G81. doi: 10.1152/ajpgi.00038.2011
17. Brown, D. R., Qin, K., Herms, J. W., Madlung, A., Manson, J., Strome, R., et al. (1997). The cellular prion protein binds copper in vivo. Nature 390, 684-687. doi: 10.1038/37733
18. Brown, L. R., and Harris, D. A. (2003). Copper and zinc cause delivery of the prion protein from the plasma membrane to a subset of early endosomes and the Golgi. J. Neurochem. 87, 353-363. doi: 10.1046/j.1471-4159.2003.01996.x
19. Bucossi, S., Mariani, S., Ventriglia, M., Polimanti, R., Gennarelli, M., Bonvicini, C., et al. (2011). Association between the c. 2495 A>G ATP7B polymorphism and sporadic Alzheimer's disease. Int. J. Alzheimers Dis. 2011, 973692. doi: 10.4061/2011/973692 Pubmed Abstract | Pubmed Full Text
20. Bucossi, S., Polimanti, R., Mariani, S., Ventriglia, M., Bonvicini, C., Migliore, S., et al. (2012). Association of K832R and R952K SNPs of Wilson's disease gene with Alzheimer's disease. J. Alzheimers Dis. 29, 913-919. doi: 10.3233/JAD-2012-111997
21. Buiakova, O. I., Xu, J., Lutsenko, S., Zeitlin, S., Das, K., Das, S., et al. (1999). Null mutation of the murine ATP7B (Wilson disease) gene results in intracellular copper accumulation and late-onset hepatic nodular transformation. Hum. Mol. Genet. 8, 1665-1671. doi: 10.1093/hmg/8.9.1665
22. Bull, P. C., Thomas, G. R., Rommens, J. M., Forbes, J. R., and Cox, D. C. (1993). The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat. Genet. 5, 327-337 (Erratum in Nat. Genet. 1994, 6, 214). doi: 10.1038/ng1293-327
23. Burke, R., Commons, E., and Camakaris, J. (2008). Expression and localisation of the essential copper transporter DmATP7 in Drosophila neuronal and intestinal tissues. Int. J. Biochem. Cell Biol. 40, 1850-1860. doi: 10.1016/j.biocel.2008.01.021
24. Bush, A. I. (2013). The metal theory of Alzheimer's disease. J. Alzheimers Dis. 33, S277-S281. doi: 10.3233/JAD-2012-129011
25. Camakaris, J., Danks, D. M., Ackland, L., Cartwright, E., Borger, P., and Cotton, R. G. H. (1980). Altered copper metabolism in cultured cells from human Menkes' syndrome and mottled mouse mutants. Biochem. Genet. 18, 117-131. doi: 10.1007/BF00504364
26. Cartwright, G. E., and Wintrobe, M. M. (1964). Copper metabolism in normal subjects. Am. J. Clin. Nutr. 14, 224-232.
27. Cater, M. A., Forbes, J., La Fontaine, S., Cox, D., and Mercer, J. F. B. (2004). Intracellular trafficking of the human Wilson protein: the role of the six N-terminal metal binding sites. Biochem. J. 380(Pt 3), 805-813. doi: 10.1042/BJ20031804
28. Cater, M. A., La Fontaine, S., Deal, Y., Shield, K., and Mercer, J. F. B. (2006). ATP7B mediates vesicular sequestration of copper: insights into biliary copper excretion. Gastroenterology 130, 493-506. doi: 10.1053/j.gastro.2005.10.054
29. Cater, M. A., La Fontaine, S., and Mercer, J. F. (2007). 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. 401, 143-153. doi: 10.1042/BJ20061055
30. Chelly, J., Tumer, Z., Tonnesen, T., Petterson, A., Ishikawa-Brush, Y., Tommerup, N., et al. (1993). Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat. Genet. 3, 14-19. doi: 10.1038/ng0193-14
31. Choi, B. S., and Zheng, W. (2009). Copper transport to the brain by the blood-brain barrier and blood-CSF barrier. Brain Res. 1248, 14-21. doi: 10.1016/j.brainres.2008.10.056
32. Culotta, V. C., and Gitlin, J. D. (2001). "Disorders of copper transport," in The Metabolic and Molecular Basis of Inherited Disease, 8th Edn, eds C. R. Scriver, A. L. Beaudet, W. S. Sly, and D. Valle (New York: McGraw-Hill), 3105-3126.
33. Danks, D. M. (1995). "Disorders of copper transport," in The Metabolic and Molecular Basis of Inherited Disease, 7th Edn, eds C. R. Scriver, A. L. Beaudet, W. M. Sly, and D. Valle. (New York: McGraw-Hill), 2211-2235.
34. Danks, D. M., Campbell, P. E., Stevens, B. J., Mayne, V., and Cartwright, E. (1972). Menkes' kinky hair syndrome. Pediatrics 50, 188-201.
35. Das, S. K., and Ray, K. (2006). Wilson's disease: an update. Nat. Clin. Pract. Neurol. 2, 482-493. doi: 10.1038/ncpneuro0291
36. Davies, K. M., Hare, D. J., Cottam, V., Chen, N., Hilgers, L., Halliday, G., et al. (2013). Localization of copper and copper transporters in the human brain. Metallomics 5, 43-51. doi: 10.1039/c2mt20151h
37. Davies, P., and Brown, D. R. (2013). "Prion diseases, metals and antioxidants," in Brain Diseases and Metalloproteins, ed. D. R. Brown (Boca Raton: Pan Standford Publishing Pte. Ltd.), 249-293.
38. de Bie, P., Muller, P., Wijmenga, C., and Klomp, L. W. (2007). Molecular pathogenesis of Wilson and Menkes disease: correlation of mutations with molecular defects and disease phenotypes. J. Med. Genet. 44, 673-688. doi: 10.1136/jmg.2007.052746
39. de Bie, P., Vandesluis, B., Burstein, E., Berghe, P. V. E. V. D., Muller, P., Berger, R., et al. (2007). Distinct Wilson's disease mutations in ATP7B are associated with enhanced binding to COMMD1 and reduced stability of ATP7B. Gastroenterology 133, 1316-1326. doi: 10.1053/j.gastro.2007.07.020
40. DeMattos, R. B., Cirrito, J. R., Parsadanian, M., May, P. C., O'Dell, M. A., Taylor, J. W., et al. (2004). ApoE and clusterin cooperatively suppress A[beta] levels and deposition: evidence that ApoE regulates extracellular A[beta] metabolism in vivo. Neuron 41, 193-202. doi: 10.1016/S0896-6273(03)00850-X
41. Dierick, H. A., Adam, A. N., Escara-Wilke, J. F., and Glover, T. W. (1997). Immunocytochemical localization of the Menkes copper transport protein (ATP7A) to the trans Golgi network. Hum. Mol. Genet. 6, 409-416. doi: 10.1093/hmg/6.3.409
42. Donsante, A., Johnson, P., Jansen, L. A., and Kaler, S. G. (2010). Somatic mosaicism in Menkes disease suggests choroid plexus-mediated copper transport to the developing brain. Am. J. Med. Genet. A 152A, 2529-2534. doi: 10.1002/ajmg.a.33632
43. Donsante, A., Yi, L., Zerfas, P. M., Brinster, L. R., Sullivan, P., Goldstein, D. S., et al. (2011). ATP7A gene addition to the choroid plexus results in long-term rescue of the lethal copper transport defect in a Menkes disease mouse model. Mol. Ther. 19, 2114-2123. doi: 10.1038/mt.2011.143
44. Duc, H. H., Hefter, H., Stremmel, W., Castaneda-Guillot, C., Hernandez Hernandez, A., Cox, D. W., et al. (1998). His1069Gln and six novel Wilson disease mutations: analysis of relevance for early diagnosis and phenotype. Eur. J. Hum. Genet. 6, 616-623.
45. Ehrhart, J., Gluck, M., Mieyal, J., and Zeevalk, G. D. (2002). Functional glutaredoxin (thioltransferase) activity in rat brain and liver mitochondria. Parkinsonism Relat. Disord. 8, 395-400. doi: 10.1016/S1353-8020(02)00020-2
46. El Meskini, R., Cline, L. B., Eipper, B. A., and Ronnett, G. V. (2005). The developmentally regulated expression of Menkes protein ATP7A suggests a role in axon extension and synaptogenesis. Dev. Neurosci. 27, 333-348. doi: 10.1159/000086713
47. El Meskini, R., Crabtree, K. L., Cline, L. B., Mains, R. E., Eipper, B. A., and Ronnett, G. V. (2007). ATP7A (Menkes protein) functions in axonal targeting and synaptogenesis. Mol. Cell. Neurosci. 34, 409-421. doi: 10.1016/j.mcn.2006.11.018
48. El Meskini, R., Culotta, V. C., Mains, R. E., and Eipper, B. A. (2003). Supplying copper to the cuproenzyme peptidylglycine alpha-amidating monooxygenase. J. Biol. Chem. 278, 12278-12284. doi: 10.1074/jbc.M211413200
49. Emre, S., Atillasoy, E. O., Ozdemir, S., Schilsky, M., Rathna Varma, C. V., Thung, S. N., et al. (2001). Orthotopic liver transplantation for Wilson's disease: a singlecenter experience. Transplantation 72, 1232-1236. doi: 10.1097/00007890-200110150-00008
50. Ferreira, R., Heckenlively, J. R., Menkes, J. H., and Bateman, B. (1998). Menkes disease. New ocular and electroretinographic findings. Ophthalmology 105, 1076- 1078. doi: 10.1016/S0161-6420(98)96010-9
51. Forbes, J. R., and Cox, D. W. (2000). Copper-dependent trafficking of Wilson disease mutant ATP7B proteins. Hum. Mol. Genet. 9, 1927-1935. doi: 10.1093/hmg/9.13.1927
52. Francis, M. J., Jones, E. E., Levy, E. R., Ponnambalam, S., Chelly, J., and Monaco, A. P. (1998). A Golgi localization signal identified in the Menkes recombinant protein. Hum. Mol. Genet. 7, 1245-1252. doi: 10.1093/hmg/7.8.1245
53. Fujii, T., Ito, M., Tsuda, H., and Mikawa, H. (1990). Biochemical study on the critical period for treatment of the mottled brindled mouse. J. Neurochem. 55, 885- 889. doi: 10.1111/j.1471-4159.1990.tb04574.x
54. Geller, T., Pan, Y., and Martin, D. (1997). Early neuroradiologic evidence of degeneration in Menkes' disease. Pediatr. Neurol. 17, 255-258. doi: 10.1016/S0887-8994 (97)00092-1
55. Gitlin, J. D. (2003). Wilson disease. Gastroenterology 125, 1868-1877. doi: 10.1053/j.gastro.2003.05.010
56. Gouider-Khouja, N. (2009). Wilson's disease. Parkinsonism Relat. Disord. 15(Suppl 3), S126-S129. doi: 10.1016/S1353-8020(09)70798-9 CrossRef Full Text
57. Greenough, M., Pase, L., Voskoboinik, I., Petris, M. J., O'Brien, A. W., and Camakaris, J. (2004). Signals regulating trafficking of the Menkes (MNK; ATP7A) copper translocating P-type ATPase in polarized MDCK cells. Am. J. Physiol. Cell Physiol. 287, C1463-C1471. doi: 10.1152/ajpcell.00179.2004
58. Grimes, A., Hearn, C. J., Lockhart, P., Newgreen, D. F., and Mercer, J. F. B. (1997). Molecular basis of the brindled mouse mutant (Mobr): a murine model of Menkes disease. Hum. Mol. Genet. 6, 1037-1042. doi: 10.1093/hmg/6.7.1037
59. Guo, Y., Nyasae, L., Braiterman, L. T., and Hubbard, A. L. (2005). NH2-terminal signals in ATP7B Cu-ATPase mediate its Cu-dependent anterograde traffic in polarized hepatic cells. Am. J. Physiol. Gastrointest. Liver Physiol. 289, 904-916. doi: 10.1152/ajpgi.00262.2005
60. Halliwell, B., and Gutteridge, J. M. (1984). Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem. J. 219, 1-14.
61. Hamza, I., Faisst, A., Prohaska, J., Chen, J., Gruss, P., and Gitlin, J. D. (2001). The metallochaperone Atox1 plays a critical role in perinatal copper homeostasis. Proc. Natl. Acad. Sci. U.S.A. 98, 6848-6852. doi: 10.1073/pnas.111058498
62. Hamza, I., Prohaska, J., and Gitlin, J. D. (2003). Essential role for Atox1 in the copper-mediated intracellular trafficking of the Menkes ATPase. Proc. Natl. Acad. Sci. U.S.A. 100, 1215-1220. doi: 10.1073/pnas.0336230100
63. Hamza, I., Schaefer, M., Klomp, L. W. J., and Gitlin, J. (1999). Interaction of the copper chaperone HAH1 with the Wilson disease protein is essential for copper homeostasis. Proc. Natl. Acad. Sci. U.S.A. 96, 13363-13368. doi: 10.1073/pnas.96.23.13363
64. Harding, A. E., and Thomas, P. K. (1980). Genetic aspects of hereditary motor and sensory neuropathy (types I and II). J. Med. Genet. 17, 329-336. doi: 10.1136/jmg.17.5.329
65. Hartter, D., and Barnea, A. (1988). Evidence for release of copper in the brain: depolarization-induced release of newly taken-up 67copper. Synapse 2, 412-415. doi: 10.1002/syn.890020408
66. Hopt, A., Korte, S., Fink, H., Panne, U., Niessner, R., Jahn, R., et al. (2003). Methods for studying synaptosomal copper release. J. Neurosci. Methods 128, 159-172. doi: 10.1016/S0165-0270(03)00173-0
67. Hornshaw, M. P., Mcdermott, J. R., and Candy, J. M. (1995a). Copper binding to the N-terminal tandem repeat regions of mammalian and avian prion protein. Biochem. Biophys. Res. Commun. 207, 621-629. doi: 10.1006/bbrc.1995.1233
68. Hornshaw, M. P., Mcdermott, J. R., Candy, J. M., and Lakey, J. H. (1995b). Copper binding to the N-terminal tandem repeat region of mammalian and avian prion protein: structural studies using synthetic peptides. Biochem. Biophys. Res. Commun. 214, 993-999. doi: 10.1006/bbrc.1995.2384
69. Hung, I. H., Suzuki, M., Yamaguchi, Y., Yuan, D. S., Klausner, R. D., and Gitlin, J. D. (1997). Biochemical characterization of the Wilson disease protein and functional expression in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 272, 21461-21466. doi: 10.1074/jbc.272.34.21461
70. Hung, Y. H., Bush, A., and Cherny, R. (2010). Copper in the brain and Alzheimer's disease. J. Biol. Inorg. Chem. 15, 61-76. doi: 10.1007/s00775-009-0600-y
71. Hung, Y. H., Layton, M. J., Voskoboinik, I., Mercer, J. F., and Camakaris, J. (2007). Purification and membrane reconstitution of catalytically active Menkes coppertransporting P-type ATPase (MNK; ATP7A). Biochem. J. 401, 569-579. doi: 10.1042/BJ20060924
72. Hung, Y. H., Robb, E. L., Volitakis, I., Ho, M., Evin, G., Li, Q. X., et al. (2009). Paradoxical condensation of copper with elevated beta-amyloid in lipid rafts under cellular copper deficiency conditions: implications for Alzheimer disease. J. Biol. Chem. 284, 21899-21907. doi: 10.1074/jbc.M109.019521
73. Huster, D., Hoppert, M., Lutsenko, S., Zinke, J., Lehmann, C., Mossner, J., et al. (2003). Defective cellular localization of mutant ATP7B in Wilson's disease patients and hepatoma cell lines. Gastroenterology 124, 335-345. doi: 10.1053/gast.2003.50066
74. Iwase, T., Nishimura, M., Sugimura, H., Igarashi, H., Ozawa, F., Shinmura, K., et al. (1996). Localization of Menkes gene expression in the mouse brain; its association with neurological manifestations in Menkes model mice. Acta Neuropathol. 91, 482-488. doi: 10.1007/s004010050455
75. Kaler, S. G. (1998). Metabolic and molecular bases of Menkes disease and occipital horn syndrome. Pediatr. Dev. Pathol. 1, 85-98. doi: 10.1007/s100249900011
76. Kaler, S. G. (2011). ATP7A-related copper transport diseases - emerging concepts and future trends. Nat. Rev. Neurol. 7, 15-29. doi: 10.1038/nrneurol.2010.180
77. Kaler, S. G., Gallo, L. K., Proud, V. K., Percy, A. K., Mark, Y., Segal, N. A., et al. (1994). Occipital horn syndrome and a mild Menkes phenotype associated with splice site mutations at the MNK locus. Nat. Genet. 8, 195-202. doi: 10.1038/ng1094-195
78. Kaler, S. G., Holmes, C. S., Goldstein, D. S., Tang, J., Godwin, S. C., Donsante, A., et al. (2008). Neonatal diagnosis and treatment of Menkes disease. N. Engl. J. Med. 358, 605-614. doi: 10.1056/NEJMoa070613
79. Kaler, S. G., and Schwartz, J. P. (1998). Expression of the Menkes disease homolog in rodent neuroglial cells. Neurosci. Res. Commun. 23, 61-66. doi: 10.1002/ (SICI)1520-6769(199807/08)23:1<61::AID-NRC7>3.0.CO;2-J CrossRef Full Text
80. 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. doi: 10.1016/0304-3940(89)90565-X
81. Ke, B.-X., Llanos, R. M., Wright, M., Deal, Y., and Mercer, J. F. B. (2006). Alteration of copper physiology in mice overexpressing the human Menkes protein ATP7A. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R1460-R1467. doi: 10.1152/ajpregu.00806.2005
82. Kennerson, M., Nicholson, G., Kowalski, B., Krajewski, K., El-Khechen, D., Feely, S., et al. (2009). X-linked distal hereditary motor neuropathy maps to the DSMAX locus on chromosome Xq13.1-q21. Neurology 72, 246-252. doi: 10.1212/01.wnl.0000339483.86094.a5
83. Kennerson, M. L., Nicholson, G. A., Kaler, S. G., Kowalski, B., Mercer, J. F. B., Tang, J., et al. (2010). Missense mutations in the copper transporter gene ATP7A cause X-linked distal hereditary motor neuropathy. Am. J. Hum. Genet. 86, 343-352. doi: 10.1016/j.ajhg.2010.01.027
84. Kjellin, K. (1963). Determination of copper in cerebrospinal fluid by activation analysis. J. Neurochem. 10, 89-93. doi: 10.1111/j.1471-4159.1963.tb11468.x
85. Ko, J. H., Son, W., Bae, G. Y., Kang, J. H., Oh, W., and Yoo, O. J. (2006). A new hepatocytic isoform of PLZF lacking the BTB domain interacts with ATP7B, the Wilson disease protein, and positively regulates ERK signal transduction. J. Cell Biochem. 99, 719-734. doi: 10.1002/jcb.20980
86. Kodama, H., Meguro, Y., Abe, T., Rayner, M. H., Suzuki, K. T., Kobayashi, S., et al. (1991). Genetic expression of Menkes disease in cultured astrocytes of the macular mouse. J. Inherit. Metab. Dis. 14, 896-901. doi: 10.1007/BF01800470
87. Kodama, H., Okabe, I., Yanagisawa, M., Nomiyama, H., Nomiyama, K., Nose, O., et al. (1988). Does CSF copper level in Wilson disease reflect copper accumulation in the brain? Pediatr. Neurol. 4, 35-37. doi: 10.1016/0887-8994(88)90022-7
88. Kozlowski, H., Janicka-Klos, A., Brasun, J., Gaggelli, E., Valensin, D., and Valensin, G. (2009). Copper, iron, and zinc ions homeostasis and their role in neurodegenerative disorders (metal uptake, transport, distribution and regulation). Coord. Chem. Rev. 253, 2665-2685. doi: 10.1016/j.ccr.2009.05.011 CrossRef Full Text
89. Krajacic, P., Qian, Y., Hahn, P., Dentchev, T., Lukinova, N., and Dunaief, J. L. (2006). Retinal localization and copper-dependent relocalization of the Wilson and Menkes disease proteins. Invest. Ophthalmol. Vis. Sci. 47, 3129-3134. doi: 10.1167/iovs.05-1601
90. Kuivaniemi, H., Peltonen, L., and Kivirikko, K. I. (1985). Type IX Ehlers-Danlos syndrome and Menkes syndrome: the decrease in lysyl oxidase activity is associated with a corresponding deficiency in the enzyme protein. Am. J. Hum. Genet. 37, 798-808.
91. Kumode, M., Yamano, T., and Shimada, M. (1993). Neuropathological study on cerebellum of macular mutant mouse heterozygote. Acta Neuropath. 86, 411-417. doi: 10.1007/BF00228573
92. Kumode, M., Yamano, T., and Shimada, M. (1994). Histochemical study of mitochondrial enzymes in cerebellar cortex of macular mutant mouse, a model of Menkes kinky hair disease. Acta Neuropath. 87, 313-316. doi: 10.1007/BF00296748
93. Kuo, Y.-M., Gitschier, J., and Packman, S. (1997). Developmental expression of the mouse mottled and toxic milk genes suggests distinct functions for the Menkes and Wilson disease copper transporters. Hum. Mol. Genet. 6, 1043-1049. doi: 10.1093/hmg/6.7.1043
94. Kuo, Y. M., Gybina, A. A., Pyatskowit, J. W., Gitschier, J., and Prohaska, J. R. (2006). Copper transport protein (Ctr1) levels in mice are tissue specific and dependent on copper status. J. Nutr. 136, 21-26.
95. La Fontaine, S., Ackland, M. L., and Mercer, J. F. B. (2010). Mammalian copper-transporting P-type ATPases, ATP7A and ATP7B: emerging roles. Int. J. Biochem. Cell Biol. 42, 206-209. doi: 10.1016/j.biocel.2009.11.007
96. La Fontaine, S., Firth, S. D., Camakaris, J., Englezou, A., Theophilos, M. B., Petris, M. J., et al. (1998a). Correction of the copper transport defect of Menkes patient fibroblasts by expression of the Menkes and Wilson ATPases. J. Biol. Chem. 273, 31375-31380. doi: 10.1074/jbc.273.47.31375
97. La Fontaine, S., Firth, S. D., Lockhart, P. J., Brooks, H., Parton, R. G., Camakaris, J., et al. (1998b). Functional analysis and intracellular localization of the human Menkes protein (MNK) stably expressed from a cDNA construct in Chinese Hamster Ovary cells (CHO-K1). Hum. Mol. Genet. 7, 1293-1300. doi: 10.1093/hmg/7.8.1293
98. La Fontaine, S., Firth, S. D., Lockhart, P. J., Brooks, H., Camakaris, J., and Mercer, J. F. B. (1999). Intracellular localization and loss of copper-responsiveness of Mnk, the murine homologue of the Menkes protein, in cells from blotchy (Moblo) and brindled (Mobr) mouse mutants. Hum. Mol. Genet. 8, 1069-1075. doi: 10.1093/hmg/8.6.1069
99. La Fontaine, S., and Mercer, J. F. B. (2007). Trafficking of the copper-ATPases, ATP7A and ATP7B: role in copper homeostasis. Arch. Biochem. Biophys. 463, 149- 167. doi: 10.1016/j.abb.2007.04.021
100. La Fontaine, S., Theophilos, M. B., Firth, S. D., Gould, R., Parton, R. G., and Mercer, J. F. B. (2001). Effect of the toxic milk mutation (tx) on the function and intracellular localization of Wnd, the murine homologue of the Wilson copper ATPase. Hum. Mol. Genet. 10, 361-370. doi: 10.1093/hmg/10.4.361
101. Larin, D., Mekios, C., Das, K., Ross, B., An-Suei, Y., and Gilliam, T. C. (1999). Characterization of the interaction between the Wilson and Menkes disease proteins and the cytoplasmic copper chaperone, HAH1P. J. Biol. Chem. 274, 28497-28504. doi: 10.1074/jbc.274.40.28497
102. Lentner, C. (1981). Geigy Scientific Tables: Units of Measurement, Body Fluids, Composition of the Body, Nutrition. West Caldwell, NJ: Medical Education Division, Ciba-Geigy Corporation.
103. Levinson, B., Vulpe, C., Elder, B., Martin, C., Verley, F., Packman, S., et al. (1994). The mottled gene is the mouse homologue of the Menkes disease gene. Nat. Genet. 6, 369-373. doi: 10.1038/ng0494-369
104. Li, X., Chen, S., Wang, Q., Zack, D. J., Snyder, S. H., and Borjigin, J. (1998). A pineal regulatory element (PIRE) mediates transactivation by the pineal/retinaspecific transcription factor CRX. Proc. Natl. Acad. Sci. U.S.A. 95, 1876-1881. doi: 10.1073/pnas.95.4.1876
105. Lim, C. M., Cater, M. A., Mercer, J. F., and La Fontaine, S. (2006a). Copper-dependent interaction of glutaredoxin with the N termini of the copper-ATPases (ATP7A and ATP7B) defective in Menkes and Wilson diseases. Biochem. Biophys. Res. Commun. 348, 428-436. doi: 10.1016/j.bbrc.2006.07.067
106. Lim, C. M., Cater, M. A., Mercer, J. F. B., and La Fontaine, S. (2006b). Copper-dependent interaction of dynactin subunit p62 with the N terminus of ATP7B but not ATP7A. J. Biol. Chem. 281, 14006-14014. doi: 10.1074/jbc.M512745200
107. Linder, M. C. (1991). Biochemistry of Copper. New York: Plenum Press. doi: 10.1007/978-1-4757-9432-8 CrossRef Full Text
108. Linz, R., Barnes, N. L., Zimnicka, A. M., Kaplan, J. H., Eipper, B., and Lutsenko, S. (2008). Intracellular targeting of copper-transporting ATPase ATP7A in a normal and Atp7b -/- kidney. Am. J. Physiol. Renal. Physiol. 294, F53-F61. doi: 10.1152/ajprenal.00314.2007
109. Litwin, T., Gromadzka, G., and Czlonkowska, A. (2012). Apolipoprotein E gene (APOE) genotype in Wilson's disease: impact on clinical presentation. Parkinsonism Relat. Disord. 18, 367-369. doi: 10.1016/j.parkreldis.2011.12.005
110. Liu, P.-C., Chen, Y.-W., Centeno, J., Quezado, M., Lem, K., and Kaler, S. (2005a). Downregulation of myelination, energy, and translational genes in Menkes disease brain. Mol. Genet. Metab. 85, 291-300. doi: 10.1016/j.ymgme.2005.04.007
111. Liu, T., Bohlken, A., Kuljaca, S., Lee, M., Nguyen, T., Smith, S., et al. (2005b). The retinoid anticancer signal: mechanisms of target gene regulation. Br. J. Cancer 93, 310-318. doi: 10.1038/sj.bjc.6602700
112. Llanos, R. M., Ke, B.-X., Wright, M., Deal, Y., Monty, F., Kramer, D. R., et al. (2006). Correction of a mouse model of Menkes disease by the human Menkes gene. Biochim. Biophys. Acta 1762, 485-493. doi: 10.1016/j.bbadis.2005.12.011
113. Lutsenko, S., Barnes, N. L., Bartee, M. Y., and Dmitriev, O. Y. (2007). Function and regulation of human copper-transporting ATPases. Physiol. Rev. 87, 1011-1046. doi: 10.1152/physrev.00004.2006
114. Lutsenko, S., Bhattacharjee, A., and Hubbard, A. L. (2010). Copper handling machinery of the brain. Metallomics 2, 596-608. doi: 10.1039/c0mt00006j
115. Lyons, J. A., and Prohaska, J. R. (2009). Perinatal copper deficiency alters rat cerebellar purkinje cell size and distribution. Cerebellum 9, 136-144. doi: 10.1007/s12311-009-0136-2
116. Madsen, E., and Gitlin, J. D. (2007). Copper and iron disorders of the brain. Annu. Rev. Neurosci. 30, 317-337. doi: 10.1146/annurev.neuro.30.051606.094232
117. Madsen, E. C., Morcos, P. A., Mendelsohn, B. A., and Gitlin, J. D. (2008). In vivo correction of a Menkes disease model using antisense oligonucleotides. Proc. Natl. Acad. Sci. U.S.A. 105, 3909-3914. doi: 10.1073/pnas.0710865105
118. Mahley, R. W., Weisgraber, K. H., and Huang, Y. (2006). Apolipoprotein E4: a causative factor and therapeutic target in neuropathology, including Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 103, 5644-5651. doi: 10.1073/pnas.0600549103
119. Mann, J. R., Camakaris, J., Danks, D. M., and Walliczek, E. G. (1979). Copper metabolism in mottled mouse mutants: copper therapy of brindled (Mobr) mice. Biochem. J. 180, 605-612.
120. Materia, S., Cater, M. A., Klomp, L. W., Mercer, J. F., and La Fontaine, S. (2011). Clusterin (APOJ): a molecular chaperone that facilitates degradation of the copper- ATPases, ATP7A and ATP7B. J. Biol. Chem. 286, 10073-10083. doi: 10.1074/jbc.M110.190546
121. Materia, S., Cater, M. A., Klomp, L. W. J., Mercer, J. F. B., and La Fontaine, S. (2012). Clusterin and COMMD1 independently regulate degradation of the mammalian copper ATPases ATP7A and ATP7B. J. Biol. Chem. 287, 2485-2499. doi: 10.1074/jbc.M111.302216
122. Mendelsohn, B. A., Yin, C., Johnson, S. L., Wilm, T. P., Solnica-Krezel, L., and Gitlin, J. D. (2006). Atp7a determines a hierarchy of copper metabolism essential for notochord development. Cell Metab. 4, 155-162. doi: 10.1016/j.cmet.2006.05.001
123. Menkes, J. H., Alter, M., Steigleder, G. K., Weakley, D. R., and Sung, J. H. (1962). A sex-linked recessive disorder with retardation of growth, peculiar hair, and focal cerebral and cerebellar degeneration. Pediatrics 29, 764-779.
124. Mercer, J. F. B. (1998). Menkes syndrome and animal models. Am. J. Clin. Nutr. 67(Suppl.), 1022S-1028S.
125. Mercer, J. F. B., Grimes, A., Ambrosini, L., Lockhart, P., Paynter, J. A., Dierick, H., et al. (1994). Mutations in the murine homologue of the Menkes disease gene in dappled and blotchy mice. Nat. Genet. 6, 374-378. doi: 10.1038/ng0494-374
126. Mercer, J. F. B., Livingston, J., Hall, B. K., Paynter, J. A., Begy, C., Chandrasekharappa, S., et al. (1993). Isolation of a partial candidate gene for Menkes disease by positional cloning. Nat. Genet. 3, 20-25. doi: 10.1038/ng0193-20
127. Merner, N. D., Dion, P. A., and Rouleau, G. A. (2010). Recent advances in the genetics of distal hereditary motor neuropathy give insight to a disease mechanism involving copper homeostasis that may extend to other motor neuron disorders. Clin. Genet. 79, 23-34. doi: 10.1111/j.1399-0004.2010.01591.x
128. Michalczyk, A., Bastow, E., Greenough, M., Camakaris, J., Freestone, D., Taylor, P., et al. (2008). ATP7B expression in human breast epithelial cells is mediated by lactational hormones. J. Histochem. Cytochem. 56, 389-399. doi: 10.1369/jhc.7A7300.2008
129. Mieyal, J. J., Gallogly, M. M., Qanungo, S., Sabens, E. A., and Shelton, M. D. (2008). Molecular mechanisms and clinical implications of reversible protein Sglutathionylation. Antioxid. Redox Signal. 10, 1941-1988. doi: 10.1089/ars.2008.2089
130. Miyata, M., and Smith, J. D. (1996). Apolipoprotein E allele-specific antioxidant activity and effects on cytotoxicity by oxidative insults and [beta]-amyloid peptides. Nat. Genet. 14, 55-61. doi: 10.1038/ng0996-55
131. Monnot, A. D., Zheng, G., and Zheng, W. (2012). Mechanism of copper transport at the blood-cerebrospinal fluid barrier: influence of iron deficiency in an in vitro model. Exp. Biol. Med. (Maywood) 237, 327-333. doi: 10.1258/ebm.2011.011170
132. Monty, J.-F., Llanos, R. M., Mercer, J. F. B., and Kramer, D. R. (2005). Copper exposure induces trafficking of the Menkes protein in intestinal epithelium of ATP7A transgenic mice. J. Nutr. 135, 2762-2766.
133. Murata, Y., Kodama, H., Abe, T., Ishida, N., Nishimura, M., Levinson, B., et al. (1997). Mutation analysis and expression of the mottled gene in the macular mouse model of Menkes disease. Pediatr. Res. 42, 436-442. doi: 10.1203/00006450-199710000-00003
134. Niciu, M. J., Ma, X. M., El Meskini, R., Pachter, J. S., Mains, R. E., and Eipper, B. A. (2007). Altered ATP7A expression and other compensatory responses in a murine model of Menkes disease. Neurobiol. Dis. 27, 278-291. doi: 10.1016/j.nbd.2007.05.004
135. Niciu, M. J., Ma, X.-M., El-Meskini, R., Ronnett, G. V., Mains, R. E., and Eipper, B. A. (2006). Developmental changes in the expression of ATP7A during a critical period in postnatal neurodevelopment. Neuroscience 139, 947-964. doi: 10.1016/j.neuroscience.2006.01.044
136. Nishihara, E., Furuyama, T., Yamashita, S., and Mori, N. (1998). Expression of copper trafficking genes in the mouse brain. NeuroReport 9, 3259-3263. doi: 10.1097/00001756-199810050-00023
137. Norgate, M., Southon, A., Zou, S., Zhan, M., Sun, Y., Batterham, P., and Camakaris, J. (2007). Copper homeostasis gene discovery in Drosophila melanogaster. Biometals 20, 683-697. doi: 10.1007/s10534-006-9075-2
138. Nuutinen, T., Suuronen, T., Kauppinen, A., and Salminen, A. (2009). Clusterin: a forgotten player in Alzheimer's disease. Brain Res. Rev. 61, 89-104. doi: 10.1016/j.brainresrev.2009.05.007
139. Nyasae, L., Bustos, R., Braiterman, L., Eipper, B., and Hubbard, A. (2007). Dynamics of endogenous ATP7A (Menkes protein) in intestinal epithelial cells: copperdependent redistribution between two intracellular sites. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1181-G1194. doi: 10.1152/ajpgi.00472.2006
140. Okabe, M., Saito, S., Saito, T., Ito, K., Kimura, S., Niioka, T., et al. (1998). Histochemical localization of superoxide dismutase activity in rat brain. Free Radic. Biol. Med. 24, 1470-1476. doi: 10.1016/S0891-5849(98)00013-6
141. Okeda, R., Gei, S., Chen, I., Okaniwa, M., Shinomiya, M., and Matsubara, O. (1991). Menkes' kinky hair disease: morphological and immunohistochemical comparison of two autopsied patients. Acta Neuropathol. (Berl.) 81, 450-457. doi: 10.1007/BF00293467
142. Petris, M. J., Camakaris, J., Greenough, M., La Fontaine, S., and Mercer, J. F. B. (1998). A C-terminal di-leucine is required for localization of the Menkes protein in the trans-Golgi network. Hum. Mol. Genet. 7, 2063-2071. doi: 10.1093/hmg/7.13.2063
143. Petris, M. J., and Mercer, J. F. B. (1999). The Menkes protein (ATP7A; MNK) cylces via the plasma membrane both in basal and elevated extracellular copper using a C-terminal di-leucine endocytic signal. Hum. Mol. Genet. 8, 2107-2115. doi: 10.1093/hmg/8.11.2107
144. Petris, M. J., Mercer, J. F. B., Culvenor, J. G., Lockhart, P., Gleeson, P. A., and Camakaris, J. (1996). Ligand-regulated transport of the Menkes copper P-type ATPase efflux pump from the Golgi apparatus to the plasma membrane: a novel mechanism of regulated trafficking. EMBO J. 15, 6084-6095.
145. Petris, M. J., Strausak, D., and Mercer, J. F. B. (2000). The Menkes copper transporter is required for the activation of tyrosinase. Hum. Mol. Genet. 9, 2845-2851. doi: 10.1093/hmg/9.19.2845
146. Petris, M. J., Voskoboinik, I., Cater, M., Smith, K., Kim, B. E., Llanos, R. M., et al. (2002). Copper-regulated trafficking of the Menkes disease copper ATPase is associated with formation of a phosphorylated catalytic intermediate. J. Biol. Chem. 277, 46736-46742. doi: 10.1074/jbc.M208864200
147. Petrukhin, K., Fischer, S. G., Pirastu, M., Tanzi, R. E., Chernov, I., Devoto, M., et al. (1993). Mapping, cloning ang genetic characterization of the region containing the Wilson disease gene. Nat. Genet. 5, 338-343. doi: 10.1038/ng1293-338
148. Pfeiffer, R. F. (2007). Wilson's disease. Semin. Neurol. 27, 123-132. doi: 10.1055/s-2007-971173
149. Phinney, A., Drisaldi, B., Sd Schmidt, A., Lugowski, S., Coronado, V., Liang, Y., et al. (2003). In vivo reduction of amyloid-beta by a mutant copper transporter. Proc. Natl. Acad. Sci. U.S.A. 100, 14193-14198. doi: 10.1073/pnas.2332851100
150. Prusiner, S. B. (1982). Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144. doi: 10.1126/science.6801762
151. Qi, M., and Byers, P. H. (1998). Constitutive skipping of alternatively spliced exon 10 in the ATP7A gene abolishes Golgi localization of the Menkes protein and produces the occipital horn syndrome. Hum. Mol. Genet. 7, 465-469. doi: 10.1093/hmg/7.3.465
152. Qian, Y., Tiffany-Castiglioni, E., and Harris, E. D. (1997). A Menkes P-type ATPase involved in copper homeostasis in the central nervous system of the rat. Brain Res. Mol. Brain Res. 48, 60-66. doi: 10.1016/S0169-328X(97)00083-1
153. Qian, Y., Tiffany-Castiglioni, E., Welsh, J., and Harris, E. D. (1998). Copper efflux from murine microvascular cells requires expression of the Menkes disease Cu- ATPase. J. Nutr. 128, 1276-1282.
154. Qin, Z., Itoh, S., Jeney, V., Ushio-Fukai, M., and Fukai, T. (2005). Essential role for the Menkes ATPase in activation of extracellular superoxide dismutase: implication for vascular oxidative stress. FASEB J. 334-336. doi: 10.1096/fj.05-4564fje
155. Rajan, K., Colburn, R., and Davis, J. (1976). Distribution of metal ions in the subcellular fractions of several rat brain areas. Life Sci. 18, 423-431. doi: 10.1016/0024- 3205(76)90220-4
156. Roberts, B. R., Ryan, T. M., Bush, A. I., Masters, C. L., and Duce, J. A. (2012). The role of metallobiology and amyloid-?? peptides in Alzheimer's disease. J. Neurochem. 120, 149-166. doi: 10.1111/j.1471-4159.2011.07500.x
157. Roelofsen, H., Wolters, H., Luyn, M. J. A. V., Miura, N., Kuipers, F., and Vonk, R. J. (2000). Copper-induced apical trafficking of ATP7B in polarized hepatoma cells provides a mechanism for biliary copper excretion. Gastroenterology 119, 782-793. doi: 10.1053/gast.2000.17834
158. Rossor, A. M., Kalmar, B., Greensmith, L., and Reilly, M. M. (2012). The distal hereditary motor neuropathies. J. Neurol. Neurosurg. Psychiatry 83, 6-14. doi:10.1136/jnnp-2011-300952
159. Royce, P. M., Camakaris, J., and Danks, D. M. (1980). Reduced lysyl oxidase activity in skin fibroblasts from patients with Menkes' syndrome. Biochem. J. 192, 579- 586.
160. Saito, T., Nagao, T., Okabe, M., and Saito, K. (1996). Neurochemical and histochemical evidence for an abnormal catecholamine metabolism in the cerebral cortex of the Long-Evans Cinnamon rat before excessive copper accumulation in the brain. Neurosci. Lett. 216, 195-198.
161. Saito, T., Okabe, M., Hosokawa, T., Kurasaki, M., Hata, A., Endo, F., et al. (1999). Immunohistochemical determination of the Wilson copper-transporting P-type ATPase in the brain tissues of the rat. Neurosci. Lett. 266, 13-16. doi: 10.1016/S0304-3940(99)00258-X
162. Sales, N., Rodolfo, K., Hassig, R., Faucheux, B., Di Giamberardino, L., and Moya, K. L. (1998). Cellular prion protein localization in rodent and primate brain. Eur. J. Neurosci. 10, 2464-2471. doi: 10.1046/j.1460-9568.1998.00258.x
163. Scheiber, I., Dringen, R., and Mercer, J. F. B. (2013). "Copper: effects of deficiency and overload," in Interrelations between Essential Metal Ions and Human Diseases, eds A. Sigel, H. Sigel, and R. K. O. Sigel (Dordrecht: Springer) (in press).
164. Scheiber, I. F., and Dringen, R. (2012). Astrocyte functions in the copper homeostasis of the brain. Neurochem. Int. 62, 556-565. doi: 10.1016/j.neuint.2012.08.017
165. Scheiber, I. F., Schmidt, M. M., and Dringen, R. (2012). Copper export from cultured astrocytes. Neurochem. Int. 60, 292-300. doi: 10.1016/j.neuint.2011.12.012
166. Schiefermeier, M., Kollegger, H., Madl, C., Polli, C., Oder, W., Kuhn, H., et al. (2000). The impact of apolipoprotein E genotypes on age at onset of symptoms and phenotypic expression in Wilson's disease. Brain 123(Pt 3), 585-590. doi: 10.1093/brain/123.3.585
167. Schlief, M. L., Craig, A. M., and Gitlin, J. D. (2005). NMDA receptor activation mediates copper homeostasis in hippocampal neurons. J. Neurosci. 25, 239-246. doi: 10.1523/JNEUROSCI.3699-04.2005
168. Schlief, M. L., West, T., Craig, A. M., Holtzman, D. M., and Gitlin, J. D. (2006). Role of the Menkes copper-transporting ATPase in NMDA receptor-mediated neuronal toxicity. Proc. Natl. Acad. Sci. U.S.A. 103, 14919-14924. doi: 10.1073/pnas.0605390103
169. Schumacher, G., Platz, K. P., Mueller, A. R., Neuhaus, R., Luck, W., Langrehr, J. M., et al. (2001). Liver transplantation in neurologic Wilson's disease. Transplant. Proc. 33, 1518-1519. doi: 10.1016/S0041-1345(00)02578-1 CrossRef Full Text
170. Setty, S. R. G., Tenza, D., Sviderskaya, E. V., Bennett, D. C., Raposo, G., and Marks, M. S. (2008). Cell-specific ATP7A transport sustains copper-dependent tyrosinase activity in melanosomes. Nature 454, 1142-1146. doi: 10.1038/nature07163
171. Siggs, O. M., Cruite, J. T., Du, X., Rutschmann, S., Masliah, E., Beutler, B., et al. (2012). Disruption of copper homeostasis due to a mutation of Atp7a delays the onset of prion disease. Proc. Natl. Acad. Sci. U.S.A. 109, 13733-13738. doi: 10.1073/pnas.1211499109
172. Sigurdsson, E. M., Brown, D. R., Alim, M. A., Scholtzova, H., Carp, R., Meeker, H. C., et al. (2003). Copper chelation delays the onset of prion disease. J. Biol. Chem. 278, 46199-46202. doi: 10.1074/jbc.C300303200
173. Singleton, W. C., Mcinnes, K. T., Cater, M. A., Winnall, W. R., Mckirdy, R., Yu, Y., et al. (2010). Role of glutaredoxin1 and glutathione in regulating the activity of the copper-transporting P-type ATPases, ATP7A and ATP7B. J. Biol. Chem. 285, 27111-27121. doi: 10.1074/jbc.M110.154468
174. Squitti, R., Polimanti, R., Bucossi, S., Ventriglia, M., Mariani, S., Manfellotto, D., et al. (2013). Linkage disequilibrium and haplotype analysis of the ATP7B gene in Alzheimer's disease. Rejuvenation Res. 16, 3-10. doi: 10.1089/rej.2012.1357
175. Stephenson, S. E. M., Dubach, D., Lim, C. M., Mercer, J. F. B., and La Fontaine, S. (2005). A single PDZ domain protein interacts with the Menkes copper ATPase, ATP7A: a new protein implicated in copper homeostasis. J. Biol. Chem. 280, 33270-33279. doi: 10.1074/jbc.M505889200
176. Steveson, T. C., Ciccotosto, D. D., Ma, X.-M., Mueller, G. P., Mains, R. E., and Eipper, B. A. (2003). Menkes protein contirbutes to the function of peptidylglycine aamidating monooxygenase. Endocrinology 144, 188-200. doi: 10.1210/en.2002-220716
177. Strand, S., Hofmann, W. J., Grambihler, A., Hug, H., Volkmann, M., Otto, G., et al. (1998). Hepatic failure and liver cell damage in acute Wilson's disease involve CD95 (APO-1/Fas) mediated apoptosis. Nat. Med. 4, 588-593. doi: 10.1038/nm0598-588
178. Strausak, D., Howie, M. K., Firth, S. D., Schlicksupp, A., Pipkorn, R., Multhaup, G., et al. (2003). Kinetic analysis of the interaction of the copper chaperone Atox1 with the metal binding sites of the Menkes protein. J. Biol. Chem. 278, 20821-20827. doi: 10.1074/jbc.M212437200
179. Strausak, D., La Fontaine, S., Hill, J., Firth, S. D., Lockhart, P. J., and Mercer, J. F. B. (1999). The role of GMXCXXC metal binding sites in the copper-induced redistribution of the Menkes protein. J. Biol. Chem. 274, 11170-11177. doi: 10.1074/jbc.274.16.11170
180. Takata, R. I., Speck Martins, C. E., Passosbueno, M. R., Abe, K. T., Nishimura, A. L., Da Silva, M. D., et al. (2004). A new locus for recessive distal spinal muscular atrophy at Xq13.1-q21. J. Med. Genet. 41, 224-229. doi: 10.1136/jmg.2003.013201
181. Tang, J., Donsante, A., Desai, V., Patronas, N., and Kaler, S. G. (2008). Clinical outcomes in Menkes disease patients with a copper-responsive ATP7A mutation, G727R. Mol. Genet. Metab. 95, 174-181. doi: 10.1016/j.ymgme.2008.06.015
182. Tanzi, R. E., Petrukhin, K., Chernov, I., Pellequer, J. L., Wasco, W., Ross, B., et al. (1993). The Wilson disease gene is a copper transporting ATPase with homology to the Menkes disease gene. Nat. Genet. 5, 344-350. doi: 10.1038/ng1293-344
183. Tchaparian, E. H., Uriu-Adams, J. Y., Keen, C. L., Mitchell, A. E., and Rucker, R. B. (2000). Lysyl oxidase and P-ATPase-7A expression during embryonic development in the rat. Arch. Biochem. Biophys. 379, 71-77. doi: 10.1006/abbi.2000.1842
184. Terada, K., Aiba, N., Yang, X.-L., Iida, M., Nakai, M., Miura, N., et al. (1999). Biliary excretion of copper in LEC rat after introduction of copper transporting P-type ATPase, ATP7B. FEBS Lett. 448, 53-56. doi: 10.1016/S0014-5793(99)00319-1
185. Terada, K., Nakako, T., Yang, X.-L., Iida, M., Aiba, N., Minamiya, Y., et al. (1998). Restoration of holoceruloplasmin synthesis in LEC rat after infusion of recombinant adenovirus bearing WND cDNA. J. Biol. Chem. 273, 1815-1820. doi: 10.1074/jbc.273.3.1815
186. Terwel, D., Loschmann, Y. N., Schmidt, H. H., Scholer, H. R., Cantz, T., and Heneka, M. T. (2011). Neuroinflammatory and behavioural changes in the Atp7B mutant mouse model of Wilson's disease. J. Neurochem. 118, 105-112. doi: 10.1111/j.1471-4159.2011.07278.x
187. Theophilos, M. B., Cox, D. W., and Mercer, J. F. B. (1996). The toxic milk mouse is a murine model of Wilson disease. Hum. Mol. Genet. 5, 1619-1624. doi: 10.1093/hmg/5.10.1619
188. Tietz, N. W. (1987). Fundamentals of Clinical Chemistry. Philadelphia: Saunders.
189. Tiffany-Castiglioni, E., Hong, S., and Qian, Y. (2011). Copper handling by astrocytes: insights into neurodegenerative diseases. Int. J. Dev. Neurosci. 29, 811-818. doi: 10.1016/j.ijdevneu.2011.09.004
190. Tsivkovskii, R., Eisses, J. F., Kaplan, J. H., and Lutsenko, S. (2002). Functional properties of the copper-transporting ATPase ATP7B (the Wilson's disease protein) expressed in insect cells. J. Biol. Chem. 277, 976-983. doi: 10.1074/jbc.M109368200
191. Tumer, Z., and Moller, L. B. (2009). Menkes disease. Eur. J. Hum. Genet. 18, 511-518. doi: 10.1038/ejhg.2009.187
192. Vanderwerf, S. M., Cooper, M. J., Stetsenko, I. V., and Lutsenko, S. (2001). Copper specifically regulates intracellular phosphorylation of the Wilson's disease protein, a human copper-transporting ATPase. J. Biol. Chem. 276, 36289-36294. doi: 10.1074/jbc.M102055200
193. Veldhuis, N., Gaeth, A., Pearson, R., Gabriel, K., and Camakaris, J. (2009a). The multi-layered regulation of copper translocating P-type ATPases. Biometals 22, 177- 190. doi: 10.1007/s10534-008-9183-2
194. Veldhuis, N. A., Valova, V. A., Gaeth, A. P., Palstra, N., Hannan, K. M., Michell, B. J., et al. (2009b). Phosphorylation regulates copper-responsive trafficking of the Menkes copper transporting P-type ATPase. Int. J. Biochem. Cell Biol. 41, 2403-2412. doi: 10.1016/j.biocel.2009.06.008
195. Voskoboinik, I., Brooks, H., Smith, S., Shen, P., and Camakaris, J. (1998). ATP-dependent copper transport by the Menkes protein in membrane vesicles isolated from cultured Chinese hamster ovary cells. FEBS Lett. 438, 178-182. doi: 10.1016/S0014-5793(98)01059-X
196. Voskoboinik, I., Fernando, R., Veldhuis, N., Hannan, K. M., Marmy-Conus, N., Pearson, R. B., et al. (2003). Protein kinase-dependent phosphorylation of the Menkes copper P-type ATPase. Biochem. Biophys. Res. Commun. 303, 337-342. doi: 10.1016/S0006-291X(03)00329-2
197. Voskoboinik, I., Greenough, M., La Fontaine, S., Mercer, J. F. B., and Camakaris, J. (2001a). Functional studies on the Wilson copper P-type ATPase and toxic milk mouse mutant. Biochem. Biophys. Res. Comm. 281, 966-970. doi: 10.1006/bbrc.2001.4445
198. Voskoboinik, I., Mar, J., Strausak, D., and Camakaris, J. (2001b). The regulation of catalytic activity of the menkes copper-translocating P-type ATPase. Role of high affinity copper-binding sites. J. Biol. Chem. 276, 28620-28627. doi: 10.1074/jbc.M103532200
199. Vulpe, C., Levinson, B., Whitney, S., Packman, S., and Gitschier, J. (1993). Isolation of a candidate gene for Menkes disease and evidence that it encodes a coppertransporting ATPase. Nat. Genet. 3, 7-13. doi: 10.1038/ng0193-7
200. Walker, J. M., Huster, D., Ralle, M., Morgan, C. T., Blackburn, N. J., and Lutsenko, S. (2004). The N-terminal metal-binding site 2 of the Wilson's Disease Protein plays a key role in the transfer of copper from Atox1. J. Biol. Chem. 279, 15376-15384. doi: 10.1074/jbc.M400053200
201. Wang, X. P., Wang, X. H., Bao, Y. C., and Zhou, J. N. (2003). Apolipoprotein E genotypes in Chinese patients with Wilson's disease. QJM 96, 541-542. doi: 10.1093/qjmed/hcg093
202. Watts, G. D., Wymer, J., Kovach, M. J., Mehta, S. G., Mumm, S., Darvish, D., et al. (2004). Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat. Genet. 36, 377-381. doi: 10.1038/ng1332
203. Weisner, B., Hartard, C., and Dieu, C. (1987). CSF copper concentration: a new parameter for diagnosis and monitoring therapy of Wilson's disease with cerebral manifestation. J. Neurol. Sci. 79, 229-237. doi: 10.1016/0022-510X(87)90275-9
204. White, C., Kambe, T., Fulcher, Y. G., Sachdev, S. W., Bush, A. I., Fritsche, K., et al. (2009). Copper transport into the secretory pathway is regulated by oxygen in macrophages. J. Cell Sci. 122, 1315-1321. doi: 10.1242/jcs.043216
205. Wilson, M. R., Yerbury, J. J., and Poon, S. (2008). Potential roles of abundant extracellular chaperones in the control of amyloid formation and toxicity. Mol. Biosyst. 4, 42-52. doi: 10.1039/b712728f
206. Wu, J., Forbes, J. R., Chen, H. S., and Cox, D. W. (1994). The LEC rat has a deletion in the copper transporting ATPase gene homologous to the Wilson disease gene. Nat. Genet. 7, 541-544. doi: 10.1038/ng0894-541
207. Yamaguchi, Y., Heiny, M. E., and Gitlin, J. D. (1993). Isolation and characterization of a human liver cDNA as a candidate gene for Wilson disease. Biochem. Biophys. Res. Comm. 197, 271-277. doi: 10.1006/bbrc.1993.2471
208. Yamaguchi, Y., Heiny, M. E., Suzuki, M., and Gitlin, J. D. (1996). Biochemical characterization and intracellular localization of the Menkes disease protein. Proc. Natl. Acad. Sci. U.S.A. 93, 14030-14035. doi: 10.1073/pnas.93.24.14030
209. Yang, X.-L., Miura, N., Kawarada, Y., Terada, K., Petrukhin, K., Gilliam, T. C., et al. (1997). Two forms of Wilson disease protein produced by alternative splicing are localized in distinct cellular compartments. Biochem. J. 326, 897-902.
210. Yi, L., Donsante, A., Kennerson, M. L., Mercer, J. F., Garbern, J. Y., and Kaler, S. G. (2012). Altered intracellular localization and valosin-containing protein (p97 VCP) interaction underlie ATP7A-related distal motor neuropathy. Hum. Mol. Genet. 21, 1794-1807. doi: 10.1093/hmg/ddr612
211. You, H., Tsutsui, S., Hameed, S., Kannanayakal, T. J., Chen, L., Xia, P., et al. (2012). Abeta neurotoxicity depends on interactions between copper ions, prion protein, and N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. U.S.A. 109, 1737-1742. doi: 10.1073/pnas.1110789109
212. Yu, J. T., and Tan, L. (2012). The role of clusterin in Alzheimer's disease: pathways, pathogenesis, and therapy. Mol. Neurobiol. 45, 314-326. doi: 10.1007/s12035- 012-8237-1
213. Zheng, Z., White, C., Lee, J., Peterson, T. S., Bush, A. I., Sun, G. Y., et al. (2010). Altered microglial copper homeostasis in a mouse model of Alzheimer's disease. J. Neurochem. 114, 1630-1638. doi: 10.1111/j.1471-4159.2010.06888.x