A delicate balance: Homeostatic control of copper uptake and distribution

Journal of Nutrition

Volumn 129, Issue 7, 1999, Pages 1251-1260

  Peña, Maria M O ^a   Lee, Jaekwon ^a   Thiele, Dennis J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Copper; Distribution; Homeostatic regulation; Menkes; Transport; Wilson's disease

Indexed keywords

BINDING PROTEIN; CHAPERONE; COPPER; COPPER COMPLEX;

ABSORPTION; CELL TRANSPORT; CELLULAR DISTRIBUTION; COPPER METABOLISM; HOMEOSTASIS; HUMAN; INTRACELLULAR TRANSPORT; MENKES SYNDROME; NONHUMAN; PATHOGENESIS; PROKARYOTE; REGULATORY MECHANISM; REVIEW; WILSON DISEASE; YEAST;

EID: 0037477740     PISSN: 00223166     EISSN: None     Source Type: Journal    
DOI: 10.1093/jn/129.7.1251     Document Type: Review

References (93)

1. Askwith, C. & Kaplan, J. (1998) Iron and copper transport in yeast and its relevance to human disease. Trends Biochem. Sci. 23: 135-138.
2. Beers, J., Glerum, D. M. & Tzagotoff, A. (1997) Purification, characterization, and localization of yeast Cox17p: a mitochondrial copper shuttle. J. Biol. Chem.272: 33191-33196.
3. Borjigin, J., Payne, A. S., Deng, J., Li, X., Wang, M. M., Ovodenko, B., Gitlin, J. D. & Snyder, S. H. (1999) A novel pineal night-specific ATPase encoded by the Wilson disease gene. J. Neurosci. 19: 1018-1026.
4. Brown, D. R., Qin, K., Herms, J. W., Madlung, A., Manson, J., Strome, R., Fraser, P. E., Kruck, T., von Bohlen, A., Schulz-Schaeffer, W., Giese, A., Westaway, D. & Kretzschmar, H. (1997) The cellular prion protein binds copper in vivo. Nature 390: 684-687.
5. Bull, P. C. & Cox, D. W. (1994) Wilson disease and Menkes disease: new handles on heavy-metal transport. Trends Genet. 10: 246-252.
6. Bull, P. C., Thomas, G. R., Rommens, J. M., Forbe, J. R. & Cox, D. W. (1993) The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat. Genet. 5: 327-337.
7. Casareno, R. L., Waggoner, D. & Gitlin, J. D. (1998) The copper chaperone CCS directly interacts with copper/zinc Superoxide dismutase. J. Biol. Chem. 273: 23625-23628.
8. Cha, J. S. & Cooksey, D. A. (1991) Copper resistance in Pseudomonas syringae mediated by periplasmic and outer membrane proteins. Proc. Natl. Acad. Sci. USA 88: 8915-8919.
9. Chelly, J., Turner, Z., Tonnesen, T., Petterson, A., Ishikawa-Brush, Y., Tommerup, N. & Monaco, A. P. (1993) Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat. Genet. 3: 14-19.
10. Crampton, R. F., Matthews, D. M. & Poisner, R. (1965) Observations on the mechanism of absorption of copper by the small intestine. J. Physiol. 178: 111-126.
11. Culotta, V. C., Klomp, L. W., Strain, J., Casareno, R. L., Krems, B. & Gitlin, J. D. (1997) The copper chaperone for Superoxide dismutase. J. Biol. Chem. 272: 23469-23472.
12. Dancis, A., Yuan, D. S., Haile, D., Askwith, C., Elde, D., Moehle, C., Kaplan, J. & Klausner, R. D. (1994a) Molecular characterization of a copper transport protein in S. cerevisiae: an unexpected role for copper in iron transport. Cell 76: 393-402.
13. Dancis, A., Haile, D., Yuan, D. S. & Klausner, R. D. (1994b) The Saccharomyces cerevisiae copper transport protein (Ctr1p). Biochemical characterization, regulation by copper, and physiologic role in copper uptake. J. Biol. Chem. 269: 25660-25667.
14. Danks, D. M., Cartwright, E., Stevens, B. J. & Townley, R. R. (1973) Menkes' kinky hair disease: further definition of the defect in copper transport. Science 179: 1140-1142.
15. Danks, D. M. (1989) Disorders of copper transport. In: The Metabolic Basis Of Inherited Disease. (Scriver, C. R., Beaudet, A. L., Sly, W. S. & Valle, D. eds.), pp. 1411-1431. McGraw-Hill, New York.
16. Davis-Kaplan, S. R., Askwith, C. C., Bengtzen, A. C., Radisky, D. & Kaplan, J. (1998) Chloride is an allosteric effector of copper assembly for the yeast multicopper oxidase Fet3p: an unexpected role for intracellular chloride channels. Proc. Natl. Acad. Sci. USA 95:13641-13645.
17. 2+-selective electrode. FEMS Microbiol. Lett. 43: 283-287.
18. DiDonato, M. & Sarkar, B. (1997) Copper transport and its alterations in Menkes and Wilson diseases. Biochim. Biophys. Acta 1360: 3-16.
19. Dijkstra, M., Vonk, R. J. & Kuipers, F. (1996) How does copper get into bile? New insights into the mechanism(s) of hepatobiliary copper transport. J. Hepatol. 24: 109-120.
20. Dix, D. R., Bridgham, J. T., Broderius, M. A., Byersdorfer, C. A. & Eide, D. J. (1994) The FET4 gene encodes the low affinity Fe(II) transport protein of Saccharomyces cerevisiae. J. Biol. Chem. 269: 26092-26099.
21. Dix, D., Bridgham, J., Broderius, M. & Eide, D. (1997) Characterization of the FET4 protein of yeast. Evidence for a direct role in the transport of iron. J. Biol. Chem. 272: 11770-11777.
22. Eide, D. J., Bridgham, J. T., Zhao, Z. & Mattoon, J. R. (1993) The vacuolar H(+)-ATPase of Saccharomyces cerevisiae is required for efficient copper detoxification, mitochondrial function, and iron metabolism. Mol. Gen. Genet. 241: 447-456.
23. Eide, D. J. (1998) The molecular biology of metal ion transport in Saccharomyces cerevisiae. Annu. Rev. Nutr. 18: 441-469.
24. Francis, M. J., Jones, E. E., Levy, E. R., Ponnambalam, S., Chelly, J. & Monaco, A. P. (1998) A Golgi localization signal identified in the Menkes recombinant protein. Hum. Mol. Genet. 7: 1245-1252.
25. Gaxiola, R. A., Yuan, D. S., Klausner, R. D. & Fink, G. R. (1998) The yeast CLC chloride channel functions in cation homeostasis. Proc. Natl. Acad. Sci. USA 95: 4046-4050.
26. Georgatsou, E., Mavrogiannis, L. A., Fragiadakis, G. S. & Alexandraki, D. (1997) The yeast Fre1p/Fre2p cupric reductases facilitate copper uptake and are regulated by the copper-modulated Mac1p activator. J. Biol. Chem.272: 13786-13792.
27. Glerum, D. M., Shtanko, A. & Tzagoloff, A. (1996a) Characterization of COX17: a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J. Biol. Chem. 271: 14504-14509.
28. Glerum, D. M., Shtanko, A. & Tzagoloff, A. (1996b) SCO1 and SCO2 act as high copy suppressors of a mitochondria! copper recruitment defect in Saccharomyces cerevisiae. J. Biol. Chem.271: 20531-20535.
29. Gunshin, H., Mackenzie, B., Berger, U. V., Gunshin, Y., Romero, M. F., Boron, W. F., Nussberger, S., Gollan, J. L. & Hediger, M. A. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388: 482-488.
30. Halliwell, B. & Gutteridge, J. M. C. (1984) Oxygen toxicity, oxygen radicals, transition metals and diseases. Biochem. J. 219: 1-4.
31. Halliwell, B. & Gutteridge, J. M. (1990) Role of free radicals and catalytic metal ions in human disease: an overview. Meth. Enzymol. 186: 1-85.
32. Harris, Z. L., Klomp, L. W. & Gitlin, J. D. (1998) Aceruloplasminemia: an inherited neurodegenerative disease with impairment of iron homeostasis. Am. J. Clin. Nutr. 67: 972S-977S.
33. Hassett, R. & Kosman, D. J. (1995) Evidence for Cu(II) reduction as a component of copper uptake by Saccharomyces cerevisiae. J. Biol. Chem. 270: 128-134.
34. Holmberg, C. G. & Laurell, C. B. (1948) Investigations in serum copper. II. Isolation of the copper containing protein and a description of some of its properties. Acta Chem. Scand. 2: 550-556.
35. Hornshaw, M. P., McDermott, J. R. & 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.
36. Hornshaw, M. P., McDermott, J. R., Candy, J. M. & 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.
37. Hung, I. H., Suzuki, M., Yamaguchi, Y., Yuan, D. S., Klausner, R. D. & 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.
38. Kampfenkel, K., Kushnir, S., Babiychuk, E., Inze, D. & Van Montagu, M. (1995) Molecular characterization of a putative Arabidopsis thaliana copper transporter and its yeast homologue. J. Biol. Chem. 270: 28479-28486.
39. Klomp, L. W., Lin, S. J., Yuan, D. S., Klausner, R. D., Culotta, V. C. & Gitlin, J. D. (1997) Identification and functional expression of HAH1: a novel human gene involved in copper homeostasis. J. Biol. Chem. 272: 9221-9226.
40. Knight, S. A. B, Labbé, S., Kwon, L. F., Kosman, D. J. & Thiele, D. J. (1996) A widespread transposable element masks expression of a yeast copper transport gene. Genes Dev. 10: 1917-1929.
41. Koch, K. A., Pena, M. M. & Thiele, D. J. (1997) Copper-binding motifs in catalysis, transport, detoxification and signaling. Chem. Biol. 4: 549-560.
42. Lee, G. R., Nacht, S., Lukens, J. N. & Cartwright, G. E. (1968) Iron Metabolism in Copper-deficient Swine. J. Clin. Invest. 47: 2058-2069.
43. Lin, C. & Kosman, D. J. (1990) Copper uptake in wild type and copper metallothionein-deficient Saccharomyces cerevisiae. J. Biol. Chem. 265: 9194-9200.
44. Lin, S. J. & Culotta, V. C. (1995) The ATX1 gene of Saccharomyces cerevisiae encodes a small metal homeostasis factor that protects cells against reactive oxygen toxicity. Proc. Natl. Acad. Sci. USA 92: 3784-3788.
45. Lin, S. J., Pufahl, R. A., Dancis, A., O'Halloran, T. V. & Culotta, V. C. (1997) A role for the Saccharomyces cerevisiae ATX1 gene in copper trafficking and iron transport. J. Biol. Chem. 272: 9215-9220.
46. Linder, M. C. (1991) Biochemistry of copper. Plenum Press, New York.
47. Linder, M. C. & Hazegh-Azam, M. (1996) Copper biochemistry and molecular biology. Am J. Clin. Nutr. 63: 797S-811S.
48. Liu, X. F., Supek, F., Nelson, N. & Culotta, V. C. (1997) Negative control of heavy metal uptake by the Saccharomyces cerevisiae BSD2 gene. J. Biol. Chem.272: 11763-11769.
49. Liu, X. F. & Culotta, V. C. (1999) Post-translation control of Nramp metal transport in yeast. Role of metal ions and the BSD2 gene. J. Biol. Chem.274: 4863-4868.
50. Lutsenko, S. & Cooper, M. J. (1998) Localization of the Wilson's disease protein product to mitochondria. Proc. Natl. Acad. Sci. USA 95: 6004-6009.
51. Martins, L. J., Jensen, L. T., Simons, J. R., Keller, G. L. & Winge, D. R. (1998) Metalloregulation of FRE1 and FRE2 homologs in Saccharomyces cerevisiae. J. Biol. Chem. 273: 23716-23721.
52. McKenzie, D., Bartz, J., Mirwald, J., Olander, D., Marsh, R. & Aiken, J. (1998) Reversibility of scrapie inactivation is enhanced by copper. J. Biol. Chem. 273: 25545-25547.
53. Mercer, J.F.B, Livingston, J., Hall, B., Paynter, J. A., Begy, C., Chandrasekharappa, S., Lockhart, P., Grimes, A., Bhave, M., Siemieniak, D. & Glover, T. W. (1993) Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat. Genet. 3: 20-25.
54. Miyajima, H., Nishimura, Y., Mizoguchi, K., Sakamoto, M., Shimizu, T. & Honda, N. (1987) Familial apoceruloplasmin deficiency associated with blepharospasm and retinal degeneration. Neurol. 37: 761-767.
55. Murata, Y., Kodama, H., Abe, T., Ishida, N., Nishimura, M., Levinson, B., Gitschier, J. & Packman, S. (1997) Mutation analysis and expression of the mottled gene in the macular mouse model of Menkes disease. Pediatr. Res. 42: 436-442.
56. Nagano, K., Nakamura, K., Urakami, K.-I., Umeyama, K., Uchiyama, H., Koiwai, K., Hattori, S., Yamanoto, T., Matsuda, I. & Endo, F. (1998) Intracellular distribution of the Wilson's disease gene product (ATPase7B) after In Vitro and In Vivo exogenous expression in hepatocytes from the LEC rat: an animal model of Wilson's disease. Hepatol. 27: 799-807.
57. Odermatt, A., Suter, H., Krapf, R. & Solioz, M. (1992) An ATPase operon involved in copper resistance by Enterococcus hirae. Ann. NY Acad. Sci. 671: 484-486.
58. Odermatt, A., Suter, H., Krapf, R. & Solioz, M. (1993) Primary structure of two P-type ATPases involved in copper homeostasis in enterococus hirae. J. Biol. Chem. 268: 12775-12779.
59. Odermatt, A., Krapf, R. & Solioz, M. (1994) Induction of the putative copper ATPases, CopA and CopB, of Enterococcus hirae by Ag+ and Cu2+: and Ag+ extrusion by CopB. Biochem. Biophys. Res. Commun. 202: 44-48.
60. Ooi, C. E., Rabinovich, E., Dancis, A., Bonifacino, J. S. & Klausner, R. D. (1996) Copper-dependent degradation of the Saccharomyces cerevisiae plasma membrane copper transporter Ctr1p in the apparent absence of endocytosis. EMBO J. 15: 3515-3523.
61. Pauly, P. C. & Harris, D. A. (1998) Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 273: 33107-33110.
62. Petris, M. J., Mercer, J.F.B, Culvenor, J. G., Lockhart, P., Gleeson, P. A. & 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.
63. Petris, M. J., Camakaris, J., Greenough, M., LaFontaine, S. & 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.
64. Predki, P. F. & Sarkar, B. (1992) Effect of replacement of "zinc finger" zinc on estrogen receptor DNA interactions. J, Biol. Chem. 267: 5842-5846.
65. Prince, R. C. & Gunson, D. E. (1998) Prions are copper-binding proteins. Trends Biochem. Sci. 23: 197-198.
66. Prusiner, S. B. (1991) Molecular biology of prion diseases. Science 252: 1515-1522.
67. Pufahl, R. A., Singer, C. P., Peariso, K. L., Lin, S. J., Schmidt, P. J., Fahrni, C. J., Culotta, V. C., Penner-Hahn, J. E. & O'Halloran, T. V. (1997) Metal ion chaperone function of the soluble Cu(I) receptor Atx1. Science 278: 853-856.
68. Radisky, D. & Kaplan, J. (1999) Regulation of transition metal transport across the yeast plasma membrane. J. Biol. Chem. 274: 4481-4484.
69. Ralle, M., Cooper, M. J., Lutsenko, S. & Blackburn, N. J. (1998) The Menkes disease protein birds copper via novel 2-coordinate Cu(I)-cysteinates in the N-terminal domain. J. Am. Chem. Soc.120: 13525-13526.
70. Rothstein, J. D., Dykes-Hoberg, M., Corson, L. B., Becker, M., Cleveland, D. W., Price, D. L., Culotta, V. C. & Wong, P. C. (1999) The copper chaperone CCS is abundant in neurons and astrocytes in human and rodent brain. J. Neurochem. 72: 422-429.
71. Sato, M. & Gitlin, J. D. (1991) Mechanisms of copper incorporation during the biosynthesis of human ceruloplasmin. J. Biol. Chem. 266: 5128-5134.
72. Shyng, S. L., Huber, M. T. & Harris, D. A. (1993) A prion protein cycles between the cell surface and an endocytic compartment in cultured neuroblastoma cells. J. Biol. Chem. 268: 15922-15928.
73. Shyng, S. L., Heuser, J. E. & Harris, D. A. (1994) A glycolipid-anchored prion protein is endocytosed via clathrin-coated pits. J. Cell. Biol. 125: 1239-1250.
74. Solioz, M., Odermatt, A. & Krapf, R. (1994) Copper pumping ATPases: common concepts in bacteria and man. FEBS Lett. 346: 44-47.
75. Solioz, M. & Odermatt, A. (1995) Copper and silver transport by CopB-ATPase in membrane vesicles of Enterococcus hirae. J. Biol. Chem. 270: 9217-9221.
76. Srinivasan, C., Posewitz, M. C., George, G. N. & Winge, D. R. (1998) Characterization of the copper chaperone Cox17 of Saccharomyces cerevisiae. Biochem. 37: 7572-7577.
77. Stearman, R., Yuan, D. S., Yamaguchi-Iwai, Y., Klausner, R. D. & Danois, A. (1996) A permease-oxidase complex involved in high-affinity Iron uptake in yeast. Science 271: 1552-1557.
78. Strausak, D., Fontaine, S. L, Hill, J., Firth, S. D., Lockhart, P. J. & Mercer, J. F. (1999) The role of GMXCXXC metal binding sites in the copper-induced redistribution of the Menkes protein. J. Biol. Chem. 274: 11170-11177.
79. Szczypka, M. S., Zhu, Z., Silar, P. & Thiele, D. J. (1997) Saccharomyces cerevisiae mutants altered in vacuole function are defective in copper detoxification and iron-responsive gene transcription. Yeast 13: 1423-1435.
80. Tanzi, R. E., Petrukhin, K., Chernov, I., Pellequer, J. L., Wasco, W., Ross, B., Romano, D. M., Parano, E., Pavone, L., Brzustowicz, L. M., Devoto, M., Peppercorn, J., Bush, A. I., Sternlieb, I., Pirastu, M., Gusalla, J. F., Evgrafov, O., Penchaszadeh, G. K., Honig, B., Edelman, I. S., Soares, M. B., Scheinberg, I. H. & Gilliam, T. C. (1993) The Wilson disease gene is a copper transporting ATPase with homology to the Menkes disease gene. Nat. Genet. 5: 344-350.
81. Terada, K., Nakako, T., Yang, X.-L., Iida, M., Aiba, N., Minamiya, Y., Nakai, M., Sakaki, T., Miura, N. & Sugiyama, T. (1998) Restoration of holoceruloplasmin synthesis in LEC rat after infusion of recombinant adenovirus bearing WND cDNA. J. Biol. Chem. 273: 1815-1820.
82. Tobler, I., Gaus, S. E., Deboer, T., Achermann, P., Fischer, M., Rulicke, T., Moser, M., Oesch, B., McBride, P. A. & Manson, J. C. (1996) Altered circadian activity rhythms and sleep in mice devoid of prion protein. Nature 380: 639-642.
83. 59 from ligated segments of the rat gastrointestinal tract. J. Nutr. 86: 120-124.
84. Viles, J. H., Cohen, F. E., Prusiner, S. B., Goodin, D. B., Wright, P. E. & 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.
85. Vulpe, C., Levinson, B. W., S., Packman, S. & Gitschier, J. (1993) Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper transporting ATPase. Nat. Genet. 3: 7-13.
86. Vulpe, C. D. & Packman, S, (1995) Cellular copper transport. Annu. Rev. Nutr. 15: 293-322.
87. Vulpe, C. D., Kuo, Y. M., Murphy, T. L., Cowley, L., Askwith, C., Libina, N., Gitschier, J. & Anderson, G. J. (1999) Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the sla mouse. Nat. Genet. 21: 195-199.
88. Winge, D. R. (1998) Copper-regulatory domain involved in gene expression. Prog. Nucleic Acid Res. Mol. Biol. 58: 165-195.
89. Winge, D. R., Jensen, L. T. & Srinivasan, C. (1998) Metal-ion regulation of gene expression in yeast. Curr. Opin. Chem. Biol. 2: 216-221.
90. Winzerling, J. J. & Law, J. H. (1997) Comparative nutrition of iron and copper. Annu. Rev. Nutr. 17: 501-526.
91. Yamaguchi, Y., Heiny, M. E. & Gitlin, J. D. (1993) Isolation and characterization of a human liver cDNA as a candidate gene for Wilson desease. Biochem. Biophys. Res. Commun. 197: 271-277.
92. Yuan, D. S., Stearman, R., Dancis, A., Dunn, T., Beeler, T. & Klausner, R. D. (1995) The Menkes/Wilson disease gene homologue in yeast provides copper to a ceruloplasmin-like oxidase required for iron uptake. Proc. Natl. Acad. Sci. USA 92: 2632-2636.
93. Zhou, B. & Gitschier, J. (1997) hCTR1: a human gene for copper uptake identified by complementation in yeast. Proc. Natl. Acad. Sci. USA 94: 7481-7486.