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)

Biochemical Journal

Volumn 401, Issue 1, 2007, Pages 143-153

  Cater, Michael A ^a   La Fontaine, Sharon ^a   Mercer, Julian F B ^a  

^a DEAKIN UNIVERSITY   (Australia)

Author keywords

ATP7B; Copper translocation; Metal binding site; P type ATPase; Wilson disease; WND

Indexed keywords

BINDING ENERGY; CATALYST ACTIVITY; CELL CULTURE; COPPER; ENZYME KINETICS;

COPPER TRANSLOCATION; METAL-BINDING SITES; P-TYPE ATPASE; WILSON DISEASES;

PROTEINS;

ACYLPHOSPHATASE; ASPARTIC ACID; COPPER; PHOSPHATASE; WILSON DISEASE PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CATALYSIS; CONTROLLED STUDY; CYTOSOL; GENE MUTATION; GENETIC REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; SITE DIRECTED MUTAGENESIS;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BINDING SITES; CATION TRANSPORT PROTEINS; COPPER; CYSTEINE; DNA PRIMERS; GLUTAMIC ACID; GLYCINE; HEPATOLENTICULAR DEGENERATION; HUMANS; MODELS, MOLECULAR; OLIGOPEPTIDES; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; THREONINE;

EID: 33846311441     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061055     Document Type: Article

References (45)

1. Petrukhin, K., Lutsenko, S., Chernov, I., Ross, B. M., Kaplan, J. H. and Gilliam, T. C. (1994) Characterization of the Wilson disease gene encoding a copper transporting ATPase: genomic organization, alternative splicing, and structure/function predictions. Hum. Mol. Genet. 3, 1647-1656
2. Moller, J. V., Juul, B. and le Maire, M. (1996) Structural organization, ion transport, and energy transduction of P-type ATPases. Biochim. Biophys. Acta 1286, 1-51
3. 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 copper-transporting ATPase. Nat. Genet. 3, 7-13
4. Solioz, M. and Vulpe, C. (1996) CPX-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem. Sci. 21, 237-241
5. Lutsenko, S., Petrukhin, K., Cooper, M. J., Gilliam, C. T. and Kaplan, J. H. (1997) N-terminal domains of human copper-transporting adenosine triphosphatases (the Wilson's and Menkes disease proteins) bind copper selectively in vivo and in vitro with stoichiometry of one copper per metal-binding repeat. J. Biol. Chem. 272, 18939-18944
6. Forbes, J. R. and Cox, D. W. (1998) Functional characterization of missense mutations in ATP7B: Wilson disease mutation or normal variant? Am. J. Hum. Genet. 63, 1663-1674
7. Myari, A., Hadjiliadis, N., Fatemi, N. and Bibudhendra, S. (2004) Copper(I) interaction with model peptides of WD6 and TM6 domains of Wilson ATPase: regulatory and mechanistic implications. J. Inorg. Biochem. 98, 1483-1494
8. Scarborough, G. A. (1999) Structure and function of the P-type ATPases. Curr. Opin. Cell Biol. 11, 517-522
9. Lutsenko, S., Tsivkovskii, R. and Walker, J. M. (2003) Functional properties of the human copper-transporting ATPase ATP7B (the Wilson's disease protein) and regulation by metallochaperone Atox1. Ann. N.Y. Acad. Sci. 986, 204-211
10. Voskoboinik, I., Mar, J., Strausak, D. and Camakaris, J. (2001) The regulation of catalytic activity of the Menkes copper-translocating P-type ATPase. J. Biol. Chem. 276, 28620-28627
11. Petris, M. J., Voskoboinik, I., Cater, M., Smith, K., Kim, B.-E., Llanos, R. M., Strausak, D., Camakaris, J. and Mercer, J. F. B. (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
12. 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
13. Tanzi, R. E., Petrukhin, K., Chernov, I., Pellequer, J. L., Wasco, W., Ross, B., Romano, D. M., Parano, E., Pavone, L., Brzustowicz, L. M. et al. (1993) The Wilson disease gene is a copper transporting ATPase with homology to the Menkes disease gene. Nat. Genet. 5, 344-350
14. Ackland, M. L., Anikijenko, P., Michalczyk, A. and Mercer, J. F. B. (1999) Expression of Menkes copper-transporting ATPase, MNK, in the lactating human breast: possible role in copper transport into milk. J. Histochem. Cytochem. 47, 1553-1561
15. Hardman, B., Manuelpillai, U., Wallace, M. E., Vaan de Waasenberg, S., Cater, M., Mercer, F. B. J. and Ackland, M. L. (2004) Expression and localization of the Menkes and Wilson copper transporting ATPases in human placenta. Placenta 24, 512-517
16. Paynter, J. A., Grimes, A., Lockhart, P. and Mercer, J. F. B. (1994) Expression of the Menkes gene homologue in mouse tissues lack of effect of copper on the mRNA levels FEBS Lett. 351, 186-190
17. Forbes, J. R. and Cox, D. W. (2000) Copper-dependent trafficking of Wilson disease mutant ATP7B proteins. Hum. Mol. Genet. 9, 1927-1935
18. 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
19. 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
20. Royce, P. M. and Steinmann, B. (1990) Markedly reduced activity of lysyl oxidase in skin and aorta from a patient with Menkes' disease showing unusually severe connective tissue manifestations. Pediatr. Res. 28, 137-141
21. Terada, K., Nakako, T., Yang, X.-L., Iida, M., Aiba, N., Minamiya, Y., Nakai, M., Sakaki, T., Miura, N. and Sugiyama, T. (1998) Restoration of holoceruloplasmin synthesis in LEC rat after infusion of recombinant adenovirus bearing WND cDNA. J. Biol. Chem. 273, 1815-1820
22. Greenough, M., Pase, L., Voskobionik, I., Petris, M., Wilson Obrien, A. 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
23. Schaefer, M., Hopkins, R. G., Failla, M. A. and Gitlin, J. D. (1999) Hepatocyte-specific localization and copper-dependent trafficking of the Wilson's disease protein in the liver. Am. J. Physiol. 276, G639-G646
24. Schaefer, M., Roelofsen, H., Wolters, H., Hofmann, W. J., Müller, M., Kuipers, F., Stremmel, W. and Vonk, R. J. (1999) Localization of the Wilson's disease protein in human liver. Gastroenterology 117, 1380-1385
25. Cater, M., La Fontaine, S., Shield, K., Deal, Y. and Mercer, F. B. J. (2006) ATP7B mediates vesicular sequestration of copper; insight into biliary copper excretion. Gastroenterology 130, 493-506.
26. Petris, M. and Mercer, J. F. B. (1999) The Menkes protein (ATP7A, MNK) cycles 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
27. 2+ ATPase subfamily. Yeast 11, 283-292
28. Elble, R. (1992) A simple and efficient procedure for transformation of yeasts. BioTechniques 13, 18-20
29. Cater, M., Forbes, J. R., La Fontaine, S., Cox, D. C. 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, 805-813
30. Vernet, T., Dignard, D. and Thomas, D. Y. (1987) A family of yeast expression vectors containing the phage f1 intergenic region. Gene 52, 225-233
31. 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
32. Clarke, D. M., Loo, T. W. and MacLennan, D. H. (1990) Functional consequences of alterations to amino acids located in the nucleotide binding domain of the Ca(2+)-ATPase of sarcoplasmic reticulum. J. Biol. Chem. 25, 22223-22227
33. Portillo, F. and Serrano, R. (1989) Dissection of functional domains of the yeast proton-pumping ATPase by direct mutagenesis. EMBO J. 6, 1793-1798
34. Matraki, A. and King, J. (1992) Amino acid substitutions influencing intracellular protein folding pathways. FEBS Lett. 307, 20-25
35. Hass, R., Gutierrez-Rivero, B., Knoche, J., Boker, K., Manns, M. P. and Schmidt, H. H. (1999) Mutation analysis in patients with Wilson disease: identification of 4 novel mutations. Hum. Mutat. 14, 88
36. Turner, Z., Moller, L. B. and Horn, N. (1999) Mutation spectrum of ATP7A, the gene defective in Menkes disease. Adv. Exp. Med. Biol. 448, 83-95
37. Huster, D. and Lutsenko, S. (2003) The distinct roles of the N-terminal copper-binding sites in regulation of catalytic activity of the Wilson's disease protein. J. Biol. Chem. 278, 32212-32218
38. Hsi, G., Lara, M., Cullen, D., Moira, G. and Cox, D. C. (2004) Functional assessment of the carboxy-terminus of the Wilson disease copper-transporting ATPase, ATP7B. Genomics 83, 473-481
39. Payne, A. S., Kelly, E. J. and Gitlin, J. D. (1998) Functional expression of the Wilson disease protein reveals mislocalization and impaired copper-dependent trafficking of the common H1069Q mutation. Proc. Natl. Acad. Sci. U.S.A. 95, 10854-10859
40. Strausak, D., Fontaine, S. L., 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
41. 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
42. 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
43. Mercer, J. F. B., Barnes, N., Steverson, J., Strausak, D. and Llanos, R. (2003) Copper-induced trafficking of the Cu-ATPases: a key mechanism for copper homeostasis. Biometals 16, 175-184
44. Voskoboinik, I., Strausak, D., Greenough, M., Brooks, H., Petris, M., Smith, S., Mercer, J. F. and Camakaris, J. (1999) Functional analysis of the N-terminal CXXC metal-binding motifs in the human Menkes copper-transporting P-type ATPase expressed in cultured mammalian cells. J. Biol. Chem. 274, 22008-22012
45. Wang, R. F. and Kushner, S. R. (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100, 195-199