A C-terminal di-leucine is required for localization of the Menkes protein in the trans-Golgi network

Human Molecular Genetics

Volumn 7, Issue 13, 1998, Pages 2063-2071

  Petris, Michael J ^a,b   Camakaris, James ^b   Greenough, Mark ^b   LaFontaine, Sharon ^a   Mercer, Julian F B ^c  

^a ROYAL CHILDREN'S HOSPITAL   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c DEAKIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; COPPER; LEUCINE;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; COPPER METABOLISM; GOLGI COMPLEX; IMMUNOFLUORESCENCE; MENKES SYNDROME; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL;

EID: 0031730641     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/7.13.2063     Document Type: Article

References (44)

1. Danks, D.M. (1995) Disorders of copper transport. In Scriver, C.R., Beaudet, A.L., Sly, W.M. and Valle, D. (eds), The Metabolic and Molecular Basis of Inherited Disease. McGraw-Hill, New York, pp. 2211-2235.
2. Chelly, J., Turmer, Z., Tonnerson, T., Petterson, A., Ishikawa-Brush, Y., Tommerup, N., Horn, N. and Monaco, A.P. (1993) Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nature Genet., 3, 14-19.
3. Mercer, J.F.B., Livingston, J., Hall, B., Paynter, J.A., Begy, C. Chandrasekharappa, S., Lockhart, P., Grimes, A., Bhave, M., Siemieniak, D. and Glover, T.W. (1993) Isolation of a partial candidate gene for Menkes disease by positional cloning. Nature Genet., 3, 20-25.
4. 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. Nature Genet., 3, 7-13.
5. Herd, S.M., Camakaris, J., Christofferson, R., Wookey, P. and Danks, D.M. (1987) Uptake and efflux of copper-64 in Menkes'-disease and normal continuous lymphoid cell lines. Biochem. J., 247, 341-347.
6. Camakaris, J., Petris, M.J., Bailey, L., Shen, P., Lockhart, P., Glover, T.W., Barcroft, C.L., Patton, J. and Mercer, J.F.B. (1995) Gene amplification of the Menkes (MNK; ATP7A) P-type ATPase gene of CHO cells is associated with copper resistance and enhanced copper efflux. Hum. Mol. Genet., 4, 2117-2123.
7. Petris, M.J., Mercer, J.F., 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.
8. 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.
9. 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. USA, 93, 14030-14035.
10. 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.
11. La Fontaine, S., Firth, S.D., Lockhart, P.J., Brooks, H., Parton, R.G., Camakaris, J. and Mercer, J.F.B. (1998) 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.
12. Munro, S. (1991) Sequences within and adjacent to the transmembrane segment of α-2,6-sialyltransferase specify Golgi retention. EMBO J., 10, 3577-3588.
13. Nilsson, T., Lucocq, J.M., Mackay, D. and Warren, G. (1991) The membrane spanning domain of β-1,4-galactosyltransferase specifies trans Golgi localization. EMBO J., 10, 3567-3575.
14. 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.
15. 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.
16. Trowbridge, I.S., Collawn, J.F. and Hopkins, C.R. (1993) Signal-dependent membrane protein trafficking in the endocytic pathway. Anna. Rev. Cell Biol., 9, 129-161.
17. Marks, M.S., Ohno, H., Kirchhausen, T. and Bonifacino, J.S. (1997) Protein sorting by tyrosine-based signals: adapting to the Ys and wherefores. Trends Cell Biol., 7, 124-128.
18. Bos, K., Wraight, C and Stanley, K.K. (1993) TGN38 is maintained in the trans-Golgi network by a tyrosine-containing motif in the cytoplasmic domain. EMBO J., 12, 2219-2228.
19. Schäfer, W., Stroh, A., Berghofer, S., Seiler, J., Vey, M., Kruse, M.L., Kem, H.F., Klenk, H.D. and Garten, W. (1995) Two independent targeting signals in the cytoplasmic domain determine trans-Golgi network localization and endosomal trafficking of the proprotein convertase furin. EMBO J., 14, 2424-2435.
20. Voorhees, P., Deignan, E., van Donselaar, E., Humphrey, J., Marks, M.S., Peters, P.J. and Bonifacino, J.S. (1995) An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface. EMBO J., 14, 4961-4975.
21. Alconada, A., Bauer, U. and Hoflack, B. (1996) A tyrosine-based motif and a casein kinase II phosphorylation site regulate the intracellular trafficking of the varicella-zoster virus glycoprotein I, a protein localized in the trans-Golgi network. EMBO J., 15, 6096-6110.
22. Corvera, S., Chawla, A., Chakrabarti, R., Joly, M., Buxton, J. and Czech, M.P. (1994) A double leucine within the GLUT4 glucose transporter COOH-terminal domain functions as an endocytosis signal. J. Cell Biol., 126, 979-989.
23. Verhey, K.J. and Birnbaum, M.J. (1994) A Leu-Leu sequence is essential for COOH-terminal targeting signal of GLUT4 glucose transporter in fibroblasts. J. Biol. Chem., 269, 2353-2356.
24. Mercer, J.F.B., Grimes, A., Ambrosini, L., Lockhart, P., Paynter, J.A., Dierick, H. and Glover, T.W. (1994) Mutations in the murine homologue of the Menkes gene in dappled and blotchy. Nature Genet., 6, 374-378.
25. Qian, Y. Tiffany-Castiglioni, E. and Harris, E.D. (1998) Sequence of a Menkes-type Cu-transporting ATPase from Rat C6 glioma cells: comparison of the rat protein with other mammalian Cu-transporting ATPases. Mol. Cell. Biochem., 181, 49-61.
26. Lin, H.C., Moore, M.S., Sanan, D.A. and Anderson, R.G.W. (1991) Reconstitution of clathrin-coated pit budding from plasma membranes. J. Cell Biol. 114, 881-891.
27. Moore, M.S., Mahaffey, D.T., Brodsky, F.M. and Anderson, R.G.W. (1987) Assembly of clathrin-coated pits onto purified plasma membranes. Science, 236, 558-563.
28. Harter, C. and Mellman, I. (1992) Transport of the lysosomal membrane glycoprotein Igp120 (Igp-A) to lysosomes does not require appearance on the plasma membrane. J. Cell Biol., 117, 311-325.
29. Marks, M.S., Woodruff, L., Ohno, H. and Bonifacino, J.S. (1996) Protein targeting by tyrosine- and di-leucine-based signals: evidence for distinct saturable components. J. Cell Biol., 135, 341-354.
30. Haft, C.R., Klausner, R.D. and Taylor, S.I. (1994) Involvement of dileucine motifs in the internalization and degradation of the insulin receptor. J. Biol. Chem., 269, 26286-26294.
31. Aiken, C., Konner, J., Landau, N.R., Lenburg, M.E. and Trono, D. (1994) Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CW cytoplasmic domain. Cell. 76, 853-864.
32. Vincent, V., Coffin, V., Rozakis, Adcock, M., Momon, J.P. and Kelly, P.A. (1997) Identification of cytoplasmic motifs required for short prolactin receptor internalization. J. Biol. Chem., 272, 7062-7068.
33. Ponnambalam, S., Rabouille, C., Luzio, J.P., Nilsson, T. and Warren, G. (1994) The TGN38 glycoprotein contains two non-overlapping signals that mediate localization to the trans-Golgi network. J. Cell Biol., 125, 253-268.
34. Sambongi, Y., Wakabayashi, T., Yoshimizu, T., Omote, H., Oka, T. and Futai, M. (1997) Caenorhabditis elegans cDN A for a Menkes/Wilson disease gene homologue and its function in a yeast CCC2 gene deletion mutant. J. Biochem., 121, 1169-1175.
35. Bull, P.C., Thomas, J.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. Nature Genet., 5, 327-337.
36. Tanzi, R.E., Petrukhin, K., Chemov, L, Pellequer, J.L., Wasco, W., Ross, B., Romano, D.M., Parano, E., Pavone, L., Brzustowicz, L.M., Devoto, M., Peppercorn, J., Bush, A.I., Sternlieh, I., Piratsu, M., Gusella, J.F., Evgrafov, O., Penchaszadeh, G.K., Honig, B., Edelman, I.S., Soares, M.B., Scheinberg, I.H. and Gilliam, T.C. (1993) The Wilson disease gene is a copper transporting ATPase with homology to the Menkes disease gene. Nature Genet., 5, 344-350.
37. 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. Commun., 197, 271-277.
38. 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.
39. Nagano, K., Nakamura, K., Urakami, K., Umeyama, K., Uchiyama, H., Koiwai, K., Hattori, S., Yamamoto, T. Matsuda, I. and 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. Hepatology, 27, 799-807.
40. 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.
41. 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. Nature Genet., 7, 541-545.
42. Lockhart, P. and Mercer, J.F.B. Genbank accession no. AF032881.
43. La Fontaine, S., Firth, S.D., Lockhart, P.J., Paynter, J.A., and Mercer, J.F.B. (1998) Low copy number plasmid vectors for eukaryotic gene expression: transient expression of the Menkes protein. Plasmid, 39. 245-251.
44. Rees, S., Coote, J., Stables, J., Goodson, S., Harris, S. and Lee, M.G. (1996) Bicistronic vector for the creation of stable mammalian cell lines that predisposes all antibiotic-resistant cells to express recombinant protein. BioTechniques, 20, 102-104.