Signals regulating trafficking of Menkes (MNK; ATP7A) copper-translocating P-type ATPase in polarized MDCK cells

American Journal of Physiology - Cell Physiology

Volumn 287, Issue 5 56-5, 2004, Pages

  Greenough, M ^a   Pase, L ^a   Voskoboinik, I ^a,b   Petris, M J ^a,c   O'Brien, A Wilson ^a   Camakaris, J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

Copper; Menkes disease; PDZ; Trafficking

Indexed keywords

ADENOSINE TRIPHOSPHATASE; COPPER;

ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; CELL MEMBRANE TRANSPORT; CELL STRAIN; CONTROLLED STUDY; ENZYME LOCALIZATION; GOLGI COMPLEX; KIDNEY CELL; MENKES SYNDROME; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ANIMALS; CATION TRANSPORT PROTEINS; CELL LINE; CELL MEMBRANE; CELL POLARITY; COPPER; DOGS; GOLGI APPARATUS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 6044261452     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00179.2004     Document Type: Article

References (56)

1. Ambrosini L and Mercer JF. Defective copper-induced trafficking and localization of the Menkes protein in patients with mild and copper-treated classical Menkes disease. Hum Mol Genet 8: 1547-1555, 1999.
2. Aroeti B, Okhrimenko H, Reich V, and Orzech E. Polarized trafficking of plasma membrane proteins: emerging roles for coats, SNAREs, GTPases and their link to the cytoskeleton. Biochim Biophys Acta 1376: 57-90, 1998.
3. Bacallao R, Antony C, Dotti C, Karsenti E, Stelzer EH, and Simons K. The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J Cell Biol 109: 2817-2832, 1989.
4. Bello V, Goding JW, Greengrass V, Sali A, Dubljevic V, Lenoir C, Trugnan G, and Maurice M. Characterization of a di-leucine-based signal in the cytoplasmic tail of the nucleotide-pyrophosphatase NPP1 that mediates basolateral targeting but not endocytosis. Mol Biol Cell 12: 3004-3015, 2001.
5. Camakaris J, Petris MJ, Bailey L, Shen P, Lockhart P, Glover TW, Barcroft C, Patton J, and Mercer JF. 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, 1995.
6. Chelly J, Tumer Z, Tonnesen T, Petterson A, Ishikawa-Brush Y, Tommerup N, Horn N, and Monaco AP. Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat Genet 3: 14-19, 1993.
7. Colosetti P, Tunwell RE, Cruttwell C, Arsanto JP, Mauger JP, and Cassio D. The type 3 inositol 1,4,5-trisphosphate receptor is concentrated at the tight junction level in polarized MDCK cells. J Cell Sci 116: 2791-2803, 2003.
8. Danks DM. Disorders of copper transport. In: The Metabolic Basis of Inherited Disease, edited by Scriver CR, Beaudet AL, Sly WS, and Valle D. New York: McGraw-Hill, 1995, p. 2211-2235.
9. Danks DM, Campbell PE, Stevens BJ, Mayne V, and Cartwright E. Menkes's kinky hair syndrome. An inherited defect in copper absorption with widespread effects. Pediatrics 50: 188-201, 1972.
10. Dempsey PJ, Meise KS, and Coffey RJ. Basolateral sorting of transforming growth factor-α precursor in polarized epithelial cells: characterization of cytoplasmic domain determinants. Exp Cell Res 285: 159-174, 2003.
11. Dierick HA, Adam AN, Escara-Wilke JF, and Glover TW. Immunocytochemical localization of the Menkes copper transport protein (ATP7A) to the trans-Golgi network. Hum Mol Genet 6: 409-416, 1997.
12. Dietrich J, Kastrup J, Nielsen BL, Odum N, and Geisler C. Regulation and function of the CD3gamma DxxxLL motif: a binding site for adaptor protein-1 and adaptor protein-2 in vitro. J Cell Biol 138: 271-281, 1997.
13. El Nemer W, Colin Y, Bauvy C, Codogno P, Fraser RH, Cartron JP, and Le Van Kim CL. Isoforms of the Lutheran/basal cell adhesion molecule glycoprotein are differentially delivered in polarized epithelial cells. Mapping of the basolateral sorting signal to a cytoplasmic di-leucine motif. J Biol Chem 274: 31903-31908, 1999.
14. Francis MJ, Jones EE, Levy ER, Martin RL, Ponnambalam S, and Monaco AP. Identification of a di-leucine motif within the C terminus domain of the Menkes disease protein that mediates endocytosis from the plasma membrane. J Cell Sci 112: 1721-1732, 1999.
15. Francis MJ, Jones EE, Levy ER, Ponnambalam S, Chelly J, and Monaco AP. A Golgi localization signal identified in the Menkes recombinant protein. Hum Mol Genet 7: 1245-1252, 1998.
16. Guo X, Rao JN, Liu L, Zou TT, Turner DJ, Bass BL, and Wang JY. Regulation of adherens junctions and epithelial paracellular permeability: a novel function for polyamines. Am J Physiol Cell Physiol 285: C1174-C1187, 2003.
17. Harhaj NS and Antonetti DA. Regulation of tight junctions and loss of barrier function in pathophysiology. Int J Biochem Cell Biol 36: 1206-1237, 2004.
18. Harris ED, Qian Y, and Reddy MC. Genes regulating copper metabolism. Mol Cell Biochem 188: 57-62, 1998.
19. Hughson E and Hirt RP. Assessment of cell polarity. In: Epithelial Cell Culture: A Practical Approach (1st ed.), edited by Shaw AJ. New York: IRL, 1996, p. 37-66.
20. Hung AY and Sheng M. PDZ domains: structural modules for protein complex assembly. J Biol Chem 277: 5699-5702, 2002.
21. Hunziker W and Fumey C. A di-leucine motif mediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells. EMBO J 13: 2963-2967, 1994.
22. Hunziker W, Harter C, Matter K, and Mellman I. Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant. Cell 66: 907-920, 1991.
23. Hurd TW, Gao L, Roh MH, Macara IG, and Margolis B. Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat Cell Biol 5: 137-142, 2003.
24. Jovov B, Wills NK, and Lewis SA. A spectroscopic method for assessing confluence of epithelial cell cultures. Am J Physiol Cell Physiol 261: C1196-C1203, 1991.
25. Keitel V, Nies AT, Brom M, Hummel-Eisenbeiss J, Spring H, and Keppler D. A common Dubin-Johnson syndrome mutation impairs protein maturation and transport activity of MRP2 (ABCC2). Am J Physiol Gastrointest Liver Physiol 284: G165-G174, 2003.
26. Kim BE, Smith K, and Petris MJ. A copper treatable Menkes disease mutation associated with defective trafficking of a functional Menkes copper ATPase. J Med Genet 40: 290-295, 2003.
27. Kleizen B, Braakman I, and de Jonge HR. Regulated trafficking of the CFTR chloride channel. Eur J Cell Biol 79: 544-556, 2000.
28. La Fontaine SL, Firth SD, Camakaris J, Englezou A, Theophilos MB, Petris MJ, Howie M, Lockhart PJ, Greenough M, Brooks H, Reddel RR, and Mercer JF. Correction of the copper transport defect of Menkes patient fibroblasts by expression of the Menkes and Wilson ATPases. J Biol Chem 273: 31375-31380, 1998.
29. + channel, Kir 2.3, is directed by a cytoplasmic COOH-terminal domain. Proc Natl Acad Sci USA 98: 10475-10480, 2001.
30. Marr N, Bichet DG, Lonergan M, Arthus MF, Jeck N, Seyberth HW, Rosenthal W, van Os CH, Oksche A, and Deen PM. Heteroligomerization of an Aquaporin-2 mutant with wild-type Aquaporin-2 and their misrouting to late endosomes/lysosomes explains dominant nephrogenic diabetes insipidus. Hum Mol Genet 11: 779-789, 2002.
31. Meerson NR, Bello V, Delaunay JL, Slimane TA, Delautier D, Lenoir C, Trugnan G, and Maurice M. Intracellular traffic of the ecto-nucleotide pyrophosphatase/phosphodiesterase NPP3 to the apical plasma membrane of MDCK and Caco-2 cells: apical targeting occurs in the absence of N-glycosylation. J Cell Sci 113: 4193-4202, 2000.
32. Mercer JF, Barnes N, Stevenson J, Strausak D, and Llanos RM. Copper-induced trafficking of the Cu-ATPases: a key mechanism for copper homeostasis. Biometals 16: 175-184, 2003.
33. Mercer JF, Livingston J, Hall B, Paynter JA, Begy C, Chandrasekharappa S, Lockhart P, Grimes A, Bhave M, Siemieniak D, and Glover TW. Isolation of a partial candidate gene for Menkes disease by positional cloning. Nat Genet 3: 20-25, 1993.
34. Muth TR and Caplan MJ. Transport protein trafficking in polarized cells. Annu Rev Cell Dev Biol 19: 333-366, 2003.
35. Nelson WJ and Yeaman C. Protein trafficking in the exocytic pathway of polarized epithelial cells. Trends Cell Biol 11: 483-486, 2001.
36. Pase L, Voskoboinik I, Greenough M, and Camakaris J. Copper stimulates trafficking of a distinct pool of the Menkes copper ATPase (ATP7A) to the plasma membrane and diverts it into a rapid recycling pool. Biochem J 378: 1031-1037, 2003.
37. Petris MJ, Camakaris J, Greenough M, LaFontaine S, and Mercer JF. A C-terminal di-leucine is required for localization of the Menkes protein in the trans-Golgi network. Hum Mol Genet 7: 2063-2071, 1998.
38. Petris MJ and Mercer JF. 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, 1999.
39. Petris MJ, Mercer JF, Culvenor JG, Lockhart P, Gleeson PA, and Camakaris J. 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, 1996.
40. Petris MJ, Strausak D, and Mercer JF. The Menkes copper transporter is required for the activation of tyrosinase. Hum Mol Genet 9: 2845-2851, 2000.
41. Petris MJ, Voskoboinik I, Cater M, Smith K, Kim BE, Llanos RM, Strausak D, Camakaris J, and Mercer JF. Copper-regulated trafficking of the Menkes disease copper ATPase is associated with formation of a phosphorylated catalytic intermediate. J Biol Chem 277: 46736-46742, 2002.
42. Procopis P, Camakaris J, and Danks DM. A mild form of Menkes steely hair syndrome. J Pediatr 98: 97-99, 1981.
43. Rajasekaran SA, Palmer LG, Quan K, Harper JF, Ball WJ Jr, Bander NH, Peralta Soler A, and Rajasekaran AK. Na,K-ATPase β-subunit is required for epithelial polarization, suppression of invasion, and cell motility. Mol Biol Cell 12: 279-295, 2001.
44. Rapoport I, Chen YC, Cupers P, Shoelson SE, and Kirchhausen T. Dileucine-based sorting signals bind to the beta chain of AP-1 at a site distinct and regulated differently from the tyrosine-based motif-binding site. EMBO J 17: 2148-2155, 1998.
45. Rapoport I, Miyazaki M, Boll W, Duckworth B, Cantley LC, Shoelson S, and Kirchhausen T. Regulatory interactions in the recognition of endocytic sorting signals by AP-2 complexes. EMBO J 16: 2240-2250, 1997.
46. Rodionov DG and Bakke O. Medium chains of adaptor complexes AP-1 and AP-2 recognize leucine-based sorting signals from the invariant chain. J Biol Chem 273: 6005-6008, 1998.
47. Sandoval IV, Arredondo JJ, Alcalde J, Gonzalez Noriega A, Vandekerckhove J, Jimenez MA, and Rico M. The residues Leu(Ile)475-Ile(Leu, Val, Ala)476, contained in the extended carboxyl cytoplasmic tail, are critical for targeting of the resident lysosomal membrane protein LIMP II to lysosomes. J Biol Chem 269: 6622-6631, 1994.
48. Sandoval IV, Martinez-Arca S, Valdueza J, Palacios S, and Holman GD. Distinct reading of different structural determinants modulates the dileucine-mediated transport steps of the lysosomal membrane protein LIMPII and the insulin-sensitive glucose transporter GLUT4. J Biol Chem 275: 39874-39885, 2000.
49. Strausak D, La Fontaine S, Hill J, Firth SD, Lockhart PJ, and Mercer JF. The role of GMXCXXC metal binding sites in the copper-induced redistribution of the Menkes protein. J Biol Chem 274: 11170-11177, 1999.
50. Voskoboinik I and Camakaris J. Menkes copper-translocating P-type ATPase (ATP7A): biochemical and cell biology properties, and role in Menkes disease. J Bioenerg Biomembr 34: 363-371, 2002.
51. Voskoboinik I, Fernando R, Veldhuis N, Hannan KM, Marmy-Conus N, Pearson RB, and Camakaris J. Protein kinase-dependent phosphorylation of the Menkes copper P-type ATPase. Biochem Biophys Res Commun 303: 337-342, 2003.
52. Voskoboinik I, Mar J, and Camakaris J. Mutational analysis of the Menkes copper P-type ATPase (ATP7A). Biochem Biophys Res Commun 301: 488-494, 2003.
53. Voskoboinik I, Strausak D, Greenough M, Brooks H, Petris M, Smith S, Mercer JF, and Camakaris J. 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, 1999.
54. Vulpe C, Levinson B, Whitney S, Packman S, and Gitschier J. Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nat Genet 3: 7-13, 1993.
55. Wilson PD, Devuyst O, Li X, Gatti L, Falkenstein D, Robinson S, Fambrough D, and Burrow CR. Apical plasma membrane mispolarization of NaK-ATPase in polycystic kidney disease epithelia is associated with aberrant expression of the β2 isoform. Am J Pathol 156: 253-268, 2000.
56. Yamaguchi Y, Heiny ME, Suzuki M, and Gitlin JD. Biochemical characterization and intracellular localization of the Menkes disease protein. Proc Natl Acad Sci USA 93: 14030-14035, 1996.