Endosomal trafficking of the Menkes copper ATPase ATP7A is mediated by vesicles containing the Rab7 and Rab5 GTPase proteins

Experimental Cell Research

Volumn 291, Issue 2, 2003, Pages 377-385

  Pascale, M C ^a   Franceschelli, S ^a   Moltedo, O ^a   Belleudi, F ^b   Torrisi, M R ^b   Bucci, C ^c   La Fontaine, S ^d   Mercer, J F B ^d   Leone, A ^a,e  

^a UNIVERSITY OF SALERNO   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF SALENTO   (Italy)

^d DEAKIN UNIVERSITY   (Australia)

^e CNR   (Italy)

Author keywords

Chinese hamster ovary cells; Copper transport; MNK protein; Rab protein s; Trans Golgi network; Vesicular trafficking

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BIOLOGICAL MARKER; COPPER ADENOSINE TRIPHOSPHATASE ATP7A; ENZYME; GUANOSINE TRIPHOSPHATASE; PROTEIN SUBUNIT; RAB PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CLONING; CELL GROWTH; CELL MEMBRANE; CELL SELECTION; CELL VACUOLE; CHO CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOSOME; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE TEST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CRICETINAE; CRICETULUS GRISEUS;

EID: 0344441418     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2003.07.001     Document Type: Article

References (46)

1. Danks D.M., Campbell P.E., Stevens B.J., Mayne V., Cartwright E. Menkes kinky hair syndrome an inherited defect in copper absorption with widespread effects . Pediatrics. 50:1972;188-201.
2. Horn N., Tønnesen T., Tümer Z. Menkes disease an X linked neurological disorder of the copper metabolism . Brain Pathol. 2:1992;351-362.
3. Mercer J.F., Livingston J., Hall B., Paynter J.A., Begy C., Chandrasekharappa S., Lockhart P., Grimes A., Bhave M., Siemienick D., et al. Isolation of a partial candidate gene for Menkes disease by positional cloning. Nat. Genet. 3:1993;20-25.
4. Chelly J., Tümer Z., Tønnesen T., Petterson A., Ishikawa Brush Y., Tommerup N., Horn N., Monaco A.P. Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat. Genet. 3:1993;14-19.
5. Vulpe C., Levinson B., Whitney S., Packman S., Gitschier J. Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nat. Genet. 3:1993;7-13.
6. Yamaguchi Y., Heiny M.E., Suzuki M., Gitlin J.D. Biochemical characterization and intracellular localization of the Menkes copper transport protein (ATP7A) to the trans-Golgi network. Proc. Natl. Acad. Sci. USA. 93:1996;14030-14035.
7. Dierick H.A., Adam A.N., Escara Wilke J.F., Glover T.W. Immuno-cytochemical localization of the Menkes copper transporting protein (ATP7A) to the trans-Golgi network. Hum. Mol. Genet. 6:1997;409-416.
8. Ackland M.L., Cornish E.J., Paynter J.A., Grimes A., Michalezyk A., Mercer J.F. Expression of Menkes disease gene in mammary carcinoma cells. Biochem. J. 328:1997;237-243.
9. La Fontaine S., Firth S.D., Lockart P.J., Brooks H., Parton R.G., Camakaris J., Mercer J.F.B. 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. 7:1998;1293-1300.
10. Petris M.J., Mercer J.F., Culvenor J.G., Lockhart P., Gleeson P.A., 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. 15:1996;6084-6095.
11. Francis M.J., Jones E.E., Levy E.R., Ponnambalam S., Chelly J., Monaco A.P. A Golgi localization signal identified in the Menkes recombinant protein. Hum. Mol. Genet. 7:1998;1245-1252.
12. Qi M., Byers P.H. Constitutive skipping of alternatively spliced exon 10 in the ATP7A gene abolishes Golgi localization of the Menkes protein and produces occipital horn syndrome. Hum. Mol. Genet. 7:1998;465-469.
13. Petris M.J., Camakaris J., Greenough M., La Fontaine S., Mercer J.F.B. A C-terminal di-leucine is required for localization of the Menkes protein in the trans-Golgi network. Hum. Mol. Genet. 13:1998;2063-2071.
14. Petris M.J., Mercer J.F.B. 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. 8:1999;2107-2115.
15. Francis M.J., Jones E.E., Levy E.R., Martin R.L., Ponnambalam S., Monaco A.P. 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. 112:1999;1721-1732.
16. Ghosh R.N., Mallet W.G., Soe T.T., McGraw T.E., Maxfiel F.R. An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking trough the endocytic recycling compartment in CHO cells. J. Cell Biol. 142:1998;923-936.
17. Jones S.M., Crosby J.R., Salomero J., Howell K.E. A cytosolic complex of p62 and rab6 associates with TGN38/41 and is involved in budding of exocytic vesicles from the trans-Golgi network. J. Cell Biol. 122:1993;775-780.
18. Gruenberg J., Maxfield F.R. Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7:1995;552-563.
19. Mellman I. Endocytosis and molecular sorting. Annu. Rev. Cell. Dev. Biol. 12:1996;575-625.
20. Aniento F., Emans N., Griffiths G., Gruenberg J. Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J. Cell Biol. 123:1993;1373-1387.
21. Mallet W.G., Maxfield F.R. Chimeric forms of furin and TGN38 are transported from the plasma membrane to the trans-Golgi network via distinct endosomal pathways. J. Cell Biol. 146:1999;345-359.
22. Gruenberg J., Griffiths G., Howell K.E. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicles fusion in vitro. J. Cell Biol. 108:1989;1301-1316.
23. Mukherjee S., Maxfield F.R. Role of membrane organization and membrane domains in endocytic lipid trafficking. Traffic. 1:2000;203-211.
24. McNew J.A., Parlati F., Fukuda R., Johnston R.J., Paz K., Paumet F., Söllner T.H., Rothman J.E. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature. 407:2000;153-159.
25. Parlati F., McNew J.A., Fukuda R., Miller R., Söllner T.H., Rothman J.E. Topological restriction of SNARE-dependent membrane fusion. Nature. 407:2000;194-198.
26. Chen Y.A., Scheller R.H. SNARE-mediate membrane fusion. Nat. Rev. Mol. Cell Biol. 2:2001;98-106.
27. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2:2001;107-117.
28. Novick P., Zerial M. The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol. 9:1997;496-504.
29. Rodman J.S., Wandinger-Ness A. Rab GTPases coordinate endocytosis. J. Cell Sci. 113:2000;183-192.
30. Lemmon S.K., Traub L.M. Sorting in the endosomal system in yeast and animal cells. Curr. Opin. Cell Biol. 12:2000;457-466.
31. Sönnichsen B., De Renzis S., Nielsen E., Rietdorf J., Zerial M. Distinct membrane domains on endosomes in the recycling visualized by multicolor imaging of Rab4, Rab5 and Rab 11. J. Cell Biol. 149:2000;901-914.
32. Gorvel J.P., Chavrier P., Zerial M., Gruenberg J. Rab5 controls early endosome fusion in vitro. Cell. 64:1991;915-925.
33. Bucci C., Parton R.G., Mather I.H., Stunnenberg H., Simons K., Hoflack B., Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell. 70:1992;715-728.
34. Chistoforidis S., McBride H.M., Burgoyne R.D., Zerial M. The Rab 5 effector EEA1 is a core component of endosome docking. Nature. 397:1999;621-625.
35. Callaghan J., Nixon S., Bucci C., Toh B.H., Stenmark H. Direct interaction of EEA1 with Rab5b. Eur. J. Biochem. 265:1999;361-366.
36. Nielsen E., Severin F., Backer J.M., Hyman A., Zerial M. Rab5 regulates motility of early endosomes on microtubules. Nat. Cell Biol. 1:1999;376-382.
37. Feng Y., Press B., Wandinger-Ness A. Rab7 an important regulator of late endocytic membrane traffic . J. Cell Biol. 131:1995;1435-1452.
38. Vitelli R., Santillo M., Lattero D., Chiariello M., Bifulco M., Bruni C.B., Bucci C. Role of the small GTPase Rab7 in the late endocytic pathway. J. Biol. Chem. 272:1997;4391-4397.
39. Stenmark H., Parton R.G., Steele-Mortimer O., Lutcke A., Gruenberg J., Zerial M. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13:1994;1287-1296.
40. Bonatti S., Migliaccio G., Simons K. Palmitylation of viral membrane glycoproteins takes place after exit from the endoplasmic reticulum. J. Biol. Chem. 264:1989;12590-12595.
41. Welch W.J., Sefton B.M. Two small virus-specific polypeptides are produced during infection with Sindbis virus. J. Virol. 29:1979;1186-1195.
42. Grewal T., Heeren J., Mewawala D., Schnitgerhans T., Wendt D., Salomon G., Enrich C.C., Beisiegel U., Jackle S. Annexin VI stimulates endocytosis and is involved in the trafficking of low density lipoprotein to the prelysosomal compartment. J. Biol. Chem. 275:2000;33806-33813.
43. Menasche G., Pastural E., Feldmann J., Certain S., Ersoy F., Dupuis S., Wulffraat N., Bianchi D., Fischer A., Le Deist F., de Saint Basile G. Mutations in RAB27A cause Griscelli syndrome associated with haematophagocytic syndrome. Nat. Genet. 25:2000;173-176.
44. Wu X.S., Rao K., Zhang H., Wang F., Sellers J.R., Matesic L.E., Copeland N.G., Jenkins N.A., Hammer J.A. 3rd. Identification of an organelle receptor for myosin-Va. Nat. Cell. Biol. 4:2002;271-278.
45. Tümer, Z., Maller, L.B., Horn, N., 1997. Mutation spectrum of ATP7A, the gene defective in Menkes disease, in: Leone, A., Mercer, F.B.J. (Eds.), Copper Transport and Its Disorders (Molecular and Cellular Aspects), Advances in Experimental Medicine and Biology, Vol. 448.
46. Tümer Z., Lund C., Tolshave J., Vural B., Tønnesen T., Horn N. Identification of point mutations in 41 unrelated patients affected with Menkes disease. Am. J. Hum. Genet. 60:1997;63-71.