The Menkes disease ATPase (ATP7A) is internalized via a Rac1-regulated, clathrin- and caveolae-independent pathway

Human Molecular Genetics

Volumn 12, Issue 13, 2003, Pages 1523-1533

  Cobbold, Christian ^a   Coventry, Julie ^a   Ponnambalam, Sreenivasan ^b   Monaco, Anthony P ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BIOLOGICAL MARKER; CD8 ANTIGEN; CLATHRIN; COPPER ION; DYNAMIN; GANGLIOSIDE; GUANOSINE TRIPHOSPHATASE; LEUCINE; MEMBRANE ENZYME; MUTANT PROTEIN; RAC1 PROTEIN; TRANSFERRIN RECEPTOR;

CARBOXY TERMINAL SEQUENCE; CAVEOLA; CELL COMPARTMENTALIZATION; CELL SURFACE; CELL TRANSPORT; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME RELEASE; GENETIC CODE; HUMAN; HUMAN CELL; HUMAN TISSUE; MEMBRANE TRANSPORT; MENKES SYNDROME; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; REVIEW; TRANS GOLGI NETWORK;

ADENOSINE TRIPHOSPHATASES; AMINO ACID MOTIFS; ANIMALS; BORON COMPOUNDS; CATION TRANSPORT PROTEINS; CAVEOLAE; CELL MEMBRANE; CLATHRIN; COPPER; COS CELLS; CYTOSOL; ENDOCYTOSIS; ENDOSOMES; GENES, DOMINANT; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; IONS; LEUCINE; LUMINESCENT PROTEINS; MENKES KINKY HAIR SYNDROME; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MUTATION; PROTEIN STRUCTURE, TERTIARY; RAC1 GTP-BINDING PROTEIN; RECEPTORS, TRANSFERRIN; RECOMBINANT FUSION PROTEINS; TEMPERATURE; TIME FACTORS; TRANS-GOLGI NETWORK; TRANSFECTION;

EID: 0037767494     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddg166     Document Type: Review

References (56)

1. Menkes, J., Alter, M., Steigleder, G., Weakley, D. and Sung, J. (1962) A sex-linked recessive disorder with retardation of growth, peculiar hair, and focal cerebral and cerebellar degeneration. Pediatrics, 29, 764-779.
2. Silver, S., Nucifora, G. and Phung, L.T. (1993) Human Menkes X-chromosome disease and the staphylococcal cadmium-resistance ATPase: a remarkable similarity in protein sequences. Mol. Microbiol., 10, 7-12.
3. Bull, P.C. and Cox, D.W. (1994) Wilson disease and Menkes disease: new handles on heavy-metal transport. Trends Genet., 10, 246-252.
4. Petris, M.J. and Mercer, J.F. (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.
5. 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.
6. 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.
7. Cobbold, C., Ponnambalam, S., Francis, M.J. and Monaco, A.P. (2002) Novel membrane traffic steps regulate the exocytosis of the Menkes disease ATPase. Hum. Mol. Genet., 11, 2855-2866.
8. 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.
9. Petris, M.J., Strausak, D. and Mercer, J.F. (2000) The Menkes copper transporter is required for the activation of tyrosinase. Hum. Mol. Genet., 9, 2845-2851.
10. Ackland, M.L., Cornish, E.J., Paynter, J.A., Grimes, A., Michalczyk, A. and Mercer, J.F. (1997) Expression of Menkes disease gene in mammary carcinoma cells. Biochem. J., 328, 237-243.
11. 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.
12. Francis, M.J., Jones, E.E., Levy, E.R., Martin, R.L., Ponnambalam, S. and Monaco, A.P. (1999) 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.
13. Petris, M.J., Camakaris, J., Greenough, M., LaFontaine, S. and Mercer, J.F. (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.
14. Boehm, M. and Bonifacino, J.S. (2001) Adaptins: the final recount. Mol. Biol. Cell, 12, 2907-2920.
15. Kirchhausen, T. (2000) Three ways to make a vesicle. Nat. Rev. Mol. Cell Biol., 1, 187-198.
16. Pelkmans, L. and Helenius, A. (2002) Endocytosis via caveolae. Traffic, 3, 311-320.
17. Orlandi, P.A. and Fishman, P.H. (1998) Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J. Cell Biol., 141, 905-915.
18. Marsh, M. and McMahon, H.T. (1999) The structural era of endocytosis. Science, 285, 215-220.
19. Benmerah, A., Begue, B., Dautry-Varsat, A. and Cerf-Bensussan, N. (1996) The ear of alpha-adaptin interacts with the COOH-terminal domain of the Eps 15 protein. J. Biol. Chem., 271, 12111-12116.
20. Damke, H., Baba, T., Warnock, D.E. and Schmid, S.L. (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol., 127, 915-934.
21. Oh, P., McIntosh, D.P. and Schnitzer, J.E. (1998) Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J. Cell Biol., 141, 101-114.
22. Damke, H., Gossen, M., Freundlieb, S., Bujard, H. and Schmid, S.L. (1995) Tightly regulated and inducible expression of dominant interfering dynamin mutant in stably transformed HeLa cells. Meth. Enzymol., 257, 209-220.
23. Schmid, S.L., McNiven, M.A. and De Camilli, P. (1998) Dynamin and its partners: a progress report. Curr. Opin. Cell Biol., 10, 504-512.
24. Benmerah, A., Lamaze, C., Begue, B., Schmid, S.L., Dautry-Varsat, A. and Cerf-Bensussan, N. (1998) AP-2/Eps15 interaction is required for receptor-mediated endocytosis. J. Cell Biol., 140, 1055-1062.
25. Kasai, K., Shin, H.W., Shinotsuka, C., Murakami, K. and Nakayama, K. (1999) Dynamin II is involved in endocytosis but not in the formation of transport vesicles from the trans-Golgi network. J. Biochem. (Tokyo), 125, 780-789.
26. Altschuler, Y., Barbas, S.M., Terlecky, L.J., Tang, K., Hardy, S., Mostov, K.E. and Schmid, S.L. (1998) Redundant and distinct functions for dynamin-1 and dynamin-2 isoforms. J. Cell Biol., 143, 1871-1881.
27. Pelkmans, L., Puntener, D. and Helenius, A. (2002) Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science, 296, 535-539.
28. Skretting, G., Torgersen, M.L., van Deurs, B. and Sandvig, K. (1999) Endocytic mechanisms responsible for uptake of GPI-linked diphtheria toxin receptor. J. Cell Sci., 112, 3899-3909.
29. Lamaze, C., Chuang, T.H., Terlecky, L.J., Bokoch, G.M. and Schmid, S.L. (1996) Regulation of receptor-mediated endocytosis by Rho and Rac. Nature, 382, 177-179.
30. Sabharanjak, S., Sharma, P., Parton, R.G. and Mayor, S. (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell, 2, 411-423.
31. Ellis, S. and Mellor, H. (2000) Regulation of endocytic traffic by rho family GTPases. Trends Cell Biol., 10, 85-88.
32. Bishop, A.L. and Hall, A. (2000) Rho GTPases and their effector proteins. Biochem. J., 348 (Pt 2), 241-255.
33. Hinshaw, J.E. and Schmid, S.L. (1995) Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature, 374, 190-192.
34. Camakaris, J., Petris, M.J., Bailey, L., Shen, P., Lockhart, P., Glover, T.W., Barcroft, C., Patton, J. and Mercer, J.F. (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.
35. LaFontaine, S., Firth, S.D., Lockhart, P.J., Brooks, H., Parton, R.G., Camakaris, J. and Mercer, J.F. (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.
36. Puri, V., Watanabe, R., Singh, R.D., Dominguez, M., Brown, J.C., Wheatley, C.L., Marks, D.L. and Pagano, R.E. (2001) Clathrin-dependent and -independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways. J. Cell Biol., 154, 535-547.
37. Sharma, D.K., Choudhury, A., Singh, R., Wheatley, C.L., Marks, D.L. and Pagano, R.E. (2002) Glycosphingolipids internalized via caveolar-related endocytosis rapidly merge with the clathrin pathway in early endosomes and form microdomains for recycling. J. Biol. Chem., 278, 7564-7572.
38. Ridley, A.J. (2001) Rho proteins: linking signaling with membrane trafficking. Traffic, 2, 303-310.
39. Frantz, C., Coppola, T. and Regazzi, R. (2002) Involvement of Rho GTPases and their effectors in the secretory process of PC12 cells. Exp. Cell Res., 273, 119-126.
40. Banting, G., Maile, R. and Roquemore, E.P. (1998) The steady state distribution of humTGN46 is not significantly altered in cells defective in clathrin-mediated endocytosis. J. Cell Sci., 111, 3451-3458.
41. Rothberg, K.G., Heuser, J.E., Donzell, W.C., Ying, Y.S., Glenney, J.R. and Anderson, R.G. (1992) Caveolin, a protein component of caveolae membrane coats. Cell, 68, 673-682.
42. Rodal, S.K., Skretting, G., Garred, O., Vilhardt, F., van Deurs, B. and Sandvig, K. (1999) Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell, 10, 961-974.
43. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science, 279, 509-514.
44. Westwick, J.K., Lambert, Q.T., Clark, G.J., Symons, M., Van Aelst, L., Pestell, R.G. and Der, C.J. (1997) Rac regulation of transformation, gene expression, and actin organization by multiple, PAK-independent pathways. Mol. Cell. Biol., 17, 1324-1335.
45. D'Souza-Schorey, C., Boshans, R.L., McDonough, M., Stahl, P.D. and Van Aelst, L. (1997) A role for POR1, a Rac1-interacting protein, in ARF6-mediated cytoskeletal rearrangements. EMBO J., 16, 5445-5454.
46. Joneson, T., McDonough, M., Bar-Sagi, D. and Van Aelst, L. (1996) RAC regulation of actin polymerization and proliferation by a pathway distinct from Jun kinase. Science, 274, 1374-1376.
47. Rennefahrt, U.E., Illert, B., Kerkhoff, E., Troppmair, J. and Rapp, U.R. (2002) Constitutive JNK activation in NIH 3T3 fibroblasts induces a partially transformed phenotype. J. Biol. Chem., 277, 29510-29518.
48. Curtin, J.F. and Cotter, T.G. (2002) Anisomycin activates JNK and sensitises DU 145 prostate carcinoma cells to Fas mediated apoptosis. Br. J. Cancer, 87, 1188-1194.
49. Mohamed, A.A., Jupp, O.J., Anderson, H.M., Littlejohn, A.F., Vandenabeele, P. and MacEwan, D.J. (2002) Tumour necrosis factor-induced activation of c-Jun N-terminal kinase is sensitive to caspase-dependent modulation while activation of mitogen-activated protein kinase (MAPK) or p38 MAPK is not. Biochem. J., 366, 145-155.
50. Al-Hasani, H., Kunamneni, R.K., Dawson, K., Hinck, C.S., Muller-Wieland, D. and Cushman, S.W. (2002) Roles of the N- and C-termini of GLUT4 in endocytosis. J. Cell Sci., 115, 131-140.
51. Yang, X., Khosravi-Far, R., Chang, H.Y. and Baltimore, D. (1997) Daxx, a novel Fas-binding protein that activates JNK and apoptosis. Cell, 89, 1067-1076.
52. Lalioti, V.S., Vergarajauregui, S., Pulido, D. and Sandoval, I.V. (2002) The insulin-sensitive glucose transporter, GLUT4, interacts physically with Daxx. Two proteins with capacity to bind Ubc9 and conjugated to SUMO1. J. Biol. Chem., 277, 19783-19791.
53. Lamaze, C., Dujeancourt, A., Baba, T., Lo, C.G., Benmerah, A. and Dautry-Varsat, A. (2001) Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell, 7, 661-671.
54. Vowels, J.J. and Payne, G.S. (1998) A dileucine-like sorting signal directs transport into an AP-3-dependent, clathrin-independent pathway to the yeast vacuole. EMBO J., 17, 2482-2493.
55. Robinson, M.S. and Bonifacino, J.S. (2001) Adaptor-related proteins. Curr. Opin. Cell Biol., 13, 444-453.
56. Cobbold, C., Whittle, J.T. and Wileman, T. (1996) Involvement of the endoplasmic reticulum in the assembly and envelopment of African swine fever virus. J. Virol., 70, 8382-8390.