The FAM Deubiquitylating Enzyme Localizes to Multiple Points of Protein Trafficking in Epithelia, where It Associates with E-cadherin and β-catenin

Molecular Biology of the Cell

Volumn 15, Issue 4, 2004, Pages 1591-1599

  Murray, Rachael Z ^a,b   Jolly, Lachlan A ^a   Wood, Stephen A ^a,b  

^a CHILD HEALTH RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; ENZYME; FAT FACETS IN MOUSE ENZYME; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ARTICLE; BIOSYNTHESIS; CELL ADHESION; CELL CULTURE; CELL INTERACTION; CELL MEMBRANE TRANSPORT; CELL POLARITY; CELL STRAIN MCF 7; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; ENZYME LOCALIZATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; FIBROBLAST; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTESTINE EPITHELIUM CELL; LYSOSOME; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; UBIQUITINATION;

ACTININ; BETA CATENIN; CADHERINS; CELL ADHESION; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; CHROMATOGRAPHY, GEL; CYTOPLASM; CYTOSKELETAL PROTEINS; DETERGENTS; ENDOPEPTIDASES; EPITHELIUM; FIBROBLASTS; GOLGI APPARATUS; HUMANS; MASS SPECTROMETRY; MICROSCOPY, FLUORESCENCE; MYOSINS; PLASMIDS; PRECIPITIN TESTS; PROTEIN TRANSPORT; TRANS-ACTIVATORS; TRANSFECTION; UBIQUITIN;

ANIMALIA; MINK CELL FOCUS-FORMING VIRUS;

EID: 1642423571     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-08-0630     Document Type: Article

References (55)

1. Aberle, H., Bauer, A., Stappert, J., Kispert, A., and Kemler, R. (1997). b-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16, 3797-3804.
2. Allan, V.J., Thompson, H.M., and McNiven, M.A. (2002). Motoring around the Golgi. Nat. Cell Biol. 4, E236-E242.
3. Amerik, A.Y., Nowak, J., Swaminathan, S., and Hochstrasser, M. (2000). The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol. Biol. Cell 11, 3365-3380.
4. Boettner, B., Govek, E.-E., Cross, J., and Van Aelst, L. (2000). The junctional multidomain protein AF-6 is a binding partner of the Rap1A GTPase and associates with the actin cytoskeletal regulator profilin. Proc. Natl. Acad. Sci. USA 97, 9064-9069.
5. Cadavid, A.L.M., Ginzel, A., and Fischer, J.A. (2000). The function of the Drosophila Fat facets deubiquitinating enzyme in limiting photoreceptor cell number is intimately associated with endocytosis. Development 127, 1727-1736.
6. Chen, L., and Davis, N.G. (2002). Ubiquitin-independent entry into the yeast recycling pathway. Traffic 3, 110-123.
7. Chen, X., Overstreet, E., Wood, S.A., and Fischer, J.A. (2000). On the conservation of function of the Drosophila Fat facets deubiquitinating enzyme and Fam, its mouse homolog. Dev. Genet Evol. 210, 603-610.
8. Chen, X., Zhang, B., and Fischer, J.A. (2002). A specific protein substrate for a deubiquitinating enzyme: liquid facets is the substrate of Fat facets. Genes Dev. 16, 289-294.
9. Chen, Y.-T., Stewart, D.B., and Nelson, W.J. (1999). Coupling assembly of the E-cadherin/beta-catenin complex to efficient enoplasmic reticulum exit and basal-lateral membrane targeting of E-cadherin in polarized MDCK cells. J. Cell Biol. 144, 687-699.
10. Cohen, M., Stutz, F., Belgareh, N., Haguenauer-Tsapis, R., and Dargemont, C. (2003). Ubp3 requires a cofactor, Bre5, to specifically de-ubiquitinate the COPII protein, Sec23. Nat. Cell Biol. 5, 661-667.
11. Conacci-Sorrell, M., Zhurinsky, J. and Ben-Ze'ev, A. (2002) The cadherincatenin adhesion system in signaling and cancer. J. Clin. Invest. 109, 987-991.
12. Davis, M.A., Ireton, R.C., and Reynolds, A.B. (2003). A core function for p120-catenin in cadherin turnover. J. Cell Biol. 163, 525-534.
13. Dupre, S. and Haguenauer-Tsapis, R. (2001) Deubiquitination step in the endocytic pathway of yeast plasma membrane proteins: crucial role of Doa4p ubiquitin isopeptidase. Mol. Cell. Biol. 21, 4482-4494.
14. Fujita, Y., Krause, G., Scheffner, M., Zechner, D., Leddy, H.E.M., Behrens, J., Sommer, T., and Birchmeier, W. (2002). Hakai, a c-Cb1-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 4, 222-231.
15. Hecht, A., and Kemler, R. (2000). Curbing the nuclear activities of beta-catenin. Control over Wnt target gene expression. EMBO Rep. 1, 24-28.
16. Helliwell, S.B., Losko, S., and Kaiser, C.A. (2001). Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease. J. Cell Biol. 153, 649-662.
17. Hicke, L. (2001). Protein regulation by monoubiquitin. Nat. Rev. Mol. Cell. Biol. 2, 195-201.
18. Hicke, L., and Riezman, H. (1996). Ubiquitiniation of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84, 277-287.
19. Huber, A.H., Stewart, D.B., Laurents, D.V., Nelson, W.J., and Weis, W.I. (2001). The cadherin cytoplasmic domain is unstructured in the absence of b-catenin. A possible mechanism for regulating cadherin turnover. J. Biol. Chem. 276, 12301-12309.
20. Ikonen, E., de Almeid, J.B., Fath, K.R., Burgess, D.R., Ashman, K., Simons, K., and Stow, J.L. (1997). Myosin II is associated with Golgi membranes: identification of p200 as nonmuscle myosin II on Golgi-derived vesicles. J. Cell Sci. 110, 2155-2164.
21. Kaminska, J., Gajewska, B., Hopper, A.K., and Zoladek, T. (2002). Rsp5p, a new link between the actin cytoskeleton and endocytosis in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 22, 6946-6948.
22. Kanai-Azuma, M., Mattick, J.S., Kaibuchi, K., and Wood, S.A. (2000). Co-localization of FAM and AF-6, the mammalian homologues of Drosophila faf and canoe, in mouse eye development. Mech. Dev. 91, 383-386.
23. Kato, M., Miyazawa, K., and Kitamura, N. (2000). A deubiquitinating enzyme UBPY interacts with the Src homology 3 domain of Hrs-binding protein via a novel binding motif PX(V/I)(D/N)RXXKP. J. Biol. Chem. 275, 37481-37487.
24. Katzmann, D.J., Babst, M., and Emr, S.D. (2001). Ubiquitin-dependent sorting into the multivesicular pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155.
25. Katzmann, D.J., Odorizzi, G., and Emr, S.D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell. Biol. 3, 893-905.
26. Kitagawa, M. et al. (1999). An F-box, FWD1, mediates ubiquitin-dependent proteolysis of b-catenin. EMBO J. 18, 2401-2410.
27. Le Bivic, A., Quaroni, A., Nichols, B., and Rodriguez-Boulan, E. (1990). Biogenetic pathways of plasma membrane proteins in Caco-2, a human intestinal epithelial cell line. J. Cell Biol. 111, 1351-1361.
28. Le, T.L., Yap, A.S., and Stow, J.L. (1999). Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J. Cell Biol. 146, 219-232.
29. Lippincott-Schwartz, J., Yuan, L.C., Bonifacino, J.S., and Klausner, R.D. (1989). Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801-813.
30. Matter, K., Brauchbar, M., Bucher, K., and Hauri, H.P. (1990). Sorting of endogenous plasma membrane proteins occurs from two sites in cultured human intestinal epithelial cells (Caco-2). Cell 60, 429-437.
31. Maurice, M., Schell, M.J., Lardeux, B., and Hubbard, A.L. (1994). Biosynthesis and intracellular transport of a bile canalicular plasma membrane protein: studies in vivo and in the perfused rat liver. Hepatology 19, 648-655.
32. Miranda, K.C., Khromykh, T., Christy, P., Le, T.L., Gottardi, C.J., Yap, A.S., Stow, J.L., and Teasdale, R.D. (2001). A dileucine motif targets E-cadherin to the basolateral cell surface in Madin-Darby canine kidney and LLC-PK1 epithelial cells. J. Biol. Chem. 276, 22565-22572.
33. Mostov, K.E., Verges, M., and Altschuler, Y. (2000). Membrane traffic in polarized epithelial cells. Curr. Opin. Cell Biol. 12, 483-490.
34. Musch, A., Cohen, D., and Rodriguez-Boulan, E. (1997). Myosin II is involved in the production of constitutive transport vesicles from the TGN. J. Cell Biol. 138, 291-306.
35. Noma, T., Kanai, Y., Kanai-Azuma, M., Ishii, M., Fujisawa, M., Kurohmaru, M., Kawakami, H., Wood, S.A., and Hayashi, Y. (2002). Stage- and sex-dependent expressions of Usp9x, an X-linked mouse ortholog of Drsosphila Fat Facets, during gonadal development and oogenesis in mice. Mech. Dev. 119, 1-5.
36. Pantaleon, M., Kanai-Azuma, M., Mattick, J.S., Kaibuchi, K., Kaye, P.L., and Wood, S.A. (2001). FAM deubiquitylating enzyme is essential for preimplantation mouse embryo development. Mech. Dev. 109, 151-160.
37. Pol, A., Ortega, D., and Enrich, C. (1997). Identification of cytoskeleton-associated proteins in isolated rat liver endosomes. Biochem. J. 327, 741-746.
38. Reggiori, F., and Pelham, H.R.B. (2002). A transmembrane ubiquitin ligase required to sort membrane proteins into multivesicular bodies. Nat. Cell Biol. 4, 117-123.
39. Saraste, J., and Kuismanen, E. (1984). Pre- and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins, to the cell surface. Cell 38, 535-549.
40. Schnell, J. D. and Hicke, L. (2003) Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J. Biol. Chem. epub Ms R300018200.
41. Shapiro, L. (2001). beta-catenin and its multiple partners: promiscuity explained. Nat. Struct. Biol. 8, 484-487.
42. Shih, S.C., Sloper-Mould, K.E., and Hicke, L. (2000). Monoubiquitin carries a novel internalization signal that is appended to activated receptors. EMBO J. 19, 187-198.
43. Speicher, K.D., Kolbas, O., Harper, S., and Speicher, D.W. (2000). Systematic analysis of peptide recoveries from in-gel digestions for protein identifications in proteome studies. J. Biomol. Tech. 11, 74-86.
44. Springael, J.Y., Nikko, E., Andre, B., and Marini, A.M. (2002). Yeast Npi3/Bro1 is involved in ubiquitin-dependent control of permease trafficking. FEBS Lett. 517, 103-109.
45. Svastova, E., Zilka, N., Zat'ovicova, M., Gibadulinova, A., Ciampor, F., Pastorek, J., and Pastorekova, S. (2003). Carbonic anhydrase IX, reduces Ecadherin-mediated adhesion of MDCK cells via interaction with beta-catenin. Exp. Cell Res. 290, 332-345.
46. Takahashi, K. et al. (1999). Nectin/PRR: an immunoglobuhn-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with Afadin, a PDZ domain-containing protein. J. Cell Biol. 145, 539-549.
47. Taya, S., Yamamoto, T., Kanai-Azuma, M., Wood, S.A., and Kaibuchi, K. (1999). The deubiquitinating enzyme Fam interacts with and stabilizes b-catenin. Genes Cells 4, 757-767.
48. Taya, S. et al. (1998). The Ras target AF-6 is a substrate of the fam deubiquitinating enzyme. J. Cell Biol., 142, 1053-1062.
49. Towbin, H., Staehelin, T., and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354.
50. Wang, G., McCaffery, J.M., Wendland, B., Dupre, S., Haguenauer-Tsapis, R., and Huibregtse, J.M. (2001). Localization of the Rsp5p ubiquitin-protein ligase at multiple sites within the endocytic pathway. Mol. Cell. Biol. 21, 3564-3575.
51. Wilkinson, K.D. (2000). Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. Semin. Cell Dev. Biol. 11, 141-148.
52. Wood, S.A., Pascoe, W.S., Ru, K., Yamada, T., Hirchenhain, J., Kemler, R., and Mattick, J.S. (1997). Cloning and expression analysis of a novel mouse gene with sequence similarity to the Drosophila fat facets gene. Mech. Dev. 63, 29-38.
53. Wu, Z., Li, Q., Fortini, M.E., and Fischer, J.A. (1999). Genetic analysis of the role of the Drosophila fat facets gene in the ubiquitin pathway. Dev. Genet. 25, 312-320.
54. Yamamoto, K., Harada, N., Kano, K., Taya, S., Canaani, E., Matsuura, Y., Mizoguchi, A., Ide, C., and Kaibuchi, K. (1997). The Ras target AF-6 interacts with ZO-1 and serves as a peripheral component of tight junctions in epithelial cells. J. Cell Biol. 139, 785-795.
55. Zhu, W., Leber, B., and Andrews, D.W. (2001). Cytoplasmic O-glycosylation prevents cell surface transport of E-cadherin during apoptosis. EMBO J. 20, 5999-6007.