STAM proteins bind ubiquitinated proteins on the early endosome via the VHS domain and ubiquitin-interacting motif

Molecular Biology of the Cell

Volumn 14, Issue 9, 2003, Pages 3675-3689

  Mizuno, Emi ^a   Kawahata, Kensuke ^a   Kato, Masaki ^a   Kitamura, Naomi ^a   Komada, Masayuki ^a  

^a Tokyo Institute of Technology ^*  (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN; SCATTER FACTOR; SIGNAL TRANSDUCING ADAPTOR MOLECULE PROTEIN; STAM PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; VPS27 PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOSOME; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOCYTOSIS; ENDOSOMES; HELA CELLS; HUMANS; PHOSPHOPROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTOR, EPIDERMAL GROWTH FACTOR; UBIQUITIN;

ANIMALIA;

EID: 0141744750     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-12-0823     Document Type: Article

References (55)

1. 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.
2. Asao, H., Sasaki, Y., Arita, T., Tanaka, N., Endo, K., Kasai, H., Takeshita, T., Endo, Y., Fujita, T., and Sugamura, K. (1997). Hrs is associated with STAM, a signal-transducing adaptor molecule. J. Biol. Chem. 272, 32785-32791.
3. Babst, M., Katzmann, D.J., Estepa-Sabal, E.J., Meerloo, T., and Emr, S.D. (2002a). ESCRT-III: an endosome-associated heterooligomeric protein complex required for MVB sorting. Dev. Cell 3, 271-282.
4. Babst, M., Katzmann, D.J., Snyder, W.B., Wendland, B., and Emr, S.D. (2002b). Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev. Cell 3, 283-289.
5. Babst, M., Odorizzi, G., Estepa, E.J., and Emr, S.D. (2000). Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1, 248-258.
6. Bean, A.J., Davanger, S., Chou, M.F., Gerhardt, B., Tsujimoto, S., and Chang, Y. (2000). Hrs-2 regulates receptor-mediated endocytosis via interactions with Eps15. J. Biol. Chem. 275, 15271-15278.
7. Bean, A.J., Seifert, R., Chen, Y.A., Sacks, R., and Scheller, R.H. (1997). Hrs-2 is an ATPase implicated in calcium-regulated secretion. Nature 385, 826-829.
8. Bilodeau, P.S., Urbanowski, J.L., Winistorfer, S.C., and Piper, R.C. (2002). The Vps27p-Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat. Cell Biol. 4, 534-539.
9. Bishop, N., and Woodman, P. (2001). TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes. J. Biol. Chem. 276, 11735-11742.
10. Bishop, N., Horman, A., and Woodman, P. (2002). Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J. Cell Biol. 157, 91-102.
11. Chin, L.-S., Raynor, M.C., Wei, X., Chen, H.-Q., and Li, L. (2001). Hrs interacts with sorting nexin 1 and regulates degradation of epidermal growth factor receptor. J. Biol. Chem. 276, 7069-7078.
12. Conibear, E. (2002). An ESCRT into the endosome. Mol. Cell 10, 215-216.
13. Dupre, S., Volland, C., and Haguenauer-Tsapis, R. (2001). Membrane transport: ubiquitylation in endosomal sorting. Curr. Biol. 11, R932-R934.
14. Endo, K., et al. (2000). STAM2, a new member of the STAM family, binding to the Janus kinases. FEBS Lett. 477, 55-61.
15. Felder, S., Miller, K., Moehren, G., Ullrich, A., Schlessinger, J., and Hopkins, C.R. (1990). Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body. Cell 61, 623-634.
16. Finley, D., and Chau, V. (1991). Ubiquitination. Annu. Rev. Cell Biol. 7, 25-69.
17. Fujimuro, M., Sawada, H., and Yokosawa, H. (1994). Production and characterization of monoclonal antibodies specific to multi-ubiquitin chains of polyubiquitinated proteins. FEBS Lett. 349, 173-180.
18. Gruenberg, J., and Maxfield, F.R. (1995). Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7, 552-563.
19. Hicke, L. (2001). A new ticket for entry into budding vesicles-ubiquitin. Cell. 106, 527-530.
20. Hofmann, K., and Falquet, L. (2001). A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem. Sci. 26, 347-350.
21. Kamura, T., Burian, D., Khalili, H., Schmidt, S.L., Sato, S., Liu, W.-J., Conrad, M.N., Conaway, R.C., Conaway, J.W., and Shilatifard, A. (2001). Cloning and characterization of ELL-associated proteins EAP45 and EAP20. J. Biol. Chem. 276, 16528-16533.
22. Kato, Y., Misra, S., Puertollano, R., Hurley, J.H., and Bonifacino, J.S. (2002). Phosphoregulation of sorting signal-VHS domain interactions by a direct electrostatic mechanism. Nat. Struct. Biol. 9, 532-536.
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. Katz, et al. (2002). Ligand-independent degradation of epidermal growth factor receptor involves receptor ubiquitylation and Hgs, an adaptor whose ubiquitin-interacting motif targets ubiquitylation by Nedd4. Traffic 3, 740-751.
25. Katzmann, D.J., Babst, M., and Emr, S.D. (2001). Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155.
26. Komada, M., and Kitamura, N. (1995). Growth factor-induced tyrosine phosphorylation of Hrs, a novel 115-kilodalton protein with a structurally conserved putative zinc finger domain. Mol. Cell. Biol. 15, 6213-6221.
27. Komada, M., Masaki, R., Yamamoto, A., and Kitamura, N. (1997). Hrs, a tyrosine kinase substrate with a conserved double zinc finger domain, is localized to the cytoplasmic surface of early endosomes. J. Biol. Chem. 272, 20538-20544.
28. Komada, M., and Soriano, P. (1999). Hrs, a FYVE finger protein localized to early endosomes, is implicated in vesicular traffic and required for ventral folding morphogenesis. Genes Dev. 13, 1475-1485.
29. 2+-dependent exocytosis. J. Cell Sci. 113, 2273-2284.
30. Lloyd, T.E., Atkinson, R., Wu, M.N., Zhou, Y., Pennetta, G., and Bellen, H.J. (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261-269.
31. Lohi, O., and Lehto, V.-P. (2001). STAM/EAST/Hbp adapter proteins - integrators of signalling pathways. FEBS Lett. 508, 287-290.
32. Lohi, O., Poussu, A., Mao, Y., Quiocho, F., and Lehto, V.-P. (2002). VHS domain - a longshoreman of vesicle lines. FEBS Lett. 513, 19-23.
33. Lohi, O., Poussu, A., Merilainen, J., Kellokumpu, S., Wasenius, V.-M., and Lehto, V.-P. (1998). EAST, an epidermal growth factor receptor- and eps15-associated protein with Src homology 3 and tyrosine-based activation motif domains. J. Biol. Chem. 273, 21408-21415.
34. Mao, Y., Nickitenko, A., Duan, X., Lloyd, T.E., Wu, M.N., Bellen, H., and Quiocho, F.A. (2000). Crystal structure of the VHS and FYVE tandem domains of Hrs, a protein involved in membrane trafficking and signal transduction. Cell 100, 447-456.
35. Misra, S., Beach, B.M., and Hurley, J.H. (2000). Structure of the VHS domain of human Tom1 (target of Myb 1): insights into interaction with proteins and membranes. Biochemistry 39, 11282-11290.
36. Misra, S., Puertollano, R., Kato, Y., Bonifacino, J.S., and Hurley, J.H. (2002). Structural basis for acidic-cluster-dileucine sorting-signal recognition by VHS domains. Nature 415, 933-937.
37. Nakatsu, F., Sakuma, M., Matsuo, Y., Arase, H., Yamasaki, S., Nakamura, N., Saito, T., and Ohno, H. (2000). A di-leucine signal in the ubiquitin moiety. J. Biol. Chem. 275, 26213-26219.
38. Naviglio, S., Matteucci, C., Matoskova, B., Nagase, T., Nomura, N., Di Fiore, P.P., and Draetta, G.F. (1998). UBPY: a growth-regulated human ubiquitin isopeptidase. EMBO J. 17, 3241-3250.
39. Nielsen, M.S., Madsen, P., Christensen, E.I., Nykjær, A., Gliemann, J., Kasper, D., Pohlmann, R., and Petersen, C.M. (2001). The sortilin cytoplasmic tail conveys Golgi-endosome transport and binds the VHS domain of the GGA2 sorting protein. EMBO J. 20, 2180-2190.
40. Pandey, A., Fernandez, M.M., Steen, H., Blagoev, B., Nielsen, M.M., Roche, S., Mann, M., and Lodish, H.F. (2000). Identification of a novel immunoreceptor tyrosine-based activation motif-containing molecule, STAM2, by mass spectrometry and its involvement in growth factor and cytokine receptor signaling pathways. J. Biol. Chem. 275, 38633-38639.
41. Piper, R.C., Cooper, A.A., Yang, H., and Stevens, T.H. (1995). VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae. J. Cell Biol. 131:603-617.
42. Polo, S., Sigismund, S., Faretta, M., Guidi, M., Capua, M.R., Bossi, G., Chen, H., De Camilli, P., and Di Fiore, P.P. (2002). A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416, 451-455.
43. Puertollano, R., Aguilar, R.C., Gorshkova, I., Crouch, R.J., and Bonifacino, J.S. (2001). Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science 292, 1712-1716.
44. Raiborg, C., Bache, K.G., Mehlum, A., Stang, E., and Stenmark, H. (2001). Hrs recruits clathrin to early endosomes. EMBO J. 20, 5008-5021.
45. Raiborg, C., Bache, K.G., Gillooly, D.J., Helene Madshus, I., Stang, E., and Stenmark, H. (2002). Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat. Cell Biol. 4, 394-398.
46. Raymond, C.K., Howald-Stevenson, I., Vater, C.A., and Stevens, T.H. (1992). Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3, 1389-1402.
47. Shiba, T., et al. (2002). Structural basis for recognition of acidic-cluster dileucine sequence by GGA1. Nature 415, 937-941.
48. Shih, S.C., Katzmann, D.J., Schnell, J.D., Sutanto, M., Emr, S.D., and Hicke, L. (2002). Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat. Cell Biol. 4, 389-393.
49. 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.
50. Sloper-Mould, K.E., Jemc, J.C., Pickart, C.M., and Hicke, L. (2001). Distinct functional surface regions on ubiquitin. J. Biol. Chem. 276, 30483-30489.
51. Takata, H., Kato, M., Denda, K., and Kitamura, N. (2000). A Hrs binding protein having a Src homology 3 domain is involved in intracellular degradation of growth factors and their receptors. Genes Cells 5, 57-69.
52. Takatsu, H., Katoh, Y., Shiba, Y., and Nakayama, K. (2001). Golgi-localizing, γ-adaptin ear homology domain, ADP-ribosylation factor-binding (GGA) proteins interact with acidic dileucine sequences within the cytoplasmic domains of sorting receptors through their Vps27p/Hrs/STAM (VHS) domains. J. Biol. Chem. 276, 28541-28545.
53. Takeshita, T., et al. (1996). Cloning of a novel signal-transducing adaptor molecule containing an SH3 domain and ITAM. Biochem. Biophys. Res. Commun. 225, 1035-1039.
54. Young, P., Deveraux, Q., Beal, R.E., Pickart, C.M., and Rechsteiner, M. (1998). Characterization of two polyubiquitin binding sites in the 26 S protease subunit 5a. J. Biol. Chem. 273, 5461-5467.
55. Zhu, Y., Doray, B., Poussu, A., Lehto, V.-P., and Kornfeld, S. (2001). Binding of GGA2 to the lysosomal enzyme sorting motif of the mannose 6-phosphate receptor. Science 292, 1716-1718.