Hrs regulates early endosome fusion by inhibiting formation of an endosomal SNARE complex

Journal of Cell Biology

Volumn 162, Issue 1, 2003, Pages 125-137

  Sun, Wei ^a   Yan, Qing ^a   Vida, Thomas A ^a   Bean, Andrew J ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

EGF; Endocytosis; Receptor; SNAP 25; Syntaxin

Indexed keywords

BOTULINUM TOXIN; HEPATOCYTE RESPONSIVE SERUM PHOSPHOPROTEIN; PHOSPHOPROTEIN; SNARE PROTEIN; SYNAPTOBREVIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN; SYNTAXIN 13; UNCLASSIFIED DRUG;

ARTICLE; BRAIN MEMBRANE; ENDOSOME; HELA CELL; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; LIGAND BINDING; MEMBRANE FUSION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION;

ANIMALS; ENDOCYTOSIS; ENDOSOMES; EUKARYOTIC CELLS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELLS; HUMANS; INTRACELLULAR MEMBRANES; MACROMOLECULAR SUBSTANCES; MEMBRANE FUSION; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; QA-SNARE PROTEINS; R-SNARE PROTEINS; RATS; SNARE PROTEINS; SUBCELLULAR FRACTIONS; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; VESICULAR TRANSPORT PROTEINS;

EID: 0038825173     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200302083     Document Type: Article

References (66)

1. Advani, R.J., H.R. Bae, J.B. Bock, D.S. Chao, Y.C. Doung, R. Prekeris, J.S. Yoo, and R.H. Scheller. 1998. Seven novel mammalian SNARE proteins localize to distinct membrane compartments. J. Biol. Chem. 273:10317-10324.
2. Antonin, W., C. Holroyd, R. Tikkanen, S. Honing, and R. Jahn. 2000. The R-SNARE endobrevin/VAMP-8 mediates homotypic fusion of early endosomes and late endosomes. Mol. Biol. Cell. 11:3289-3298.
3. Asao, H., Y. Sasaki, T. Arita, N. Tanaka, K. Endo, H. Kasai, T. Takeshita, Y. Endo, T. Fujita, and K. Sugamura. 1997. Hrs is associated with STAM, a signal-transducing adaptor molecule. Its suppressive effect on cytokine-induced cell growth. J. Biol. Chem. 272:32785-32791.
4. 2+-dependent exocytosis. J. Biol. Chem. 271:20227-20230.
5. Barbieri, M.A., R.L. Roberts, A. Gumusboga, H. Highfield, C. Alvarez-Dominguez, A. Wells, and P.D. Stahl. 2000. Epidermal growth factor and membrane trafficking. EGF receptor activation of endocytosis requires Rab5a. J. Cell Biol. 151:539-550.
6. Bean, A.J., R. Seifert, Y.A. Chen, R. Sacks, and R.H. Scheller. 1997. Hrs-2 is an ATPase implicated in calcium-regulated secretion. Nature. 385:826-829.
7. Bean, A.J., S. Davanger, M.F. Chou, B. Gerhardt, S. Tsujimoto, and Y. Chang. 2000. Hrs-2 regulates receptor-mediated endocytosis via interactions with Eps15. J. Biol. Chem. 275:15271-15278.
8. Bilodeau, P.S., J.L. Urbanowski, S.C. Winistorfer, and R.C. Piper. 2002. The Vps27p Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat. Cell Biol. 4:534-539.
9. Braell, W.A. 1987. Fusion between endocytic vesicles in a cell-free system. Proc. Natl. Acad. Sci. USA. 84:1137-1141.
10. Braell, W.A. 1992. Detection of endocytic vesicle fusion in vitro, using assay based on avidin-biotin association reaction. Methods Enzymol. 219:12-21.
11. Burke, P., K. Schooler, and H.S. Wiley. 2001. Regulation of epidermal growth factor receptor signaling by endocytosis and intracellular trafficking. Mol. Biol. Cell. 12:1897-1910.
12. Carpenter, G. 2000. The EGF receptor: a nexus for trafficking and signaling. Bioessays. 22:697-707.
13. Chen, D., and S.W. Whiteheart. 1999. Intracellular localization of SNAP-23 to endosomal compartments. Biochem. Biophys. Res. Commun. 255:340-346.
14. Chen, Y.A., and R.H. Scheller. 2001. SNARE-mediated membrane fusion. Nat. Rev. Mol. Cell Biol. 2:98-106.
15. 2+ and drives membrane fusion. Cell. 97:165-174.
16. Chin, L.S., M.C. Raynor, X. Wei, H.Q. Chen, and L. Li. 2001. Hrs interacts with sorting nexin 1 and regulates degradation of epidermal growth factor receptor. J. Biol. Chem. 276:7069-7078.
17. Diaz, R., L. Mayorga, and P. Stahl. 1988. In vitro fusion of endosomes following receptor-mediated endocytosis. J. Biol. Chem. 263:6093-6100.
18. Fasshauer, D., R.B. Sutton, A.T. Brunger, and R. Jahn. 1998. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q-and R-SNAREs. Proc. Natl. Acad. Sci. USA. 95:15781-15786.
19. Futter, C.E., A. Pearse, L.J. Hewlett, and C.R. Hopkins. 1996. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 132:1011-1023.
20. Futter, C.E., L.M. Collinson, J.M. Backer, and C.R. Hopkins. 2001. Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J. Cell Biol. 155:1251-1264.
21. Gorvel, J.P., P. Chavrier, M. Zerial, and J. Gruenberg. 1991. rab5 controls early endosome fusion in vitro. Cell. 64:915-925.
22. Gruenberg, J. 2001. The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2:721-730.
23. Gruenberg, J., and F.R. Maxfield. 1995. Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7:552-563.
24. Gruenberg, J., G. Griffiths, and K.E. Howell. 1989. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108:1301-1316.
25. Hayakawa, A., and N. Kitamura. 2000. Early endosomal localization of Hrs requires a sequence within the proline- and glutamine-rich region but not the FYVE finger. J. Biol. Chem. 275:29636-29642.
26. Honegger, A.M., A. Schmidt, A. Ullrich, and J. Schlessinger. 1990. Separate endocytic pathways of kinase-defective and -active EGF receptor mutants expressed in same cells. J. Cell Biol. 110:1541-1548.
27. Hopkins, C.R., K. Miller, and J.M. Beardmore. 1985. Receptor-mediated endocytosis of transferrin and epidermal growth factor receptors: a comparison of constitutive and ligand-induced uptake. J. Cell Sci. Suppl. 3:173-186.
28. Jahn, R., and T.C. Sudhof. 1999. Membrane fusion and exocytosis. Annu. Rev. Biochem. 68:863-911.
29. Katzmann D.J., M. Babst, and S.D. Emr. 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.
30. Komada, M., and N. Kitamura. 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.
31. Komada, M., and P. Soriano. 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.
32. Komada, M., R. Masaki, A. Yamamoto, and N. Kitamura. 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.
33. Lin, R.C., and R.H. Scheller. 2000. Mechanisms of synaptic vesicle exocytosis. Annu. Rev. Cell Dev. Biol. 16:19-49.
34. Lloyd, T.E., R. Atkinson, M.N. Wu, Y. Zhou, G. Pennetta, and H.J. Bellen. 2002. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell. 108:261-269.
35. McBride, H.M., V. Rybin, C. Murphy, A. Giner, R. Teasdale, and M. Zerial. 1999. Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell. 98:377-386.
36. Mullock, B.M., C.W. Smith, G. Ihrke, N.A. Bright, M. Lindsay, E.J. Parkinson, D.A. Brooks, R.G. Parton, D.E. James, J.P. Luzio, and R.C. Piper. 2000. Syntaxin 7 is localized to late endosome compartments, associates with Vamp 8, and is required for late endosome-lysosome fusion. Mol. Biol. Cell. 11:3137-3153.
37. Murai, S., and N. Kitamura. 2000. Involvement of Hrs binding protein in IgE receptor-triggered exocytosis in RBL-2H3 mast cells. Biochem. Biophys. Res. Commun. 277:752-756.
38. Muthuswamy, S.K., M. Gilman, and J.S. Brugge. 1999. Controlled dimerization of ErbB receptors provides evidence for differential signaling by homo- and heterodimers. Mol. Cell. Biol. 19:6845-6857.
39. Polo, S., S. Sigismund, M. Faretta, M. Guidi, M.R. Capua, G. Bossi, H. Chen, P. De Camilli, and P.P. Di Fiore. 2002. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature. 416:451-455.
40. Prekeris, R., J. Klumperman, Y.A. Chen, and R.H. Scheller. 1998. Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicular recycling endosomes. J. Cell Biol. 143:957-971.
41. Prekeris, R., B. Yang, V. Oorschot, J. Klumperman, and R.H. Scheller. 1999. Differential roles of syntaxin 7 and syntaxin 8 in endosomal trafficking. Mol. Biol. Cell. 10:3891-3908.
42. Raiborg, C., K.G. Bache, A. Mehlum, E. Stang, and H. Stenmark. 2001a. Hrs recruits clathrin to early endosomes. EMBO J. 20:5008-5021.
43. Raiborg, C., B. Bremnes, A. Mehlum, D.J. Gillooly, A. D'Arrigo, E. Stang, and H. Stenmark. 2001b. FYVE and coiled-coil domains determine the specific localisation of Hrs to early endosomes. J. Cell Sci. 114:2255-2263.
44. Raiborg, C., K.G. Bache, D.J. Gillooly, I.H. Madshus, E. Stang, and H. Stenmark. 2002. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat. Cell Biol. 4:394-398.
45. Raymond, C.K., I. Howald-Stevenson, C.A. Vater, and T.H. Stevens. 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.
46. Saito, Y., J. Haendeler, Y. Hojo, K. Yamamoto, and B.C. Berk. 2001. Receptor heterodimerization: essential mechanism for platelet-derived growth factor-induced epidermal growth factor receptor transactivation. Mol. Cell. Biol. 21:6387-6394.
47. Salzman, N.H., and F.R. Maxfield. 1988. Intracellular fusion of sequentially formed endocytic compartments. J. Cell Biol. 106:1083-1091.
48. Satin, B., N. Norais, J. Telford, R. Rappuoli, M. Murgia, C. Montecucco, and E. Papini. 1997. Effect of helicobacter pylori vacuolating toxin on maturation and extracellular release of procathepsin D and on epidermal growth factor degradation. J. Biol. Chem. 272:25022-25028.
49. Schlessinger, J. 2002. Ligand-induced, receptor-mediated dimerization and activation of EGF receptor. Cell. 110:669-672.
50. Shih, S.C., D.J. Katzmann, J.D. Schnell, M. Sutanto, S.D. Emr, and L. Hicke. 2002. Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat. Cell Biol. 4:389-393.
51. Sollnet, T., S.W. Whiteheart, M. Brunner, H. Erdjument-Bromage, S. Geromanos, P. Tempst, and J.E. Rothman. 1993. SNAP receptors implicated in vesicle targeting and fusion. Nature. 362:318-324.
52. Sutton, R.B., D. Fasshauer, R. Jahn, and A.T. Brunger. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature. 395:347-353.
53. Tao-Cheng, J.H., J. Du, and C.J. McBain. 2000. Snap-25 is polarized to axons and abundant along the axolemma: an immunogold study of intact neurons. J. Neurocytol. 29:67-77.
54. Trischler, M., W. Stoorvogel, and O. Ullrich. 1999. Biochemical analysis of distinct Rab5- and Rab11-positive endosomes along the transferrin pathway. J. Cell Sci. 112:4773-4783.
55. Tsujimoto, S., and A.J. Bean. 2000. Distinct protein domains are responsible for the interaction of Hrs-2 with SNAP-25. The role of Hrs-2 in 7 S complex formation. J. Biol. Chem. 275:2938-2942.
56. Tsujimoto, S., M. Pelto-Huikko, M. Aitola, B. Meister, E.O. Vik-Mo, S. Davanger, R.H. Scheller, and A.J. Bean. 1999. The cellular and developmental expression of Hrs-2 in rat. Eur. J. Neurosci. 11:3047-3063.
57. Ullrich, O., S. Reinsch, S. Urbe, M. Zerial, and R.G. Parton. 1996. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135:913-924.
58. Urbe, S., I.G. Mills, H. Stenmark, N. Kitamura, and M.J. Clague. 2000. Endosomal localization and receptor dynamics determine tyrosine phosphorylation of hepatocyte growth factor-regulated tyrosine kinase substrate. Mol. Cell. Biol. 20:7685-7692.
59. Wang, Z., L. Zhang, T.K. Yeung, and X. Chen. 1999. Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation. Mol. Biol. Cell. 10:1621-1636.
60. Ward, D.M., R. Ajioka, and J. Kaplan. 1989. Cohort movement of different ligands and receptors in the intracellular endocytic pathway of alveolar macrophages. J. Biol. Chem. 264:8164-8170.
61. Ward, D.M., D.P. Hackenyos, and J. Kaplan. 1990. Fusion of sequentially internalized vesicles in alveolar macrophages. J. Cell Biol. 110:1013-1022.
62. Ward, D.M., C.M. Perou, M. Lloyd, and J. Kaplan. 1995. "Synchronized" endocytosis and intracellular sorting in alveolar macrophages: the early sorting endosome is a transient organelle. J. Cell Biol. 129:1229-1240.
63. Ward, D.M., J.D. Leslie, and J. Kaplan. 1997. Homotypic lysosome fusion in macrophages: analysis using an in vitro assay. J. Cell Biol. 139:665-673.
64. Ward, D.M., J. Pevsner, M.A. Scullion, M. Vaughn, and J. Kaplan. 2000. Syntaxin 7 and VAMP-7 are soluble N-ethylmaleimide-sensitive factor attachment protein receptors required for late endosome-lysosome and homotypic lysosome fusion in alveolar macrophages. Mol. Biol. Cell. 11:2327-2333.
65. Weber, T., B.V. Zemelman, J.A. McNew, B. Westermann, M. Gmachl, F. Parlati, T.H. Sollner, and J.E. Rothman. 1998. SNAREpins: minimal machinery for membrane fusion. Cell. 92:759-772.
66. Zuk, P.A., and L.A. Elferink. 1999. Rab15 mediates an early endocytic event in Chinese hamster ovary cells. J. Biol. Chem. 274:22303-22312.