Depletion of TSG101 forms a mammalian 'class E' compartment: A multicisternal early endosome with multiple sorting defects

Journal of Cell Science

Volumn 118, Issue 14, 2005, Pages 3003-3017

  Doyette, Aurelie ^a   Russel, Matthew R G ^b   Hopkins, Colin R ^b   Woodman, Philip G ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Endocytosis; ESCRT; GFR; Multi vescicular body (MVB); Transferrin

Indexed keywords

CELL RECEPTOR; CLATHRIN; EPIDERMAL GROWTH FACTOR RECEPTOR; MEMBRANE PROTEIN; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL SELECTION; CELL SURFACE; CELL VACUOLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOSOME; FLOW KINETICS; FLUORESCENCE MICROSCOPY; GOLGI COMPLEX; HELA CELL; HUMAN; HUMAN CELL; LYSOSOME; MAMMAL; MEMBRANE TRANSPORT; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; TRANSPORT KINETICS;

ANIMALS; BLOTTING, WESTERN; CATHEPSIN D; DNA-BINDING PROTEINS; ENDOSOMES; HELA CELLS; HUMANS; MICE; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; RABBITS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, TRANSFERRIN; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; VACUOLES; VESICULAR TRANSPORT PROTEINS;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 23844481792     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02421     Document Type: Article

References (47)

1. Babst, M., Sato, T. K., Banta, L. M. and Emr, S. D. (1997). Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO J. 16, 1820-1831.
2. 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.
3. Bache, K. G., Brech, A., Mehlum, A. and Stenmark, H. (2003a). Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol. 162, 435-442.
4. Bache, K. G., Raiborg, C., Mehlum, A. and Stenmark, H. (2003b). STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278, 12513-12521.
5. Bilodeau, P. S., Winistorfer, S. C., Kearney, W. R., Robertson, A. D. and Piper, R. C. (2003). Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J. Cell Biol. 163, 237-243.
6. 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.
7. 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.
8. Diao, A., Rahman, D., Pappin, D. J. C., Lucocq, J. and Lowe, M. (2003). The coiled-coil membrane protein golgin-84 is a novel rab effector required for Golgi ribbon formation. J. Cell Biol. 160, 201-212.
9. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498.
10. 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, 623-624.
11. Futter, C. E., Pearse, A., Hewlett, L. J. and Hopkins, C. R. (1996). Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse with lysosomes. J. Cell Biol. 132, 1011-1023.
12. Futter, C. E., Collinson, L. M., Backer, J. M. and Hopkins, C. R. (2001). Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J. Cell Biol. 155, 1251-1108.
13. Garrus, J. E., von Schwedler, U. K., Pornillos, O. W., Morham, S. G., Zavitz, K. H., Wang, H. E., Wettstein, D. A., Stray, K. M., Côté, M., Rich, R. L. et al. (2001). Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107, 1-20.
14. Ghosh, P., Dahms, N. M. and Kornfeld, S. (2003). Mannose 6-phosphate receptors: new twists in the tale. Nat. Rev. Mol. Cell Biol. 4, 202-212.
15. Gillingham, A. K. and Munro, S. (2003). Long coiled-coil proteins and membrane traffic. Biochim. Biophys. Acta 1641, 71-85.
16. Gruenberg, J. and Maxfield, F. R. (1995). Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7, 552-563.
17. Haglund, K., Sigismund, S., Polo, S., Szymkiewicz, I., Fiore, P. P. D. and Dikic, I. (2003). Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5, 461-466.
18. Hopkins, C. R., Gibson, A., Shipman, M. and Miller, K. (1990). Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum. Nature 346, 335-340.
19. Jing, S., Spencer, T., Miller, K., Hopkins, C. and Trowbridge, I. (1990). Role of the human transferrin receptor cytoplasmic domain in endocytosis: localization of a specific signal sequence for internalization. J. Cell Biol. 110, 283-294.
20. Katzmann, D. J., Odorizzi, G. and Emr, S. D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Cell Mol. Biol. 3, 893-905.
21. Katzmann, D. J., Stefan, C. J., Babst, M. and Emr, S. D. (2003). Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162, 413-423.
22. Komada, M. and Kitamura, N. (1995). Growth factor-induced phosphorylation of Hrs, a novel 115 kDa protein with a structurally conserved putative zinc finger domain. Mol. Cell. Biol. 15, 6213-6221.
23. 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.
24. 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.
25. Martin-Serrano, J., Zang, T. and Bieniasz, P. D. (2001). HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7, 1313-1319.
26. Mellman, I. (1996). Endocytosis and molecular sorting. Ann. Rev. Cell Dev. Biol. 12, 575-625.
27. Nothwehr, S. F., Bryant, N. J. and Stevens, T. H. (1996). The newly identified yeast GRD genes are required for retention of late-Golgi membrane proteins. Mol. Cell. Biol. 16, 2700-2707.
28. Odorizzi, G., Babst, M. and Emr, S. D. (1998). Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95, 847-858.
29. Petiot, A., Faure, J., Stenmark, H. and Gruenberg, J. (2003). PI3P signaling regulates receptor sorting but not transport in the endosomal pathway. J. Cell Biol. 162, 971-979.
30. 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.
31. Polo, S., Sigismund, S., Faretta, M., Guidi, M., Capua, M. R., Bossi, G., Chen, H., Camilli, P. D. and Fiore, P. P. D. (2002). A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416, 451-455.
32. Pornillos, O., Higginson, D. S., Stray, K. M., Fisher, R. D., Garrus, J. E., Payne, M., He, G.-P., Wang, H. E., Morham, S. G. and Sundquist, W. I. (2003). HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. J. Cell Biol. 162, 425-434.
33. Raiborg, C., Gronvold Bache, K., Mehlum, A., Stang, E. and Stenmark, H. (2001). Hrs recruits clathrin to early endosomes. EMBO J. 20, 5008-5021.
34. Raiborg, C., Bache, K. G., Gillooly, D. J., Madshus, I. H., Stang, E. and Stenmark, H. (2002). Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat. Cell Biol. 4, 394-398.
35. 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.
36. Richardson, S. C. W., Winistorfer, S. C., Poupon, V., Luzio, J. P. and Piper, R. C. (2004). Mammalian late vacuole protein sorting orthologues participate in early endosomal fusion and interact with the cytoskeleton. Mol. Biol. Cell 15, 1197-1210.
37. Rieder, S. E., Banta, L. M., Köhrer, K., McCaffery, J. M. and Emr, S. D. (1996). Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. Mol. Biol. Cell 7, 985-999.
38. Sachse, M., Urbe, S., Oorschot, V., Strous, G. J. and Klumperman, J. (2002). Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol. Biol. Cell 13, 1313-1328.
39. Sachse, M., Strous, G. J. and Klumperman, J. (2004). ATPase-deficient hVPS4 impairs formation of internal endosomal vesicles and stabilizes bilayered clathrin coats on endosomal vacuoles. J. Cell Sci. 117, 1699-1708.
40. Seaman, M. N. J. (2004). Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165, 111-122.
41. Stinchcombe, J. C., Nomoto, H., Cutler, D. F. and Hopkins., C. R. (1995). Anterograde and retrograde traffic between the rough endoplasmic reticulum and the Golgi complex. J. Cell Biol. 131, 1387-1401.
42. Trowbridge, I. S., Collawn, J. F. and Hopkins, C. R. (1993). Signal-dependent membrane trafficking in the endocytic pathway. Ann. Rev. Cell Biol. 9, 129-161.
43. Urbe, S., Sachse, M., Row, P. E., Preisinger, C., Barr, F. A., Strous, G., Klumperman, J. and Clague, M. J. (2003). The UIM domain of Hrs couples receptor sorting to vesicle formation. J. Cell Sci. 116, 4169-4179.
44. van Delft, S., Govers, R., Strous, G. J., Verkleij, A. J. and van Bergen en Henegouwen, P. M. P. (1997). Epidermal growth factor induces ubiquitination of Eps15. J. Biol. Chem. 272, 14013-14016.
45. van Kerkhof, P., Alves dos Santos, C. M., Sachse, M., Klumperman, J., Bu, G. and Strous, G. J. (2001). Proteasome inhibitors block a late step it lysosomal transport of selected membrane but not soluble proteins. Mol. Biol. Cell 12, 2556-2566.
46. Gag. Proc. Natl. Acad. Sci. USA 98, 7724-7729.
47. Zahn, R., Stevenson, B., Schroder-Kohne, S., Zanolari, B., Riezman, H. and Munn, A. (2001). End13p/Vps4p is required for efficient transport from early to late endosomes in Saccharomyces cerevisiae. J. Cell Sci. 114, 1935-1947.