Hse1, a component of the yeast Hrs-STAM ubiquitin-sorting complex, associates with ubiquitin peptidases and a ligase to control sorting efficiency into multivesicular bodies

Molecular Biology of the Cell

Volumn 18, Issue 1, 2007, Pages 324-335

  Ren, Jihui ^a   Kee, Younghoon ^b   Huibregtse, Jon M ^b   Piper, Robert C ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; FUNGAL PROTEIN; MEMBRANE PROTEIN; PEPTIDASE; PROTEIN HEPATOCYTE RECEPTOR SUBSTRATE; PROTEIN HSE1; PROTEIN HUA1; PROTEIN RSP5; PROTEIN RUP1; PROTEIN SH3; PROTEIN SIGNAL TRANSDUCING ADAPTOR MOLECULE; PROTEIN UBP2; PROTEIN UBP7; PROTEIN VPS27; SIGNAL TRANSDUCING ADAPTOR PROTEIN; UBIQUITIN; UBIQUITIN PEPTIDASE; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL VACUOLE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM VESICLE; ENDOSOME; ENZYME ACTIVITY; GENE DELETION; GENE DISRUPTION; LYSOSOME; MULTIVESICULAR BODY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; UBIQUITINATION;

ENDOPEPTIDASES; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SRC HOMOLOGY DOMAINS; TRANSCRIPTION FACTORS; TRANSPORT VESICLES; UBIQUITIN; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 33846137688     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-06-0557     Document Type: Article

References (79)

1. Alwan, H. A., van Zoelen, E. J., and van Leeuwen, J. E. (2003). Ligand-induced lysosomal epidermal growth factor receptor (EGFR) degradation is preceded by proteasome-dependent EGFR de-ubiquitination. J. Biol. Chem, 278, 35781-35790.
2. Andreasson, C., Neve, E. P., and Ljungdahl, P. O. (2004). Four permeases import proline and the toxic proline analogue azetidine-2-carboxylate into yeast. Yeast 21, 193-199.
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 20, 3365-3380.
4. Bache, K. G., Raiborg, C., Mehlum, A., and Stenmark, H. (2003). STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278, 12513-12521.
5. Beck, T., Schmidt, A., and Hall, M. N. (1999). Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J. Cell Biol. 146, 1227-1238.
6. 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.
7. Bilodeau, P. S., Winistorfer, S. C., Allaman, M. M., Surendhran, K., Kearney, W. R., Robertson, A. D., and Piper, R. C. (2004). The GAT domains of clathrin-associated GGA proteins have two ubiquitin binding motifs. J. Biol. Chem. 279, 54808-54816.
8. Bilodeau, P. S., Winistorfer, S. C., Kearney, W. R., Robertson, A. D., and Piper, R. C. (2003). Vps27-Hse1 and ESCRT-1 complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J. Cell Biol. 163, 237-243.
9. Blondel, M. O., Morvan, J., Dupre, S., Urban-Grimal, D., Haguenauer-Tsapis, R., and Volland, C. (2004). Direct sorting of the yeast uracil permease to the endosomal system is controlled by uracil binding and Rsp5p-dependent ubiquitylation. Mol. Biol. Cell 15, 883-895.
10. Borodovsky, A., Kessler, B. M., Casagrande, R., Overkleeft, H. S., Wilkinson, K. D., and Ploegh, H. L. (2001). A novel active site-directed probe specific for deubiquitylating enzymes reveals proteasome association of USP14. EMBO J. 20, 5187-5196.
11. Borodovsky, A., Ovaa, H., Kolli, N., Gan-Erdene, T., Wilkinson, K. D., Ploegh, H. L., and Kessler, B. M. (2002). Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem. Biol. 9, 1149-1159.
12. Bowers, K., Lottridge, J., Helliwell, S. B., Goldthwaite, L. M., Luzio, J. P., and Stevens, T. H. (2004). Protein-protein interactions of ESCRT complexes in the yeast Saccharomyces cerevisiae. Traffic 5, 194-210.
13. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P., and Boeke, J. D. (1998). Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132.
14. Bugnicourt, A., Froissard, M., Sereti, K., Ulrich, H. D., Haguenauer-Tsapis, R., and Galan, J. M. (2004). Antagonistic roles of ESCRT and Vps class C/HOPS complexes in the recycling of yeast membrane proteins. Mol. Biol. Cell 15, 4203-4214.
15. Burri, L., Vascotto, K., Fredersdorf, S., Tiedt, R., Hall, M. N., and Lithgow, T. (2004). Zim17, a novel zinc finger protein essential for protein import into mitochondria. J. Biol. Chem. 279, 50243-50249.
16. Cooper, A. A., and Stevens, T. H. (1996). Vps10p cycles between the late-Golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolases. J. Cell Biol. 133, 529-541.
17. Davis, N. G., Horecka, J. L., and Sprague, G. F., Jr. (1993). Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors. J. Cell Biol. 122, 53-65.
18. de Melker, A. A., van der Horst, G., Calafat, J., Jansen, H., and Borst, J. (2001). c-Cbl ubiquitinates the EGF receptor at the plasma membrane and remains receptor associated throughout the endocytic route. J. Cell Sci. 114, 2167-2178.
19. Dunn, R., and Hicke, L. (2001). Domains of the Rsp5 ubiquitin-protein ligase required for receptor-mediated and fluid-phase endocytosis. Mol. Biol. Cell 12, 421-435.
20. Dunn, R., Klos, D. A., Adler, A. S., and Hicke, L. (2004). The C2 domain of the Rsp5 ubiquitin ligase binds membrane phosphoinositides and directs ubiquitination of endosomal cargo. J. Cell Biol. 165, 135-144.
21. Gajewska, B., Kaminska, J., Jesionowska, A., Martin, N. C., Hopper, A. K., and Zoladek, T. (2001). WW domains of Rsp5p define different functions: determination of roles in fluid phase and uracil permease endocytosis in Saccharomyces cerevisiae. Genetics 157, 91-101.
22. Ghaemmaghami, S., Huh, W. K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K., and Weissman, J. S. (2003). Global analysis of protein expression in yeast. Nature 425, 737-741.
23. Giaever, G., et al. (2002). Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391.
24. Gruenberg, J., and Stenmark, H. (2004). The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 5, 317-323.
25. Gueldener, U., Heinisch, J., Koehler, G. J., Voss, D., and Hegemann, J. H. (2002). A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res. 30, e23.
26. 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.
27. Hettema, E. H., Valdez-Taubas, J., and Pelham, H. R. (2004). Bsd2 binds the ubiquitin ligase Rsp5 and mediates the ubiquitination of transmembrane proteins. EMBO J. 23, 1279-1288.
28. Hicke, L., and Dunn, R. (2003). Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141-172.
29. Hoeller, D., et al. (2006). Regulation of ubiquitin-binding proteins by monoubiquitination. Nat. Cell Biol. 8, 163-169.
30. Hoshikawa, C., Shichiri, M., Nakamori, S., and Takagi, H. (2003). A nonconserved Ala401 in the yeast Rsp5 ubiquitin ligase is involved in degradation of Gap1 permease and stress-induced abnormal proteins. Proc. Natl. Acad. Sci. USA 100, 11505-11510.
31. Ito, T., Chiba, T., Ozawa, R., Yoshida, M., Hattori, M., and Sakaki, Y. (2001). A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA 98, 4569-4574.
32. Kaelin, W. G., Jr., et al. (1992). Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell 70, 351-364.
33. 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.
34. 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-1. Cell 106, 145-155.
35. Katzmann, D. J., Odorizzi, G., and Emr, S. D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3, 893-905.
36. Katzmann, D. J., Sarkar, S., Chu, T., Audhya, A., and Emr, S. D. (2004). Multivesicular body sorting: ubiquitin ligase Rsp5 is required for the modification and sorting of carboxypeptidase S. Mol. Biol. Cell 15, 468-480.
37. Kee, Y., Lyon, N., and Huibregtse, J. M. (2005). The Rsp5 ubiquitin ligase is coupled to and antagonized by the Ubp2 deubiquitinating enzyme. EMBO J. 24, 2414-2424.
38. Kee, Y., Munoz, W., Lyon, N., and Huibregtse, J. M. (2006). The Ubp2 deubiquitinating enzyme modulates Rsp5-dependent K63-linked polyubiquitin conjugates in Saccharomyces cerevisiae. J. Biol. Chem. (in press).
39. Komada, M., and Kitamura, N. (2005). The Hrs/STAM complex in the down-regulation of receptor tyrosine kinases. J. Biochem. (Tokyo) 137, 1-8.
40. 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.
41. Levkowitz, G., Waterman, H., Zamir, E., Kam, Z., Oved, S., Langdon, W. Y., Beguinot, L., Geiger, B., and Yarden, Y. (1998). c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 12, 3663-3674.
42. Lill, N. L., Douillard, P., Awwad, R. A., Ola, S., Lupher, M. L., Jr., Miyake, S., Meissner-Lula, N., Hsu, V. W., and Band, H. (2000). The evolutionary conserved N-terminal region of Cb1 is sufficient to enhance down-regulation of the epidermal growth factor receptor. J. Biol. Chem. 275, 367-377.
43. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N, G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
44. Longva, K. E., Blystad, F. D., Slang, E., Larsen. A, M., Johannessen, L. E., and Madshus, I. H. (2002). Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies. J. Cell Biol. 156, 843-854.
45. Marchese, A., Raiborg, C., Santini, F., Keen, J. H., Stenmark, H., and Benovic, J. L. (2003). The E3 ubiquitin ligase A1P4 mediates ubiquitination and sorting of the G protein-coupled receptor CXCR4. Dev. Cell 5, 709-722.
46. McCullough, J., Clague, M. J., and Urbe, S. (2004). AMSH is an endosome-associated ubiquitin isopeptidase. J. Cell Biol. 166, 487-492.
47. McCullough, J., Row, P. E., Lorenzo, O., Doherty, M., Beynon, R., Clague, M. J., and Urbe, S. (2006). Activation of the endnsome-associated ubiquitin isopeptidase AMSH by STAM, a component of the multivesicular body-sorting machinery. Curr. Biol. 16, 160-165.
48. Millard, S. M., and Wood, S. A. (2006). Riding the DUBway: regulation of protein trafficking by deubiquitylating enzymes. J. Cell Biol. 173, 463-468.
49. Mizuno, E., Iura, T., Mukai, A., Yoshimori, T., Kitamura, N., and Komada, M. (2005). Regulation of epidermal growth factor receptor down-regulation by UBPY-mediated deubiquitination at endosomes. Mol. Biol. Cell 16, 5163-5174.
50. Mizuno, E., Kobayashi, K., Yamamoto, A., Kitamura, N., and Komada, M. (2006). A deubiquitinating enzyme UBPY regulates the level of protein ubiquitination on endosomes. Traffic 7, 1017-1031.
51. Nikko, E., Marini, A. M., and Andre, B. (2003). Permease recycling and ubiquitination status reveal a particular role for Bro1 in the multivesicular body pathway. J. Biol. Chem. 278, 50732-50743.
52. Odorizzi, G., Babst, M., and Emr, S. D. (1998). Fab1p Ptdlns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95, 847-858.
53. Pizzirusso, M., and Chang, A. (2004). Ubiquitin-mediated targeting of a mutant plasma membrane ATPase, Pma1-7, to the endosomal/vacuolar system in yeast. Mol. Biol. Cell 15, 2401-2409.
54. 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.
55. Raiborg, C., Rusten, T. E., and Stenmark, H. (2003). Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15, 446-455.
56. Raths, S., Rohrer, J., Crausaz, F., and Riezman, H. (1993). end3 and end4, two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces-cerevisiae. J. Cell Biol. 120, 55-65.
57. 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.
58. Reggiori, F., and Pelham, H. R. (2002). A transmembrane ubiquitin ligase required to sort membrane proteins into multivesicular bodies. Nat. Cell Biol. 4, 117-123.
59. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Seraphin, B. (1999). A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17, 1030-1032.
60. Roberg, K. J., Rowluy, N., and Kaiser, C. A. (1997). Physiological regulation of membrane protein sorting late in the secretory pathway of Saccharomyces cerevisiae. J. Cell Biol. 137, 1469-1482.
61. Roth, A. F., and Davis, N. G. (2000). Ubiquitination of the PEST-like endocytosis signal of the yeast a-factor receptor. J. Biol. Chem. 275, 8143-8153.
62. Row, P. E., Clague, M. J., and Urbe, S. (2005). Growth factors induce differential phosphorylation profiles of the Hrs-STAM complex: a common node in signalling networks with signal-specific properties. Biochem. J. 389, 629-636.
63. Row, P. E., Prior, I. A., McCullough, J., Clague, M. J., and Urbe, S. (2006). The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. J. Biol. Chem. 281, 12618-12624.
64. Scott, P. M., Bilodeau, P. S., Zhdankina, O., Winistorfer, S. C., Hauglund, M. J., Allaman, M. M., Kearney, W. R., Robertson, A. D., Boman, A. L., and Piper, R. C. (2004). GGA proteins bind ubiquitin to facilitate sorting at the trans-Golgi network. Nat. Cell Biol. 6, 252-259.
65. Shcherbik, N., Kee, Y., Lyon, N., Huibregtse, J. M., and Haines, D. S. (2004). A single PXY motif located within the carboxyl terminus of Spt23p and Mga2p mediates a physical and functional interaction with ubiquitin ligase Rsp5p. J. Biol. Chem, 279, 53892-53898.
66. Smith, D. B., Rubira, M. R., Simpson, R. J., Davern, K. M., Tiu, W. U., Board, P. G., and Mitchell, G. F. (1988). Expression of an enzymatically active parasite molecule in Escherichia coli: Schistosoma japonicum glutathione S-transferase. Mol. Biochem. Parasitol. 27, 249-256.
67. Soetens, O., De Craene, J. O., and Andre, B. (2001). Ubiquitin is required for sorting to the vacuole of the yeast general amino acid permease, Gap1. J. Biol. Chem. 276, 43949-43957.
68. Staub, O., and Rotin, D. (2006). Role of ubiquitylation in cellular membrane transport. Physiol. Rev. 86, 669-707.
69. Stimpson, H. E., Lewis, M. J., and Pelham, H. R. (2006). Transferrin receptor-like proteins control the degradation of a yeast metal transporter. EMBO J. 25, 662-672.
70. Tanaka, N., Kaneko, K., Asao, H., Kasai, H., Endo, Y., Fujita, T., Takeshita, T., and Sugamura, K. (1999). Possible involvement of a novel STAM-associated molecule "AMSH" in intracellular signal transduction mediated by cytokines. J. Biol. Chem. 274, 19129-19135.
71. Totig, A. H., et al. (2002). A combined experimental and computational strategy to define protein interaction networks for peptide recognition modules. Science 295, 321-324.
72. Urbanowski, J. L., and Piper, R. C. (1999). The iron transporter Fth1p forms a complex with the Fet5 iron oxidase and resides on the vacuolar membrane. J. Biol. Chem. 274, 38061-38070.
73. Urbanowski, J. L., and Piper, R. C. (2001). Ubiquitin sorts proteins into the intralumenal degradative compartment of the late-endosome/vacuole. Traffic 2, 622-630.
74. Urbe, S. (2005). Ubiquitin and endocytic protein sorting. Essays Biochem. 41, 81-98.
75. 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. 27, 3564-3575.
76. Wang, G., Yang, J., and Huibregtse, J. M. (1999). Functional domains of the Rsp5 ubiquitin-protein ligase. Mol. Cell. Biol. 19, 342-352.
77. Yashiroda, H., Kaida, D., Toh-e, A., and Kikuchi, Y. (1998). The PY-motif of Bul1 protein is essential for growth of Saccharomyces cerevisiae under various stress conditions. Gene 225, 39-46.
78. Yu, H., Chen, J. K., Feng, S., Dalgarno, D. C., Brauer, A. W., and Schreiber, S. L. (1994). Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76, 933-945.
79. Zheng, B., Lavoie, C., Tang, T. D., Ma, P., Meerloo, T., Beas, A., and Farquhar, M. G. (2004). Regulation of epidermal growth factor receptor degradation by heterotrimeric Galphas protein. Mol. Biol. Cell 15, 5538-5550.