The transmembrane domain of acid trehalase mediates ubiquitin-independent multivesicular body pathway sorting

Molecular Biology of the Cell

Volumn 18, Issue 7, 2007, Pages 2511-2524

  Huang, Ju ^a   Reggiori, Fulvio ^a,b   Klionsky, Daniel J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; TREHALASE; TREHALOSE; UBIQUITIN;

ARTICLE; CATALYSIS; CELL SELECTION; ENZYME ACTIVITY; HYDROLYSIS; MEMBRANE STRUCTURE; MUTAGENESIS; MUTANT; NONHUMAN; NUTRIENT SUPPLY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STRESS; UBIQUITINATION;

CYTOSOL; GLYCOSYLATION; MEMBRANE PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSPORT VESICLES; UBIQUITIN; VACUOLES;

SACCHAROMYCES CEREVISIAE;

EID: 34347377736     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-11-0995     Document Type: Article

References (67)

1. Alizadeh, P., and Klionsky, D. J. (1996). Purification and biochemical characterization of the ATH1 gene product, vacuolar acid trehalase, from Saccharomyces cerevisiae. FEBS Lett. 391, 273-278.
2. Avaro, S., Belgareh-Touze, N., Sibella-Arguelles, C., Volland, C., and Haguenauer-Tsapis, R. (2002). Mutants defective in secretory/vacuolar pathways in the EUROFAN collection of yeast disruptants. Yeast 19, 351-371.
3. Babst, M. (2005). A protein's final ESCRT. Traffic 6, 2-9.
4. 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.
5. Bonifacino, J. S., Cosson, P., and Klausner, R. D. (1990). Colocalized transmembrane determinants for ER degradation and subunit assembly explain the intracellular fate of TCR chains. Cell 63, 503-513.
6. Chen, L., and Davis, N. G. (2002). Ubiquitin-independent entry into the yeast recycling pathway. Traffic 3, 110-123.
7. Cheong, H., Yorimitsu, T., Reggiori, F., Legakis, J. E., Wang, C.-W., and Klionsky, D. J. (2005). Atg17 regulates the magnitude of the autophagic response. Mol. Biol. Cell 16, 3438-3453.
8. Cowles, C. R., Snyder, W. B., Burd, C. G., and Emr, S. D. (1997). Novel Golgi to vacuole delivery pathway in yeast: identification of a sorting determinant and required transport component. EMBO J. 16, 2769-2782.
9. Crowe, L. M., Mouradian, R., Crowe, J. H., Jackson, S. A., and Womersley, C. (1984). Effects of carbohydrates on membrane stability at low water activities. Biochim. Biophys. Acta 769, 141-150.
10. 2 synthesis and Fab1-dependent protein trafficking to the multivesicular body. Curr. Biol. 12, 885-893.
11. Elbein, A. D. (1974). The metabolism of α-α-trehalose. Adv. Carbohydr. Chem. Biochem. 30, 227-256.
12. Elbein, A. D., Pan, Y. T., Pastuszak, I., and Carroll, D. (2003). New insights on trehalose: a multifunctional molecule. Glycobiology 13, 17R-27R.
13. Epple, U. D., Eskelinen, E.-L., and Thumm, M. (2003). Intravacuolar membrane lysis in Saccharomyces cerevisiae. Does vacuolar targeting of Cvt17/Aut5p affect its function? J. Biol. Chem. 278, 7810-7821.
14. Epple, U. D., Suriapranata, I., Eskelinen, E.-L., and Thumm, M. (2001). Aut5/Cvt17p, a putative lipase essential for disintegration of autophagic bodies inside the vacuole. J. Bacteriol. 183, 5942-5955.
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. Gruenberg, J., and Stenmark, H. (2004). The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 5, 317-323.
17. Haas, A. (1995). A quantitative assay to measure homotypic vacuole fusion in vitro. Methods Cell Sci. 17, 283-294.
18. Harris, S. D., and Cotter, D. A. (1987). Vacuolar (lysosomal) trehalase of Saccharomyces cerevisiae. Curr. Microbiol. 15, 247-249.
19. Harris, S. D., and Cotter, D. A. (1988). Transport of yeast vacuolar trehalase to the vacuole. Can. J. Microbiol. 34, 835-838.
20. Hettema, E. H., Valdez-Taubas, J., and Pelham, H.R.B. (2004). Bsd2 binds the ubiquitin ligase Rsp5 and mediates the ubiquitination of transmembrane proteins. EMBO J. 23, 1279-1288.
21. Hicke, L., and Riezman, H. (1996). Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84, 277-287.
22. Hislop, J. N., Marley, A., and Von Zastrow, M. (2004). Role of mammalian vacuolar protein-sorting proteins in endocytic trafficking of a non-ubiquitinated G protein-coupled receptor to lysosomes. J. Biol. Chem. 279, 22522-22531.
23. Hochstrasser, M., Ellison, M. J., Chau, V., and Varshavsky, A. (1991). The short-lived MATα2 transcriptional regulator is ubiquitinated in vivo. Proc. Natl. Acad. Sci. USA. 88, 4606-4610.
24. Hong, E., Davidson, A. R., and Kaiser, C. A. (1996). A pathway for targeting soluble misfolded proteins to the yeast vacuole. J. Cell Biol. 135, 623-633.
25. Horton, R. M., Cai, Z. L., Ho, S. N., and Pease, L. R. (1990). Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. BioTechniques 8, 528-535.
26. Hurley, J. H., and Emr, S. D. (2006). The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35, 277-298.
27. Hutchins, M. U., and Klionsky, D. J. (2001). Vacuolar localization of oligomeric α-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae. J. Biol. Chem. 276, 20491-20498.
28. Johnson, L. M., Bankaitis, V. A., and Emr, S. D. (1987). Distinct sequence determinants direct intracellular sorting and modification of a yeast vacuolar protease. Cell 48, 875-885.
29. Jules, M., Guillou, V., Francois, J., and Parrou, J. L. (2004). Two distinct pathways for trehalose assimilation in the yeast Saccharomyces cerevisiae. Appl. Environ. Microbiol. 70, 2771-2778.
30. 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.
31. Katzmann, D. J., Odorizzi, G., and Emr, S. D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3, 893-905.
32. Keller, F., Schellenberg, M., and Wiemken, A. (1982). Localization of trehalase in vacuoles and of trehalose in the cytosol of yeast (Saccharomyces cerevisiae). Arch Microbiol. 131, 298-301.
33. Klionsky, D. J., Cueva, R., and Yaver, D. S. (1992). Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J. Cell Biol. 119, 287-299.
34. Kopp, M., Muller, H., and Holzer, H. (1993). Molecular analysis of the neutral trehalase gene from Saccharomyces cerevisiae. J. Biol. Chem. 268, 4766-4774.
35. Kyte, J., and Doolittle, R. F. (1982). A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
36. Letourneur, F., and Cosson, P. (1998). Targeting to the endoplasmic reticulum in yeast cells by determinants present in transmembrane domains. J. Biol. Chem. 273, 33273-33278.
37. Lewis, M. J., Nichols, B. J., Prescianotto-Baschong, C., Riezman, H., and Pelham, H.R.B. (2000). Specific retrieval of the exocytic SNARE Snc1p from early yeast endosomes. Mol. Biol. Cell 11, 23-38.
38. Longtine, M. S., McKenzie, A., III, 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.
39. Marcusson, E. G., Horazdovsky, B. F., Cereghino, J. L., Gharakhanian, E., and Emr, S. D. (1994). The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell 77, 579-586.
40. Matsuura, A., Tsukada, M., Wada, Y., and Ohsumi, Y. (1997). Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 192, 245-250.
41. McNatt, M. W., McKittrick, I., West, M., and Odorizzi, G. (2007). Direct binding to Rsp5 mediates ubiquitin-independent sorting of Sna3 via the multivesicular body pathway. Mol. Biol. Cell 18, 697-706.
42. Mittenbuhler, K., and Holzer, H. (1988). Purification and characterization of acid trehalase from the yeast suc2 mutant. J. Biol. Chem. 263, 8537-8543.
43. Munro, S. (1995). An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J. 14, 4695-4704.
44. Nwaka, S., and Holzer, H. (1998). Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae. Prog. Nucleic Acid Res. Mol. Biol. 58, 197-237.
45. Nwaka, S., Mechler, B., and Holzer, H. (1996). Deletion of the ATH1 gene in Saccharomyces cerevisiae prevents growth on trehalose. FEBS Lett. 386, 235-238.
46. 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.
47. Oestreich, A. J., Aboian, M., Lee, J., Azmi, I., Payne, J., Issaka, R., Davies, B. A., and Katzmann, D. J. (2007). Characterization of multiple multivesicular body sorting determinants within Sna3, A role for the ubiquitin ligase Rsp5. Mol. Biol. Cell 18, 707-720.
48. Opheim, D. J. (1978). α-D-Mannosidase of Saccharomyces cerevisiae. Characterization and modulation of activity. Biochim. Biophys. Acta 524, 121-130.
49. Papa, F. R., and Hochstrasser, M. (1993). The yeast DOA4 gene encodes a deubiquitinating enzyme related to a product of the human tre-2 oncogene. Nature 366, 313-319.
50. Peng, J., Schwartz, D., Elias, J. E., Thoreen, C. C., Cheng, D., Marsischky, G., Roelofs, J., Finley, D., and Gygi, S. P. (2003). A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 21, 921-926.
51. 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.
52. 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.
53. Rayner, J. C., and Pelham, H.R.B. (1997). Transmembrane domain-dependent sorting of proteins to the ER and plasma membrane in yeast. EMBO J. 16, 1832-1841.
54. Reggiori, F., Black, M. W., and Pelham, H.R.B. (2000). Polar transmembrane domains target proteins to the interior of the yeast vacuole. Mol. Biol. Cell 11, 3737-3749.
55. Reggiori, F., and Pelham, H.R.B. (2001). Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J. 20, 5176-5186.
56. 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.
57. Rieder, S. E., and Emr, S. D. (2000). Current Protocols in Cell Biology. Somerset, NJ: John Wiley & Sons, 3.7.1-3.7.11.
58. Roth, A. F., and Davis, N. G. (1996). Ubiquitination of the yeast a-factor receptor. J. Cell Biol. 134, 661-674.
59. Russell, M.R.G., Nickerson, D. P., and Odorizzi, G. (2006). Molecular mechanisms of late endosome morphology, identity and sorting. Curr. Opin. Cell Biol. 18, 422-428.
60. Sato, M., Sato, K., and Nakano, A. (1996). Endoplasmic reticulum localization of Sec12p is achieved by two mechanisms: Rer1p-dependent retrieval that requires the transmembrane domain and Rer1p-independent retention that involves the cytoplasmic domain. J. Cell Biol. 134, 279-293.
61. Slagsvold, T., Pattni, K., Malerod, L., and Stenmark, H. (2006). Endosomal and non-endosomal functions of ESCRT proteins. Trends Cell Biol. 16, 317-326.
62. Teter, S. A., Eggerton, K. P., Scott, S. V., Kim, J., Fischer, A. M., and Klionsky, D. J. (2001). Degradation of lipid vesicles in the yeast vacuole requires function of Cvt17, a putative lipase. J. Biol. Chem. 276, 2083-2087.
63. Theos, A. C., Truschel, S. T., Tenza, D., Hurbain, I., Harper, D. C., Berson, J. F., Thomas, P. C., Raposo, G., and Marks, M. S. (2006). A lumenal domain-dependent pathway for sorting to intralumenal vesicles of multivesicular endosomes involved in organelle morphogenesis. Dev. Cell 10, 343-354.
64. Thevelein, J. M. (1984). Cyclic-AMP content and trehalase activation in vegetative cells and ascospores of yeast. Arch Microbiol. 138, 64-67.
65. Van Dijck, P., Colavizza, D., Smet, P., and Thevelein, J. M. (1995). Differential importance of trehalose in stress resistance in fermenting and nonfermenting Saccharomyces cerevisiae cells. Appl. Environ. Microbiol. 61, 109-115.
66. Vida, T. A., and Emr, S. D. (1995). A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128, 779-792.
67. Zahn, R., Stevenson, B. J., Schroder-Kohne, S., Zanolari, B., Riezman, H., and Munn, A. L. (2001). End13p/Vps4p is required for efficient transport from early to late endosomes in Saccharomyces cerevisiae. J. Cell Sci. 114, 1935-1947.