Bsd2 binds the ubiquitin ligase Rsp5 and mediates the ubiquitination of transmembrane proteins

EMBO Journal

Volumn 23, Issue 6, 2004, Pages 1279-1288

  Hettema, Ewald H ^a   Valdez Taubas, Javier ^a   Pelham, Hugh R B ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Bsd2; Multivesicular bodies; Rsp5; Transmembrane domain; Ubiquitin ligase

Indexed keywords

CARBOXYPEPTIDASE; CARBOXYPEPTIDASE S; LIGASE; MEMBRANE PROTEIN; PHOSPHATASE; PROTEIN BSD2; UBIQUITIN LIGASE RSP5; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME MECHANISM; ION TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; SEQUENCE HOMOLOGY; UBIQUITINATION;

AMINO ACID SEQUENCE; CARBOXYPEPTIDASES; GENE EXPRESSION REGULATION, FUNGAL; ION TRANSPORT; MEMBRANE PROTEINS; METALS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 1942439642     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600137     Document Type: Article

References (49)

1. Beck T, Schmidt A, Hall MN (1999) Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J Cell Biol 146: 1227-1238
2. Bilodeau PS, Urbanowski JL, Winistorfer SC, Piper RC (2002) The Vps27p Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat Cell Biol 4: 534-539
3. Black MW, Pelham HR (2000) A selective transport route from Golgi to late endosomes that requires the yeast GGA proteins. J Cell Biol 151: 587-600
4. Cristillo AD, Nie L, Macri MJ, Bierer BE (2003) Cloning and characterization of N4WBP5A, an inducible, cyclosporine-sensitive, Nedd4-binding protein in human T lymphocytes. J Biol Chem 278: 34587-34597
5. Dupre S, Haguenauer-Tsapis R (2001) Deubiquitination step in the endocytic pathway of yeast plasma membrane proteins: crucial role of Doa4p ubiquitin isopeptidase. Mol Cell Biol 21: 4482-4494
6. Ellgaard L, Helenius A (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4: 181-191
7. Fayadat L, Kopito RR (2003) Recognition of a single transmembrane degron by sequential quality control checkpoints. Mol Biol Cell 14: 1268-1278
8. Futter CE, Pearse A, Hewlett LJ, Hopkins CR (1996) Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol 132: 1011-1023
9. Galan JM, Moreau V, Andre B, Volland C, Haguenauer-Tsapis R (1996) Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J Biol Chem 271: 10946-10952
10. Gietz RD, Sugino A (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74: 527-534
11. Gitan RS, Eide DJ (2000) Zinc-regulated ubiquitin conjugation signals endocytosis of the yeast ZRT1 zinc transporter. Biochem J 346: 329-336
12. Harty RN, Brown ME, Wang G, Huibregtse J, Hayes FP (2000) A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding. Proc Natl Acad Sci USA 97: 13871-13876
13. Harvey KF, Shearwin-Whyatt LM, Fotia A, Parton RG, Kumar S (2002) N4WBP5, a potential target for ubiquitination by the Nedd4 family of proteins, is a novel Golgi-associated protein. J Biol Chem 277: 9307-9317
14. Hein C, Springael JY, Volland C, Haguenauer-Tsapis R, Andre B (1995) NPl1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol Microbiol 18: 77-87
15. Heinemeyer W, Kleinschmidt JA, Saidowsky J, Escher C, Wolf DH (1991) Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J 10: 555-562
16. Helliwell SB, Losko S, Kaiser CA (2001) Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease. J Cell Biol 153: 649-662
17. Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67: 425-479
18. Hicke L (1999) Gettin' down with ubiquitin: turning off cell-surface receptors, transporters and channels. Trends Cell Biol 9: 107-112
19. Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19: 141-172
20. Hicke L, Riezman H (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84: 277-287
21. Hoshikawa C, Shichiri M, Nakamori S, Takagi H (2003) A non-conserved 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
22. Jarosch E, Lenk U, Sommer T (2003) Endoplasmic reticulum-associated protein degradation. Int Rev Cytol 223: 39-81
23. Katzmann DJ, Babst M, Emr SD (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
24. Katzmann DJ, Odorizzi G, Emr SD (2002) Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol 3: 893-905
25. Katzmann DJ, Sarkar S, Chu T, Audhya A, Emr SD (2004) Multivesicular Body Sorting: Ubiquitin Ligase Rsp5 is Required for the Modification and Sorting of Carboxypeptidase S. Mol Biol Cell 15: 468-480
26. Katzmann DJ, Stefan CJ, Babst M, Emr SD (2003) Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J Cell Biol 162: 413-423
27. Kolling R, Hollenberg CP (1994) The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J 13: 3261-3271
28. Lewis MJ, Nichols BJ, Prescianotto-Baschong C, Riezman H, Pelham HR (2000) Specific retrieval of the exocytic SNARE Snc1p from early yeast endosomes. Mol Biol Cell 11: 23-38
29. Liu XF, Culotta VC (1999a) Mutational analysis of Saccharomyces cerevisiae Smf1p, a member of the Nramp family of metal transporters. J Mol Biol 289: 885-891
30. Liu XF, Culotta VC (1999b) Post-translation control of Nramp metal transport in yeast. Role of metal ions and the BSD2 gene. J Biol Chem 274: 4863-4868
31. Liu XF, Supek F, Nelson N, Culotta VC (1997) Negative control of heavy metal uptake by the Saccharomyces cerevisiae BSD2 gene. J Biol Chem 272: 11763-11769
32. Luo W, Chang A (1997) Novel genes involved in endosomal traffic in yeast revealed by suppression of a targeting-defective plasma membrane ATPase mutant. J Cell Biol 138: 731-746
33. Odorizzi G, Babst M, Emr SD (1998) Fab1p Ptdlns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95: 847-858
34. Rayner JC, Pelham HR (1997) Transmembrane domain-dependent sorting of proteins to the ER and plasma membrane in yeast. EMBO J 16: 1832-1841
35. Reggiori F, Black MW, Pelham HR (2000) Polar transmembrane domains target proteins to the interior of the yeast vacuole. Mol Biol Cell 11: 3737-3749
36. Reggiori F, Pelham HR (2001) Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J 20: 5176-5186
37. Reggiori F, Pelham HR (2002) A transmembrane ubiquitin ligase required to sort membrane proteins into multivesicular bodies. Nat Cell Biol 4: 117-123
38. Sato K, Sato M, Nakano A (1997) Rer1p as common machinery for the endoplasmic reticulum localization of membrane proteins. Proc Natl Acad Sci USA 94: 9693-9698
39. Sato K, Sato M, Nakano A (2001) Rer1p, a retrieval receptor for endoplasmic reticulum membrane proteins, is dynamically localized to the Golgi apparatus by coatomer. J Cell Biol 152: 935-944
40. Sato K, Sato M, Nakano A (2003) Rer1p, a retrieval receptor for ER membrane proteins, recognizes transmembrane domains in multiple modes. Mol Biol Cell 14: 3605-3616
41. Shiba Y, Katoh Y, Shiba T, Yoshino K, Takatsu H, Kobayashi H, Shin HW, Wakatsuki S, Nakayama K (2004) GAT (GGA and Tom1) domain responsible for ubiquitin binding and ubiquitination. J Biol Chem, In press
42. Shih SC, Sloper-Mould KE, Hicke L (2000) Monoubiquitin carries a novel internalization signal that is appended to activated receptors. EMBO J 19: 187-198
43. Soetens O, De Craene JO, 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
44. Sudol M (1996) Structure and function of the WW domain. Prog Biophys Mol Biol 65: 113-132
45. Trombetta ES, Parodi AJ (2003) Quality control and protein folding in the secretory pathway. Annu Rev Cell Dev Biol 19: 649-676
46. Urbanowski JL, Piper RC (2001) Ubiquitin sorts proteins into the intralumenal degradative compartment of the late-endosome/ vacuole. Traffic 2: 622-630
47. Wilson MH, Highfield HA, Limbird LE (2001) The role of a conserved inter-transmembrane domain interface in regulating alpha(2a)-adrenergic receptor conformational stability and cell-surface turnover. Mol Pharmacol 59: 929-938
48. Yashiroda H, Oguchi T, Yasuda Y, Toh EA, Kikuchi Y (1996) Bul1, a new protein that binds to the Rsp5 ubiquitin ligase in Saccharomyces cerevisiae. Mol Cell Biol 16: 3255-3263
49. Zaliauskiene L, Kang S, Brouillette CG, Lebowitz J, Arani RB, Collawn JF (2000) Down-regulation of cell surface receptors is modulated by polar residues within the transmembrane domain. Mol Biol Cell 11: 2643-2655