Localization of the Rsp5p Ubiquitin-Protein Ligase at Multiple Sites within the Endocytic Pathway

REFERENCES

• Americk, A. Y., J. Nowak, S. Swaminathan, and M. Hochstrasser. 2000. The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol. Biol. Cell 11:3365–3380.
   PubMedGoogle Scholar
• Babst, M., B. Wendland, E. J. Estepa, and S. D. Emr. 1998. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosomal function. EMBO J. 17:2982–2993.
   PubMed Web of Science ®Google Scholar
• Beaudenon, S. L., M. R. Huacani, G. Wang, D. P. McDonnell, and J. M. Huibregtse. 1999. Rsp5 ubiquitin-protein ligase mediates DNA damage-induced degradation of the large subunit of RNA polymerase II in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:6972–6979.
   PubMed Web of Science ®Google Scholar
• Becherer, K. A., S. E. Rieder, S. D. Emr, and E. W. Jones. 1996. Novel syntaxin homologue, Pep12p, required for the sorting of lumenal hydrolases to the lysosome-like vacuole in yeast. Mol. Biol. Cell 7:579–594.
   PubMedGoogle Scholar
• Beck, T., A. Schmidt, and M. N. Hall. 1999. Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J. Cell Biol. 146:1227–1238.
   PubMed Web of Science ®Google Scholar
• Cadavid, A. L., A. Ginzel, and J. A. Fischer. 2000. The function of the Drosophila Fat facets deubiquitinating enzyme in limiting photoreceptor cell number is intimately associated with endocytosis. Development 127:1727–1736.
   PubMed Web of Science ®Google Scholar
• Chen, H. I., and M. Sudol. 1995. The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc. Natl. Acad. Sci. USA 92:7819–7823.
   PubMedGoogle Scholar
• Ecker, D. J., M. Ishaq Khan, J. Marsh, T. R. Butt, and S. T. Crooke. 1987. Chemical synthesis and expression of a cassette adapted ubiquitin gene. J. Biol. Chem. 262:3524–3527.
   PubMed Web of Science ®Google Scholar
• Egner, R., and K. Kuchler. 1996. The yeast multidrug transporter Pdr5 of the plasma membrane is ubiquitinated prior to endocytosis and degradation in the vacuole. FEBS Lett. 378:177–181.
   PubMedGoogle Scholar
• Erdeniz, N., and R. Rothstein. 2000. Rsp5, a ubiquitin-protein ligase, is involved in degradation of the single-stranded DNA binding protein Rfa1 in Saccharomyces cerevisiae. Mol. Cell. Biol. 20:224–232.
   PubMedGoogle Scholar
• Esnault, Y., D. Feldheim, M. O. Blondel, R. Schekman, and F. Kepes. 1993. The yeast SSS1 gene is essential for secretory protein translocation and encodes a conserved protein of the endoplasmic reticulum. EMBO J. 12:4083–4093.
   PubMed Web of Science ®Google Scholar
• Fisk, H. A., and M. P. Yaffe. 1999. A role for ubiquitination in mitochondrial inheritance in Saccharomyces cerevisiae. J. Cell Biol. 145:1199–1208.
   PubMed Web of Science ®Google Scholar
• Freedman, D. A., and A. J. Levine. 1998. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol. Cell. Biol. 18:7288–7293.
   PubMed Web of Science ®Google Scholar
• Galan, J., and R. Haguenauer-Tsapis. 1997. Ubiquitin lys63 is involved in ubiquitination of a yeast plasma membrane protein. EMBO J. 16:5847–5854.
   PubMedGoogle Scholar
• Galan, J. M., V. Moreau, B. Andre, C. Volland, and R. Haguenauer-Tsapis. 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.
   PubMed Web of Science ®Google Scholar
• Gerrard, S. R., N. J. Bryant, and T. H. Stevens. 2000. VPS21 controls entry of endocytosed and biosynthetic proteins into the yeast prevacuolar compartment. Mol. Biol. Cell 11:613–626.
   PubMed Web of Science ®Google Scholar
• Guthrie, C., and R. G. Fink. 1991. Guide to yeast genetics and molecular biology 194, Academic Press, Inc., San Diego, Calif
   Google Scholar
• Hein, C., and B. Andre. 1997. A C-terminal di-leucine motif and nearby sequences are required for NH4(+)-induced inactivation and degradation of the general amino acid permease, Gap1p, of Saccharomyces cerevisiae. Mol. Microbiol. 24:607–616.
   PubMedGoogle Scholar
• Hein, C., J. Y. Springael, C. Volland, R. Haguenauer-Tsapis, and B. Andre. 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.
   PubMed Web of Science ®Google Scholar
• Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425–479.
   PubMed Web of Science ®Google Scholar
• Hicke, L.. 1999. Gettin' down with ubiquitin: turning off cell-surface receptors, transporters and channels. Trends Cell Biol. 9:107–112.
   PubMed Web of Science ®Google Scholar
• Hicke, L.. 1997. Ubiquitin-dependent internalization and down-regulation of plasma membrane proteins. FASEB J. 11:1215–1226.
   PubMed Web of Science ®Google Scholar
• Hicke, L., and H. Riezman. 1996. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84:277–287.
   PubMed Web of Science ®Google Scholar
• Hicke, L., B. Zanolari, and H. Riezman. 1998. Cytoplasmic tail phosphorylation of the alpha-factor receptor is required for its ubiquitination and internalization. J. Cell Biol. 141:349–358.
   PubMed Web of Science ®Google Scholar
• Hochstrasser, M.. 1996. Ubiquitin-dependent protein degradation. Annu. Rev. Genet. 30:405–439.
   PubMed Web of Science ®Google Scholar
• Hoppe, T., K. Matuschewski, M. Rape, S. Schlenker, H. D. Ulrich, and S. Jentsch. 2000. Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102:577–586.
   PubMed Web of Science ®Google Scholar
• Horak, J., and D. H. Wolf. 1997. Catabolite inactivation of the galactose transporter in the yeast Saccharomyces cerevisiae: ubiquitination, endocytosis, and degradation in the vacuole. J. Bacteriol. 179:1541–1549.
   PubMedGoogle Scholar
• Huang, L., E. Kinnucan, G. Wang, S. Beaudenon, P. M. Howley, J. M. Huibregtse, and N. P. Pavletich. 1999. Structure of an E6AP-UbcH7 complex: insights into ubiquitination by the E2–E3 enzyme cascade. Science 286:1321–1326.
   PubMed Web of Science ®Google Scholar
• Huibregtse, J. M., M. Scheffner, S. Beaudenon, and P. M. Howley. 1995. A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA 92:2563–2567.
   PubMed Web of Science ®Google Scholar
• Huibregtse, J. M., M. Scheffner, and P. M. Howley. 1993. Localization of the E6-AP regions that direct human papillomavirus E6 binding, association with p53, and ubiquitination of associated proteins. Mol. Cell. Biol. 13:4918–4927.
   PubMed Web of Science ®Google Scholar
• Huibregtse, J. M., J. C. Yang, and S. L. Beaudenon. 1997. The large subunit of RNA polymerase II is a substrate of the Rsp5 ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA 94:3656–3661.
   PubMedGoogle Scholar
• Jenness, D. D., Y. Li, C. Tipper, and P. Spatrick. 1997. Elimination of defective α-factor pheromone receptors. Mol. Cell. Biol. 17:6236–6245.
   PubMedGoogle Scholar
• Jund, R., E. Weber, and M. R. Chevallier. 1988. Primary structure of the uracil transport protein of Saccharomyces cerevisiae. Eur. J. Biochem. 171:417–424.
   PubMedGoogle Scholar
• Kolling, R., and C. P. Hollenberg. 1994. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 13:3261–3271.
   PubMedGoogle Scholar
• Krampe, S., O. Stamm, C. P. Hollenberg, and E. Boles. 1998. Catabolite inactivation of the high-affinity hexose transporters Hxt6 and Hxt7 of Saccharomyces cerevisiae occurs in the vacuole after internalization by endocytosis. FEBS Lett. 441:343–347.
   PubMed Web of Science ®Google Scholar
• Lisztwan, J., G. Imbert, C. Wirbelauer, M. Gstaiger, and W. Krek. 1999. The von Hippel-Lindau tumor suppressor protein is a component of an E3 ubiquitin-protein ligase activity. Genes Dev. 13:1822–1833.
   PubMed Web of Science ®Google Scholar
• Lorick, K. L., J. P. Jensen, S. Fang, A. M. Ong, S. Hatakeyama, and A. M. Weissman. 1999. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl. Acad. Sci. USA 96:11364–11369.
   PubMed Web of Science ®Google Scholar
• Lu, P.-J., X. Z. Zhou, M. Shen, and K. P. Lu. 1999. Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 283:1325–1328.
   PubMed Web of Science ®Google Scholar
• Marchal, C., R. Haguenauer-Tsapis, and D. Urban-Grimal. 2000. Casein kinase I-dependent phosphorylation within a PEST sequence and ubiquitination at nearby lysines signal endocytosis of yeast uracil permease. J. Biol. Chem. 275:23608–23614.
   PubMedGoogle Scholar
• Marchal, C., R. Haguenauer-Tsapis, and D. Urban-Grimal. 1998. A PEST-like sequence mediates phosphorylation and efficient ubiquitination of yeast uracil permease. Mol. Cell. Biol. 18:314–321.
   PubMed Web of Science ®Google Scholar
• Marsh, M., and H. T. McMahon. 1999. The structural era of endocytosis. Science 285:215–220.
   PubMed Web of Science ®Google Scholar
• Martinez-Noel, G., R. Niedenthal, T. Tamura, and K. Harbers. 1999. A family of structurally related RING finger proteins interacts specifically with the ubiquitin-conjugating enzyme UbcM4. FEBS Lett. 454:257–261.
   PubMedGoogle Scholar
• Medintz, I., H. Jiang, and C. A. Michels. 1998. The role of ubiquitin conjugation in glucose-induced proteolysis of Saccharomyces maltose permease. J. Biol. Chem. 273:34454–34462.
   PubMedGoogle Scholar
• Moreau, V., J.-M. Galan, G. Devilliers, R. Haguenauer-Tsapis, and B. Winsor. 1997. The yeast actin-related protein Arp2p is required for the internalization step of endocytosis. Mol. Biol. Cell 8:1361–1375.
   PubMedGoogle Scholar
• Nguyen, J. T., C. W. Turck, F. E. Cohen, R. N. Zuckermann, and W. A. Lim. 1998. Exploiting the basis of proline recognition by SH3 and WW domains: design of N-substituted inhibitors. Science 282:2088–2092.
   PubMed Web of Science ®Google Scholar
• Peters, J. M.. 1998. SCF and APC: the Yin and Yang of cell cycle regulated proteolysis. Curr. Opin. Cell Biol. 10:759–768.
   PubMedGoogle Scholar
• Pickart, C. M.. 1997. Targeting of substrates to the 26S proteasome. FASEB J. 11:1055–1066.
   PubMed Web of Science ®Google Scholar
• Plant, P. J., H. Yeger, O. Staub, P. Howard, and D. Rotin. 1997. The C2 domain of the ubiquitin protein ligase Nedd4 mediates Ca2+-dependent plasma membrane localization. J. Biol. Chem. 272:32329–32336.
   PubMedGoogle Scholar
• Raths, S., J. Rohrer, F. Crausaz, and H. Riezman. 1993. end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae. J. Cell Biol. 120:55–65.
   PubMedGoogle Scholar
• Rieder, S. E., L. M. Banta, K. Kohrer, J. M. McCaffery, and S. D. Emr. 1996. Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. Mol. Biol. Cell 7:985–999.
   PubMedGoogle Scholar
• Riezman, H.. 1997. The ins and outs of protein translocation. Science 278:1728–1729.
   PubMedGoogle Scholar
• Rizo, J., and T. C. Sudhof. 1998. C2-domains, structure and function of a universal Ca2+-binding domain. J. Biol. Chem. 273:15879–15882.
   PubMed Web of Science ®Google Scholar
• Roberg, K. J., N. Rowley, and C. A. Kaiser. 1997. Physiological regulation of membrane protein sorting late in the secretory pathway of Saccharomyces cerevisiae. J. Cell Biol. 137:1469–1482.
   PubMed Web of Science ®Google Scholar
• Robinson, M. S., C. Watts, and M. Zerial. 1996. Membrane dynamics in endocytosis. Cell 84:13–21.
   PubMed Web of Science ®Google Scholar
• Roth, A. F., and N. G. Davis. 1996. Ubiquitination of the yeast a-factor receptor. J. Cell Biol. 134:661–674.
   PubMedGoogle Scholar
• Roth, A. F., D. M. Sullivan, and N. G. Davis. 1998. A large PEST-like sequence directs the ubiquitination, endocytosis, and vacuolar degradation of the yeast a-factor receptor. J. Cell Biol. 142:949–961.
   PubMedGoogle Scholar
• Scheffner, M., U. Nuber, and J. M. Huibregtse. 1995. Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 373:81–83.
   PubMed Web of Science ®Google Scholar
• Schmid, S. L.. 1997. Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66:511–548.
   PubMed Web of Science ®Google Scholar
• Seron, K., M. O. Blondel, R. Haguenauer-Tsapis, and C. Volland. 1999. Uracil-induced down-regulation of the yeast uracil permease. J. Bacteriol. 181:1793–1800.
   PubMed Web of Science ®Google Scholar
• Shih, S. C., K. E. Sloper-Mould, and L. Hicke. 2000. Monoubiquitin carries a novel internalization signal that is appended to activated receptors. EMBO J. 19:187–198.
   PubMed Web of Science ®Google Scholar
• Sorkina, T., A. Bild, F. Tebar, and A. Sorkin. 1999. Clathrin, adaptors and eps15 in endosomes containing activated epidermal growth factor receptors. J. Cell Sci. 112:317–327.
   PubMedGoogle Scholar
• Springael, J. Y., and B. Andre. 1998. Nitrogen-regulated ubiquitination of the gap1 permease of Saccharomyces cerevisiae. Mol. Biol. Cell 9:1253–1263.
   PubMed Web of Science ®Google Scholar
• Springael, J. Y., J. O. De Craene, and B. Andre. 1999. The yeast Npi1/Rsp5 ubiquitin ligase lacking its N-terminal C2 domain is competent for ubiquitination but not for subsequent endocytosis of the gap1 permease. Biochem. Biophys. Res. Commun. 257:561–566.
   PubMedGoogle Scholar
• Springael, J. Y., J. M. Galan, R. Haguenauer-Tsapis, and B. Andre. 1999. NH4+-induced down-regulation of the Saccharomyces cerevisiae Gap1p permease involves its ubiquitination with lysine-63-linked chains. J. Cell Sci. 112:1375–1383.
   PubMedGoogle Scholar
• Stewart, L. C., and M. P. Yaffe. 1991. A role for unsaturated fatty acids in mitochondrial movement and inheritance. J. Cell Biol. 115:1249–1257.
   PubMedGoogle Scholar
• Tang, H. Y., A. Munn, and M. Cai. 1997. EH domain proteins Pan1p and End3p are components of a complex that plays a dual role in organization of the cortical actin cytoskeleton and endocytosis in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:4294–4304.
   PubMed Web of Science ®Google Scholar
• Tang, H. Y., J. Xu, and M. Cai. 2000. Pan1p, End3p, and Sla1p, three yeast proteins required for normal cortical actin cytoskeleton organization, associate with each other and play essential roles in cell wall morphogenesis. Mol. Cell. Biol. 20:12–25.
   PubMed Web of Science ®Google Scholar
• Terrell, J., S. Shih, R. Dunn, and L. Hicke. 1998. A function for monoubiquitination in the internalization of a G protein-coupled receptor. Mol. Cell 1:193–202.
   PubMed Web of Science ®Google Scholar
• Tomoda, K., Y. Kubota, and J. Kato. 1999. Degradation of the cyclin-dependent kinase inhibitor p27kip1 is instigated by Jab1. Nature 398:160–165.
   PubMed Web of Science ®Google Scholar
• Torrisi, M. R., L. V. Lotti, F. Belleudi, R. Gradini, A. E. Salcini, S. Confalonieri, P. G. Pelicci, and P. P. Di Fiore. 1999. Eps15 is recruited to the plasma membrane upon epidermal growth factor receptor activation and localizes to components of the endocytic pathway during receptor internalization. Mol. Biol. Cell 10:417–434.
   PubMed Web of Science ®Google Scholar
• van Delft, S., R. Govers, G. J. Strous, A. J. Verkleij, and P. M. van Bergen en Henegouwen. 1997. Epidermal growth factor induces ubiquitination of Eps15. J. Biol. Chem. 272:14013–14016.
   PubMed Web of Science ®Google Scholar
• Volland, C., C. Garnier, and R. Haguenauer-Tsapis. 1992. In vivo phosphorylation of the yeast uracil permease. J. Biol. Chem. 267:23767–23771.
   PubMedGoogle Scholar
• Wang, G., J. Yang, and J. M. Huibregtse. 1999. Functional domains of the Rsp5 ubiquitin-protein ligase. Mol. Cell. Biol. 19:342–352.
   PubMed Web of Science ®Google Scholar
• Waterman, H., G. Levkowitz, I. Alroy, and Y. Yarden. 1999. The RING finger of c-Cb1 mediates desensitization of the epidermal growth factor receptor. J. Biol. Chem. 274:22151–22154.
   PubMedGoogle Scholar
• Wendland, B., S. D. Emr, and H. Riezman. 1998. Protein traffic in the yeast endocytic and vacuolar protein sorting pathways. Curr. Opin. Cell Biol. 10:513–522.
   PubMed Web of Science ®Google Scholar
• Wendland, B., K. E. Steece, and S. D. Emr. 1999. Yeast epsins contain an essential N-terminal ENTH domain, bind clathrin and are required for endocytosis. EMBO J. 18:4383–4393.
   PubMed Web of Science ®Google Scholar
• Wesp, A., L. Hicke, J. Palecek, R. Lombardi, T. Aust, A. L. Munn, and H. Riezman. 1997. End4p/Sla2p interacts with actin-associated proteins for endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell 8:2291–2306.
   PubMedGoogle Scholar
• Xie, Y., and A. Varshavsky. 2000. Physical association of ubiquitin ligases and the 26S proteasome. Proc. Natl. Acad. Sci. USA 14:2497–2502.
   Google Scholar
• Zoladek, T., A. Tobiasz, G. Vaduva, M. Boguta, N. C. Martin, and A. K. Hopper. 1997. MDP1, a Saccharomyces cerevisiae gene involved in mitochondrial/cytoplasmic protein distribution, is identical to the ubiquitin-protein ligase gene RSP5. Genetics 145:595–603.
   PubMed Web of Science ®Google Scholar