This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Marchal, C.
Right arrow Articles by Urban-Grimal, D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Marchal, C.
Right arrow Articles by Urban-Grimal, D.

 Previous Article  |  Next Article 

Mol. Cell. Biol., 01 1998, 314-321, Vol 18, No. 1
Copyright © 1998, American Society for Microbiology

A PEST-like sequence mediates phosphorylation and efficient ubiquitination of yeast uracil permease

C Marchal, R Haguenauer-Tsapis and D Urban-Grimal
Institut Jacques Monod, CNRS-UMRC9922, Universite Paris 7-Denis Diderot, France.

Uptake of uracil by the yeast Saccharomyces cerevisiae is mediated by a specific permease encoded by the FUR4 gene. Uracil permease located at the cell surface is subject to two covalent modifications: phosphorylation and ubiquitination. The ubiquitination step is necessary prior to permease endocytosis and subsequent vacuolar degradation. Here, we demonstrate that a PEST-like sequence located within the cytoplasmic N terminus of the protein is essential for uracil permease turnover. Internalization of the transporter was reduced when some of the serines within the region were converted to alanines and severely impaired when all five serines within the region were mutated or when this region was absent. The phosphorylation and degree of ubiquitination of variant permeases were inversely correlated with the number of serines replaced by alanines. A serine-free version of this sequence was very poorly phosphorylated, and elimination of this sequence prevented ubiquitination. Thus, it appears that the serine residues in the PEST-like sequence are required for phosphorylation and ubiquitination of uracil permease. A PEST-like sequence in which the serines were replaced by glutamic acids allowed efficient permease turnover, suggesting that the PEST serines are phosphoacceptors.


This article has been cited by other articles:

  • Paiva, S., Vieira, N., Nondier, I., Haguenauer-Tsapis, R., Casal, M., Urban-Grimal, D. (2009). Glucose-induced Ubiquitylation and Endocytosis of the Yeast Jen1 Transporter: ROLE OF LYSINE 63-LINKED UBIQUITIN CHAINS. J. Biol. Chem. 284: 19228-19236 [Abstract] [Full Text]  
  • Hatanaka, H., Omura, F., Kodama, Y., Ashikari, T. (2009). Gly-46 and His-50 of Yeast Maltose Transporter Mal21p Are Essential for Its Resistance against Glucose-induced Degradation. J. Biol. Chem. 284: 15448-15457 [Abstract] [Full Text]  
  • Navarro, F. J., Martin, Y., Siverio, J. M. (2008). Phosphorylation of the Yeast Nitrate Transporter Ynt1 Is Essential for Delivery to the Plasma Membrane during Nitrogen Limitation. J. Biol. Chem. 283: 31208-31217 [Abstract] [Full Text]  
  • Annan, R. B., Wu, C., Waller, D. D., Whiteway, M., Thomas, D. Y. (2008). Rho5p Is Involved in Mediating the Osmotic Stress Response in Saccharomyces cerevisiae, and Its Activity Is Regulated via Msi1p and Npr1p by Phosphorylation and Ubiquitination. Eukaryot Cell 7: 1441-1449 [Abstract] [Full Text]  
  • Belenky, P. A., Moga, T. G., Brenner, C. (2008). Saccharomyces cerevisiae YOR071C Encodes the High Affinity Nicotinamide Riboside Transporter Nrt1. J. Biol. Chem. 283: 8075-8079 [Abstract] [Full Text]  
  • Estrella, L. A., Krishnamurthy, S., Timme, C. R., Hampsey, M. (2008). The Rsp5 E3 Ligase Mediates Turnover of Low Affinity Phosphate Transporters in Saccharomyces cerevisiae. J. Biol. Chem. 283: 5327-5334 [Abstract] [Full Text]  
  • Kota, J., Melin-Larsson, M., Ljungdahl, P. O., Forsberg, H. (2007). Ssh4, Rcr2 and Rcr1 Affect Plasma Membrane Transporter Activity in Saccharomyces cerevisiae. Genetics 175: 1681-1694 [Abstract] [Full Text]  
  • Navarro, F. J., Machin, F., Martin, Y., Siverio, J. M. (2006). Down-regulation of Eukaryotic Nitrate Transporter by Nitrogen-dependent Ubiquitinylation. J. Biol. Chem. 281: 13268-13274 [Abstract] [Full Text]  
  • Brunner, M., Schafmeier, T. (2006). Transcriptional and post-transcriptional regulation of the circadian clock of cyanobacteria and Neurospora.. Genes Dev. 20: 1061-1074 [Abstract] [Full Text]  
  • Staub, O., Rotin, D. (2006). Role of Ubiquitylation in Cellular Membrane Transport. Physiol. Rev. 86: 669-707 [Abstract] [Full Text]  
  • Gadura, N., Robinson, L. C., Michels, C. A. (2006). Glc7-Reg1 Phosphatase Signals to Yck1,2 Casein Kinase 1 to Regulate Transport Activity and Glucose-Induced Inactivation of Saccharomyces Maltose Permease. Genetics 172: 1427-1439 [Abstract] [Full Text]  
  • Zhang, Z., Wu, J.-Y., Hait, W. N., Yang, J.-M. (2004). Regulation of the Stability of P-Glycoprotein by Ubiquitination. Mol. Pharmacol. 66: 395-403 [Abstract] [Full Text]  
  • Papandreou, C. N., Logothetis, C. J. (2004). Bortezomib as a Potential Treatment for Prostate Cancer. Cancer Res. 64: 5036-5043 [Abstract] [Full Text]  
  • Blondel, M.-O., Morvan, J., Dupre, S., Urban-Grimal, D., Haguenauer-Tsapis, R., 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 [Abstract] [Full Text]  
  • Gitan, R. S., Shababi, M., Kramer, M., Eide, D. J. (2003). A Cytosolic Domain of the Yeast Zrt1 Zinc Transporter Is Required for Its Post-translational Inactivation in Response to Zinc and Cadmium. J. Biol. Chem. 278: 39558-39564 [Abstract] [Full Text]  
  • Klapisz, E., Sorokina, I., Lemeer, S., Pijnenburg, M., Verkleij, A. J., van Bergen en Henegouwen, P. M. P. (2002). A Ubiquitin-interacting Motif (UIM) Is Essential for Eps15 and Eps15R Ubiquitination. J. Biol. Chem. 277: 30746-30753 [Abstract] [Full Text]  
  • Marchal, C., Dupre, S., Urban-Grimal, D. (2002). Casein kinase I controls a late step in the endocytic trafficking of yeast uracil permease. J. Cell Sci. 115: 217-226 [Abstract] [Full Text]  
  • Soetens, O., De Craene, J.-O., 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 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Wang, G., McCaffery, J. M., Wendland, B., Dupré, S., Haguenauer-Tsapis, R., Huibregtse, J. M. (2001). Localization of the Rsp5p Ubiquitin-Protein Ligase at Multiple Sites within the Endocytic Pathway. Mol. Cell. Biol. 21: 3564-3575 [Abstract] [Full Text]  
  • Gajewska, B., Kaminska, J., Jesionowska, A., Martin, N. C., Hopper, A. K., 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 [Abstract] [Full Text]  
  • Feng, Y., Davis, N. G. (2000). Akr1p and the Type I Casein Kinases Act prior to the Ubiquitination Step of Yeast Endocytosis: Akr1p Is Required for Kinase Localization to the Plasma Membrane. Mol. Cell. Biol. 20: 5350-5359 [Abstract] [Full Text]  
  • Penrose, K. J., McBride, A. A. (2000). Proteasome-Mediated Degradation of the Papillomavirus E2-TA Protein Is Regulated by Phosphorylation and Can Modulate Viral Genome Copy Number. J. Virol. 74: 6031-6038 [Abstract] [Full Text]  
  • Roth, A. F., Davis, N. G. (2000). Ubiquitination of the PEST-like Endocytosis Signal of the Yeast a-Factor Receptor. J. Biol. Chem. 275: 8143-8153 [Abstract] [Full Text]  
  • Gillissen, B., Bürkle, L., André, B., Kühn, C., Rentsch, D., Brandl, B., Frommer, W. B. (2000). A New Family of High-Affinity Transporters for Adenine, Cytosine, and Purine Derivatives in Arabidopsis. Plant Cell 12: 291-300 [Abstract] [Full Text]  
  • Decottignies, A., Owsianik, G., Ghislain, M. (1999). Casein Kinase I-dependent Phosphorylation and Stability of the Yeast Multidrug Transporter Pdr5p. J. Biol. Chem. 274: 37139-37146 [Abstract] [Full Text]  
  • Shumway, S. D., Maki, M., Miyamoto, S. (1999). The PEST Domain of Ikappa Balpha Is Necessary and Sufficient for in Vitro Degradation by {micro}-Calpain. J. Biol. Chem. 274: 30874-30881 [Abstract] [Full Text]  
  • Huggins, G. S., Chin, M. T., Sibinga, N. E. S., Lee, S.-L., Haber, E., Lee, M.-E. (1999). Characterization of the mUBC9-binding Sites Required for E2A Protein Degradation. J. Biol. Chem. 274: 28690-28696 [Abstract] [Full Text]  
  • Séron, K., Blondel, M.-O., Haguenauer-Tsapis, R., Volland, C. (1999). Uracil-Induced Down-Regulation of the Yeast Uracil Permease. J. Bacteriol. 181: 1793-1800 [Abstract] [Full Text]  
  • Lu, P., Zhou, X. Z., Shen, M., Lu, K. P. (1999). Function of WW Domains as Phosphoserine- or Phosphothreonine-Binding Modules. Science 283: 1325-1328 [Abstract] [Full Text]  
  • Strous, G., Govers, R (1999). The ubiquitin-proteasome system and endocytosis. J. Cell Sci. 112: 1417-1423 [Abstract]  
  • Roth, A. F., Sullivan, D. M., Davis, N. G. (1998). A Large PEST-like Sequence Directs the Ubiquitination, Endocytosis, and Vacuolar Degradation of the Yeast a-Factor Receptor. JCB 142: 949-961 [Abstract] [Full Text]  
  • Marchal, C., Haguenauer-Tsapis, R., Urban-Grimal, D. (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 [Abstract] [Full Text]  
  • Kopf, E., Plassat, J.-L., Vivat, V., de The, H., Chambon, P., Rochette-Egly, C. (2000). Dimerization with Retinoid X Receptors and Phosphorylation Modulate the Retinoic Acid-induced Degradation of Retinoic Acid Receptors alpha and gamma through the Ubiquitin-Proteasome Pathway. J. Biol. Chem. 275: 33280-33288 [Abstract] [Full Text]  
  • Hautbergue, G., Goguel, V. (2001). Activation of the Cyclin-dependent Kinase CTDK-I Requires the Heterodimerization of Two Unstable Subunits. J. Biol. Chem. 276: 8005-8013 [Abstract] [Full Text]