The sequence NPFXD defines a new class of endocytosis signal in Saccharomyces cerevisiae

doi:10.1083/jcb.135.6.1789

This Article

Full Text (PDF, 1577K)

Alert me when this article is cited

Citation Map

Services

Email this article

Similar articles in this journal

Similar articles in PubMed

Alert me to new content in the JCB

Download to citation manager

Citing Articles

Citing Articles via HighWire

Citing Articles via CrossRef

Citing Articles via Google Scholar

Google Scholar

Articles by Tan, P. K.

Articles by Payne, G. S.

Search for Related Content

PubMed

PubMed Citation

Articles by Tan, P. K.

Articles by Payne, G. S.

Pubmed/NCBI databases

Hazardous Substances DB
Protein
Compound via MeSH
Substance via MeSH
L-LYSINE
L-TYROSINE

Social Bookmarking

What's this?

ARTICLES

The sequence NPFXD defines a new class of endocytosis signal in Saccharomyces cerevisiae

PK Tan, JP Howard and GS Payne
Department of Biological Chemistry, UCLA School of Medicine 90095, USA.

The yeast membrane protein Kex2p uses a tyrosine-containing motif within the cytoplasmic domain for localization to a late Golgi compartment. Because Golgi membrane proteins mislocalized to the plasma membrane in yeast can undergo endocytosis, we examined whether the Golgi localization sequence or other sequences in the Kex2p cytoplasmic domain mediate endocytosis. To assess endocytic function, the Kex2p cytoplasmic domain was fused to an endocytosis-defective form of the alpha-factor receptor. Ste2p. Like intact Ste2p, the chimeric protein, Stex22p, undergoes rapid endocytosis that is dependent on clathrin and End3p. Uptake of Stex22p does not require the Kex2p Golgi localization motif. Instead, the sequence NPFSD, located 37 amino acids from the COOH terminus, is essential for Stex22p endocytosis. Internalization was abolished when the N, P, or F residues were converted to alanine and severely impaired upon conversion of D to A. NPFSD restored uptake when added to the COOH terminus of an endocytosis-defective Ste2p chimera lacking lysine-based endocytosis signals present in wild-type Ste2p. An NPF sequence is present in the cytoplasmic domain of the a- factor receptor, Ste3p. Mutation of this sequence prevented pheromone- stimulated endocytosis of a truncated form of Ste3p. Our results identify NPFSD as a clathrin-dependent endocytosis signal that is distinct from the aromatic amino acid-containing Golgi localization motif and lysine-based, ubiquitin-dependent endocytosis signals in yeast.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Liu, K., Hua, Z., Nepute, J. A., Graham, T. R. (2007). Yeast P4-ATPases Drs2p and Dnf1p Are Essential Cargos of the NPFXD/Sla1p Endocytic Pathway. Mol. Biol. Cell 18: 487-500 [Abstract] [Full Text]
Piao, H. L., Machado, I. M.P., Payne, G. S. (2007). NPFXD-mediated Endocytosis Is Required for Polarity and Function of a Yeast Cell Wall Stress Sensor. Mol. Biol. Cell 18: 57-65 [Abstract] [Full Text]
Moseley, J. B., Goode, B. L. (2006). The Yeast Actin Cytoskeleton: from Cellular Function to Biochemical Mechanism. Microbiol. Mol. Biol. Rev. 70: 605-645 [Abstract] [Full Text]
Doss-Pepe, E. W., Chen, L., Madura, K. (2005). {alpha}-Synuclein and Parkin Contribute to the Assembly of Ubiquitin Lysine 63-linked Multiubiquitin Chains. J. Biol. Chem. 280: 16619-16624 [Abstract] [Full Text]
Chantalat, S., Park, S.-K., Hua, Z., Liu, K., Gobin, R., Peyroche, A., Rambourg, A., Graham, T. R., Jackson, C. L. (2004). The Arf activator Gea2p and the P-type ATPase Drs2p interact at the Golgi in Saccharomyces cerevisiae. J. Cell Sci. 117: 711-722 [Abstract] [Full Text]
Townsley, F. M., Thompson, B., Bienz, M. (2004). Pygopus Residues Required for its Binding to Legless Are Critical for Transcription and Development. J. Biol. Chem. 279: 5177-5183 [Abstract] [Full Text]
Baggett, J. J., D'Aquino, K. E., Wendland, B. (2003). The Sla2p Talin Domain Plays a Role in Endocytosis in Saccharomyces cerevisiae. Genetics 165: 1661-1674 [Abstract] [Full Text]
Howard, J. P., Hutton, J. L., Olson, J. M., Payne, G. S. (2002). Sla1p serves as the targeting signal recognition factor for NPFX(1,2)D-mediated endocytosis. JCB 157: 315-326 [Abstract] [Full Text]
Rohrer, J., Kornfeld, R. (2001). Lysosomal Hydrolase Mannose 6-Phosphate Uncovering Enzyme Resides in the trans-Golgi Network. Mol. Biol. Cell 12: 1623-1631 [Abstract] [Full Text]
Chen, L., Davis, N. G. (2000). Recycling of the Yeast a-Factor Receptor. JCB 151: 731-738 [Abstract] [Full Text]
Hubbard, C., Singleton, D., Rauch, M., Jayasinghe, S., Cafiso, D., Castle, D. (2000). The Secretory Carrier Membrane Protein Family: Structure and Membrane Topology. Mol. Biol. Cell 11: 2933-2947 [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]
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]
Kornfeld, R., Bao, M., Brewer, K., Noll, C., Canfield, W. (1999). Molecular Cloning and Functional Expression of Two Splice Forms of Human N-Acetylglucosamine-1-phosphodiester alpha -N-Acetylglucosaminidase. J. Biol. Chem. 274: 32778-32785 [Abstract] [Full Text]
Lodder, A. L., Lee, T. K., Ballester, R. (1999). Characterization of the Wsc1 Protein, a Putative Receptor in the Stress Response of Saccharomyces cerevisiae. Genetics 152: 1487-1499 [Abstract] [Full Text]
Calvo, P. A., Frank, D. W., Bieler, B. M., Berson, J. F., Marks, M. S. (1999). A Cytoplasmic Sequence in Human Tyrosinase Defines a Second Class of Di-leucine-based Sorting Signals for Late Endosomal and Lysosomal Delivery. J. Biol. Chem. 274: 12780-12789 [Abstract] [Full Text]
Torrisi, M. R., Lotti, L. V., Belleudi, F., Gradini, R., Salcini, A. E., Confalonieri, S., Pelicci, P. G., Di Fiore, P. P. (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 [Abstract] [Full Text]
Yamabhai, M., Hoffman, N. G., Hardison, N. L., McPherson, P. S., Castagnoli, L., Cesareni, G., Kay, B. K. (1998). Intersectin, a Novel Adaptor Protein with Two Eps15 Homology and Five Src Homology 3�Domains. J. Biol. Chem. 273: 31401-31407 [Abstract] [Full Text]
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]
Tan, P. K., Waites, C., Liu, Y., Krantz, D. E., Edwards, R. H. (1998). A Leucine-based Motif Mediates the Endocytosis of Vesicular Monoamine and Acetylcholine Transporters. J. Biol. Chem. 273: 17351-17360 [Abstract] [Full Text]
Wendland, B., Emr, S. D. (1998). Pan1p, Yeast eps15, Functions as a Multivalent Adaptor That Coordinates Protein-Protein Interactions Essential for Endocytosis. JCB 141: 71-84 [Abstract] [Full Text]
Coda, L., Salcini, A. E., Confalonieri, S., Pelicci, G., Sorkina, T., Sorkin, A., Pelicci, P. G., Di Fiore, P. P. (1998). Eps15R Is a Tyrosine Kinase Substrate with Characteristics of a Docking Protein Possibly Involved in Coated Pits-mediated Internalization. J. Biol. Chem. 273: 3003-3012 [Abstract] [Full Text]
Salcini, A. E., Confalonieri, S., Doria, M., Santolini, E., Tassi, E., Minenkova, O., Cesareni, G., Pelicci, P. G., Di Fiore, P. P. (1997). Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction�module. Genes Dev. 11: 2239-2249 [Abstract] [Full Text]
Dunn, R., Hicke, L. (2001). Multiple Roles for Rsp5p-dependent Ubiquitination at the Internalization Step of Endocytosis. J. Biol. Chem. 276: 25974-25981 [Abstract] [Full Text]
deHart, A. K.A., Schnell, J. D., Allen, D. A., Hicke, L. (2002). The conserved Pkh-Ypk kinase cascade is required for endocytosis in yeast. JCB 156: 241-248 [Abstract] [Full Text]
Howard, J. P., Hutton, J. L., Olson, J. M., Payne, G. S. (2002). Sla1p serves as the targeting signal recognition factor for NPFX(1,2)D-mediated endocytosis. JCB 157: 315-326 [Abstract] [Full Text]