Ent3p and Ent5p exhibit cargo-specific functions in trafficking proteins between the trans-Golgi network and the endosomes in yeast

Molecular Biology of the Cell

Volumn 18, Issue 5, 2007, Pages 1803-1815

  Čopič, Alenka ^a,b   Starr, Trevor L ^a   Schekman, Randy ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BINDING PROTEIN; CHS3P PROTEIN; CLATHRIN; CLATHRIN ASSEMBLY PROTEIN; ENT3P PROTEIN; ENT5P PROTEIN; GGA2P PROTEIN; PEP12P PROTEIN; PHOSPHATIDYLINOSITIDE; PROTEIN DERIVATIVE; SYNTAXIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MIGRATION; CELL SURFACE; CELL VACUOLE; ENDOSOME; MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; TRANS GOLGI NETWORK; YEAST;

ADAPTOR PROTEIN COMPLEX 1; ADAPTOR PROTEINS, VESICULAR TRANSPORT; BIOLOGICAL TRANSPORT, ACTIVE; CLATHRIN; ENDOSOMES; GENES, FUNGAL; GREEN FLUORESCENT PROTEINS; MODELS, BIOLOGICAL; MUTATION; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-GOLGI NETWORK;

SACCHAROMYCES CEREVISIAE;

EID: 34248138913     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-11-1000     Document Type: Article

References (59)

1. Becherer, K. A., Rieder, S. E., Emr, S. D., and Jones, E. W. (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.
2. Black, M. W., and Pelham, H. R. (2000). A selective transport route from Golgi to late endosomes that requires the yeast GGA proteins. J. Cell Biol. 151, 587-600.
3. Boman, A. L., Salo, P. D., Hauglund, M. J., Strand, N. L., Rensink, S. J., and Zhdankina, O. (2002). ADP-ribosylation factor (ARF) interaction is not sufficient for yeast GGA protein function or localization. Mol. Biol. Cell 13, 3078-3095.
4. Bonifacino, J. S. (2004). The GGA proteins: adaptors on the move. Nat. Rev. Mol. Cell Biol. 5, 23-32.
5. Bonifacino, J. S., and Traub, L. M. (2003). Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395-447.
6. Bowers, K., and Stevens, T. H. (2005). Protein transport from the late Golgi to the vacuole in the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1744, 438-454.
7. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P., and Boeke, J. D. (1998). Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132.
8. Bryant, N. J., and Stevens, T. H. (1997). Two separate signals act independently to localize a yeast late Golgi membrane protein through a combination of retrieval and retention. J. Cell Biol. 136, 287-297.
9. Chidambaram, S., Mullers, N., Wiederhold, K., Haucke, V., and von Mollard, G. F. (2004). Specific interaction between SNAREs and epsin N-terminal homology (ENTH) domains of epsin-related proteins in trans-Golgi network to endosome transport. J. Biol. Chem. 279, 4175-4179.
10. Chuang, J. S., and Schekman, R. W. (1996). Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p. J. Cell Biol. 135, 597-610.
11. Costaguta, G., Duncan, M. C., Fernandez, G. E., Huang, G. H., and Payne, G. S. (2006). Distinct roles for TGN/endosome epsin-like adaptors Ent3p and Ent5p. Mol. Biol. Cell 17, 3907-3920.
12. Costaguta, G., Stefan, C. J., Bensen, E. S., Emr, S. D., and Payne, G. S. (2001). Yeast Gga coat proteins function with clathrin in Golgi to endosome transport. Mol. Biol. Cell 12, 1885-1896.
13. Crump, C. M., Xiang, Y., Thomas, L., Gu, F., Austin, C., Tooze, S. A., and Thomas, G. (2001). PACS-1 binding to adaptors is required for acidic cluster motif-mediated protein traffic. EMBO J. 20, 2191-2201.
14. Doray, B., Ghosh, P., Griffith, J., Geuze, H. J., and Kornfeld, S. (2002). Cooperation of GGAs and AP-1 in packaging MPRs at the trans-Golgi network. Science 297, 1700-1703.
15. Duncan, M. C., Costaguta, G., and Payne, G. S. (2003). Yeast epsin-related proteins required for Golgi-endosome traffic define a gamma-adaptin ear-binding motif. Nat. Cell Biol. 5, 77-81.
16. Eugster, A., Pecheur, E. I., Michel, F., Winsor, B., Letourneur, F., and Friant, S. (2004). Ent5p is required with Ent3p and Vps27p for ubiquitin-dependent protein sorting into the multivesicular body. Mol. Biol. Cell 15, 3031-3041.
17. Friant, S., Pecheur, E. I., Eugster, A., Michel, F., Lefkir, Y., Nourrisson, D., and Letourneur, F. (2003). Ent3p is a PtdIns(3,5)P2 effector required for protein sorting to the multivesicular body. Dev. Cell 5, 499-511.
18. Foote, C., and Nothwehr, S. F. (2006). The clathrin adaptor complex 1 directly binds to a sorting signal in Ste13p to reduce the rate of its trafficking to the late endosome of yeast. J. Cell Biol. 173, 615-626.
19. Ghosh, P., Griffith, J., Geuze, H. J., and Kornfeld, S. (2003). Mammalian GGAs act together to sort mannose 6-phosphate receptors. J. Cell Biol. 163, 755-766.
20. Ha, S. A., Bunch, J. T., Hama, H., DeWald, D. B., and Nothwehr, S. F. (2001). A novel mechanism for localizing membrane proteins to yeast trans-Golgi network requires function of synaptojanin-like protein. Mol. Biol. Cell 12, 3175-3190.
21. Ha, S. A., Torabinejad, J., DeWald, D. B., Wenk, M. R., Lucasi, L., De Camilli, P., Newitt, R. A., Aebersold, R., and Nothwehr, S. F. (2003). The synaptojanin-like protein Inp53/Sjl3 functions with clathrin in a yeast TGN-to-endosome pathway distinct from the GGA protein-dependent pathway. Mol. Biol. Cell 14, 1319-1333.
22. Harsay, E., and Schekman, R. (2002). A subset of yeast vacuolar protein sorting mutants is blocked in one branch of the exocytic pathway. J. Cell Biol. 156, 271-285.
23. Hirst, J., Lindsay, M. R., and Robinson, M. S. (2001). GGAs: roles of the different domains and comparison with AP-1 and clathrin. Mol. Biol. Cell 12, 3573-3588.
24. Hirst, J., Lui, W. W., Bright, N. A., Totty, N., Seaman, M. N., and Robinson, M. S. (2000). A family of proteins with gamma-adaptin and VHS domains that facilitate trafficking between the trans-Golgi network and the vacuole/lysosome. J. Cell Biol. 149, 67-80.
25. Hirst, J., Miller, S. E., Taylor, M. J., von Mollard, G. F., and Robinson, M. S. (2004). EpsinR is an adaptor for the SNARE protein Vti1b. Mol. Biol. Cell 15, 5593-5602.
26. Hirst, J., Motley, A., Harasaki, K., Peak Chew, S. Y., and Robinson, M. S. (2003). EpsinR: an ENTH domain-containing protein that interacts with AP-1. Mol. Biol. Cell 14, 625-641.
27. Janvier, K., Kato, Y., Boehm, M., Rose, J. R., Martina, J. A., Kim, B. Y., Venkatesan, S., and Bonifacino, J. S. (2003). Recognition of dileucine-based sorting signals from HIV-1 Nef and LIMP-II by the AP-1 gamma-sigma1 and AP-3 delta-sigma3 hemicomplexes. J. Cell Biol. 163, 1281-1290.
28. Jimenez, C. R. et al. (1998). Direct mass spectrometric peptide profiling and sequencing of single neurons reveals differential peptide patterns in a small neuronal network. Biochemistry 37, 2070-2076.
29. Kaiser, C. A., Chen, E. J., and Losko, S. (2002). Subcellular fractionation of secretory organelles. Methods Enzymol. 351, 325-338.
30. Kalthoff, C., Groos, S., Kohl, R., Mahrhold, S., and Ungewickell, E. J. (2002). Clint: a novel clathrin-binding ENTH-domain protein at the Golgi. Mol. Biol. Cell 13, 4060-4073.
31. Kim, J. S., and Raines, R. T. (1993). Ribonuclease S-peptide as a carrier in fusion proteins. Protein Sci. 2, 348-356.
32. Kolling, R., and Hollenberg, C. P. (1994). The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 13, 3261-3271.
33. Legendre-Guillemin, V., Wasiak, S., Hussain, N. K., Angers, A., and McPherson, P. S. (2004). ENTH/ANTH proteins and clathrin-mediated membrane budding. J. Cell Sci. 117, 9-18.
34. Longtine, M. S., McKenzie, A., 3rd, 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.
35. Meyer, C., Zizioli, D., Lausmann, S., Eskelinen, E. L., Hamann, J., Saftig, P., von Figura, K., and Schu, P. (2000). mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J. 19, 2193-2203.
36. Meyer, D. M., Crottet, P., Maco, B., Degtyar, E., Cassel, D., and Spiess, M. (2005). Oligomerization and dissociation of AP-1 adaptors are regulated by cargo signals and by ArfGAP1-induced GTP hydrolysis. Mol. Biol. Cell 16, 4745-4754.
37. Mills, I. G., Praefcke, G. J., Vallis, Y., Peter, B. J., Olesen, L. E., Gallop, J. L., Butler, P. J., Evans, P. R., and McMahon, H. T. (2003). EpsinR: an AP1/clathrin interacting protein involved in vesicle trafficking. J. Cell Biol. 160, 213-222.
38. Misra, S., Puertollano, R., Kato, Y., Bonifacino, J. S., and Hurley, J. H. (2002). Structural basis for acidic-cluster-dileucine sorting-signal recognition by VHS domains. Nature 415, 933-937.
39. Mullins, C., and Bonifacino, J. S. (2001). Structural requirements for function of yeast GGAs in vacuolar protein sorting, alpha-factor maturation, and interactions with clathrin. Mol. Cell. Biol. 21, 7981-7994.
40. Neubrand, V. E., Will, R. D., Mobius, W., Poustka, A., Wiemann, S., Schu, P., Dotti, C. G., Pepperkok, R., and Simpson, J. C. (2005). gamma-BAR, a novel AP-1-interacting protein involved in post-Golgi trafficking. EMBO J. 24, 1122-1133.
41. Nothwehr, S. F., Roberts, C. J., and Stevens, T. H. (1993). Membrane protein retention in the yeast Golgi apparatus: dipeptidyl aminopeptidase A is retained by a cytoplasmic signal containing aromatic residues. J. Cell Biol. 121, 1197-1209.
42. Owen, D. J., Collins, B. M., and Evans, P. R. (2004). Adaptors for clathrin coats: structure and function. Annu. Rev. Cell Dev. Biol. 20, 153-191.
43. Peden, A. A., Park, G. Y., and Scheller, R. H. (2001). The Di-leucine motif of vesicle-associated membrane protein 4 is required for its localization and AP-1 binding. J. Biol. Chem. 276, 49183-49187.
44. Puertollano, R., van der Wel, N. N., Greene, L. E., Eisenberg, E., Peters, P. J., and Bonifacino, J. S. (2003). Morphology and dynamics of clathrin/GGA1-coated carriers budding from the trans-Golgi network. Mol. Biol. Cell 14, 1545-1557.
45. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Seraphin, B. (1999). A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17, 1030-1032.
46. Saint-Pol, A. et al. (2004). Clathrin adaptor epsinR is required for retrograde sorting on early endosomal membranes. Dev. Cell 6, 525-538.
47. Sanchatjate, S., and Schekman, R. (2006). Chs5/6 complex: a multi-protein complex that interacts with and conveys chitin synthase III from the trans-Golgi network to the cell surface. Mol. Biol. Cell 17, 4157-4166.
48. Scott, P. M. et al. (2004). GGA proteins bind ubiquitin to facilitate sorting at the trans-Golgi network. Nat. Cell Biol. 6, 252-259.
49. Seeger, M., and Payne, G. S. (1992). Selective and immediate effects of clathrin heavy chain mutations on Golgi membrane protein retention in Saccharomyces cerevisiae. J. Cell Biol. 118, 531-540.
50. Sikorski, R. S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
51. Tong, A. H. et al. (2004). Global mapping of the yeast genetic interaction network. Science 303, 808-813.
52. Traub, L. M. (2005). Common principles in clathrin-mediated sorting at the Golgi and the plasma membrane. Biochim. Biophys. Acta 1744, 415-437.
53. Trilla, J. A., Duran, A., and Roncero, C. (1999). Chs7p, a new protein involved in the control of protein export from the endoplasmic reticulum that is specifically engaged in the regulation of chitin synthesis in Saccharomyces cerevisiae. J. Cell Biol. 145, 1153-1163.
54. Valdivia, R. H., Baggott, D., Chuang, J. S., and Schekman, R. W. (2002). The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins. Dev. Cell 2, 283-294.
55. Waguri, S., Dewitte, F., Le Borgne, R., Rouille, Y., Uchiyama, Y., Dubremetz, J. F., and Hoflack, B. (2003). Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol. Biol. Cell 14, 142-155.
56. Wang, Y. J. et al. (2003). Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114, 299-310.
57. Wasiak, S. et al. (2002). Enthoprotin: a novel clathrin-associated protein identified through subcellular proteomics. J. Cell Biol. 158, 855-862.
58. Yeung, B. G., and Payne, G. S. (2001). Clathrin interactions with C-terminal regions of the yeast AP-1 beta and gamma subunits are important for AP-1 association with clathrin coats. Traffic 2, 565-576.
59. Ziman, M., Chuang, J. S., Tsung, M., Hamamoto, S., and Schekman, R. (1998). Chs6p-dependent anterograde transport of Chs3p from the chitosome to the plasma membrane in Saccharomyces cerevisiae. Mol. Biol. Cell 9, 1565-1576.