Pan1p, yeast eps15, functions as a multivalent adaptor that coordinates protein-protein interactions essential for endocytosis

Journal of Cell Biology

Volumn 141, Issue 1, 1998, Pages 71-84

  Wendland, Beverly ^a   Emr, Scott D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; PHOSPHATASE; PHOSPHATIDYLINOSITIDE;

AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE TRANSPORT; CYTOSKELETON; ENDOCYTOSIS; GENETIC SCREENING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM-BINDING PROTEINS; CLATHRIN; ENDOCYTOSIS; FUNGAL PROTEINS; GENE DELETION; GENOTYPE; MAMMALS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; NERVE TISSUE PROTEINS; PHOSPHOPROTEINS; PHOSPHORIC MONOESTER HYDROLASES; PLASMIDS; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SEQUENCE DELETION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 0032489873     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.1.71     Document Type: Article

References (95)

1. Ahle, S. and E. Ungewickell. 1986. Purification and properties of a new clathrin assembly protein. EMBO (Eur. Mol. Biol. Organ.) J. 5:3143-3149.
2. Ayscough, K.R., J. Stryker, N. Pokala, M. Sanders, P. Crews, and D.G. Drubin. 1997. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J. Cell Biol. 137:399-416.
3. Bauer, F., M. Urdaci, M. Aigle, and M. Crouzet. 1993. Alteration of a yeast SH3 protein leads to conditional viability with defects in cytoskeletal and budding patterns. Mol. Cell. Biol. 13:5070-5084.
4. 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.
5. Bedford, M.T., D.C. Chan, and P. Leder. 1997. FBP WW domains and the Abl SH3 domain bind to a specific class of proline-rich ligands. EMBO (Eur. Mol. Biol. Organ.) J. 16:2376-2383.
6. Benedetti, H., S. Raths, F. Crausaz, and H. Riezman. 1994. The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast. Mol. Biol. Cell. 5:1023-1037.
7. Benmerah, A., B. Begue, A. Dautry-Varsat, and N. Cerf-Bensussan. 1996. The ear of alpha-adaptin interacts with the COOH-terminal domain of the Eps 15 protein. J. Biol. Chem. 271:12111-12116.
8. Carraway, K.L., and C.A. Carraway. 1995. Signaling, mitogenesis, and the cytoskeleton: where the action is. Bioessays. 17:171-175.
9. Chalfie, M., Y. Tu, G. Euskirchen, W.W. Ward, and D.C. Prasher. 1994. Green fluorescent protein as a marker for gene expression. Science. 263:802-805.
10. Chan, D.C., M.T. Bedford, and P. Leder. 1996. Formin binding proteins bear WWP/WW domains that bind proline-rich peptides and functionally resemble SH3 domains. EMBO (Eur. Mol. Biol. Organ.) J. 15:1045-1054.
11. Cowles, C.R., G. Odorizzi, G.S. Payne, and S.D. Emr. 1997. The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell. 91:109-118.
12. David, C., P.S. McPherson, O. Mundigl, and P. de Camilli. 1996. A role of amphiphysin in synaptic vesicle endocytosis suggested by its binding to dynamin in nerve terminals. Proc. Natl. Acad. Sci. USA. 93:331-335.
13. Davis, N.G., J.L. Horecka, and G. Sprague, Jr. 1993. Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors. J. Cell Biol. 122:53-65.
14. de Heuvel, E., A.W. Bell, A.R. Ramjaun, K. Wong, W.S. Sossin, and P.S. McPherson. 1997. Identification of the major synaptojanin-hinding proteins in brain. J. Biol. Chem. 272:8710-8716.
15. Dreyling, M.H., J.A. Martinez-Climent, M. Zheng, J. Mao, J.D. Rowley, and S.K. Bohlander. 1996. The t(10;11)(p13;q14) in the U937 cell line results in the fusion of the AF10 gene and CALM, encoding a new member of the AP-3 clathrin assembly protein family. Proc. Natl. Acad. Sci. USA. 93:4804-4809.
16. Fields, S., and O. Song. 1989. A novel genetic system to detect protein-protein interactions. Nature. 340:245-246.
17. Galan, J.M., V. Moreau, B. Andre, 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.
18. Galan, J.M., C. Volland, D. Urban-Grimal, and R. Haguenauer-Tsapis. 1994. The yeast plasma membrane uracil permease is stabilized against stress induced degradation by a point mutation in a cyclin-like "destruction box" Biochem. Biophys. Res. Commun. 201:769-775.
19. Geli, M.I. and H. Riezman. 1996. Role of type I myosins in receptor-mediated endocytosis in yeast. Science. 272:533-535.
20. Graham, T.R., P.A. Scott, and S.D. Emr. 1993. Brefeldin A reversibly blocks early but not late protein transport steps in the yeast secretory pathway. EMBO (Eur. Mol. Biol. Organ.) J. 12:869-877.
21. Haffner, C., K. Takei, H. Chen, N. Ringstad, A. Hudson, M. Butler, A.E. Salcini, P.P. Di Fiore, and P. De Camilli. 1997. Synaptojanin 1: localization on coated endocytic membrane intermediates in nerve terminals and interaction of its 170 kDa isoform with Eps15. FEBS Lett. 419:157-180.
22. Hammonds-Odie, L.P., T.R. Jackson, A.A. Profit, I.J. Blader, C.W. Turck, G.D. Prestwich, and A.B. Theibert. 1996. Identification and cloning of centaurin-alpha. A novel phosphatidylinositol 3,4,5-trisphosphate-binding protein from rat brain. J. Biol. Chem. 271:18859-18868.
23. Hao, W., Z. Tan, K. Prasad, K.K. Reddy, J. Chen, G.D. Prestwich, J.R. Falck, S.B. Shears, and E.M. Lafer. 1997. Regulation of AP-3 function by inositides. Identification of phosphatidylinositol 3,4,5-trisphosphate as a potent ligand. J. Biol. Chem. 272:6393-639 8.
24. Hicke, L., and H. Riezman. 1996. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell. 84:277-287.
25. Hein, C., J.Y. Springael, C. Volland, R. Haguenauer-Tsapis, and B. Andre. 1995. NPI1, an essential yeast gene involved in induced degradation of Gap1p and Fur4p permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18:77-87.
26. Holtzman, D.A., S. Yang, and D.G. Drubin. 1993. Synthetic lethal interactions identify two novel genes, SLA1 and SLA2, that control membrane cytoskeleton assembly in Saccharomyces cerevisiae. J. Cell Biol. 122:635-644.
27. Janmey, P.A., K. Iida, H.L. Yin, and T.P. Stossel. 1987. Polyphosphoinositide micells and polyphosphoinositide-containing vesicles dissociate endogenous gelsolin-actin complexes and promote actin assembly from the fast-growing end of actin filaments blocked by gelsolin. J. Biol. Chem. 262:12228-12236.
28. Keen, J.H., and M.M. Black. 1986. The phosphorylation of coated membrane proteins in intact neurons. J. Cell Biol. 102:1325-1333.
29. Kilmartin, J.V., and A.E. Adams. 1984. Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. J. Cell Biol. 98: 922-933.
30. Kohtz, D.S., and S. Puszkin. 1988. A neuronal protein (NP185) associated with clathrin-coated vesicles. Characterization of NP185 with monoclonal antibodies. J. Biol. Chem. 263:7418-7425.
31. Kolling, R., and C.P. Hollenberg. 1994. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO (Eur. Mol. Biol. Organ.) J. 13:3261-3271.
32. Kubler, E., and H. Riezman. 1993. Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO (Eur. Mol. Biol. Organ.) J. 12: 2855-2862.
33. Lamaze, C., L.M. Fujimoto, H.L. Yin, and S.L. Schmid. 1997. The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J. Biol. Chem. 272:20332-20335.
34. Lappalainen, P., and D.G. Drubin. 1997. Cofilin promotes rapid actin filament turnover in vivo. Nature. 388:78-82.
35. Lemmon, S., V.P. Lemmon, and E.W. Jones. 1988. Characterization of yeast clathrin and anticlathrin heavy-chain monoclonal antibodies. J. Cell Biochem. 36:329-340.
36. Lichte, B., R.W. Veh, H.E. Meyer, and M.W. Kilimann. 1992. Amphiphysin, a novel protein associated with synaptic vesicles. EMBO (Eur. Mol. Biol. Organ.) J. 11:2521-2530.
37. Linn, H., K.S. Ermekova, S. Rentschler, A.B. Sparks, B.K. Kay, and M. Sudol. 1997. Using molecular repertoires to identify high-affinity peptide ligands of the WW domain of human and mouse YAP. Biol. Chem. 378:531-537.
38. Luo, W., and A. Chang. 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.
39. Maniatas, T., E.F. Fritsch, and J. Sambrook. 1982. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Marcusson, E.G., B.F. Horazdovsky, J.L. Cereghino, E. Gharakhanian, and S.D. Emr. 1994. The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell. 77:579-586.
41. McPherson, P.S., E.P. Garcia, V.I. Slepnev, C. David, X. Zhang, D. Grabs, W.S. Sossin, R. Bauerfeind, Y. Nemoto, and P. De Camilli. 1996. A presynaptic inositol-5-phosphatase. Nature. 379:353-357.
42. Morris, S.A., A. Mann, and E. Ungewickell. 1990. Analysis of 100-180 kDa phosphoproteins in clathrin-coated vesicles from bovine brain. J. Biol. Chem. 265:3354-3357.
43. Morris, S.A., S. Schroder, U. Plessmann, K. Weber, and E. Ungewickell. 1993. Clathrin assembly protein AP180: primary structure, domain organization and identification of a clathrin binding site. EMBO (Eur. Mol. Biol. Organ.) J. 12:667-675.
44. Mueller, S.C., and D. Branton. 1984. Identification of coated vesicles in Saccharomyces cerevisiae. J. Cell Biol. 98:341-346.
45. Mulholland, J., D. Preuss, A. Moon, A. Wong, D. Drubin, and D. Botstein. 1994. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J. Cell Biol. 125:381-391.
46. Munn, A.L., and H. Riezman. 1994. Endocytosis is required for the growth of vacuolar H(+)-ATPase-defective yeast: identification of six new END genes. J. Cell Biol. 127:373-386.
47. Munn, A.L., B.J. Stevenson, M.I. Geli, and H. Riezman. 1995. end5, end6, and end7: mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell. 6:1721-1742.
48. Murphy, J.E., I.T. Pleasure, S. Puszkin, K. Prasad, and J.H. Keen. 1991. Clathrin assembly protein AP-3. The identity of the 155K protein, AP 180, and NP185 and demonstration of a clathrin binding domain. J. Biol. Chem. 266:4401-1408.
49. Myers, M.G. Jr., X.J. Sun, and M.F. White. 1994. The IRS-1 signaling system. Trends Biochem. Sci. 19:289-293.
50. Norris, F.A., E. Ungewickell, and P.W. Majerus. 1995. Inositol hexakisphosphate binds to clathrin assembly protein 3 (AP-3/AP180) and inhibits clathrin cage assembly in vitro. J. Biol. Chem. 270:214-217.
51. Payne, G.S., and R. Schekman. 1985. A test of clathrin function in protein secretion and cell growth. Science. 230:1009-1014.
52. Pearse, B.M., and M.S. Robinson. 1990. Clathrin, adaptors, and sorting. Annu. Rev. Cell Biol. 6:151-171.
53. Perry, D.G., V. Hanson, M.L. Benuck, and S. Puszkin. 1991. Neuronal protein NP185 in avian and murine cerebellum: expression during development and evidence for its presence in nerve endings. J. Histochem. Cytochem. 39:1461-1470.
54. Perry, D.G., S. Li, V. Hanson, and S. Puszkin. 1992. Neuromuscular junctions contain NP185: the multifunctional protein is located at the presynaptic site. J. Neurosci. Res. 33:408-417.
55. Phan, H.L., J.A. Finlay, D.S. Chu, P.K. Tan, T. Kirchhausen, and G.S. Payne. 1994. The Saccharomyces cerevisiae APS1 gene encodes a homolog of the small subunit of the mammalian clathrin AP-1 complex: evidence for functional interaction with clathrin at the Golgi complex. EMBO (Eur. Mol. Biol. Organ.) J. 13:1706-1717.
56. Prasad, K., and R.E. Lippoldt. 1988. Molecular characterization of the AP180 coated vesicle assembly protein. Biochemistry. 27:6098-6104.
57. Rad, M.R., H.L. Phan, L. Kirchrath, P.K. Tan, T. Kirchausen, C.P. Hollenberg, and G.S. Payne. 1995. Saccharomyces cerevisiae Apl2p, a homologue of the mammalian clathrin AP beta subunit, plays a role in clathrin-dependent Golgi functions. J. Cell Sci. 108:1605-1615.
58. 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.
59. Ren, R., B.J. Mayer, P. Cicchetti, and D. Baltimore. 1993. Identification of a ten-amino acid proline-rich SH3 binding site. Science. 259:1157-1161.
60. 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.
61. Robinson, M.S. 1997. Coats and budding vesicles. Trends Cell Biol. 7:99-102.
62. Roth, A.F., and N.G. Davis. 1996. Ubiquitination of the yeast a-factor receptor. J. Cell Biol. 134:661-674.
63. Rothman, J.E., and L. Orci. 1992. Molecular dissection of the secretory pathway. Nature. 355:409-415.
64. Sachs, A.B., and J.A. Deardorff. 1992. Translation initiation requires the PAB-dependent poly(A) ribonuclease in yeast. Cell. 70:961-973.
65. Sakisaka, T., T. Itoh, K. Miura, and T. Takenawa. 1997. Phosphatidylinositol 4,5-bisphosphate phosphatase regulates the rearrangement of actin filaments. Mol. Cell Biol. 17:3841-3849.
66. Salcini, A.E., S. Confalonieri, M. Doria, E. Santolini, E. Tassi, O. Minenkova, G. Cesareni, P.G. Pelicci, and P.P. Di Fiore. 1997. Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module. Genes Dev. 11:2239-2249.
67. Schekman, R., and L. Orci. 1996. Coal proteins and vesicle budding. Science. 271:1526-1533.
68. Schmid, S.L. 1997. Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66:511-548.
69. Silveira, L.A., D.H. Wong, F.R. Masiarz, and R. Schekman. 1990. Yeast clathrin has a distinctive light chain that is important for cell growth. J. Cell Biol. 111:1437-1449.
70. Sivadon, P., F. Bauer, M. Aigle, and M. Crouzet. 1995. Actin cytoskeleton and budding pattern are altered in the yeast rvs161 mutant: the Rvs161 protein shares common domains with the brain protein amphiphysin. Mol. Gen. Genet. 246:485-495.
71. Smith, D.B., and K.S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 67:31-40.
72. Sousa, R., N.H. Tannery, S. Zhou, and E.M. Lafer. 1992. Characterization of a novel synapse-specific protein. I. Developmental expression and cellular localization of the F1-20 protein and mRNA. J. Neurosci. 12:2130-2143.
73. Srinivasan, S., M. Seaman, Y. Nemoto, L. Daniell, S. Emr, P. De Camilli, and R. Nussbaum. 1997. Disruption of three phosphatidyl-polyphosphate 5-phosphatase genes from Saccharomyces cerevisiae results in pleiotropic abnormalities of vacuole morphology, cell shape, and osmohomeostasis. Eur. J. Cell Biol. 74:350-360.
74. Strous, G.J., P. van Kerkhof, R. Govers, A. Ciechanover, and A.L. Schwartz. 1996. The ubiquitin conjugation system is required for ligand-induced endocytosis and degradation of the growth hormone receptor. EMBO (Eur. Mol. Biol. Organ.) J. 15:3806-3812.
75. Sudol, M. 1996. The WW module competes with the SH3 domain? Trends Biochem. Sci. 21:161-163.
76. Sudol, M., H.I. Chen, C. Bougeret, A. Einbond, and P. Bork. 1995. Characterization of a novel protein-binding module - the WW domain. FEBS Lett. 369:67-71.
77. Takei, K., O. Mundigl, L. Daniell, and P. De Camilli. 1996. The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J. Cell Biol. 133:1237-1250.
78. Tan, P.K., N.G. Davis, G.F. Sprague, and G.S. Payne. 1993. Clathrin facilitates the internalization of seven transmembrane segment receptors for mating pheromones in yeast. J. Cell Biol. 123:1707-1716.
79. Tan, P.K., J.P. Howard, and G.S. Payne. 1996. The sequence NPFXD defines a new class of endocytosis signal in Saccharomyces cerevisiae. J. Cell Biol. 135: 1789-1800.
80. Tang, H.Y., and M. Cai. 1996. The EH-domain-containing protein Pan1 is required for normal organization of the actin cytoskeleton in Saccharomyces cerevisiae. Mol. Cell Biol. 16:4897-4914.
81. 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.
82. Tebar, F., S. Confalonieri, R.E. Carter, P.P. Di Fiore, and A. Sorkin. 1997. Eps15 is constitutively oligomerized due to homophilic interaction of its coiled-coil region. J. Biol. Chem. 272:15413-15418.
83. Vallee, R.B., J.S. Herskovits, J.G. Aghajanian, C.C. Burgess, and H.S. Shpetner. 1993. Dynamin, a GTPase involved in the initial stages of endocytosis. Ciba Found Symp. 176:185-197.
84. van Delft, S., R. Govers, G.J. Strous, A.J. Verkleij, and P.M. van Bergen en Henegouwen. 1997a. Epidermal growth factor induces ubiquitination of Eps15. J. Biol. Chem. 272:14013-14016.
85. van Delft, S., C. Schumacher, W. Hage, A.J. Verkleij, and P.M. van Bergen en Henegouwen. 1997b. Association and colocalization of Eps15 with adaptor protein-2 and clathrin. J. Cell Biol. 136:811-821.
86. Wendland, B., J.M. McCaffery, Q. Xiao, and S.D. Emr. 1996. A novel fluorescence-activated cell sorter-based screen for yeast endocytosis mutants identifies a yeast homologue of mammalian eps15. J. Cell Biol. 135:1485-1500.
87. Wilson, R., R. Ainscough, K. Anderson, C. Baynes, M. Berks, J. Bonfield, J. Burton, M. Connell, T. Copsey, J. Cooper et al., 1994. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature. 368:32-38.
88. Wong, W.T., C. Schumacher, A.E. Salcini, A. Romano, P. Castagnino, P.G. Pelicci, and P. Di Fiore. 1995. A protein-binding domain, EH, identified in the receptor tyrosine kinase substrate Eps15 and conserved in evolution. Proc. Natl. Acad. Sci. USA. 92:9530-9534.
89. Ye, W., and E.M. Lafer. 1995. Clathrin binding and assembly activities of expressed domains of the synapse-specific clathrin assembly protein AP-3. J. Biol. Chem. 270:10933-10939.
90. Ye, W., N. Ali, M.E. Bembenek, S.B. Shears, and E.M. Lafer. 1995. Inhibition of clathrin assembly by high affinity binding of specific inositol polyphosphates to the synapse-specific clathrin assembly protein AP-3. J. Biol. Chem. 270:1564-1568.
91. Yonezawa, N., E. Nishida, K. Iida, I. Yahara, and H. Sakai. 1990. Inhibition of the interactions of cofilin, destrin, and deoxyribonuclease I with actin by phosphoinositides. J. Biol. Chem. 265:8382-8386.
92. Yu, H., J.K. Chen, S. Feng, D.C. Dalgarno, A.W. Brauer, and S.L. Schreiber. 1994. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell. 76:933-945.
93. Zhou, S., R. Sousa, N.H. Tannery, and E.M. Lafer. 1992. Characterization of a novel synapse-specific protein. II. cDNA cloning and sequence analysis of the F1-20 protein. J. Neurosci. 12:2144-2155.
94. Zhou, S., N.H. Tannery, J. Yang, S. Puszkin, and E.M. Lafer. 1993. The synapse-specific phosphoprotein F1-20 is identical to the clathrin assembly protein AP-3. J. Biol. Chem. 268:12655-12662.
95. 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.