Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits

Journal of Cell Biology

Volumn 146, Issue 4, 1999, Pages 755-764

  Gaidarov, Ibragim ^a   Keen, James H ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Adaptins; Adaptor; Clathrin; Endocytosis; Phosphatidylinositols

Indexed keywords

ADAPTOR PROTEIN; CLATHRIN; PHOSPHATIDYLINOSITIDE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL MEMBRANE; ENDOCYTOSIS; INTERNALIZATION; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS;

ADAPTOR PROTEIN COMPLEX ALPHA SUBUNITS; ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; BIOLOGICAL TRANSPORT; BRAIN; CATTLE; CELL LINE; CELL MEMBRANE; CIRCULAR DICHROISM; CLATHRIN; COATED PITS, CELL-MEMBRANE; GLUTAMINE; LYSINE; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHATIDYLINOSITOLS; PROTEIN STRUCTURE, SECONDARY; SEQUENCE DELETION; TRANSFECTION;

ANIMALIA; MAMMALIA;

EID: 0033598129     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.146.4.755     Document Type: Article

References (77)

1. Ahle, S., A. Mann, U. Eichelsbacher, and E. Ungewickell. 1988. Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO (Eur. Mol. Biol. Organ.) J. 7:919-929.
2. Andrade, M.A., P. Chacon, J.J. Merelo, and F. Moran. 1993. Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng. 6:383-390.
3. Barylko, B., D. Binns, K. Lin, M.A. Atkinson, D.M. Jameson, H.L. Yin, and J.P. Albanesi. 1998. Synergistic activation of dynamin GTPase by Grb2 and phosphoinositides. J. Biol. Chem. 273:3791-3797.
4. Beck, K.A., and J.H. Keen. 1991. Interaction of phosphoinositide cycle intermediates with the plasma membrane-associated clathrin assembly protein AP-2. J. Biol. Chem. 266:4442-4447.
5. 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.
6. Boll, W., H. Ohno, Z. Songyang, I. Rapoport, L.C. Cantley, J.S. Bonifacino, and T. Kirchhausen. 1996. Sequence requirements for the recognition of tyrosine-based endocytic signals by clathrin AP-2 complexes. EMBO (Eur. Mol. Biol. Organ.) J. 15:5789-5795.
7. Brown, W.J., D.B. DeWald, S.D. Emr, H. Plutner, and W.E. Balch. 1995. Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells. J. Cell Biol. 130:781-796.
8. Chaudhary, A., Q.M. Gu, O. Thum, A.A. Profit, Y. Qi, L. Jeyakumar, S. Fleischer, and G.D. Prestwich. 1998. Specific interaction of Golgi coatomer protein alpha-Cop with phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 273:8344-8350.
9. 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.
10. Davidson, H.W. 1995. Wortmannin causes mistargeting of procathepsin D. Evidence for the involvement of a phosphatidylinositol 3-kinase in vesicular transport to lysosomes. J. Cell Biol. 130:797-805.
11. Donaldson, J.G., D. Cassel, R.A. Kahn, and R.D. Klausner. 1992. ADP-ribosylation factor, a small GTP-binding protein, is required for binding of the coatomer protein beta-COP to Golgi membranes. Proc. Natl. Acad. Sci. USA. 89:6408-6412.
12. Ferguson, S.S., W.E. Downey, Jr., A.M. Colapietro, L.S. Barak, L. Menard, and M.G. Caron. 1996. Role of beta-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science. 271:363-366.
13. Fleischer, B., J. Xie, M. Mayrleitner, S.B. Shears, D.J. Palmer, and A. Fleischer. 1994. Golgi coatomer binds, and forms K(+)-selective channels gated by, inositol polyphosphates. J. Biol. Chem. 269:17826-17832.
14. Fukuda, M., J. Aruga, M. Niinobe, S. Aimoto, and K. Mikoshiba. 1994. Inositol1,3,4,5-tetrakisphosphate binding to C2B domain of IP4BP/synaptotagmin II. J. Biol. Chem. 269:29206-29211.
15. Fukuda, M., T. Kojima, J. Aruga, M. Niinobe, and K. Mikoshiba. 1995. Functional diversity of C2 domains of synaptotagmin family. Mutational analysis of inositol high polyphosphate binding domain. J. Biol. Chem. 270:26523-26527.
16. Fukuda, M., and K. Mikoshiba. 1997. The function of inositol high polyphosphate binding proteins. Bioessays. 19:593-603.
17. Gaidarov, I., Q. Chen, J.R. Falck, K.K. Reddy, and J.H. Keen. 1996. A functional phosphatidylinositol 3,4,5-trisphosphate/phosphoinositide binding domain in the clathrin adaptor AP-2 alpha subunit. Implications for the endocytic pathway [published erratum appears in J. Biol. Chem. 271:27188]. J. Biol. Chem. 271:20922-20929.
18. Gaidarov, I., J.G. Krupnick, J.R. Falck, J.L. Benovic, and J.H. Keen. 1999. Arrestin function in G protein-coupled receptor endocytosis requires phosphoinositide binding. EMBO (Eur. Mol. Biol. Organ.) J. 18:871-881.
19. Gaidarov, I., F. Santini, R.A. Warren, and J.H. Keen. 1999. Spatial control of coated-pit dynamics in living cells. Nat. Cell Biol. 1:1-7.
20. 2+ influx dependence for ligand-stimulated internalization of the C-kit receptor. J. Biol. Chem. 272:30519-30525.
21. Goodman, O.B., Jr., and J.H. Keen. 1995. The alpha chain of the AP-2 adaptor is a clathrin binding subunit. J. Biol. Chem. 270:23768-23773.
22. Goodman, O.B., Jr., J.G. Krupnick, F. Santini, V.V Gurevich, R.B. Penn, A.W. Gagnon, J.H. Keen, and J.L. Benovic. 1996. Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor. Nature. 383:447-450.
23. Haffner, C. K. Takei, H. Chen, N. Ringstad, A. Hudson, M.H. Butler, A.E. Salcini, P.P. Di Fiore, and P. De Camilli. 1997. Synaptojanin 1: localization on coated endocytic intermediates in nerve terminals and interaction of its 170 kDa isoform with Eps15. FEBS Lett. 419:175-180.
24. Hao, W., A. 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. 272:6393-6398.
25. Heilker, R., U. Manning-Krieg, J.F. Zuber, and M. Spiess. 1996. In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting. EMBO (Eur. Mol. Biol. Organ.) J. 15:2893-2899.
26. Hyvonen, M., M.J. Macias, M. Nilges, H. Oschkinat, M. Saraste, and M. Wilmanns. 1995. Structure of the binding site for inositol phosphates in a PH domain. EMBO (Eur. Mol. Biol. Organ.) J. 14:4676-4685.
27. Iannolo, G., A.E. Salcini, I. Gaidarov, O.B. Goodman, Jr., J. Baulida, G. Carpenter, P.G. Pelicci, P.P. Di Fiore, and J.H. Keen. 1997. Mapping of the molecular determinants involved in the interaction between eps15 and AP-2. Cancer Res. 57:240-245.
28. Janmey, P.A., J. Lamb, P.G. Alle, and P.T. Matsudaira. 1992. Phosphoinositide-binding peptides derived from the sequences of gelsolin and villin. J. Biol. Chem. 267:11818-11823.
29. Joly, M., A. Kazlauskas, and S. Corvera. 1995. Phosphatidylinositol 3-kinase activity is required at a postendocytic step in platelet-derived growth factor receptor trafficking. J. Biol. Chem. 270:13225-13230.
30. Joly, M., A. Kazlauskas, F.S. Fay, and S. Corvera. 1994. Disruption of PDGF receptor trafficking by mutation of its PI-3 kinase binding sites. Science. 263: 684-687.
31. Jones, S.M., and K.E. Howell. 1997. Phosphatidylinositol 3-kinase is required for the formation of constitutive transport vesicles from the Tgn. J. Cell Biol. 139:339-349.
32. Jost, M., F. Simpson, J.M. Kavran, M.A. Lemmon, and S.L. Schmid. 1998. Phosphatidylinositol-4,5-bisphosphate is required for endocytic coated vesicle formation. Curr. Biol. 8:1399-1402.
33. Keen, J.H. 1987. Clathrin assembly proteins: affinity purification and a model for coat assembly. J. Cell Biol. 105:1989-1998.
34. Keen, J.H. 1990. Clathrin and associated assembly and disassembly proteins. Annu. Rev. Biochem. 59:415-138.
35. Ktistakis, N.T., H.A. Brown, M.G. Waters, P.C. Sternweis, and M.G. Roth. 1996. Evidence that phospholipase D mediates ADP ribosylation factor-dependent formation of Golgi coated vesicles. J. Cell Biol. 134:295-306.
36. Lemmon, M.A., and K.M. Ferguson. 1998. Pleckstrin homology domains. Curr. Topics Microbiol. Immunol. 228:39-74.
37. 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.
38. Moore, M.S., D.T. Mahaffey, F.M. Brodsky, and R.G. Anderson. 1987. Assembly of clathrin-coated pits onto purified plasma membranes. Science. 236: 558-563.
39. Niinobe, M., Y. Yamaguchi, M. Fukuda, and K. Mikoshiba. 1994. Synaptotagmin is an inositol polyphosphate binding protein: isolation and characterization as an Ins 1,3,4,5-P4 binding protein. Biochem. Biophys. Res. Commun. 205: 1036-1042.
40. Ohno, H., J. Stewart, M.C. Fournier, H. Bosshart, I. Rhee, S. Miyatake, T. Saito, A. Gallusser, T. Kirchhausen, and J.S. Bonifacino. 1995. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science. 269: 1872-1875.
41. Okabayashi, Y., Y. Sugimoto, N.F. Totty, J. Hsuan, Y. Kido, K. Sakaguchi, I. Gout, M.D. Waterfield, and M. Kasuga. 1996. Interaction of Shc with adaptor protein adaptins. J. Biol. Chem. 271:5265-5269.
42. Page, L.J., and M.S. Robinson. 1995. Targeting signals and subunit interactions in coated vesicle adaptor complexes. J. Cell Biol. 131:619-630.
43. Palmer, D.J., J.B. Helms, C.J. Beckers, L. Orci, and J.E. Rothman. 1993. Binding of coatomer to Golgi membranes requires ADP-ribosylation factor. J. Biol. Chem. 268:12083-12089.
44. Prasad, K., and J.H. Keen. 1991. Interaction of AP-2 and its isolated subunits with clathrin. Biochemistry. 30:5590-5597.
45. Raghunathan, V., P. Mowery, M. Rozycki, U. Lindberg, and C. Schutt. 1992. Structural changes in profilin accompany its binding to phosphatidylinositol, 4,5-bisphosphate. FEBS Lett. 297:46-50.
46. Rapoport, I., Y.C. Chen, P. Cupers, S.E. Shoelson, and T. Kirchhausen. 1998. Dileucine-based sorting signals bind to the beta chain of Ap-1 at a site distinct and regulated differently from the tyrosine-nased motif-binding site. EMBO (Eur. Mol. Biol. Organ.) J. 17:2148-2155.
47. Robinson, M.S. 1989. Cloning of cDNAs encoding two related 100-kD coated vesicle proteins (alpha-adaptins). J. Cell Biol. 108:833-842.
48. Robinson, M.S. 1993. Assembly and targeting of adaptin chimeras in transfected cells. J. Cell Biol. 123:67-77.
49. Rodionov, D.G., and O. Bakke. 1998. Medium chains of adaptor complexes AP-1 and AP-2 recognize leucine-based sorting signals from the invariant chain. J. Biol. Chem. 273:6005-6008.
50. Salim, K., M.J. Bottomley, E. Querfurth, M.J. Zvelebil, I. Gout, R. Scaife, R.L. Margolis, R. Gigg, C.I. Smith, P.C. Driscoll, M.D. Waterfield, and G. Panay-otou. 1996. Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO (Eur. Mol. Biol. Organ.) J. 15:6241-6250.
51. Santini, F., and J.H. Keen. 1996. Endocytosis of activated receptors and clathrin-coated pit formation: deciphering the chicken or egg relationship. J. Cell Biol. 132:1025-1036.
52. Santini, F., M.S. Marks, and J.H. Keen. 1998. Endocytic clathrin-coated pit formation is independent of receptor internalization signal levels. Mol. Biol. Cell. 9:1177-1194.
53. Schiavo, G., Q.M. Gu, G.D. Prestwich, T.H. Sollner, and J.E. Rothman. 1996. Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin [published erratum appears in Proc. Natl. Acad. Sci. USA. 94:1047]. Proc. Natl. Acad. Sci. USA. 93:13327-13332.
54. Schmid, S.L. 1997. Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66:511-548.
55. Schu, P.V., K. Takegawa, M.J. Fry, J.H. Stack, M.D. Waterfield, and S.D. Emr. 1993. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science. 260:88-91.
56. Shaw, G. 1996. The pleckstrin homology domain: an intriguing multifunctional protein module. Bioessays. 18:35-46.
57. Shih, W., A. Gallusser, and T. Kirchhausen. 1995. A clathrin-binding site in the hinge of the beta 2 chain of mammalian AP-2 complexes. J. Biol. Chem. 270: 31083-31090.
58. Shiratori, T., S. Miyatake, H. Ohno, C. Nakaseko, K. Isono, J.S. Bonifacino, and T. Saito. 1997. Tyrosine phosphorylation controls internalization of CTLA-4 by regulating its interaction with clathrin-associated adaptor complex AP-2. Immunity. 6:583-589.
59. Sohn, R.H., J. Chen, K.S. Koblan, P.F. Bray, and P.J. Goldschmidt-Clermont. 1995. Localization of a binding site for phosphatidylinositol 4,5-bisphosphate on human profilin. J. Biol. Chem. 270:21114-21120.
60. Sonnichsen, F.D., J.E. Van Eyk, R.S. Hodges, and B.D. Sykes. 1992. Effect of trifluoroethanol on protein secondary structure: an NMR and CD study using a synthetic actin peptide. Biochemistry. 31:8790-8798.
61. Sorkin, A., T. McKinsey, W. Shih, T. Kirchhausen, and G. Carpenter. 1995. Stoichiometric interaction of the epidermal growth factor receptor with the clathrin-associated protein complex AP-2. J. Biol. Chem. 270:619-625.
62. Stack, J.H., and S.D. Emr. 1994. Vps34p required for yeast vacuolar protein sorting is a multiple specificity kinase that exhibits both protein kinase and phosphatidylinositol-specific PI 3-kinase activities. J. Biol. Chem. 269:31552-31562.
63. Stack, J.H., P.K. Herman, P.V. Schu, and S.D. Emr. 1993. A membrane-associated complex containing the Vps15 protein kinase and the Vps34 PI 3-kinase is essential for protein sorting to the yeast lysosome-like vacuole. EMBO (Eur. Mol. Biol. Organ.) J. 12:2195-2204.
64. Stamnes, M., G. Schiavo, G. Stenbeck, T.H. Sollner, and J.E. Rothman. 1998. ADP-ribosylation factor and phosphatidic acid levels in Golgi membranes during budding of coatomer-coated vesicles. Proc. Natl. Acad. Sci. USA. 95: 13676-13680.
65. Subtil, A., I. Gaidarov, K. Kubylarz, J.H. Keen, and T.E. McGraw. 1999. Acute cholesterol-depletion inhibits clathrin-coated pit budding. Proc. Natl. Acad. Sci. USA. 96:6775-6780.
66. Timerman, A.P., M.M. Mayrleitner, T.J. Lukas, C.C. Chadwick, A. Saito, D.M. Watterson, H. Schindler, and S. Fleischer. 1992. Inositol polyphosphate receptor and clathrin assembly protein AP-2 are related proteins that form potassium-selective ion channels in planar lipid bilayers. Proc. Natl. Acad. Sci. USA. 89:8976-8980.
67. Voglmaier, S.M., J.H. Keen, J.E. Murphy, C.D. Ferris, G.D. Prestwich, S.H. Snyder, and A.B. Theibert. 1992. Inositol hexakisphosphate receptor identified as the clathrin assembly protein AP-2. Biochem. Biophys. Res. Commun. 187:158-163.
68. Wang, L.H., T.C. Sudhof, and R.G. Anderson. 1995. The appendage domain of alpha-adaptin is a high affinity binding site for dynamin. J. Biol. Chem. 270: 10079-10083.
69. West, M.A., N.A. Bright, and M.S. Robinson. 1997. The role of ADP-ribosylation factor and phospholipase D in adaptor recruitment. J. Cell Biol. 138: 1239-1254.
70. Wilde, A., and F.M. Brodsky. 1996. In vivo phosphorylation of adaptors regulates their interaction with clathrin. J. Cell Biol. 135:635-645.
71. Willingham, M.C., J.H. Keen, and I.H. Pastan. 1981. Ultrastructural immunocytochemical localization of clathrin in cultured fibroblasts. Exp. Cell Res. 132: 329-338.
72. Woscholski, R., P.M. Finan, E. Radley, N.F. Totty, A.E. Sterling, J.J. Hsuan, M.D. Waterfield, and P.J. Parker. 1997. Synaptojanin is the major constitutively active phosphatidylinositol-3,4,5-trisphosphate 5-phosphatase in rodent brain. J. Biol. Chem. 272:9625-9628.
73. 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.
74. Yu, F.X., H.Q. Sun, P.A. Janmey, and H.L. Yin. 1992. Identification of a polyphosphoinositide-binding sequence in an actin monomer-binding domain of gelsolin. J. Biol. Chem. 267:14616-14621.
75. Zaremba, S., and J.H. Keen. 1985. Limited proteolytic digestion of coated vesicle assembly polypeptides abolishes reassembly activity. J. Cell. Biochem. 28: 47-58.
76. Zhang, J.Z., B.A. Davletov, T.C. Sudhof, and R.G. Anderson. 1994. Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell. 78:751-760.
77. Zheng, J., S.M. Cahill, M.A. Lemmon, D. Fushman, J. Schlessinger, and D. Cowburn. 1996. Identification of the binding site for acidic phospholipids on the pH domain of dynamin: implications for stimulation of GTPase activity. J. Mol. Biol. 255:14-21.