Linking cargo to vesicle formation: Receptor tail interactions with coat proteins

Current Opinion in Cell Biology

Volumn 9, Issue 4, 1997, Pages 488-495

  Kirchhausen, Tomas ^a   Bonifacino, Juan S ^b   Riezman, Howard ^c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; RETINA S ANTIGEN; TRANSCRIPTION FACTOR AP 2;

COATED VESICLE; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; INTERNALIZATION; LIGAND BINDING; MEMBRANE VESICLE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN TRANSPORT; REVIEW;

EID: 0030794182     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(97)80024-5     Document Type: Article

References (59)

1. Kirchhausen T: Coated pits and vesicles - sorting it all out Curr Opin Struct Biol 1993, 3:182-188.
2. Robinson MS: Adaptins. Trends Cell Biol 1992, 2:293-297.
3. Robinson MS: The role of clathrin, adaptors and dynamin in endocytosis. Curr Opin Cell Biol 1994, 6:538-544.
4. Kirchhausen T: Identification of a putative yeast homolog of the mammalian beta chains of the clathrin-associated protein complexes. Mol Cell Biol 1990, 10:6089-6090.
5. Stepp JD, Pellicena-Palle A, Kirchhausen T, Lemmon SK A late secretory sorting function from Saccharomyces cerevicae Apm1p, but not for Apm2p, a second yeast clathrin AP medium chain-related protein. Mol Biol Cell 1995, 6:41-58.
6. Dell'Angelica EC, Ohno H, Ooi CE, Rabinovich E, Roche KW, Bonifacino JS: AP-3: an adaptor-like protein complex with ubiquitous expression. EMBO J 1997, 16:917-928. Reports the existence of a rovel adaptor-like complex (AP-3) that is expressed in all cells; the complex has a subunit structure that is similar to that of AP-1 and AP-2. See also [7*].
7. Simpson F, Peden AA, Christopoulou L, Robinson MS: Characterization of the adaptor-related protein complex, AP-3. J Cell Biol 1997, 137:835-845. Describes the AP-3 complex. See also [6*].
8. Stamnes MA, Rothman JE: The binding of AP-1 clathrin adaptor complexes to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein. Cell 1993, 73:999-1005.
9. Traub LM, Ostrom JA, Kornfeld S: Biochemical dissection of AP-1 recruitment onto Golgi membranes. J Cell Biol 1993, 123:561-573.
10. Le Borgne R, Griffiths G, Hoflack B: Mannose 6-phosphate receptors and ADP-ribosylation factors cooperate for high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J Biol Chem 1996, 271:2162-2170.
11. Salamero J, Le Borgne R, Saudrais C, Goud B, Hoflack B: Expression of major histocompatibility complex class I molecules on HeLa cells promotes the recruitment of AP-1 Golgi-specific assembly proteins on Golgi membranes. J Biol Chem 1996, 271:30318-30321.
12. Mallet WG, Brodsky RM: A membrane-associated protein complex with selective binding to the clathrin coat adaptor AP1. J Cell Sci 1996, 109:3059-3068.
13. Seaman MN, Sowerby PJ, Robinson MS: Cytosolic and membrane-associated proteins involved in the recruitment of AP-1 adaptors onto the trans-Golgi network. J Biol Chem 1996, 271:25446-25451.
14. Vigers GP, Crowther RA, Pearse BM: Location of the 100 kd-50 kd accessory proteins in clathrin coats. EMBO J 1986, 5:2079-2085.
15. Gallusser A, Kirchhausen T: The β1 and β2 subunits of the AP complexes are the clathrin coat assembly components. EMBO J 1993, 12:5237-5244.
16. Shih W, Gallusser A, Kirchhausen T: A clathrin-binding site in the hinge of the beta-2 chain of mammalian AP-2 complexes. J Biol Chem 1995, 270:31083-31090.
17. Wilde A, Brodsky FM: In vivo phosphorylation of adaptors regulates their interaction with clathrin. J Cell Biol 1996, 135:635-645. Shows that cytosolic but not membrane-bound subunits of AP-2 (subunits α, β2 and μ2) are phosphorylated in vivo. Phosphorylated AP-2 failed to bind in vitro to preformed clathrin cages, suggesting that phosphorylation may regulate recruitment of clathrin to the plasma membrane.
18. Goodman OB Jr, Keen JH: The α chain of the AP-2 adaptor is a clathrin binding subunit J Biol Chem 1995, 270:23768-23773.
19. Dell'Angelica EC, Ooi CE, Bonifacino JS: β3A-adaptin: a subunit of the adaptor-like complex AP-3. J Biol Chem 1997, 272:15078-15084.
20. Fazioli F, Minichiello L, Matoskova B, Wong WT, DiFiore PP: Eps15, a novel tyrosine kinase substrate, exhibits transforming activity. Mol Cell Biol 1993, 13:5814-5828.
21. Benmerah A, Bègue B, Dautry-Varsat A, Cerf-Bensussan N: The ear of alpha-adaptin interacts with the COOH-terminal domain of the Eps15 protein. J Biol Chem 1996, 271:12111-12116.
22. Tebar F, Sorkina T, Sorkin A, Ericsson M, Kirchhausen T: Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits. J Biol Chem 1996, 271:28727-28730.
23. Vandelft S, Schumacher C, Hage W, Verkleij AJ, Henegouwen P: Association and colocalization of Eps15 with adaptor protein-2 and clathrin. J Cell Biol 1997, 136:811-821.
24. Iannolo G, Salcini AE, Gaidorov I, Goodman OB, Baulida J, Carpenter G, Pelicci PG, DiFiore PP, Keen JH: Mapping of the molecular determinants involved in the interaction between Eps15 and AP-2. Cancer Res 1997, 57:240-245.
25. Bénédetti H, Raths S, Crausaz F, Riezman H: 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 1994, 5:1023-1037.
26. Wendland B, McCaffery JM, Xiao Q, Emr SD: A novel fluorescence-activated cell sorter-based screen for yeast endocytosis mutants identifies a yeast homologue of mammalian Eps15. J Cell Biol 1996, 135:1485-1500.
27. Tang HY, Cai M: The EH-domain-containing protein pan1 is required for normal organization of the actin cytoskeleton in Saccharomyces cerevisiae. Mol Cell Biol 1996, 16:4897-4914.
28. Schumacher C, Knudsen BS, Ohuchi T, DiFiore PP, Glassman RH, Hanafusa H: The SH3 domain of Crk binds specifically to a conserved proline-rich motif in Eps15 and Eps15R. J Biol Chem 1995, 270:15341-15347
29. Trowbridge IS, Collawn JF, Hopkins CR: Signal-dependent membrane protein trafficking in the endocytic pathway. Annu Rev Cell Biol 1993, 9:129-161.
30. Mellman I: Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 1996, 12:575-625.
31. Marks MS, Ohno H, Kirchhausen T, Bonifacino JS: Protein sorting by tyrosine-based signals: adapting to the Ys and wherefores. Trends Cell Biol 1997, 7:124-128.
32. Chen WJ, Goldstein JL, Brown MS: NPXY, a sequence often found in cytoplasmic tails is required for coated pit-mediated internalization of the low density lipoprotein receptor. J Biol Chem 1990, 265:3116-3123.
33. Canfield WM, Johnson KF, Ye RD, Gregory W, Kornfeld S7 Localization of the signal for rapid internalization of the bovine cation-independent mannose 6-phosphate/insulin-like growth factor-II receptor to amino acids 24-29 of the cytoplasmic tail. J Biol Chem 1991, 266:5682-5688.
34. Letourneur F, Klausner RD: A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CDS chains. Cell 1992, 69:1143-1157.
35. Voorhees P, Deignan E, van Donselaar E, Humphrey J, Marks MS, Peters PJ, Bonifacino JS: An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface. EMBO J 1995, 14:4961-4975.
36. Itin C, Kappeler F, Linstedt AD, Hauri HP: A novel endocytosis signal related to the KKXX ER-retrieval signal. EMBO J 1995, 14:2250-2256.
37. Hicke L, Riezman H: Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 1996, 6:1721-1742.
38. Grote E, Kelly RB: Endocytosis of VAMP is facilitated by a synaptic vesicle targeting signal. J Cell Biol 1996, 132:537-547
39. Glickman JN, Conibear E, Pearse BM: Specificity of binding of clathrin adaptors to signals on the mannose-6-phosphate/insulin-like growth factor II receptor. EMBO J 1989, 8:1041-1047.
40. Heilker R, Manning-Krieg U, Zuber JF, Spiess M: In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting. EMBO J 1996, 15:2893-2899. Shows that both tyrosine-based and dileucine-based receptor signals interact with the AP-1 and AP-2 adaptors.
41. Marks MS, Woodruff L, Ohno H, Bonifacino JS: Protein targeting by tyrosine- and di-leucine-based signals: evidence for distinct saturable components. J Cell Biol 1996, 135:341-354. Demonstrates that sorting processes mediated by both tyrosine-based and dileucine-based signals are saturable in vivo. However, tyrosine-based and dileucine-based signals do not compete with one another, suggesting that they bind to different sites of the sorting machinery.
42. Kornfeld S: Structure and function of the mannose 6-phosphate/insulinlike growth factor II receptors. Annu Rev Biochem 1992, 61:307-330.
43. Ohno H, Stewart J, Fournier MC, Bosshart H, Rhee I, Miyatake S, Saito T, Gallusser A, Kirchhausen T, Bonifacino JS: Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 1995, 269:1872-1875.
44. Honing S, Griffith J, Geuze HJ, Hunziker W: The tyrosine-based lysosomal targeting signal in lamp-1 mediates sorting into Golgi-derived ciathrin-coated vesicles. EMBO J 1996, 15:5230-5239. The cytosolic tail of the lysosomal membrane protein lamp-1, which contains a tyrosine-based sorting signal, is shown to interact with both the AP-1 and the AP-2 adaptors. In addition, the study shows that lamp-1 is concentrated in AP-1-containing vesicles in the TGN, suggesting that the protein can be transported to lysosomes from the TGN.
45. Rapoport I, Miyazali M, Boll W, Duckworth B, Cantley LC, Shoelson S, Kirchhausen T: Regulatory interactions in the recognition of endocytic sorting signals by AP-2 complexes. EMBO J 1997, 9:2240-2250. Demonstrates two ways by which the interaction of AP-2 with tyrosine-based sorting signals can be regulated. Phosphoinositide-3′-phosphate association with AP-2 or co-assembly of AP-2 with clathrin to form coats increases the affinity of AP-2 for tyrosine-based endocytic signals.
46. Boll W, Ohno H, Songyang Z, Rapoport I, Cantley LC, Bonifacino JS, Kirchhausen T: Sequence requirements for the recognition of tyrosine-based endocytic signals by clathrin AP-2 complexes. EMBO J 1996, 15:5789-5795. Screening of combinatorial libraries shows that both μ2 and AP-2 prefer to bind to YXXØ-type sorting signals that have arginine residues at the X positions. The sequence requirements for binding to μ2 and AP-2 are similar, further suggesting that μ2 is the signal-recognition component of AP-2.
47. Ohno H, Fournier MC, Poy G, Bonifacino JS: Structural determinants of interaction of tyrosine-based sorting signals with the adaptor medium chains. J Biol Chem 1996, 271:29009-29015. The authors of this paper used a yeast two-hybrid screen to examine the sequence factors that determine the avidity and specificity of interactions of tyrosine-based signals with isolated μ1, μ2, and μ3A. The authors demonstrate that both the exact sequence of the signal and its position within the receptor tail are important determinants of this interaction with isolated μ chains.
48. Shiratori T, Miyatake S, Ohno H, Nakaseko C, Bonifacino JS, Saito T: Tyrosine phosphorylation controls the internalization of CTLA4 by regulating its interaction with the clathrin-associated complex AP-2. Immunity 1997, in press. Shows that a tyrosine-based signal in the cytosolic tail of the CTLA4 T cell co-receptor can function as either an internalization signal recognized by μ2 or a binding site for SH2-containing signal transduction molecules depending on whether it is unphosphorylated or phosphorylated, respectively. Suggests that phosphorylation of the critical tyrosine residue functions as a switch to determine either internalization of CTLA4 or coupling of CTLA4 activation to signal transduction pathways.
49. Matsui W, Kirchhausen T: Stabilization of clathrin coats by the core of the clathrin-associated protein complex AP-2. Biochemistry 1990, 29:10791-10798.
50. 2-adrenergic receptor within clathrin-coated pits and subsequent internalization of the receptor.
51. Mizuno M, Singer SJ: A soluble secretory protein is first concentrated in the endoplasmic reticulum before transfer to the Golgi apparatus. Proc Natl Acad Sci USA 1993, 90:5732-5736.
52. Balch WE, McCaffery JM, Plutner H, Farquhar MG: Vesicular stomatitis virus glycoprotein is sorted and concentrated during export from the endoplasmic reticulum. Cell 1994, 76:841-852.
53. Schimmöller F, Singer-Krüger B, Schröder S, Krüger U, Barlowe C, Riezman H: The absence of Emp24p, a component of ER-derived COPII-coated vesicles, causes a defect in transport of selected proteins to the Golgi. EMBO J 1995, 14:1329-1339.
54. Elrod-Erickson MJ, Kaiser CA: Genes that control the fidelity of endoplasmic reticulum to Golgi transport identified as suppressors of vesicle budding mutations. Mol Biol Cell 1996, 7:1943-1058.
55. Stamnes MA, Craighead MW, Hoe MH, Lampen N, Geromanos S, Tempst P, Rothman JE: An integral membrane component of coatomer-coated transport vesicles defines a family of proteins involved in budding. Proc Natl Acad Sci USA 1995, 92:8011-8015.
56. Beiden WJ, Barlowe C: Erv25p, a component of COPII-coated vesicles, forms a complex with Emp24p that is required for efficient endoplasmic reticulum to Golgi transport J Biol Chem 1996, 271:26939-26946. This paper shows that two members of the Emp24 family form a complex and that deletion of EMP24 causes another member, Erv25p, to become unstable. The authors also show directly that membranes without Emp24p or Erv25p form ER-derived COPII-coated vesicles as well as do wild-type membranes.
57. Wada I, Rindress D, Cameron PH, Ou WJ, Doherty JJ, Louvard D, Bell AW, Dignard D, Thomas DY, Bergeron JJ: SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J Biol Chem 1991, 266:19599-19610.
58. Sohn K, Orci L, Ravazzola M, Amherdt M, Bremser M, Lottspeich F, Fiedler K, Helms JB, Wieland FT: A major transmembrane protein of Golgi-derived COPI-coated vesicles involved in coatomer binding. J Cell Biol 1996, 135:1239-1248. Shows that a member of the Emp24 family is found in COPI-coated structures near the Golgi. Demonstrates the binding of the tail sequence of the Emp24 family member to COPI proteins and dependence of this binding on the Phe-Phe motif in the tail.
59. Fiedler K, Veit M, Stamnes MA, Rothman JE: Bimodal interaction of coatomer with the p24 family of putative cargo receptors. Science 1996, 273:1396-1399.