Mechanisms of protein sorting and coat assembly: Insights from the clathrin-coated vesicle pathway

Current Opinion in Cell Biology

Volumn 10, Issue 4, 1998, Pages 499-503

  Borgne, Roland Le ^a   Hoflack, Bernard ^a  

^a INSTITUT PASTEUR DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CLATHRIN; COAT PROTEIN;

CELL MEMBRANE TRANSPORT; COATED VESICLE; CYTOSOL; PRIORITY JOURNAL; PROTEIN TARGETING; REVIEW;

EID: 0032145879     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(98)80065-3     Document Type: Article

References (61)

1. Mellman I. Endocytosis and molecular sorting. Annu Rev Cell Dev Biol. 12:1996;575-625.
2. Schmid SL. Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu Rev Biochem. 66:1997;511-548.
3. Traub LM, Kornfeld S. The trans-Golgi network: a late secretory sorting station. Curr Opin Cell Biol. 9:1997;527-533.
4. Kirchhausen T, Bonifacino JS, Riezman H. Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr Opin Cell Biol. 9:1997;488-495.
5. Robinson MS. The role of clathrin, adaptors and dynamin in endocytosis. Curr Opin Cell Biol. 6:1994;538-544.
6. Newman LS, McKeever MO, Okano HJ, Darnell RB. Beta-NAP, a cerebellar degeneration antigen, is a neuron-specific vesicle coat protein. Cell. 82:1995;773-783.
7. Pevsner J, Volknandt W, Wong BR, Scheller RH. Two rat homologs of clathrin-associated adaptor proteins. Gene. 146:1994;279-283.
8. 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. 16:1997;917-928.
9. Simpson F, Bright NA, West MA, Newman LS, Darnell RB, Robinson MS. A novel adaptor-related protein complex. J Cell Biol. 133:1996;749-760.
10. Simpson F, Peden AA, Christopoulou L, Robinson MS. Characterization of the adaptor-related protein complex, AP-3. J Cell Biol. 137:1997;835-845.
11. Ooi CE, Moreira JE, Dell'Angelica EC, Poy G, Wassarman DA, Bonifacino JS. Altered expression of a novel adaptin leads to defective pigment granule biogenesis in the Drosophila eye color mutant garnet. EMBO J. 16:1997;4508-4518.
12. Cowles CR, Odorizzi G, Payne GS, Emr SD. The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. of outstanding interest Cell. 91:1997;109-118 A screen for factors specifically involved in transport of alkaline phosphatase to the vacuole identified the Ap16P and Ap15p of the yeast AP-3 complex. It is shown that deletion of each of the four AP-3 subunits results in the selective mislocalization of alkaline phosphatase.
13. of outstanding interest Stepp JD, Huang K, Lemmon SK. The yeast adaptor protein complex, AP-3, is essential for the efficient delivery of alkaline phosphatase by the alternate pathway to the vacuole. of special interest J Cell Biol. 139:1997;1761-1774 This paper demonstrates the function of AP-3 in yeast as a component of the system that transports alkaline phosphatase to the vacuole. See also Cowles [12].
14. Vowels JJ, Payne GS. A dileucine-like sorting signal directs transport into an AP-3-dependent, clathrin-independent pathway to the yeast vacuole. EMBO J. 17:1998;2482-2493.
15. Le Borgne R, Alconada A, Bauer U, Hoflack B. Differential sorting of transmembrane proteins with the AP-1 and AP-3 adaptor complexes. Mol Biol Cell Suppl. 8:1997;351a.
16. Swank RT, Novak EK, McGarry MP, Rusiniak ME, Feng L. Mouse models of Hermansky Pudlak syndrome: a review. Pigment Cell Res. 11:1998;60-80.
17. Seymour AB, Feng L, Novak EK, Robinson MS, Swank RT, Gorin MB. A candidate gene for the mouse PEARL (pe) mutation with affects subcellular organelles. Mol Biol Cell Suppl. 8:1997;227a.
18. Dell'Angelica EC, Klumperman J, Stoorvogel W, Bonifacino JS. Association of the AP-3 adaptor complex with clathrin. of special interest Science. 280:1998;431-434 The authors show that AP-3 interacts in vitro with clathrin. Affinity purification of cytosolic extracts on immobilized GST - β3A fusion protein resulted in the isolation of a protein identified as the clathrin heavy chain. AP-3 is also shown to colocalize with clathrin in HeLa cells.
19. Faundez V, Horng JT, Kelly RB. A function for the AP3 coat complex in synaptic vesicle formation from endosomes. of special interest Cell. 93:1998;423-432 This paper shows that synaptic vesicles can be coated in vitro with AP-3 in an ARF-, ATP-, and temperature-dependent manner and that vessicle budding can be reconstituted with purified AP-3 and recombinant ARF-1.
20. Cremona O, De Camilli P. Synaptic vesicle endocytosis. Curr Opin Neurobiol. 7:1997;323-330.
21. Gallusser A, Kirchhausen T. The beta 1 and beta 2 subunits of the AP complexes are the clathrin coat assembly components. EMBO J. 12:1993;5237-5244.
22. 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. 15:1996;2893-2899.
23. 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. 269:1995;1872-1875.
24. Honing S, Griffith J, Geuze HJ, Hunziker W. The tyrosine-based lysosomal targeting signal in lamp-1 mediates sorting into Golgi-derived clathrin-coated vesicles. EMBO J. 15:1996;5230-5239.
25. Honing S, Sosa M, Hille-Rehfeld A, von Figura K. The 46-kDa mannose 6-phosphate receptor contains multiple binding sites for clathrin adaptors. J Biol Chem. 272:1997;19884-19890.
26. Honing S, Sandoval IV, von Figura K. A di-leucine-based motif in the cytoplasmic tail of LIMP-II and tyrosinase mediates selective binding of AP-3. EMBO J. 17:1998;1304-1314.
27. 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. 271:1996;29009-29015.
28. Aguilar RC, Ohno H, Roche KW, Bonifacino JS. Functional domain mapping of the clathrin-associated adaptor medium chains mu1 and mu2. J Biol Chem. 272:1997;27160-27166.
29. 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. 135:1996;341-354.
30. Rapoport I, Chen YC, Cupers P, Shoelson SE, Kirchhausen T. Dileucine-based sorting signals bind to the beta chain of AP-1 at a site distinct and regulated differently from the tyrosine-based motif-binding site. of special interest EMBO J. 17:1998;2148-2155 Using cross-linking of short peptides to purified adaptors, the authors show that dileucine-based motifs bind to the β subunit of AP-1 and that these interactions are inhibited by the phosphatidylinositol phosphates (Pdtdlns 3, 4-P2 and Ptdlns 3, 4, 5-P3).
31. Johnson KF, Kornfeld S. The cytoplasmic tail of the mannose 6-phosphate/insulin-like growth factor-II receptor has two signals for lysosomal enzyme sorting in the Golgi. J Cell Biol. 119:1992;249-257.
32. 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. 15:1996;5789-5795.
33. 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. 14:1995;4961-4975.
34. Alconada A, Bauer U, Hoflack B. A tyrosine-based motif and a casein kinase II phosphorylation site regulate the intracellular trafficking of the varicella-zoster virus glycoprotein I, a protein localized in the trans-Golgi network. EMBO J. 15:1996;6096-6110.
35. Mauxion F, Le Borgne R, Munier-Lehmann H, Hoflack B. A casein kinase II phosphorylation site in the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor determines the high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J Biol Chem. 271:1996;2171-2178.
36. Jones BG, Thomas L, Molloy SS, Thulin CD, Fry MD, Walsh KA, Thomas G. Intracellular trafficking of furin is modulated by the phosphorylation state of a casein kinase II site in its cytoplasmic tail. EMBO J. 14:1995;5869-5883.
37. Schafer W, Stroh A, Berghofer S, Seiler J, Vey M, Kruse ML, Kern HF, Klenk HD, Garten W. Two independent targeting signals in the cytoplasmic domain determine trans-Golgi network localization and endosomal trafficking of the proprotein convertase furin. EMBO J. 14:1995;2424-2435.
38. Le Borgne R, Schmidt A, Mauxion F, Griffiths G, Hoflack B. Binding of AP-1 Golgi adaptors to membranes requires phosphorylated cytoplasmic domains of the mannose 6-phosphate/insulin-like growth factor II receptor. J Biol Chem. 268:1993;22552-22556.
39. Le Borgne R, Hoflack B. Mannose 6-phosphate receptors regulate the formation of clathrin-coated vesicles in the TGN. J Cell Biol. 137:1997;335-345.
40. Dittie AS, Thomas L, Thomas G, Tooze SA. Interaction of furin in immature secretory granules from neuroendocrine cells with the AP-1 adaptor complex is modulated by casein kinase II phosphorylation. EMBO J. 16:1997;4859-4870.
41. Schweizer A, Kornfeld S, Rohrer J. Cysteine34 of the cytoplasmic tail of the cation-dependent mannose 6-phosphate receptor is reversibly palmitoylated and required for normal trafficking and lysosomal enzyme sorting. J Cell Biol. 132:1996;565-576.
42. Hicke L. Ubiquitin-dependent internalization and down-regulation of plasma membrane proteins. FASEB J. 11:1997;1215-1226.
43. Wolins N, Bosshart H, Kuster H, Bonifacino JS. Aggregation as a determinant of protein fate in post-Golgi compartments: role of the luminal domain of furin in lysosomal targeting. J Cell Biol. 139:1997;1735-1745.
44. Liu G, Thomas L, Warren RA, Enns CA, Cunningham CC, Hartwig JH, Thomas G. Cytoskeletal protein ABP-280 directs the intracellular trafficking of furin and modulates proprotein processing in the endocytic pathway. J Cell Biol. 139:1997;1719-1733.
45. Greenberg ME, Bronson S, Lock M, Neumann M, Pavlakis GN, Skowronski J. Co-localization of HIV-1 Nef with the AP-2 adaptor protein complex correlates with Nef-induced CD4 down-regulation. EMBO J. 16:1997;6964-6976.
46. Foti M, Mangasarian A, Piguet V, Lew DP, Krause KH, Trono D, Carpentier JL. Nef-mediated clathrin-coated pit formation. of special interest J Cell Biol. 139:1997;37-47 This paper shows that Nef promotes CD4 internalization via an increased association with clathrin-coated pits. This association with clathrin-coated pits also requires a dileucine-based signal in the CD4 cytoplasmic domain.
47. Piguet V, Chen YL, Mangasarian A, Foti M, Carpentier JL, Trono D. Mechanism of Nef-induced CD4 endocytosis: Nef connects CD4 with the mu chain of adaptor complexes. of special interest EMBO J. 17:1998;2472-2481 It is shown here that the Nef protein of the human or simian immunodeficiency virus downregulates the cell surface expression of CD4, and probably MHC Class I, by connecting these membrane proteins with the endocytic machinery. Nef contains a tyrosine-based motif which interacts with the μ chain of adaptors.
48. De Camilli P, Emr SD, McPherson PS, Novick P. Phosphoinositides as regulators in membrane traffic. Science. 271:1996;1533-1539.
49. Roth MG, Sternweis PC. The role of lipid signaling in constitutive membrane traffic. Curr Opin Cell Biol. 9:1997;519-526.
50. Rothman JE, Wieland FT. Protein sorting by transport vesicles. Science. 272:1996;227-234.
51. Zhao L, Helms JB, Brugger B, Harter C, Martoglio B, Graf R, Brunner J, Wieland FT. Direct and GTP-dependent interaction of ADP ribosylation factor 1 with coatomer subunit beta. Proc Natl Acad Sci USA. 94:1997;4418-4423.
52. Ktistakis NT, Brown HA, Waters MG, Sternweis PC, Roth MG. Evidence that phospholipase D mediates ADP ribosylation factor-dependent formation of Golgi coated vesicles. J Cell Biol. 134:1996;295-306.
53. Traub LM, Bannykh SI, Rodel JE, Aridor M, Balch WE, Kornfeld S. AP-2-containing clathrin coats assemble on mature lysosomes. J Cell Biol. 135:1996;1801-1814.
54. West MA, Bright NA, Robinson MS. The role of ADP-ribosylation factor and phospholipase D in adaptor recruitment. J Cell Biol. 138:1997;1239-1254.
55. Iacopetta BJ, Rothenberger S, Kuhn LC. A role for the cytoplasmic domain in transferrin receptor sorting and coated pit formation during endocytosis. Cell. 54:1988;485-489.
56. Miller K, Shipman M, Trowbridge IS, Hopkins CR. Transferrin receptors promote the formation of clathrin lattices. Cell. 65:1991;621-632.
57. 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. 271:1996;2162-2170.
58. Rapoport I, Miyazaki 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. 16:1997;2240-2250.
59. Matsuoka K, Orci L, Amherdt M, Bednarek SY, Hamamoto S, Schekman R, Yeung T. COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. of outstanding interest Cell. 93:1998;263-275 This work shows that Sar1p, Sec13/31p and Sec23/24p, the three coat proteins of COP II, bind to liposomes containing specific lipids, in particular phosphatidylinositol 4-phosphate or phosphatidylinositol 4,5-diphosphate, and that this assembly promotes the budding of vesicles coated with COP II.
60. Schweizer A, Kornfeld S, Rohrer J. Proper sorting of the cation-dependent mannose 6-phosphate receptor in endosomes depends on a pair of aromatic amino acids in its cytoplasmic tail. Proc Natl Acad Sci USA. 94:1997;14471-14476.
61. Diaz E, Pfeffer SR. TIP47: a cargo selection device for mannose 6 phosphate receptor trafficking. of outstanding interest Cell. 93:1998;433-443 Using the two-hybrid system, the authors identified a 47 kDa protein that binds selectively to a phenylalanine/tryptophan signal in the tail of the cation-dependent mannose-6-phosphate receptor that is essential for its proper sorting within the endosomal pathway.