Clathrin-dependent endocytosis

Biochemical Journal

Volumn 377, Issue 1, 2004, Pages 1-16

  Mousavi, Seyed Ali ^a   Malerød, Lene ^a   Berg, Trond ^a   Kjeken, Rune ^a  

^a UNIVERSITY OF OSLO   (Norway)

Author keywords

Adaptor protein; AP 2; Clathrin; Coated pit; Endocytosis; Receptor

Indexed keywords

BIOCHEMISTRY; CELL MEMBRANES; PROTEINS; REACTION KINETICS;

ENDOCYTOSIS;

CYTOLOGY;

ADAPTOR PROTEIN; AMPHIPHYSIN; CELL SURFACE RECEPTOR; CLATHRIN; DYNAMIN; EPSIN; G PROTEIN COUPLED RECEPTOR; PHOSPHATIDYLINOSITIDE; PROTEIN; PROTEIN AP 2; UNCLASSIFIED DRUG;

CELL MEMBRANE; CHEMICAL INTERACTION; ENDOCYTOSIS; EUKARYOTIC CELL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION;

ADAPTOR PROTEIN COMPLEX 2; ANIMALS; ARRESTINS; CALCIUM-BINDING PROTEINS; CELL MEMBRANE; CLATHRIN; COATED PITS, CELL-MEMBRANE; COATED VESICLES; ENDOCYTOSIS; MEMBRANE GLYCOPROTEINS; NERVE TISSUE PROTEINS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SYNAPTOTAGMINS;

EUKARYOTA;

EID: 1342273834     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031000     Document Type: Review

References (196)

1. Schmid, S. L. (1997) Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66, 511-548
2. Greene, B., Liu, S. H., Wilde, A. and Brodsky, F. M. (2000) Complete reconstitution of clathrin basket formation with recombinant protein fragments: adaptor control of clathrin self-assembly. Traffic 1, 69-75
3. Liu, S. H., Wong, M. L., Craik, C. S. and Brodsky, F. M. (1995) Regulation of clathrin assembly and trimerization defined using recombinant triskelion hubs. Cell 83, 257-267
4. ter Haar, E., Harrison, S. C. and Kirchhausen, T. (2000) Peptide-in-groove interactions link target proteins to the beta-propeller of clathrin. Proc. Natl. Acad. Sci. U.S.A. 97, 1096-1100
5. Kirchhausen, T. (2000) Clathrin. Annu. Rev. Biochem. 69, 699-727
6. Brodsky, F. M., Chen, C. Y., Knuehl, C., Towler, M. C. and Wakeham, D. E. (2001) Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17, 517-568
7. Ybe, J. A., Greene, B., Liu, S. H., Pley, U., Parham, P. and Brodsky, F. M. (1998) Clathrin self-assembly is regulated by three light-chain residues controlling the formation of critical salt bridges. EMBO J. 17, 1297-1303
8. Heuser, J. E. and Keen, J. (1988) Deep-etch visualization of proteins involved in clathrin assembly. J. Cell Biol. 107, 877-886
9. Pearse, B. M., Smith, C. J. and Owen, D. J. (2000) Clathrin coat construction in endocytosis. Curr. Opin. Struct, Biol. 10, 220-228
10. Owen, D. J., Vallis, Y., Pearse, B. M., McMahon, H. T. and Evans, P. R. (2000) The structure and function of the beta 2-adaptin appendage domain. EMBO J. 19, 4216-4227
11. Rapoport, I., Chen, Y. C., Cupers, P., Shoelson, S. E. and Kirchhausen, T. (1998) 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. EMBO J. 17, 2148-2155
12. Rohde, G., Wenzel, D. and Haucke, V. (2002) A phosphatidylinositol (4,5)-bisphosphate binding site within μ2-adaptin regulates clathrin-mediated endocytosis. J. Cell Biol. 158, 209-214
13. Aguilar, R. C., Ohno, H., Roche, K. W. and Bonifacino, J. S. (1997) Functional domain mapping of the clathrin-associated adaptor medium chains mu1 and mu2. J. Biol. Chem. 272, 27160-27166
14. Page, L. J. and Robinson, M. S. (1995) Targeting signals and subunit interactions in coated vesicle adaptor complexes. J. Cell Biol. 131, 619-630
15. Ye, W. and Lafer, E. M. (1995) Clathrin binding and assembly activities of expressed domains of the synapse-specific clathrin assembly protein AP-3. J. Biol. Chem. 270, 10933-10939
16. Tebar, F., Bohlander, S. K. and Sorkin, A. (1999) Clathrin assembly lymphoid myeloid leukemia (CALM) protein: localization in endocytic-coated pits, interactions with clathrin, and the impact of overexpression on clathrin-mediated traffic. Mol. Biol. Cell 10, 2687-2702
17. Ford, M. G., Pearse, B. M., Higgins, M. K., Vallis, Y., Owen, D. J., Gibson, A., Hopkins, C. R., Evans, P. R. and McMahon, H. T. (2001) Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291, 1051-1055
18. Hao, W., Luo, Z., Zheng, L., Prasad, K. and Later, E. M. (1999) AP180 and AP-2 interact directly in a complex that cooperatively assembles clathrin. J. Biol. Chem. 274, 22785-22794
19. Itoh, T., Koshiba, S., Kigawa, T., Kikuchi, A., Yokoyama, S. and Takenawa, T. (2001) Role of the ENTH domain in phosphatidylinositol-4,5- bisphosphate binding and endocytosis. Science 291, 1047-1051
20. Hofmann, K. and Falquet, L. (2001) A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem. Sci. 26, 347-350
21. Chen, H., Fre, S., Slepnev, V. I., Capua, M. R., Takei, K., Butler, M. H., Di Fiore, P. P. and De Camilli, P. (1998) Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature (London) 394, 793-797
22. Owen, D. J., Vallis, Y., Noble, M. E., Hunter, J. B., Dafforn, T. R., Evans, P. R. and McMahon, H. T. (1999) A structural explanation for the binding of multiple ligands by the alpna-adaptin appendage domain. Cell 97, 805-815
23. Drake, M. T., Downs, M. A. and Traub, L. M. (2000) Epsin binds to clathrin by associating directly with the clathrin-terminal domain. Evidence for cooperative binding through two discrete sites. J. Biol. Chem. 275, 6479-6489
24. Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J., Evans, P. R. and McMahon, H. T. (2002) Curvature of clathrin-coated pits driven by epsin. Nature (London) 419, 361-366
25. Kalthoff, C., Alves, J., Urbanke, C., Knorr, R. and Ungewickell, E. J. (2002) Unusual structural organization of the endocytic proteins AP180 and Epsin 1. J. Biol. Chem. 277, 8209-8216
26. Cupers, P., ter Haar, E., Boll, W. and Kirchhausen, T. (1997) Parallel dimers and anti-parallel tetramers formed by epidermal growth factor receptor pathway substrate clone 15. J. Biol. Chem. 272, 33430-33434
27. Salcini, A. E., Chen, H., Iannolo, G., De Camilli, P. and Di Fiore, P. P. (1999) Epidermal growth factor pathway substrate 15, Eps15. Int. J. Biochem. Cell Biol. 31, 805-809
28. Mishra, S. K., Keyel, P. A., Hawryluk, M. J., Agostinelli, N. R., Watkins, S. C. and Traub, L. M. (2002) Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J. 21, 4915-4926
29. Oleinikov, A. V., Zhao, J. and Makker, S. P. (2000) Cytosolic adaptor protein Dab2 is an intracellular ligand of endocytic receptor gp600/megalin. Biochem. J. 347, 613-621
30. Morris, S. M. and Cooper, J. A. (2001) Disabled-2 colocalizes with the LDLR in clathrin-coated pits and interacts with AP-2. Traffic 2, 111-123
31. Morris, S. M., Tallquist, M. D., Rock, C. O. and Cooper, J. A. (2002) Dual roles for the Dab2 adaptor protein in embryonic development and kidney transport. EMBO J. 21, 1555-1564
32. Metzler, M., Legendre-Guillemin, V., Gan, L., Chopra, V., Kwok, A., McPherson, P. S. and Hayden, M. R. (2001) HIP1 functions in clathrin-mediated endocytosis through binding to clathrin and adaptor protein 2. J. Biol. Chem. 276, 39271-39276
33. Martina, J. A., Bonangelino, C. J., Aguilar, R. C. and Bonifacino, J. S. (2001) Stonin 2: an adaptor-like protein that interacts with components of the endocytic machinery. J. Cell Biol. 153, 1111-1120
34. Sengar, A. S., Wang, W., Bishay, J., Cohen, S. and Egan, S. E. (1999) The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15. EMBO J. 18, 1159-1171
35. Santolini, E., Puri, C., Salcini, A. E., Gagliani, M. C., Pelicci, P. G., Tacchetti, C. and Di Fiore, P. P. (2000) Numb is an endocytic protein. J. Cell Biol. 151, 1345-1352
36. Liu, J. P. and Robinson, P. J. (1995) Dynamin and endocytosis. Endocr. Rev. 16, 590-607
37. Muhlberg, A. B., Warnock, D. E. and Schmid, S. L. (1997) Domain structure and intramolecular regulation of dynamin GTPase. EMBO J. 16, 6676-6683
38. Schmid, S. L., McNiven, M. A. and De Camilli, P. (1998) Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10, 504-512
39. Hinshaw, J. E. (1999) Dynamin spirals. Curr. Opin. Struct. Biol. 9, 260-267
40. Kessels, M. M., Engqvist-Goldstein, A. E., Drubin, D. G. and Qualmann, B. (2001) Mammalian Abp1, a signal-responsive F-actin-binding protein, links the actin cytoskeleton to endocytosis via the GTPase dynamin. J. Cell Biol. 153, 351-366
41. McNiven, M. A., Kim, L., Krueger, E. W., Orth, J. D., Cao, H. and Wong, T. W. (2000) Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J. Cell Biol. 151, 187-198
42. Wigge, P. and McMahon, H. T. (1998) The amphiphysin family of proteins and their role in endocytosis at the synapse. Trends Neurosci. 21, 339-344
43. Zhang, B. and Zelhof, A. C. (2002) Amphiphysins: raising the BAR for synaptic vesicle recycling and membrane dynamics. Bin-Amphiphysin-Rvsp. Traffic 3, 452-460
44. Ringstad, N., Nemoto, Y. and De Camilli, P. (1997) The SH3p4/Sh3p8/ SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc. Natl. Acad. Sci. U.S.A. 94, 8569-8574
45. Ringstad, N., Gad, H., Low, P., Di Paolo, G., Brodin, L., Shupliakov, O. and De Camilli, P. (1999) Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron 24, 143-154
46. Micheva, K. D., Ramjaun, A. R., Kay, B. K. and McPherson, P. S. (1997) SH3 domain-dependent interactions of endophilin with amphiphysin. FEBS Lett, 414, 308-312
47. Gad, H., Ringstad, N., Low, P., Kjaerulff, O., Gustafsson, J., Wenk, M., Di Paolo, G., Nemoto, Y., Crun, J., Ellisman, M. H., De Camilli, P. et al. (2000) Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27, 301-312
48. Kanaseki, T. and Kadota, K. (1969) The "vesicle in a basket". A morphological study of the coated vesicle isolated from the nerve endings of the guinea pig brain, with special reference to the mechanism of membrane movements. J. Cell Biol. 42, 202-220
49. Heuser, J. (1980) Three-dimensional visualization of coated vesicle formation in fibroblasts. J. Cell Biol. 84, 560-583
50. Heuser, J. and Kirchhausen, T. (1985) Deep-etch views of clathrin assemblies. J. Ultrastruct. Res. 92, 1-27
51. Pearse, B. M. and Bretscher, M. S. (1981) Membrane recycling by coated vesicles. Annu. Rev. Biochem. 50, 85-101
52. Santini, F. and Keen, J. H. (2002) A glimpse of coated vesicle creation? Well almost! Nat. Cell Biol. 4. E230-E232
53. Kirchhausen, T. (1993) Coated pits and coated vesicles - sorting it all out. Curr. Opin. Struct. Biol. 3, 182-188
54. Kirchhausen, T. (2000) Three ways to make a vesicle. Nat. Rev. Mol. Cell Biol. 1, 187-198
55. Harrison, S. C. and Kirchhausen, T. (1983) Clathrin, cages, and coated vesicles. Cell 33, 650-652
56. Lipowsky, R. (1993) Domain-induced budding of fluid membranes. Biophys. J. 64, 1133-1138
57. Zhang, B., Ganetzky, B., Bellen, H. J. and Murthy, V. N. (1999) Tailoring uniform coats for synaptic vesicles during endocytosis. Neuron 23, 419-422
58. Jin, A. J. and Nossal, R. (1993) Topological mechanisms involved in the formation of clathrin-coated vesicles. Biophys. J. 65, 1523-1537
59. Nossal, R. (2001) Energetics of clathrin basket assembly. Traffic 2, 138-147
60. Wu, X., Zhao, X., Baylor, L., Kaushal, S., Eisenberg, E. and Greene, L. E. (2001) Clathrin exchange during clathrin-mediated endocytosis. J. Cell Biol. 155, 291-300
61. Musacchio, A., Smith, C. J., Roseman, A. M., Harrison, S. C., Kirchhausen, T. and Pearse, B. M. (1999) Functional organization of clathrin in coats: combining electron cryomicroscopyand X-ray crystallography. Mol. Cell 3, 761-770
62. Vigers, G. P., Crowther, R. A. and Pearse, B. M. (1986) Location of the 100 kD-50 kD accessory proteins in clathrin coats. EMBO J. 5, 2079-2085
63. Vigers, G. P., Crowther, R. A. and Pearse, B. M. (1986) Three-dimensional structure of clathrin cages in ice. EMBO J. 5, 529-534
64. Smith, C. J., Grigorieff, N. and Pearse, B. M. (1998) Clathrin coats at 21 Å resolution: a cellular assembly designed to recycle multiple membrane receptors. EMBO J. 17, 4943-4953
65. Brown, C. M. and Petersen, N. O. (1999) Free clathrin triskelions are required for the stability of clathrin-associated adaptor protein (AP-2) coated pit nucleation sites. Biochem. Cell Biol. 77, 439-448
66. Santini, F., Gaidarov, I. and Keen, J. H. (2002) G protein-coupled receptor/arrestin3 modulation of the endocytic machinery. J. Cell Biol. 156, 665-676
67. Moore, M. S., Mahaffey, D. T., Brodsky, F. M. and Anderson, R. G. (1987) Assembly of clathrin-coated pits onto purified plasma membranes. Science 236, 558-563
68. Mahaffey, D. T., Peeler, J. S., Brodsky, F. M. and Anderson, R. G. (1990) Clathrin-coated pits contain an integral membrane protein that binds the AP-2 subunit with high affinity. J. Biol. Chem. 265, 16514-16520
69. Gaidarov, I., Santini, F., Warren, R. A. and Keen, J. H. (1999) Spatial control of coated-pit dynamics in living cells. Nat. Cell Biol. 1, 1-7
70. Brodsky, F. M. (1988) Living with clathrin: its role in intracellular membrane traffic. Science 242, 1396-1402
71. Gaidarov, I., Chen, Q., Falck, J. R., Reddy, K. K. and Keen, J. H. (1996) A functional phosphatidylinositol 3,4,5-trisphosphate/phosphoinositide binding domain in the clathrin adaptor AP-2 alpha subunit. Implications for the endocytic pathway. J. Biol. Chem. 271, 20922-20929
72. West, M. A., Bright, N. A. and Robinson, M. S. (1997) The role of ADP-ribosylation factor and phospholipase D in adaptor recruitment. J. Cell Biol. 138, 1239-1254
73. Jost, M., Simpson, F. Kavran, J. M., Lemmon, M. A. and Schmid, S. L. (1998) Phosphatidylinositol-4,5-bisphosphate is required for endocytic coated vesicle formation. Curr. Biol. 8, 1399-1402
74. Gaidarov, I. and Keen, J. H. (1999) Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits. J. Cell Biol. 146, 755-764
75. Shin, W., Gallusser, A. and Kirchhausen, T. (1995) A clathrin-binding site in the hinge of the beta 2 chain of mammalian AP-2 complexes. J. Biol. Chem. 270, 31083-31090
76. Hansen, S. H., Sandvig, K. and van Deurs, B. (1993) Clathrin and HA2 adaptors: effects of potassium depletion, hypertonic medium, and cytosol acidification. J Cell Biol. 121, 61-72
77. Brown, C. M., Roth, M. G., Henis, Y. I. and Petersen, N. O. (1999) An internalization-competent influenza hemagglutinin mutant causes the redistribution of AP-2 to existing coated pits and is colocalized with AP-2 in clathrin free clusters. Biochemistry 38, 15166-15173
78. Zhao, X., Greener, T., Al-Hasani, H., Cushman, S. W., Eisenberg, E. and Greene, L. E. (2001) Expression of auxilin or AP180 inhibits endocytosis by mislocalizing clathrin: evidence for formation of nascent pits containing AP1 or AP2 but not clathrin. J. Cell Sci. 114, 353-365
79. Beck, K. A. and Keen, J. H. (1991) Self-association of the plasma membrane-associated clathrin assembly protein AP-2. J. Biol. Chem. 266, 4437-4441
80. Ungewickell, E. (1999) Clathrin: a good view of a shapely leg. Curr Biol. 9, R32-R35
81. 2 regulation of surface membrane traffic. Curr. Opin. Cell Biol. 13, 493-499
82. Zhang, J. Z., Davletov, B. A., Sudhof, T. C. and Anderson, R. G. (1994) Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell 78, 751-760
83. Pearse, B. M. and Crowther, R. A. (1987) Structure and assembly of coated vesicles. Annu. Rev. Biophys. Biophys. Chem. 16, 49-68
84. Iacopetta, B. J., Rothenberger, S. and Kuhn, L. C. (1988) A role for the cytoplasmic domain in transferrin receptor sorting and coated pit formation during endocytosis. Cell 54, 485-489
85. Miller, K., Shipman, M., Trowbridge, I. S. and Hopkins, C. R. (1991) Transferrin receptors promote the formation of clathrin lattices. Cell 65, 621-632
86. Goldstein, J. L., Brown, M. S., Anderson, R. G., Russell, D. W. and Schneider, W. J. (1985) Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu. Rev. Cell Biol. 1, 1-39
87. Pearse, B. M. (1988) Receptors compete for adaptors found in plasma membrane coated pits. EMBO J. 7, 3331-3336
88. Warren, R. A., Green, F. A. and Enns, C. A. (1997) Saturation of the endocytic pathway for the transferrin receptor does not affect the endocytosis of the epidermal growth factor receptor. J. Biol. Chem. 272, 2116-2121
89. Santini, F., Marks, M. S. and Keen, J. H. (1998) Endocytic clathrin-coated pit formation is independent of receptor internalization signal levels. Mol. Biol. Cell 9, 1177-1194
90. Nesterov, A., Carter, R. E., Sorkina, T., Gill, G. N. and Sorkin, A. (1999) Inhibition of the receptor-binding function of clathrin adaptor protein AP-2 by dominant-negative mutant μ2 subunit and its effects on endocytosis. EMBO J. 18, 2489-2499
91. Olusanya, O., Andrews, P. D., Swedlow, J. R. and Smythe, E. (2001) Phosphorylation of threonine 156 of the μ2 subunit of the AP2 complex is essential for endocytosis in vitro and in vivo. Curr. Biol. 11, 896-900
92. Fingerhut, A., von Figura, K. and Honing, S. (2001) Binding of AP2 to sorting signals is modulated by AP2 phosphorylation. J. Biol. Chem. 276, 5476-5482
93. Sudhof, T. C. (2002) Synaptotagmins: why so many? J. Biol. Chem. 277, 7629-7632
94. Haucke, V., Wenk, M. R., Chapman, E. R., Farsad, K. and De Camilli, P. (2000) Dual interaction of synaptotagmin with μ2- and alpha-adaptin facilitates clathrin-coated pit nucleation. EMBO J. 19, 6011-6019
95. Li, C., Ullrich, B., Zhang, J. Z., Anderson, R. G., Brose, N. and Sudhof, T. C. (1995) Ca(2+)-dependent and -independent activities of neural and non-neural synaptotagmins. Nature (London) 375, 594-599
96. Marqueze, B., Berton, F. and Seagar, M. (2000) Synaptotagmins in membrane traffic: which vesicles do the tagmins tag? Biochimie 82, 409-420
97. von Poser, C., Zhang, J. Z., Mineo, C., Ding, W., Ying, Y., Sudhof, T. C. and Anderson, R. G. (2000) Synaptotagmin regulation of coated pit assembly. J. Biol. Chem. 275, 30916-30924
98. Haucke, V. and De Camilli, P. (1999) AP-2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs. Science 285, 1268-1271
99. Tebar, F., Sorkina, T., Sorkin, A., Ericsson, M. and Kirchhausen, T. (1996) Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits. J. Biol. Chem. 271, 28727-28730
100. Cupers, P., Jadhav, A. P. and Kirchhausen, T. (1998) Assembly of clathrin coats disrupts the association between Eps15 and AP-2 adaptors. J. Biol. Chem. 273, 1847-1850
101. Ye, W. and Later, E. M. (1995) Bacterially expressed F1-20/AP-3 assembles clathrin into cages with a narrow size distribution: implications for the regulation of quantal size during neurotransmission. J. Neurosci. Res. 41, 15-26
102. Zaremba, S. and Keen, J. H. (1983) Assembly polypeptides from coated vesicles mediate reassembly of unique clathrin coats. J. Cell Biol. 97, 1339-1347
103. Larkin, J. M., Donzell, W. C. and Anderson, R. G. (1986) Potassium-dependent assembly of coated pits: new coated pits form as planar clathrin lattices. J. Cell Biol. 103, 2619-2627
104. Mahaffey, D. T., Moore, M. S., Brodsky, F. M. and Anderson, R. G. (1989) Coat proteins isolated from clathrin coated vesicles can assemble into coated pits. J. Cell Biol. 108, 1615-1624
105. Lin, H. C., Moore, M. S., Sanan, D. A. and Anderson, R. G. (1991) Reconstitution of clathrin-coated pit budding from plasma membranes. J. Cell Biol. 114, 881-891
106. Owen, D. J. and Evans, P. R. (1998) A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282, 1327-1332
107. Farge, E., Ojcius, D. M., Subtil, A. and Dautry-Varsat, A. (1999) Enhancement of endocytosis due to aminophospholipid transport across the plasma membrane of living cells. Am. J. Physiol. 276, C725-C733
108. Cupers, P., Veithen, A., Kiss, A., Baudhuin, P. and Courtoy, P. J. (1994) Clathrin polymerization is not required for bulk-phase endocytosis in rat fetal fibroblasts. J. Cell Biol. 127, 725-735
109. Maddox, J. (1993) How and why of vesicle formation. Nature (London) 363, 205
110. Sackmann, E. (1994) The seventh Datta Lecture. Membrane bending energy concept of vesicle- and cell-shapes and shape-transitions. FEBS Lett. 346, 3-16
111. Sheetz, M. P. and Singer, S. J. (1974) Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. U.S.A. 71, 4457-4461
112. Kozlov, M. M. (2001) Fission of biological membranes: interplay between dynamin and lipids. Traffic 2, 51-65
113. Zha, X., Pierini, L. M., Leopold, P. L., Skiba, P. J., Tabas, I. and Maxfield, F. R. (1998) Sphingomyelinase treatment induces ATP-independent endocytosis. J. Cell Biol. 140, 39-47
114. Schmidt, A. A. (2002) Membrane transport: the making of a vesicle. Nature (London) 419, 347-349
115. Subtil, A., Gaidarov, I., Kobylarz, K., Lampson, M. A., Keen, J. H. and McGraw, T. E. (1999) Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl. Acad. Sci. U.S.A. 96, 6775-6780
116. Thiele, C., Hannah, M. J., Fahrenholz, F. and Huttner, W. B. (2000) Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol. 2, 42-49
117. Zerial, M. and McBride, H. (2001) Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117
118. McLauchlan, H., Newell, J., Morrice, N., Osborne, A., West, M. and Smythe, E. (1998) A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr. Biol. 8, 34-45
119. Seachrist, J. L., Laporte, S. A., Dale, L. B., Babwah, A. V., Caron, M. G., Anborgh, P. H. and Ferguson, S. S. (2002) Rab5 association with the angiotensin II type 1A receptor promotes Rab5 GTP binding and vesicular fusion. J. Biol. Chem. 277, 679-685
120. Farsad, K., Ringstad, N., Takei, K., Floyd, S. R., Rose, K. and De Camilli, P. (2001) Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155, 193-200
121. Hill, E., van Der Kaay, J., Downes, C. P. and Smythe, E. (2001) The role of dynamin and its binding partners in coated pit invagination and scission. J. Cell Biol. 152, 309-323
122. Morris, S. M., Arden, S. D., Roberts, R. C., Kendrick-Jones, J., Cooper, J. A., Luzio, J. P. and Buss, F. (2002) Myosin VI binds to and localises with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton. Traffic 3, 331-341
123. Takei, K., Slepnev, V. I., Haucke, V. and De Camilli, P. (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1, 33-39
124. Smirnova, E., Shurland, D. L., Newman-Smith, E. D., Pishvaee, B. and van der Bliek, A. M. (1999) A model for dynamin self-assembly based on binding between three different protein domains. J. Biol. Chem. 274, 14942-14947
125. Hinshaw, J. E. and Schmid, S. L. (1995) Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature (London) 374, 190-192
126. Takei, K., McPherson, P. S., Schmid, S. L. and De Camilli, P. (1995) Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature (London) 374, 186-190
127. Sever, S., Muhlberg, A. B. and Schmid, S. L. (1999) Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature (London) 398, 481-486
128. McNiven, M. A. (1998) Dynamin: a molecular motor with pinchase action. Cell 94, 151-154
129. Sweitzer, S. M. and Hinshaw, J. E. (1998) Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021-1029
130. Stowell, M. H., Marks, B., Wigge, P. and McMahon, H. T. (1999) Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat. Cell Biol. 1, 27-32
131. Marks, B., Stowell, M. H., Vallis, Y., Mills, I. G., Gibson, A., Hopkins, C. R. and McMahon, H. T. (2001) GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature (London) 410, 231-235
132. Schmidt, A., Wolde, M., Thiele, C., Fest, W., Kratzin, H., Podtelejnikov, A. V., Witke, W., Huttner, W. B. and Soling, H. D. (1999) Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature (London) 401, 133-141
133. Huttner, W. B. and Zimmerberg, J. (2001) Implications of lipid microdomains for membrane curvature, budding and fission. Curr. Opin. Cell Biol. 13, 478-484
134. Gottlieb, T. A., Ivanov, I. E., Adesnik, M. and Sabatini, D. D. (1993) Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120, 695-710
135. Lamaze, C., Fujimoto, L. M., Yin, H. L. and Schmid, S. L. (1997) The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J. Biol. Chem. 272, 20332-20335
136. Shupliakov, O., Bloom, O., Gustafsson, J. S., Kjaerulff, O., Low, P., Tomilin, N., Pieribone, V. A., Greengard, P. and Brodin, L. (2002) Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc. Natl. Acad. Sci. U.S.A. 99, 14476-14481
137. Witke, W., Podtelejnikov, A. V., Di Nardo, A., Sutherland, J. D., Gurniak, C. B., Dotti, C. and Mann, M. (1998) In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly. EMBO J. 17, 967-976
138. Uruno, T., Liu, J., Zhang, P., Fan, Y., Egile, C., Li, R., Mueller, S. C. and Zhan, X. (2001) Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat. Cell Biol. 3, 259-266
139. Schafer, D. A., Weed, S. A., Binns, D., Karginov, A. V. Parsons, J. T. and Cooper, J. A. (2002) Dynamin2 and cortactin regulate actin assembly and filament organization. Curr. Biol. 12, 1852-1857
140. Lee, E. and De Camilli, P. (2002) Dynamin at actin tails. Proc. Natl. Acad. Sci. U.S.A. 99, 161-166
141. Merrifield, C. J., Feldman, M. E., Wan, L. and Aimers, W. (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat. Cell Biol. 4, 691-698
142. Waterman, H. and Yarden, Y. (2001) Molecular mechanisms underlying endocytosis and sorting of ErbB receptor tyrosine kinases. FEBS Lett. 490, 142-152
143. Parent, J. L., Labrecque, P., Driss Rochdi, M. and Benovic, J. L. (2001) Role of the differentially spliced carboxyl terminus in thromboxane A2 receptor trafficking: identification of a distinct motif for tonic internalization. J. Biol. Chem. 276, 7079-7085
144. Bretscher, M. S. and Pearse, B. M. (1984) Coated pits in action. Cell 38, 3-4
145. Hanover, J. A., Beguinot, L., Willingham, M. C. and Pastan, I. H. (1985) Transit of receptors for epidermal growth factor and transferrin through clathrin-coated pits. Analysis of the kinetics of receptor entry. J. Biol. Chem. 260, 15938-15945
146. Bider, M. D. and Spiess, M. (1998) Ligand-induced endocytosis of the asialoglycoprotein receptor: evidence for heterogeneity in subunit oligomerization. FEBS Lett. 434, 37-41
147. Schwake, L., Henkel, A. W., Riedel, H. D., Schlenker, T., Both, M., Migala, A., Hadaschik, B., Henfling, N. and Stremmel, W. (2002) Regulation of transferrin-induced endocytosis by wild-type and C282Y-mutant HFE in transfected HeLa cells. Am. J. Physiol. Cell Physiol. 282, C973-C979
148. Davis, C. G., Lehrman, M. A., Russell, D. W., Anderson, R. G., Brown, M. S. and Goldstein, J. L. (1986) The J.D. mutation in familial hypercholesterolemia: amino acid substitution in cytoplasmic domain impedes internalization of LDL receptors. Cell 45, 15-24
149. Rothenberger, S., Iacopetta, B. J. and Kuhn, L. C. (1987) Endocytosis of the transferrin receptor requires the cytoplasmic domain but not its phosphorylation site. Cell 49, 423-431
150. Collawn, J. F., Stangel, M., Kuhn, L. A., Esekogwu, V., Jing, S. Q., Trowbridge, I. S. and Tainer, J. A. (1990) Transferrin receptor internalization sequence YXRF implicates a tight turn as the structural recognition motif for endocytosis. Cell 63, 1061-1072
151. Ohno, H., Stewart, J., Fournier, M. C., Bosshart, H., Rhee, I., Miyatake, S., Saito, T., Gallusser, A., Kirchhausen, T. and Bonifacino, J. S. (1995) Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269, 1872-1875
152. Verhey, K. J. and Birnbaum, M. J. (1994) A Leu-Leu sequence is essential for COOH-terminal targeting signal of GLUT4 glucose transporter in fibroblasts. J. Biol. Chem. 269, 2353-2356
153. Simonsen, A., Bremnes, B., Nordeng, T. W., and Bakke, O. (1998) The leucine-based motif DDQxxLI is recognized both for internalization and basolateral sorting of invariant chain in MDCK cells. Eur J. Cell Biol. 76, 25-32
154. Pitcher, C., Honing, S., Fingerhut, A., Bowers, K. and Marsh, M. (1999) Cluster of differentiation antigen 4 (CD4) endocytosis and adaptor complex binding require activation of the CD4 endocytosis signal by serine phosphorylation. Mol. Biol. Cell 10, 677-691
155. Fuhrer, C., Geffen, I., Huggel, K. and Spiess, M. (1994) The two subunits of the asialoglycoprotein receptor contain different sorting information. J. Biol. Chem. 269, 3277-3282
156. Pond, L., Kuhn, L. A., Teyton, L., Schutze, M. P., Tainer, J. A., Jackson, M. R. and Peterson, P. A. (1995) A role for acidic residues in di-leucine motif-based targeting to the endocytic pathway. J. Biol. Chem. 270, 19989-19997
157. Owen, D. J., Setiadi, H., Evans, P. R., McEver, R. P. and Green, S. A. (2001) A third specificity-determining site in mu2 adaptin for sequences upstream of Yxx φ sorting motifs. Traffic 2, 105-110
158. Williams, M. A. and Fukuda, M. (1990) Accumulation of membrane glycoproteins in iysosomes requires a tyrosine residue at a particular position in the cytoplasmic tail. J. Cell Biol. 111, 955-966
159. Boll, W., Rapoport, I., Brunner, C., Modis, Y., Prehn, S. and Kirchhausen, T. (2002) The mu2 subunit of the clathrin adaptor AP-2 binds to FDNPVY and Ypp φ sorting signals at distinct sites. Traffic 3, 590-600
160. Willnow, T. E., Nykjaer, A. and Herz, J. (1999) Lipoprotein receptors: new roles for ancient proteins. Nat. Cell Biol. 1, E157-E162
161. Honing, S., Sandoval, I. V. and von Figura, K. (1998) A di-leucine-based motif in the cytoplasmic tail of LIMP-II and tyrosinase mediates selective binding of AP-3. EMBO J. 17, 1304-1314
162. Rodionov, D. G. and Bakke, O. (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
163. Foti, M., Mangasarian, A., Piguet, V., Lew, D. P., Krause, K. H., Trono, D. and Carpentier, J. L. (1997) Nef-mediated clathrin-coated pit formation. J. Cell Biol. 139, 37-47
164. Laporte, S. A., Oakley, R. H., Zhang, J., Holt, J. A., Ferguson, S. S., Caron, M. G. and Barak, L. S. (1999) The beta2-adrenergic receptor/betaarrestin complex recruits the clathrin adaptor AP-2 during endocytosis. Proc. Natl. Acad. Sci. U.S.A. 96, 3712-3717
165. Weissman, A. M. (2001) Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell Biol. 2, 169-178
166. Lemmon, M. A., Bu, Z., Ladbury, J. E., Zhou, M., Pinchasi, D., Lax, I., Engelman, D. M. and Schlessinger, J. (1997) Two EGF molecules contribute additively to stabilization of the EGFR dimer. EMBO J. 16, 281-294
167. Chang, C. P., Lazar, C. S., Walsh, B. J., Komuro, M., Collawn, J. F., Kuhn, L. A., Tainer, J. A., Trowbridge, I. S., Farquhar, M. G., Rosenfeld, M. G. et al. (1993) Ligand-induced internalization of the epidermal growth factor receptor is mediated by multiple endocytic codes analogous to the tyrosine motif found in constitutively internalized receptors. J. Biol. Chem. 268, 19312-19320
168. Nesterov, A., Wiley, H. S. and Gill, G. N. (1995) Ligand-induced endocytosis of epidermal growth factor receptors that are defective in binding adaptor proteins. Proc. Natl. Acad. Sci. U.S.A. 92, 8719-8723
169. Lamaze, C., Baba, T., Redelmeier, T. E. and Schmid, S. L. (1993) Recruitment of epidermal growth factor and transferrin receptors into coated pits in vitro: differing biochemical requirements. Mol. Biol. Cell 4, 715-727
170. Chang, C. P., Kao, J. P., Lazar, C. S., Walsh, B. J., Wells, A., Wiley, H. S., Gill, G. N. and Rosenfeld, M. G. (1991) Ligand-induced internalization and increased cell calcium are mediated via distinct structural elements in the carboxyl terminus of the epidermal growth factor receptor. J. Biol. Chem. 266, 23467-23470
171. Confalonieri, S., Salcini, A. E., Puri, C., Tacchetti, C. and Di Fiore, P. P. (2000) Tyrosine phosphorylation of Eps15 is required for ligand-regulated, but not constitutive, endocytosis. J. Cell Biol. 150, 905-912
172. van Delft, S., Schumacher, C., Hage, W., Verkleij, A. J. and van Bergen en Henegouwen, P. M. (1997) Association and colocalization of Eps15 with adaptor protein-2 and clathrin. J. Cell Biol. 136, 811-821
173. Wang, Z. and Moran, M. F. (1996) Requirement for the adapter protein GRB2 in EGF receptor endocytosis. Science 272, 1935-1939
174. Levkowitz, G., Waterman, H., Ettenberg, S. A., Katz, M., Tsygankov, A. Y., Alroy I., Lavi, S., Iwai, K., Reiss, Y., Ciechanover, A. et al. (1999) Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 4, 1029-1040
175. Polo, S., Sigismund, S., Faretta, M., Guidi, M., Capua, M. R., Bossi, G., Chen, H., De Camilli, P. and Di Fiore, P. P. (2002) A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature (London) 416, 451-455
176. Lee, P. S., Wang, Y., Dominguez, M. G., Yeung, Y. G., Murphy, M. A., Bowtell, D. D. and Stanley, E. R. (1999) The CbI protooncoprotein stimulates CSF-1 receptor multiubiquitination and endocytosis, and attenuates macrophage proliferation. EMBO J. 18, 3616-3628
177. Soubeyran, P., Kowanetz, K., Szymkiewicz, I., Langdon, W. Y. and Dikic, I. (2002) Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature (London) 416, 183-187
178. Petrelli, A., Gilestro, G. F., Lanzardo, S., Comoglio, P. M., Migone, N. and Giordano, S. (2002) The endophilin-CIN85-Cbl complex mediates ligand-dependent downregulation of c-Met. Nature (London) 416, 187-190
179. Thien, C. B. and Langdon, W. Y. (2001) Cbl: many adaptations to regulate protein tyrosine kinases. Nat. Rev. Mol. Cell Biol. 2, 294-307
180. Argetsinger, L. S., Campbell, G. S., Yang, X., Witthuhn, B. A., Silvennoinen, O., Ihle, J. N. and Carter-Su, C. (1993) Identification of JAK2 as a growth hormone receptor-associated tyrosine kinase. Cell 74, 237-244
181. Strous, G. J. and van Kerkhof, P. (2002) The ubiquitin-proteasome pathway and the regulation of growth hormone receptor availability. Mol. Cell. Endocrinol. 197, 143-151
182. Alves dos Santos, C. M., ten Broeke, T. and Strous, G. J. (2001) Growth hormone receptor ubiquitination, endocytosis, and degradation are independent
183. Strous, G. J., van Kerkhof, P., Covers, R., Ciechanover, A. and Schwartz, A. L. (1996) The ubiquitin conjugation system is required for ligand-induced endocytosis and degradation of the growth hormone receptor. EMBO J. 15, 3806-3812
184. Govers, R., ten Broeke, T., van Kerkhof, P., Schwartz, A. L. and Strous, G. J. (1999) Identification of a novel ubiquitin conjugation motif, required for ligand-induced internalization of the growth hormone receptor. EMBO J. 18, 28-36
185. Sachse, M., van Kerkhof, P., Strous, G. J. and Klumperman, J. (2001) The ubiquitin-dependent endocytosis motif is required for efficient incorporation of growth hormone receptor in clathrin-coated pits, but not clathrin-coated lattices. J. Cell Sci. 114, 3943-3952
186. Gether, U. (2000) Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr. Rev. 21, 90-113
187. Rocheville, M., Lange, D. C., Kumar, U., Sasi, R., Patel, R. C. and Patel, Y. C. (2000) Subtypes of the somatostatin receptor assemble as functional homo- and heterodimers. J. Biol. Chem. 275, 7862-7869
188. Ferguson, S. S. (2001) Evolving concepts in G protein-coupled receptor endocytosis: The role in receptor desensitization and signaling. Pharmacol. Rev. 53, 1-24
189. Lelkowitz, R. J. (1998) G protein-coupled receptors. J. Biol. Chem. 273, 18677-18680
190. Oakley, R. H., Laporte, S. A., Holt, J. A., Caron, M. G. and Barak, L. S. (2000) Differential affinities of visual arrestin, beta arrestin1, and beta arrestin2 for G protein-coupled receptors delineate two major classes of receptors. J. Biol. Chem. 275, 17201-17210
191. Luttrell, L. M. and Lefkowitz, R. J. (2002) The role of beta-arrestins in the termination and transduction of G-protein-coupled receptor signals. J. Cell Sci. 115, 455-465
192. Goodman, Jr. O. B., Krupnick, J. G., Santini, F., Gurevich, V. V., Penn, R. B., Gagnon, A. W., Keen, J. H. and Benovic, J. L. (1996) Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor. Nature (London) 383, 447-450
193. Laporte, S. A., Oakley, R. H., Holt, J. A., Barak, L. S. and Caron, M. G. (2000) The interaction of beta-arrestin with the AP-2 adaptor is required for the clustering of beta 2-adrenergic receptor into clathrin-coated pits. J. Biol. Chem, 275, 23120-23126
194. Gaidarov, I., Krupnick, J. G., Falck, J. R., Benovic, J. L. and Keen, J. H. (1999) Arrestin function in G protein-coupled receptor endocytosis requires phosphoinositide binding. EMBO J. 18, 871-881
195. Shenoy, S. K., McDonald, P. H., Kohout, T. A. and Lefkowitz, R. J. (2001) Regulation of receptor fate by ubiquitination of activated beta 2-adrenergic receptor and beta-arrestin. Science 294, 1307-1313
196. Takei, K. and Haucke, V. (2001) Clathrin-mediated endocytosis: membrane factors pull the trigger. Trends Cell Biol. 11, 385-391