Structural insights into the clathrin coat

Seminars in Cell and Developmental Biology

Volumn 18, Issue 4, 2007, Pages 448-458

  Young, Anna ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Clathrin lattice; Clathrin triskelion; Endocytosis

Indexed keywords

ADENOSINE TRIPHOSPHATE; AUXILIN; CHAPERONE; CHOLERA TOXIN; CLATHRIN; GREEN FLUORESCENT PROTEIN; HEAT SHOCK COGNATE PROTEIN 70; IRON; SHIGA TOXIN; TRANSFERRIN;

AGING; ALZHEIMER DISEASE; ANIMAL CELL; CHROMOSOME SEGREGATION; CRYOELECTRON MICROSCOPY; DEGENERATIVE DISEASE; ENDOCYTOSIS; FOOT AND MOUTH DISEASE VIRUS; GOLGI COMPLEX; HEPATITIS C VIRUS; HUMAN; HUNTINGTON CHOREA; LOWE SYNDROME; MEMBRANE TRANSPORT; MEMBRANE VESICLE; MITOSIS; NERVE CELL; NEUROLOGIC DISEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PARKINSON DISEASE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SHIGELLA DYSENTERIAE; TOXIN ANALYSIS; VIBRIO CHOLERAE; VIRUS CELL INTERACTION; X RAY CRYSTALLOGRAPHY;

TRISKELION;

EID: 34548396892     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2007.07.006     Document Type: Review

References (91)

1. Roth T.F., and Porter K.R. Yolk protein uptake in the oocyte of the mosquito Aedes aegypti L. J Cell Biol 20 (1964) 313-332
2. Kanaseki T., and Kadota K. 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 1 (1969) 202-220
3. Pearse B.M. Coated vesicles from pig brain: purification and biochemical characterisation. J Mol Biol 97 1 (1975) 93-98
4. Ungewickell E., and Branton D. Assembly units of clathrin coats. Nature 289 5796 (1981) 420-422
5. Pearse B.M. On the structural and functional components of coated vesicles. J Mol Biol 126 4 (1978) 803-812
6. Kirchhausen T., and Harrison S.C. Protein organization in clathrin trimers. Cell 23 3 (1981) 755-761
7. Vigers G.P., Crowther R.A., and Pearse B.M. Three-dimensional structure of clathrin cages in ice. EMBO J 5 3 (1986) 529-534
8. Lafer E.M. Clathrin-protein interactions. Traffic 3 8 (2002) 513-520
9. Blondeau F., Ritter B., Allaire P.D., Wasiak S., Girard M., Hussain N.K., et al. Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc Natl Acad Sci USA 101 11 (2004) 3833-3838
10. Borner G.H., Harbour M., Hester S., Lilley K.S., and Robinson M.S. Comparative proteomics of clathrin-coated vesicles. J Cell Biol 175 4 (2006) 571-578
11. Ehrlich M., Boll W., Van Oijen A., Hariharan R., Chandran K., Nibert M.L., et al. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118 5 (2004) 591-605
12. Ohno H., Stewart J., Fournier M.C., Bosshart H., Rhee I., Miyatake S., et al. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269 5232 (1995) 1872-1875
13. Haucke V., Wenk M.R., Chapman E.R., Farsad K., and De Camilli P. Dual interaction of synaptotagmin with mu2- and alpha-adaptin facilitates clathrin-coated pit nucleation. EMBO J 19 22 (2000) 6011-6019
14. Rohde G., Wenzel D., and Haucke V. A phosphatidylinositol (4,5)-bisphosphate binding site within mu2-adaptin regulates clathrin-mediated endocytosis. J Cell Biol 158 2 (2002) 209-214
15. Jost M., Simpson F., Kavran J.M., Lemmon M.A., and Schmid S.L. Phosphatidylinositol-4,5-bisphosphate is required for endocytic coated vesicle formation. Curr Biol 8 25 (1998) 1399-1402
16. Takei K., and Haucke V. Clathrin-mediated endocytosis: membrane factors pull the trigger. Trends Cell Biol 11 9 (2001) 385-391
17. Hinrichsen L., Meyerholz A., Groos S., and Ungewickell E.J. Bending a membrane: how clathrin affects budding. Proc Natl Acad Sci USA 103 23 (2006) 8715-8720
18. Kalthoff C., Alves J., Urbanke C., Knorr R., and Ungewickell E.J. Unusual structural organization of the endocytic proteins AP180 and epsin 1. J Biol Chem 277 10 (2002) 8209-8216
19. Edeling M.A., Mishra S.K., Keyel P.A., Steinhauser A.L., Collins B.M., Roth R., et al. Molecular switches involving the AP-2 beta2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev Cell 10 3 (2006) 329-342
20. Honing S., Ricotta D., Krauss M., Spate K., Spolaore B., Motley A., et al. Phosphatidylinositol-(4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol Cell 18 5 (2005) 519-531
21. Lauritsen J.P., Menne C., Kastrup J., Dietrich J., Odum N., and Geisler C. Beta2-adaptin is constitutively de-phosphorylated by serine/threonine protein phosphatase PP2A and phosphorylated by a staurosporine-sensitive kinase. Biochim Biophys Acta 1497 3 (2000) 297-307
22. Ricotta D., Conner S.D., Schmid S.L., von Figura K., and Honing S. Phosphorylation of the AP2 mu subunit by AAK1 mediates high affinity binding to membrane protein sorting signals. J Cell Biol 156 5 (2002) 791-795
23. Schmid E.M., Ford M.G., Burtey A., Praefcke G.J., Peak-Chew S.Y., Mills I.G., et al. Role of the AP2 beta-appendage hub in recruiting partners for clathrin-coated vesicle assembly. PLoS Biol 4 9 (2006)
24. Meyerholz A., Hinrichsen L., Groos S., Esk P.C., Brandes G., and Ungewickell E.J. Effect of clathrin assembly lymphoid myeloid leukemia protein depletion on clathrin coat formation. Traffic 6 12 (2005) 1225-1234
25. Blood P.D., and Voth G.A. Direct observation of Bin/amphiphysin/Rvs (BAR) domain-induced membrane curvature by means of molecular dynamics simulations. Proc Natl Acad Sci USA 103 41 (2006) 15068-15072
26. Takei K., Slepnev V.I., Haucke V., and De Camilli P. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1 1 (1999) 33-39
27. Farsad K., Ringstad N., Takei K., Floyd S.R., Rose K., and De Camilli P. Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J Cell Biol 155 2 (2001) 193-200
28. Casal E., Federici L., Zhang W., Fernandez-Recio J., Priego E.M., Miguel R.N., et al. The crystal structure of the BAR domain from human Bin1/Amphiphysin II and its implications for molecular recognition. Biochemistry 45 43 (2006) 12917-12928
29. Ford M.G., Mills I.G., Peter B.J., Vallis Y., Praefcke G.J., Evans P.R., et al. Curvature of clathrin-coated pits driven by epsin. Nature 419 6905 (2002) 361-366
30. Yoshida Y., Kinuta M., Abe T., Liang S., Araki K., Cremona O., et al. The stimulatory action of amphiphysin on dynamin function is dependent on lipid bilayer curvature. EMBO J 23 17 (2004) 3483-3491
31. Achiriloaie M., Barylko B., and Albanesi J.P. Essential role of the dynamin pleckstrin homology domain in receptor-mediated endocytosis. Mol Cell Biol 19 2 (1999) 1410-1415
32. Sever S., Skoch J., Newmyer S., Ramachandran R., Ko D., McKee M., et al. Physical and functional connection between auxilin and dynamin during endocytosis. EMBO J 25 18 (2006) 4163-4174
33. Sever S., Damke H., and Schmid S.L. Dynamin:GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J Cell Biol 150 5 (2000) 1137-1148
34. Sever S., Damke H., and Schmid S.L. Garrotes, springs, ratchets, and whips: putting dynamin models to the test. Traffic 1 5 (2000) 385-392
35. Barouch W., Prasad K., Greene L., and Eisenberg E. Auxilin-induced interaction of the molecular chaperone Hsc70 with clathrin baskets. Biochemistry 36 14 (1997) 4303-4308
36. Ungewickell E., Ungewickell H., Holstein S.E., Lindner R., Prasad K., Barouch W., et al. Role of auxilin in uncoating clathrin-coated vesicles. Nature 378 6557 (1995) 632-635
37. Ghosh P., and Kornfeld S. AP-1 binding to sorting signals and release from clathrin-coated vesicles is regulated by phosphorylation. J Cell Biol 160 5 (2003) 699-708
38. Verstreken P., Koh T.W., Schulze K.L., Zhai R.G., Hiesinger P.R., Zhou Y., et al. Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40 4 (2003) 733-748
39. Okamoto C.T., McKinney J., and Jeng Y.Y. Clathrin in mitotic spindles. Am J Physiol Cell Physiol 279 2 (2000) C369-C374
40. Royle S.J., Bright N.A., and Lagnado L. Clathrin is required for the function of the mitotic spindle. Nature 434 7037 (2005) 1152-1157
41. Royle S.J., and Lagnado L. Trimerisation is important for the function of clathrin at the mitotic spindle. J Cell Sci 119 Pt 19 (2006) 4071-4078
42. Cayrol C., Cougoule C., and Wright M. The beta2-adaptin clathrin adaptor interacts with the mitotic checkpoint kinase BubR1. Biochem Biophys Res Commun 298 5 (2002) 720-730
43. Radulescu A.E., Siddhanta A., and Shields D. A role for clathrin in reassembly of the Golgi apparatus. Mol Biol Cell 18 1 (2007) 94-105
44. O'Donnell V., LaRocco M., Duque H., and Baxt B. Analysis of foot-and-mouth disease virus internalization events in cultured cells. J Virol 79 13 (2005) 8506-8518
45. Meertens L., Bertaux C., and Dragic T. Hepatitis C virus entry requires a critical post-internalization step and delivery to early endosomes via clathrin coated vesicles. J Virol 80 23 (2006) 11571-11578
46. Sandvig K. Shiga toxins. Toxicon 39 11 (2001) 1629-1635
47. Hansen G.H., Dalskov S.M., Rasmussen C.R., Immerdal L., Niels-Christiansen L.L., and Danielsen E.M. Cholera toxin entry into pig enterocytes occurs via a lipid raft- and clathrin-dependent mechanism. Biochemistry 44 3 (2005) 873-882
48. Blanpied T.A., Scott D.B., and Ehlers M.D. Age-related regulation of dendritic endocytosis associated with altered clathrin dynamics. Neurobiol Aging 24 8 (2003) 1095-1104
49. Blanpied T.A., Scott D.B., and Ehlers M.D. Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 36 3 (2002) 435-449
50. Nakamura Y., Takeda M., Yoshimi K., Hattori H., Hariguchi S., Kitajima S., et al. Involvement of clathrin light chains in the pathology of Alzheimer's disease. Acta Neuropathol (Berl) 87 1 (1994) 23-31
51. Yao P.J. Synaptic frailty and clathrin-mediated synaptic vesicle trafficking in Alzheimer's disease. Trends Neurosci 27 1 (2004) 24-29
52. Nakamura Y., Takeda M., Yoshimi K., Hattori H., Hariguchi S., Hashimoto S., et al. Involvement of clathrin light chains in the pathology of Pick's disease; implication for impairment of axonal transport. Neurosci Lett 180 1 (1994) 25-28
53. Strehlow A.N., Li J.Z., and Myers R.M. Wild-type huntingtin participates in protein trafficking between the Golgi and the extracellular space. Hum Mol Genet 16 4 (2006) 391-409
54. Browne S.E., and Beal M.F. Oxidative damage in Huntington's disease pathogenesis. Antioxid Redox Signal 8 1112 (2006) 2061-2073
55. Lowe M. Structure and function of the Lowe syndrome protein OCRL1. Traffic 6 9 (2005) 711-719
56. Choudhury R., Diao A., Zhang F., Eisenberg E., Saint-Pol A., Williams C., et al. Lowe syndrome protein OCRL1 interacts with clathrin and regulates protein trafficking between endosomes and the trans-Golgi network. Mol Biol Cell 16 8 (2005) 3467-3479
57. Ferguson M.L., Prasad K., Sackett D.L., Boukari H., Lafer E.M., and Nossal R. Conformation of a clathrin triskelion in solution. Biochemistry 45 18 (2006) 5916-5922
58. Smith C.J., Grigorieff N., and Pearse B.M. Clathrin coats at 21 A resolution: a cellular assembly designed to recycle multiple membrane receptors. EMBO J 17 17 (1998) 4943-4953
59. Fotin A., Cheng Y., Sliz P., Grigorieff N., Harrison S.C., Kirchhausen T., et al. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432 7017 (2004) 573-579
60. Kirchhausen T., and Harrison S.C. Structural domains of clathrin heavy chains. J Cell Biol 99 5 (1984) 1725-1734
61. Ybe J.A., Brodsky F.M., Hofmann K., Lin K., Liu S.H., Chen L., et al. Clathrin self-assembly is mediated by a tandemly repeated superhelix. Nature 399 6734 (1999) 371-375
62. Blank G.S., and Brodsky F.M. Site-specific disruption of clathrin assembly produces novel structures. EMBO J 5 9 (1986) 2087-2095
63. Blank G.S., and Brodsky F.M. Clathrin assembly involves a light chain-binding region. J Cell Biol 105 5 (1987) 2011-2019
64. Ybe J.A., Ruppel N., Mishra S., and VanHaaften E. Contribution of cysteines to clathrin trimerization domain stability and mapping of light chain binding. Traffic 4 12 (2003) 850-856
65. ter Haar E., Musacchio A., Harrison S.C., and Kirchhausen T. Atomic structure of clathrin: a beta propeller terminal domain joins an alpha zigzag linker. Cell 95 4 (1998) 563-573
66. Colman P.M., Varghese J.N., and Laver W.G. Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 303 5912 (1983) 41-44
67. Renault L., Nassar N., Vetter I., Becker J., Klebe C., Roth M., et al. The 1.7 A crystal structure of the regulator of chromosome condensation (RCC1) reveals a seven-bladed propeller. Nature 392 6671 (1998) 97-101
68. Ramjaun A.R., and McPherson P.S. Multiple amphiphysin II splice variants display differential clathrin binding: identification of two distinct clathrin-binding sites. J Neurochem 70 6 (1998) 2369-2376
69. Miele A.E., Watson P.J., Evans P.R., Traub L.M., and Owen D.J. Two distinct interaction motifs in amphiphysin bind two independent sites on the clathrin terminal domain beta-propeller. Nat Struct Mol Biol 11 3 (2004) 242-248
70. ter Haar E., Harrison S.C., and Kirchhausen T. Peptide-in-groove interactions link target proteins to the beta-propeller of clathrin. Proc Natl Acad Sci USA 97 3 (2000) 1096-1100
71. Jackson A.P., and Parham P. Structure of human clathrin light chains. Conservation of light chain polymorphism in three mammalian species. J Biol Chem 263 32 (1988) 16688-16695
72. Ungewickell E. Biochemical and immunological studies on clathrin light chains and their binding sites on clathrin triskelions. EMBO J 2 8 (1983) 1401-1408
73. Chen C.Y., Reese M.L., Hwang P.K., Ota N., Agard D., and Brodsky F.M. Clathrin light and heavy chain interface: alpha-helix binding superhelix loops via critical tryptophans. EMBO J 21 22 (2002) 6072-6082
74. Nathke I.S., Heuser J., Lupas A., Stock J., Turck C.W., and Brodsky F.M. Folding and trimerization of clathrin subunits at the triskelion hub. Cell 68 5 (1992) 899-910
75. Wang J., Wang Y., and O'Halloran J. Clathrin light chain: importance of the conserved carboxy terminal domain to function in living cells. Traffic 7 7 (2006) 824-832
76. Pishvaee B., Munn A., and Payne G.S. A novel structural model for regulation of clathrin function. EMBO J 16 9 (1997) 2227-2239
77. Heuser J. Three-dimensional visualization of coated vesicle formation in fibroblasts. J Cell Biol 84 3 (1980) 560-583
78. Crowther R.A., Finch J.T., and Pearse B.M. On the structure of coated vesicles. J Mol Biol 103 4 (1976) 785-798
79. Wakeham D.E., Chen C.Y., Greene B., Hwang P.K., and Brodsky F.M. Clathrin self-assembly involves coordinated weak interactions favorable for cellular regulation. EMBO J 22 19 (2003) 4980-4990
80. Greene B., Liu S.H., Wilde A., and Brodsky F.M. Complete reconstitution of clathrin basket formation with recombinant protein fragments: adaptor control of clathrin self-assembly. Traffic 1 1 (2000) 69-75
81. Musacchio A., Smith C.J., Roseman A.M., Harrison S.C., Kirchhausen T., and Pearse B.M. Functional organization of clathrin in coats: combining electron cryomicroscopy and X-ray crystallography. Mol Cell 3 6 (1999) 761-770
82. Fotin A., Cheng Y., Grigorieff N., Walz T., Harrison S.C., and Kirchhausen T. Structure of an auxilin-bound clathrin coat and its implications for the mechanism of uncoating. Nature 432 7017 (2004) 649-653
83. Cheng Y., Boll W., Kirchhausen T., Harrison S.C., and Walz T. Cryo-electron tomography of clathrin-coated vesicles: structural implications for coat assembly. J Mol Biol 365 3 (2007) 892-899
84. Smith C.J., Dafforn T.R., Kent H., Sims C.A., Khubchandani-Aswani K., Zhang L., et al. Location of auxilin within a clathrin cage. J Mol Biol 336 2 (2004) 461-471
85. Takenaka I.M., Leung S.M., McAndrew S.J., Brown J.P., and Hightower L.E. Hsc70-binding peptides selected from a phage display peptide library that resemble organellar targeting sequences. J Biol Chem 270 34 (1995) 19839-19844
86. Greene L.E., and Eisenberg E. Dissociation of clathrin from coated vesicles by the uncoating ATPase. J Biol Chem 265 12 (1990) 6682-6687
87. Barouch W., Prasad K., Greene L.E., and Eisenberg E. ATPase activity associated with the uncoating of clathrin baskets by Hsp70. J Biol Chem 269 46 (1994) 28563-28568
88. Ma Y., Greener T., Pacold M.E., Kaushal S., Greene L.E., and Eisenberg E. Identification of domain required for catalytic activity of auxilin in supporting clathrin uncoating by Hsc70. J Biol Chem 277 51 (2002) 49267-49274
89. Heuser J., and Steer C.J. Trimeric binding of the 70-kD uncoating ATPase to the vertices of clathrin triskelia: a candidate intermediate in the vesicle uncoating reaction. J Cell Biol 109 4 Pt 1 (1989) 1457-1466
90. Heymann J.B., Iwasaki K., Yim Y.I., Cheng N., Belnap D.M., Greene L.E., et al. Visualization of the binding of Hsc70 ATPase to clathrin baskets: implications for an uncoating mechanism. J Biol Chem 280 8 (2005) 7156-7161
91. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., et al. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25 13 (2004) 1605-1612